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Connections between area 3b of the somatosensory cortex and subdivisions of the ventroposterior nuclear complex and the anterior pulvinar nucleus in squirrel monkeys
Abstract
The goal of this study was to determine whether somatosensory thalamic nuclei other than the ventroposterior nucleus proper VP have connections with area 3b of the postcentral cortex in squirrel monkeys. Small injections of the anatomical tracers wheat germ agglutinin conjugated to horseradish peroxidaseWGA-HRP or H-proline were placed in electrophysiologically identified representations of body parts. The results indicate that, besides the well-established somatotopically organized connections with VP, area 3b has connections with three other nuclei of the somatosensory thalamus: the ventroposterior superior nucleus VPS [“shell” of VP], the ventroposterior inferior nucleus VPI, and the anterior pulvinar nucleus Pa. Injections confined to area 3b or involving adjacent parts of area 3a or area 1 indicate that connections between VPS, VPI, and Pa and the postcentral cortex are somatotopically organized. In VPS, connections related to the hand were found medially, and connections related to the foot were lateral. In VPI, connections with the cortical representations of the mouth, hand, and foot were successively more lateral. In Pa, connections related to the mouth, hand and foot were successively more ventral, lateral, and caudal, and the trunk region was caudomedial. The findings suggest that VPI contains a representation of all parts of the body, including the face. The connections of Pa with the primary somatosensory cortex, area 3b, the location of Pa relative to the ventroposterior nucleus, and the high degree of topographic order in the connections of Pa with the postcentral cortex suggest that Pa is an integral part of the somatosensory thalamus in monkeys and is homologous to the medial nucleus of the posterior group Pom in other mammals. Overall, the results contribute to the growing evidence that individual somatosensory cortical areas in monkeys receive inputs from multiple thalamic sources, and that a single thalamic nucleus has several cortical targets.
... Body representations within the anterior pulvinar abutted the body map in area VP and were situated anterior to retinotopic maps within the ventral pulvinar 25 . The organization of these maps was consistent with prior electrophysiological recordings and tracer studies in monkeys [26][27][28][29][30][31][32][33] . The distribution of face, hand, and foot representations within each region was similar between newborn and juvenile monkeys. ...
... http://dx.doi.org/10.1101/565390 doi: bioRxiv preprint first posted online Mar. 1, 2019; anatomical tracer and electrophysiological studies [16][17][18][19][20][21][22][23][24][26][27][28][29][30][31][32][33] . To our knowledge, our data constitute the first comprehensive account of somatotopic organization across the entire macaque brain. ...
Topographic sensory maps are a prominent feature of the adult primate brain. Here, we asked whether topographic representations of the environment are fundamental to early development. Using fMRI, we find that the newborn somato-motor system, spanning frontoparietal cortex and subcortex, comprises multiple topographic body representations. The organization of these large-scale body maps was indistinguishable from those in adults and already exhibited features stereotypical of adult maps. Finer-scale differentiation of individual fingers increased over the first two years, suggesting that topographic representations are refined during early development. Last, we found that somato-motor representations were unchanged in two visually impaired monkeys who relied entirely on touch for interacting with their environment, demonstrating that massive shifts in early sensory experience in an otherwise anatomically intact brain are not sufficient for driving cross-modal plasticity. We propose that a topographic scaffolding is present at birth that both directs and constrains experience-driven modifications throughout sensory systems.
... Selon Nelson & Kaas (1981) certains neurones thalamiques des noyaux VPM et VPL envoient des projections sur l'aire 3b, mais également sur l'aire 1. Ces projections divergentes ont été confirmées par d'autres travaux (Mayner & Kaas 1986 ;Cusick & Gould 1990 ;Shi et al. 1993 ;Shi & Apkarian 1995 ;Rausell et al. 1998 ;Padberg et Krubitzer 2007). Pons & Kaas (1985) ont également démontré que l'aire 2 recevait des afférences thalamiques en provenance du complexe VP mais dans une plus petite mesure que les aires 3b et 1. ...
... Enfin, une expansion et un affinement de la topographie interne se mettent en place. Le décours temporel et l'étendue de la plasticité diffèrent selon les conditions de désafférentation, notamment la combinaison des nerfs sectionnés et l'étendue de la dénervation cutanée (Merzenich 1983a,b ;1984 ;Cusick et al. 1990 ;Garraghty & Kaas 1991 ;Garraghty et al. 1994 ;Kolarik et al. 1994 ;. ...
Thanks to the high-density electro-encephalography (HD-EEG) technique, this work aimed to evaluate the human hand somatosensory representation plasticity induced by a non-invasive neurostimulation . Increasing interest in cortical plasticity has prompted the growing use of somatosensory evoked potentials (SEPs) to estimate changes in the cortical representation of body regions. Here we first tested the effect of different sites of hand stimulation and of the density of spatial sampling in the quality of estimation of somatosensory sources. Sources of two SEP components from the primary somatosensory cortex (N20/P20 and P45) were estimated using two levels of spatial sampling (64- vs. 128-channel) and stimulation of four distal sites in the upper limbs, including single digits (1st vs. 5th) and distal nerves with comparable cortical projection (superficial branch of the radial nerve and distal ulnar nerve). The most robust separation of somatosensory sources was achieved by comparing the cortical representations of the 1st digit and the distal ulnar nerve territories on the N20/P20 component of SEPs. While both the 64- and the 128-electrode montages correctly discriminated these two areas, only the 128-electrode montage was able to significantly separate sources in the other cases, notably when using 1st vs. 5th digit stimulation. Trustworthy somatotopic distinction of cortical representations was not obtainable for the P45 component, probably because of greater activation volume, radial orientation of sources in areas 1-2 and increased variability with attention and vigilance, which may need a denser sampling and better covering of the lower part of the head. Assessment of tangential SEP components to stimulation of 1st digit vs. ulnar nerve appears the best option to assess plastic somatosensory changes, especially when using relatively low electrode sampling. Abnormal reorganization of the primary somatosensory cortex (SI) after nerve damage, in particular shrinking of deafferented regions, is thought to participate in the emergence of pain, and pain-relieving procedures have been reported to induce normalization of altered somatotopic maps. Repetitive transcranial magnetic stimulation (rTMS) of the motor cortex is able to lessen neuropathic pain, but there is no direct evidence that it may also induce plastic somatotopic changes related to pain sensation. In the second study we assessed the ability of two modes of rTMS to induce such plastic phenomena in the primary somatosensory cortex (S1), and the possibility for this effect to be correlated with variations in pain perception in healthy subjects. Source reconstruction of S1 responses elicited by peripheral electrical stimulation and recorded with high-density (128-channel) EEG revealed significant expansion of the cortical representation of the hand following a single 20-min session of high-frequency (20 Hz) rTMS. This was associated with a specific increase of pain thresholds in this same hand. A similar trend was observed using a "theta-burst" rTMS paradigm, but changes in hand representation were significantly lesser, and not associated to pain threshold increase. No plastic somatotopic changes were observed after a sham rTMS session. These results demonstrate in humans the capability of motor cortex stimulation to induce rapid plastic somatosensory changes that may counterbalance those induced by a nerve lesion, and substantiate the use of this technique as a powerful measure to treat human pain.
... In the study of Sur et al. (1982) no ipsilateral representation in the squirrel monkey cortex was reported; however, the question of an ipsilateral representation appears not to have been addressed. Studies of the connections of area 3b of the squirrel monkey with the ventroposterior nuclear complex of the thalamus also make no mention of an ipsilateral representation (Cusick et al., 1985;Cusick and Gould, 1990). ...
... Benjamin and Welker (1957) describe a similar topography for the face representation of 3b. Cytoarchitectonic and connectional studies of the somatosensory cortex of squirrel monkeys (Sanides, 1968;Jones and Burton, 1976;Cusick et al., 1985;Cusick and Gould, 1990;Guldin et al., 1992) also show area 3b making a rostra1 flexure to follow the line of the lateral sulcus without entering the lateral sulcus. This surface location makes the squirrel monkey a good candidate for investigations of the organization of the trigeminal representation in primates. ...
Studies of the representation of the trigeminal nerve in the thalamus and cerebral cortex of mammals have revealed representations of both contra- and ipsilateral intraoral structures. However, the relative extent of both representations is subject to considerable species variation. The present study employed microelectrode mapping and anatomical tracing to investigate the location and extent of the ipsilateral representation in area 3b of the somatosensory cortex of squirrel monkeys. A small region, approximately 2 mm2, was found to be responsive to stimulation of ipsilateral intraoral structures. This region was located on the anteromedial border of area 3b, surrounded by the representation of the contralateral roof of the mouth. This region corresponded to areas of intense anterograde labeling following injections placed in the ventromedial portion of the ventral posterior medial nucleus of the thalamus at the only sites where neural responses could be elicited by stimulation of ipsilateral intraoral structures. The amount of thalamus and cortex given over to the ipsilateral representation in the squirrel monkey is small compared with that of the macaque monkey. This difference may be related to the lack of cheek pouches in the squirrel monkey, and therefore a different strategy for eating.
The representation of the contralateral lower lip in area 3b was split by the representation of the contralateral upper lip. This split representation is in agreement with previous studies of the trigeminal representation in area 3b of the macaque monkey and may be a general feature of the representation of the trigeminal nerve in area 3b of primate cerebral cortex.
... The cortical connections of area 3a are distinct from other somatosensory areas in that area 3a receives its densest input from cortical areas associated with the motor system, including the primary (M1), supplementary (SMA), and premotor (PM) areas. Area 3a is also densely interconnected with areas in the posterior parietal cortex (Huffman and Krubitzer, 2001), which is associated with complex behaviors such as goal-directed reaching (Ferraina and Bianchi, 1994;Snyder et al., 1997Snyder et al., , 1998Andersen et al., 1997; for reviews, see Mountcastle et al., 1984;Andersen et al., 2000) Although the thalamic connections of other anterior parietal fields have been well investigated (Whitsel et al., 1978;Jones et al., 1979;Nelson and Kaas, 1981;Cusick et al., 1985;Mayner and Kaas, 1986;Cusick and Gould, 1990;Krubitzer and Kaas, 1992; for reviews, see Jones, 1985;Kaas and Pons, 1988), only a few previous studies in monkeys have exam-ined the thalamo-cortical connections of area 3a. Furthermore, most studies define area 3a by using architectonic criteria alone, which can be problematic (Jones and Porter, 1980). ...
... Area 3a also receives input from somato-sensory nuclei of the thalamus. Thalamo-cortical patterns of connections for area 3b are from Gould, 1990, andKaas, 1992; those for S2 and PV are from Krubitzer and Kaas, 1992; and those for areas 1 and 2 are from ; see also Kaas and Pons, 1988. Conventions as in previous figures. ...
The present investigation is part of a broader effort to examine cortical areas that contribute to manual dexterity, reaching, and grasping. In this study we examine the thalamic connections of electrophysiologically defined regions in area 3a and architectonically defined primary motor cortex (M1). Our studies demonstrate that area 3a receives input from nuclei associated with the somatosensory system: the superior, inferior, and lateral divisions of the ventral posterior complex (VPs, VPi, and VPl, respectively). Surprisingly, area 3a receives the majority of its input from thalamic nuclei associated with the motor system, posterior division of the ventral lateral nucleus of the thalamus (VL), the mediodorsal nucleus (MD), and intralaminar nuclei including the central lateral nucleus (CL) and the centre median nucleus (CM). In addition, sparse but consistent projections to area 3a are from the anterior pulvinar (Pla). Projections from the thalamus to the cortex immediately rostral to area 3a, in the architectonically defined M1, are predominantly from VL, VA, CL, and MD. There is a conspicuous absence of inputs from the nuclei associated with processing somatic inputs (VP complex). Our results indicate that area 3a is much like a motor area, in part because of its substantial connections with motor nuclei of the thalamus and motor areas of the neocortex (Huffman et al. [2000] Soc. Neurosci. Abstr. 25:1116). The indirect input from the cerebellum and basal ganglia via the ventral lateral nucleus of the thalamus supports its role in proprioception. Furthermore, the presence of input from somatosensory thalamic nuclei suggests that it plays an important role in somatosensory and motor integration.
... The medial pulvinar (MPul) nucleus has few or no connections to V1, but is connected to a wide expanse of temporal, parietal, cingulate, and frontal cortices, including higher-order visual association areas (macaque: Trojanowski and Jacobson 1997; Gutierrez et al. 2000;marmoset: Homman-Ludiye et al. 2020). Similarly, the anterior (or oral) pulvinar has no connections with V1, being functionally connected primarily with somatic and motor processing areas (Grieve et al. 2000), including oculomotor control areas (macaque: Pons and Kaas 1985;Cusick et al. 1990;marmoset: Burman et al. 2015). In contrast, both the lateral (LPul) and the inferior pulvinar (IPul) nuclei have reciprocal connections with V1 and many extrastriate areas (macaque: Benevento and Rezak 1976;Ungerleider et al. 1983;Adams et al. 2000;Shipp 2001;marmoset: Dick et al. 1991;Huo et al. 2019;squirrel monkey: Cusick et al. 1993;Ogren and Hendrickson 1976; owl monkey: Beck and Kaas 1998; Cebus monkey: Soares et al. 2001). ...
Lesions in the primary visual cortex (V1) cause extensive retrograde degeneration in the lateral geniculate nucleus, but it remains unclear whether they also trigger any neuronal loss in other subcortical visual centers. The inferior (IPul) and lateral (LPul) pulvinar nuclei have been regarded as part of the pathways that convey visual information to both V1 and extrastriate cortex. Here, we apply stereological analysis techniques to NeuN-stained sections of marmoset brain, in order to investigate whether the volume of these nuclei, and the number of neurons they comprise, change following unilateral long-term V1 lesions. For comparison, the medial pulvinar nucleus (MPul), which has no connections with V1, was also studied. Compared to control animals, animals with lesions incurred either 6 weeks after birth or in adulthood showed significant LPul volume loss following long (> 11 months) survival times. However, no obvious areas of neuronal degeneration were observed. In addition, estimates of neuronal density in lesioned hemispheres were similar to those in the non-lesioned hemispheres of same animals. Our results support the view that, in marked contrast with the geniculocortical projection, the pulvinar pathway is largely spared from the most severe long-term effects of V1 lesions, whether incurred in early postnatal or adult life. This difference can be linked to the more divergent pattern of pulvinar connectivity to the visual cortex, including strong reciprocal connections with extrastriate areas. The results also caution against interpretation of volume loss in brain structures as a marker for neuronal degeneration.
... Neurons in the VPI region of both monkeys (Apkarian and Shi 1994) and humans (Lenz et al. 1993a) respond to noxious stimulation. In monkeys, the VPI projects densely to areas S2 and PV of the lateral parietal cortex and less densely and more superficially to areas of the anterior parietal cortex Cusick and Gould 1990;Krubitzer and Kaas 1992). Although the VPI relays spinothalamic tract information and includes neurons responsive to noxious stimuli, it seems likely that the role of VPI projections to the cortex is largely modulatory (Kaas 2004(Kaas , 2012. ...
The somatosensory system has by far the largest number of receptor types of any of the primate sensory systems, including mechanoreceptors, chemoreceptors, nociceptors and thermoreceptors. The sensation of touch is mainly mediated by mechanoreceptors, but there are a number of other processing channels within the somatosensory system for proprioception, pain and temperature. The classic view of two independent channels for somatosensory information from the trunk and the extremities, i.e. the dorsal column-medial lemniscus system for tactile sensitivity and position sense and the anterolateral or spinothalamic system for pain and temperature sensitivity, has been modified through the discovery of additional spinal pathways for the transmission of sensory impulses to the brain and by new views on pain mechanisms. Somatosensory information from the face is transmitted via the trigeminal nerve.
... All body representations in the thalamus were situated anterior to and were discrete from retinotopic maps within the ventral pulvinar (32). The distribution of face, hand, and foot representations within each region was similar between newborn and older juvenile monkeys, and was consistent with prior electrophysiological recordings and tracer studies in adult monkeys (6,30,(33)(34)(35)(36)(37)(38). Together, these data demonstrate the presence of large-scale topographic body maps in subcortical nuclei of newborn monkeys. ...
Significance
This study reports the discovery that large-scale topographic maps of the body exist throughout the entire primate somatosensory and motor systems at birth. Our results suggest that this proto-organization is established prenatally, even in areas that are crucial for coordinating and executing complex, ethologically relevant actions in adults. Given the behavioral immaturity of neonates, this suggests that large-scale body maps precede these action domains. Furthermore, our data can explain how these domains arise in stereotypical locations without the need for prespecification of function. This study demonstrates that topographic representations are a fundamental and pervasive principle of early development, providing the protoarchitecture of the entire brain on which experience-dependent specializations are elaborated postnatally.
... The localization of the activation in S1 in and around the hand knob (Yousry et al., 1997), the anatomically identifiable cortical region of the hand/arm representation in somatosensory cortex, is consistent with the somatotopic organization of SMC. In the monkey, somatosensory cortex is connected with the anterior pulvinar which is involved in somatosensory functions (Cusick & Gould, 1990;Pons & Kaas, 1985). ...
Reach movements are characterized by multiple kinematic variables that can change with age or due to medical conditions such as movement disorders. While the neural control of reach direction is well investigated, the elements of the neural network regulating speed (the nondirectional component of velocity) remain uncertain. Here, we used a custom made magnetic resonance (MR)‐compatible arm movement tracking system to capture the real kinematics of the arm movements while measuring brain activation with functional magnetic resonance imaging to reveal areas in the human brain in which BOLD‐activation covaries with the speed of arm movements. We found significant activation in multiple cortical and subcortical brain regions positively correlated with endpoint (wrist) speed (speed‐related activation), including contralateral premotor cortex (PMC), supplementary motor area (SMA), thalamus (putative VL/VA nuclei), and bilateral putamen. The hand and arm regions of primary sensorimotor cortex (SMC) and a posterior region of thalamus were significantly activated by reach movements but showed a more binary response characteristics (movement present or absent) than with continuously varying speed. Moreover, a subregion of contralateral SMA also showed binary movement activation but no speed‐related BOLD‐activation. Effect size analysis revealed bilateral putamen as the most speed‐specific region among the speed‐related clusters whereas primary SMC showed the strongest specificity for movement versus non‐movement discrimination, independent of speed variations. The results reveal a network of multiple cortical and subcortical brain regions that are involved in speed regulation among which putamen, anterior thalamus, and PMC show highest specificity to speed, suggesting a basal‐ganglia‐thalamo‐cortical loop for speed regulation.
... Cluster 5 consisted of the PuA, the anterior and medial and inferior VP, posterior nuclus (PO), suprageniculate nucleus (SG) as well as the MGN. Previous animal studies on macaques suggested that both the anterior pulvinar and ventral posterior superior nuclei are connected to the area 2 of somatosensory cortex (Cusick et al., 1990;Pons et al., 1985;Sherman and Guillery, 2013). The ventral posterior inferior nucleus (VPI) is essentially related to the sensory motor system, having been shown in primate studies to have afferent connection from the spinothalamic system and efferent connections to the second somatosensory area (Friedman and Murray, 1986;Stevens et al., 1993) and to a lesser extent S1 (Stevens et al., 1993). ...
Meta-analysis of neuroimaging results has proven to be a popular and valuable method to study human brain functions. A number of studies have used meta-analysis to parcellate distinct brain regions. A popular way to perform meta-analysis is typically based on the reported activation coordinates from a number of published papers. However, in addition to the coordinates associated with the different brain regions, the text itself contains considerably amount of additional information. This textual information has been largely ignored in meta-analyses where it may be useful for simultaneously parcellating brain regions and studying their characteristics. By leveraging recent advances in document clustering techniques, we introduce an approach to parcellate the brain into meaningful regions primarily based on the text features present in a document from a large number of studies. This new method is called MAPBOT (Meta-Analytic Parcellation Based On Text). Here, we first describe how the method works and then the application case of understanding the sub-divisions of the thalamus. The thalamus was chosen because of the substantial body of research that has been reported studying this functional and structural structure for both healthy and clinical populations. However, MAPBOT is a general-purpose method that is applicable to parcellating any region(s) of the brain. The present study demonstrates the powerful utility of using text information from neuroimaging studies to parcellate brain regions.
... This sprouting in part leads to the reorganization of somatosensory maps in the cuneate nucleus (Churchill et al., 2001;Xu and Wall, 1997) as well as its primary target, the ventroposterior nucleus of the thalamus (Churchill et al., 2001;Florence et al., 2000;Garraghty and Kaas, 1991a). To some extent, then, cortical plasticity reflects reorganization at lower levels, suggesting that cortical areas receiving similar thalamic connections to area 3b, such as area 1 (Cusick and Gould, 1990;Mayner and Kaas, 1986;Nelson and Kaas, 1981), would similarly reorganize. ...
... Nearby neurons have similar receptive fields, and a systematic partial map of the hand representation in area 3b can be reconstructed from a dense array of microelectrode recordings across the hand region by outlining all electrode penetration sites with receptive fields centered on any digit phalanges or pad of the palm, or part of the body (Merzenich et al., 1978;Nelson et al., 1980;Sur et al., 1982;Krubitzer and Kaas, 1990). Such maps are extremely consistent in somatotopy across individuals, and they conform to the orderly arrangement of projections from VP to area 3b (Jones et al., 1982;Kaas et al., 1984;Cusick and Gould, 1990;Qi et al., 2011b;Liao et al., 2013). In addition, narrow cellpoor septa separate the representations of digits in area 3b so that digit territories are histologically visible (Qi and Kaas, 2004). ...
In our experiments, we removed a major source of activation of somatosensory cortex in mature monkeys by unilaterally sectioning the sensory afferents in the dorsal columns of the spinal cord at a high cervical level. At this level, the ascending branches of tactile afferents from the hand are cut, while other branches of these afferents remain intact to terminate on neurons in the dorsal horn of the spinal cord. Immediately after such a lesion, the monkeys seem relatively unimpaired in locomotion and often use the forelimb, but further inspection reveals that they prefer to use the unaffected hand in reaching for food. In addition, systematic testing indicates that they make more errors in retrieving pieces of food, and start using visual inspection of the rotated hand to confirm the success of the grasping of the food. Such difficulties are not surprising as a complete dorsal column lesion totally deactivates the contralateral hand representation in primary somatosensory cortex (area 3b). However, hand use rapidly improves over the first post-lesion weeks, and much of the hand representational territory in contralateral area 3b is reactivated by inputs from the hand in roughly a normal somatotopic pattern. Quantitative measures of single neuron response properties reveal that reactivated neurons respond to tactile stimulation on the hand with high firing rates and only slightly longer latencies. We conclude that preserved dorsal column afferents after nearly complete lesions contribute to the reactivation of cortex and the recovery of the behavior, but second-order sensory pathways in the spinal cord may also play an important role. Our microelectrode recordings indicate that these preserved first-order, and second-order pathways are initially weak and largely ineffective in activating cortex, but they are potentiated during the recovery process. Therapies that would promote this potentiation could usefully enhance recovery after spinal cord injury.
... In primates, thalamic connections of area 3b are predominantly from the ventral posterior nucleus, both VPm and VPl (e.g., Jones et al., 1979;Nelson & Kaas, 1981;Mayner & Kaas, 1986;Darian-Smith et al., 1990;Krubitzer & Kaas, 1992;Rausell & Jones, 1995;Coq et al., 2005;Padberg et al., 2006). However, sparse projections from VPi, VPs, and Pa have also been observed (e.g., Cusick & Gould, 1990). ...
... The differences should be due to the different species and also, perhaps, to differences in methodology. In the monkey, VPI neurons project to both SII (Friedman and Murray, 1986; Stevens et al., 1993) and SI (Cusick and Gould, 1990; Gingold et al., 1991; Shi et al., 1993). Because little is known about the neuronal morphology in VPI, we explored many SI-projecting neurons in this nucleus. ...
This study examined the morphology of thalamocortical neurons projecting to the primary somatosensory cortex (SI; hand region of areas 3a, 3b, 1, and 2) and their relationship to the spinothalamic (STT) terminals in the squirrel monkey. Retrogradely labeled thalamocortical neurons were intracellularly filled with Lucifer yellow (LY), and the STT terminals were anterogradely labeled with biotinylated dextran. Both filled neurons and labeled terminals were differentially visualized in the same field by a dual immunocytochemical staining method. SI-projecting neurons appeared at the light level to be in contact with STT terminal boutons in the ventroposterior lateral (VPL), ventroposterior inferior (VPI), and centrolateral (CL) nuclei and the posterior complex (PO). The analyses of the neuronal morphology revealed that somatic and dendritic morphologies of SI-projecting neurons in these thalamic nuclei, as well as in the anterior pulvinlar (Pub), centromedial (CM), and ventrolateral (VL) nuclei, were generally comparable with some exceptions: VPL neurons had the largest soma sizes, the most primary dendrites, and the longest total dendritic length among all neurons studied; VPI neurons had the smallest soma sizes; VPL SI-projecting neurons were different from those in VPI in their soma sizes, shape factors, and orientations; in VPL the cells projecting to the superficial layers of SI were smaller than those projecting to the deeper layers, but in VPI the two groups of neurons were similar in soma sizes. In general, the SI-projecting neurons in VPL, VPI, and CL were similar in their dendritic morphologies and branching patterns, and varied from those in Pub, PO, CM, and VL. © 1995 Wiley-Liss, Inc.
... Nevertheless, in a recent study, local field potential source analysis of LEPs obtained from subdural grids over sensori-motor cortex showed a dipole that could be located in area 3b, with the limitations mentioned above regarding the difficulty of modeling sources of potentials generated close to the central fissure from surface recordings [Baumgärtner et al., 2011]. It is noteworthy that, although four spinothalamic recipient structures in the thalamus (ventro-posterior lateral, ventro-posterior inferior, anterior pulvinar and central lateral nuclei) send nociceptive afferents to area 3b [Cusick and Gould, 1990;Darian-Smith and Darian-Smith, 1993;Dum et al., 2009;Jones and Leavitt, 1974;Minciacchi et al., 1995;Padberg et al., 2009], S1 receives quantitatively very limited nociceptive inputs [Dum et al., 2009;Gingold et al., 1991]. In accordance with the paucity of local 3b nociceptive responses observed in the present work, neurophysiological studies in animals have shown that only a limited number of neurons responding to noxious thermal and mechanical stimuli are present in this area [Kenshalo and Isensee, 1983;Kenshalo and Willis, 1991;Kenshalo et al., 1988Kenshalo et al., , 2000. ...
Intracortical evoked potentials to nonnoxious Aβ (electrical) and noxious Aδ (laser) stimuli within the human primary somatosensory (S1) and motor (M1) areas were recorded from 71 electrode sites in 9 epileptic patients. All cortical sites responding to specific noxious inputs also responded to nonnoxious stimuli, while the reverse was not always true. Evoked responses in S1 area 3b were systematic for nonnoxious inputs, but seen in only half of cases after nociceptive stimulation. Nociceptive responses were systematically recorded when electrode tracks reached the crown of the postcentral gyrus, consistent with an origin in somatosensory areas 1-2. Sites in the precentral cortex also exhibited noxious and nonnoxious responses with phase reversals indicating a local origin in area 4 (M1). We conclude that a representation of thermal nociceptive information does exist in human S1, although to a much lesser extent than the nonnociceptive one. Notably, area 3b, which responds massively to nonnoxious Aβ activation was less involved in the processing of noxious heat. S1 and M1 responses to noxious heat occurred at latencies comparable to those observed in the supra-sylvian opercular region of the same patients, suggesting a parallel, rather than hierarchical, processing of noxious inputs in S1, M1 and opercular cortex. This study provides the first direct evidence for a spinothalamic related input to the motor cortex in humans. Hum Brain Mapp, 2012. © 2012 Wiley Periodicals, Inc.
... Thus, the same neuron in VP can project to 2 different representations in 3b (D3 and the thenar pad), and the same representation in VP (hand) can project to different representations in 3b (D3, Th, Dor). nucleus and the primary somatosensory area of the cortex, area 3b (Jones and Powell 1970; Whitsel et al. 1978; Lin et al. 1979; Nelson and Kaas 1981; Cusick et al. 1985; Mayner and Kaas 1986; Cusick and Gould 1990; Darian-Smith et al. 1990; Krubitzer and Kaas 1992; Qi et al. 2002). One previous study examined the thalamocortical connections of 2 closely placed injections in area 3b (Rausell and Jones 1995) and found double-labeled cells in VP only when injections were less than 600 lm apart. ...
We examined the organization and cortical projections of the somatosensory thalamus using multiunit microelectrode recording techniques in anesthetized monkeys combined with neuroanatomical tracings techniques and architectonic analysis. Different portions of the hand representation in area 3b were injected with different anatomical tracers in the same animal, or matched body part representations in parietal areas 3a, 3b, 1, 2, and areas 2 and 5 were injected with different anatomical tracers in the same animal to directly compare their thalamocortical connections. We found that the somatosensory thalamus is composed of several representations of cutaneous and deep receptors of the contralateral body. These nuclei include the ventral posterior nucleus, the ventral posterior superior nucleus, the ventral posterior inferior nucleus, and the ventral lateral nucleus. Each nucleus projects to several different cortical fields, and each cortical field receives projections from multiple thalamic nuclei. In contrast to other sensory systems, each of these somatosensory cortical fields is uniquely innervated by multiple thalamic nuclei. These data indicate that multiple inputs are processed simultaneously within and across several, "hierarchically connected" cortical fields.
... Possibly this entire region consists of layer I-projecting cells, but data are only available for the calbindin cells of VPM, VPL, and VLp. Although PLa is known to project to area 2 of SI and to area 5 Jones et al., 1979;Pons and Kaas, 1985;Cusick and Gould, 1990), terminations of its axons have previously only been localized in layer III ). ...
The ventral posterior lateral nucleus (VPL) of the monkey thalamus was investigated by histochemical staining for cytochrome oxidase (CO) activity and by immunocytochemical staining for the calcium-binding proteins parvalbumin and 28 kDa calbindin. Anterograde and retrograde tracing experiments were used to correlate patterns of differential distribution of CO activity and of parvalbumin and calbindin cells with the terminations of spinothalamic tract fibers and with the types of cells projecting differentially to superficial and deeper layers of primary somatosensory cortex (SI). VPL is composed of CO-rich and CO-weak compartments. Cells are generally smaller in the CO-weak compartment. Parvalbumin-immunoreactive cells and parvalbumin-immunoreactive medial lemniscal fiber terminations are confined to the CO-rich compartment. Calbindin-immunoreactive cells are found in both the CO-rich and CO-weak compartments. The CO-weak compartment, containing only calbindin cells, forms isolated zones throughout VPL and expands as a cap covering the posterior surface of the ventral posterior medial nucleus (VPM). Spinothalamic tract terminations tend to be concentrated in the CO-weak compartment, especially in the posterior cap. Other CO-weak, parvalbumin-negative, calbindin-positive nuclei, including the posterior, ventral posterior inferior, and anterior pulvinar and the small-celled matrix of VPM are also associated with concentrations of spinothalamic and caudal trigeminothalamic terminations. Parvalbumin cells are consistently larger than calbindin cells and are retrogradely labeled only after injections of tracers in middle and deep layers of SI. The smaller calbindin cells are the only cells retrogradely labeled after placement of retrograde tracers that primarily involve layer I of SI. The compartmental organization of VPL is similar to but less rigid than that previously reported in VPM. VPL and VPM relay cells projecting to different layers of SI cortex can be distinguished by differential immunoreactivity for the two calcium-binding proteins. The small-celled, CO-weak, calbindin-positive zones of VPL and VPM appear to form part of a wider system of smaller thalamic neurons unconstrained by traditional nuclear boundaries that are preferentially the targets of spinothalamic and caudal trigeminal inputs, and that may have preferential access to layer I of SI.
In this study, thalamic connections of the caudal part of the posterior parietal cortex (PPCc) are described and compared to connections of the rostral part of PPC (PPCr) in strepsirrhine galagos. PPC of galagos is divided into two parts, PPCr and PPCc, based on the responsiveness to electrical stimulation. Stimulation of PPC with long trains of electrical pulses evokes different types of ethologically relevant movements from different subregions (“domains”) of PPCr, while it fails to evoke any movements from PPCc. Anatomical tracers were placed in both dorsal and ventral divisions of PPCc to reveal thalamic origins and targets of PPCc connections. We found major thalamic connections of PPCc with the lateral posterior and lateral pulvinar nuclei, distinct from those of PPCr that were mainly with the ventral lateral, anterior pulvinar, and posterior nuclei. The anterior, medial, and inferior pulvinar, ventral anterior, ventral lateral, and intralaminar nuclei had fewer connections with PPCc. Dominant connections of PPCc with lateral posterior and lateral pulvinar nuclei provide evidence that unlike the sensorimotor‐orientated PPCr, PPCc is more involved in visual‐related functions.
Almost all functional processing in the cortex strongly depends on thalamic interactions. However, in terms of functional interactions with the cerebral cortex, the human thalamus nuclei still partly constitute a terra incognita. Hence, for a deeper understanding of thalamic-cortical cooperation, it is essential to know how the different thalamic nuclei are associated with cortical networks. The present work examines network-specific connectivity and task-related topical mapping of cortical areas with the thalamus. The study finds that the relay and higher-order thalamic nuclei show an intertwined functional association with different cortical networks. In addition, the study indicates that relay-specific thalamic nuclei are not only involved with relay-specific behavior but also in higher-order functions. The study enriches our understanding of interactions between large-scale cortical networks and the thalamus, which may interest a broader audience in neuroscience and clinical research.
In prosimian galagos, the posterior parietal cortex (PPC) is subdivided into a number of functional domains where long‐train intracortical microstimulation evoked different types of complex movements. Here, we placed anatomical tracers in multiple locations of PPC to reveal the origins and targets of thalamic connections of four PPC domains for different types of hindlimb, forelimb, or face movements. Thalamic connections of all four domains included nuclei of the motor thalamus, ventral anterior and ventral lateral nuclei, as well as parts of the sensory thalamus, the anterior pulvinar, posterior and ventral posterior superior nuclei, consistent with the sensorimotor functions of PPC domains. PPC domains also projected to the thalamic reticular nucleus in a somatotopic pattern. Quantitative differences in the distributions of labeled neurons in thalamic nuclei suggested that connectional patterns of these domains differed from each other. The posterior parietal cortex (PPC) of galagos contains a series of domains where electrical stimulation evokes different types of complex movements. The medial domains have more connections with the motor thalamus, whereas the lateral domains connect more densely with the posterior thalamus that involves in somatosensory processing.
The primary somatosensory cortex (S1) plays a key role in the processing and integration of afferent somatosensory inputs along an anterior-to-posterior axis, contributing towards necessary human function. It is believed that anatomical connectivity can be used to probe hierarchical organization, however direct characterization of this principle in-vivo within humans remains elusive. Here, we use resting-state functional connectivity as a complement to anatomical connectivity to investigate topographical principles of human S1. We employ a novel approach to examine mesoscopic variations of functional connectivity, and demonstrate a topographic organisation spanning the region's hierarchical axis that strongly correlates with underlying microstructure while tracing along architectonic Brodmann areas. Our findings characterize anatomical hierarchy of S1 as a ‘continuous spectrum’ with evidence supporting a functional boundary between areas 3b and 1. The identification of this topography bridges the gap between structure and connectivity, and may be used to help further current understanding of sensorimotor deficits.
Chronic, pathological pain remains a global health problem and a challenge to basic and clinical sciences. A major obstacle to preventing, treating or reverting chronic pain has been that the nature of neural circuits underlying the diverse components of the complex, multidimensional experience of pain is not well understood. Moreover, chronic pain involves diverse maladaptive plasticity processes, which have not been decoded mechanistically in terms of involvement of specific circuits and cause-effect relationships. This review aims to discuss recent advances in our understanding of circuit connectivity in the mammalian brain at the level of regional contributions and specific cell types in acute and chronic pain. A major focus is placed on functional dissection of sub-neocortical brain circuits using optogenetics, chemogenetics and imaging technological tools in rodent models with a view towards decoding sensory, affective and motivational-cognitive dimensions of pain. The review summarizes recent breakthroughs and insights on structure-function properties in nociceptive circuits and higher order sub-neocortical modulatory circuits involved in aversion, learning, reward and mood and their modulation by endogenous GABAergic inhibition, noradrenergic, cholinergic, dopaminergic, serotonergic and peptidergic pathways. The knowledge of neural circuits and their dynamic regulation via functional and structural plasticity will be beneficial towards designing and improving targeted therapies.
The sense of proprioception allows us to keep track of our limb posture and movements and the sense of touch provides us with information about objects with which we come into contact. In both senses, mechanoreceptors convert the deformation of tissues—skin, muscles, tendons, ligaments, or joints—into neural signals. Tactile and proprioceptive signals are then relayed by the peripheral nerves to the central nervous system, where they are processed to give rise to percepts of objects and of the state of our body. In this review, we first examine briefly the receptors that mediate touch and proprioception, their associated nerve fibers, and pathways they follow to the cerebral cortex. We then provide an overview of the different cortical areas that process tactile and proprioceptive information. Next, we discuss how various features of objects—their shape, motion, and texture, for example—are encoded in the various cortical fields, and the susceptibility of these neural codes to attention and other forms of higher‐order modulation. Finally, we summarize recent efforts to restore the senses of touch and proprioception by electrically stimulating somatosensory cortex. © 2018 American Physiological Society. Compr Physiol 8:1575‐1602, 2018.
The somatosensory system processes information from low threshold mechanoreceptors in the skin and deep receptors in muscles and joints to allow the active identification of objects by touch. The basic components of the somatosensory pathways from receptors through an array of cortical areas are partly known for monkeys, and processing in humans is likely to depend on comparable pathways. Information from classes of rapidly adapting (RA) and slowly adapting (SA) cutaneous receptors and muscle spindle (MS) receptors remain segregated in relays through the dorsal column-trigeminal complex and the ventroposterior thalamus. In the ventroposterior complex, we distinguish a ventroposterior nucleus that relays SA and RA information to cortical area 3b and to area 1. Muscle spindle information is relayed via the ventroposterior superior nucleus to areas 3a and 2. The ventroposterior inferior nucleus receives inputs from the spinothalamic system and relays to the second somatosensory area(S-II), the adjoining parietal ventral area (PV) and other fields. The VPI relay appears to only modulate cortical neurons and it may provide information about intense stimuli that extend into the painful range. Area 1 is dependent on 3b projections for activation even though it receives direct thalamic inputs. Area 2; S-II, and PV also depend on area 3b directly or indirectly for activation via cutaneous receptors. Activation via deep receptors remains as a result of VPS projections to area 3a and area 2, and cortical relays to S-II and PV. Further steps in a lateral stream of cortical processing involve limbic system structures that are critical in memory storage, while other projections to subdivisions of posterior parietal cortex are presumably concerned with the sensory attention and control of movements in space. The somatosensory fields also project in different patterns to two subdivisions of primary motor cortex, the supplementary motor area, premotor cortex, and motor eye fields to have presumptive roles in initiating and guiding motor behavior.
This chapter focuses on the early stages of the large part of the somatosensory system that is concerned with tactile sensations and perception. To a great extent, these abilities depend on afferent pathways from low-threshold mechanoreceptors in the skin for information about skin contact and vibration, and receptors in muscles and joints (and probably skin) for information about the relative positions of body parts. Branches of these afferent pathways reach nuclei in the dorsal column-trigeminal complex in the cervical spinal cord and lower brainstem to relay to the contralateral ventroposterior complex in the thalamus. Neurons activated by receptors in the mouth and on parts of the face project to the ipsilateral as well as the contralateral thalamus. The ventroposterior complex of primates includes a ventroposterior proper nucleus, composed of ventroposterior medial division and ventroposterior lateral division. Ventroposterior nucleus (VP) of monkeys is activated by slowly adapting and rapidly adapting classes of cutaneous mechanoreceptors. This information is relayed to areas 3b and 1, and, to a limited extent, area 2 of the anterior parietal cortex. Area 3b corresponds to S1 of nonprimates such as rats and cats, where both S1 and S2 receive inputs from VP. Ventroposterior superior nucleus (VPS), which has only been identified as such in primates, receives inputs relayed from muscle spindle and probably joint receptors, and projects to areas 3a and 2 of the anterior parietal cortex. A group of cells along the dorsorostral margin of VP responds to muscle spindle receptor stimulation in other mammals such as cats and rats, with this group of cells variously recognized as a distinct nucleus or a part of the VP. These neurons project to a strip of the cortex along the rostral border of S1 variously described as area 3a or the dysgranular cortex. Ventroposterior inferior nucleus (VPI) of primates receives inputs from the spinothalamic subsystem that includes a relay of wide dynamic range afferent information, and this information is relayed most densely to second somatosensory (S2) and parietal ventral area (PV). VPI also projects less densely to superficial cortical layers in other somatosensory areas (3a, 3b, 1, and 2). VPI is seldom recognized in nonprimate mammals, as it is often poorly developed, but VPI has been identified in cats and raccoons, where it also projects densely to S2. A VPI is apparent in squirrels, where a projection to PV has been described, but VPI is at best a thin layer of cells on the ventral surface of VP in rats. VPI projections appear to provide a modulating influence on the responses of cortical neurons that are activated by the thalamic relay of information from cutaneous and deep receptors in VP and VPS. Information from cutaneous receptors about skin indentations and from deep receptors about position sense is combined in higher-order somatosensory areas to allow objects to be identified by shape and texture during active touch.
This chapter provides an overview of the organization of the somatosensory system of humans. It emphasizes on the components of somatosensory system that are important in identifying objects and features of surfaces by touch. Even though small shapes can be perceived with information solely from tactile receptors, most discrimination involves an active process of tactile exploration with multiple contacts on the skin and an integration of cutaneous and proprioceptive information as well as efferent control. Thus, this chapter concentrates on the pathways and neural centers for processing information from the low-threshold mechanoreceptors of the skin that provide information about touch, and the deeper receptors in joints and especially muscles that provide information about position. It is observed that conclusions are based on both studies in humans and studies in other primates, especially the frequently studied macaque monkeys. Moreover, the early stages of processing are likely to be similar in humans and monkeys, but humans appear to have a more expanded cortical network for processing somatosensory information.
The somatosensory system has by far the largest number of receptor types of any of the primate sensory systems, including mechanoreceptors, chemoreceptors, nociceptors and thermoreceptors. The sensation of touch is mainly mediated by mechanoreceptors, but there are a number of other processing channels within the somatosensory system for proprioception, pain and temperature. The classic view of two independent channels for somatosensory information from the trunk and the extremities, i.e. the dorsal column-medial lemniscus system for tactile sensitivity and position sense and the anterolateral or spinothalamic system for pain and temperature sensitivity, has been modified through the discovery of additional spinal pathways for the transmission of sensory impulses to the brain (Willis and Coggeshall 1991) and by new views on pain mechanisms. Somatosensory information from the face is transmitted via the trigeminal nerve. Pain is conventionally viewed as a submodality of cutaneous sensation. Functional, anatomical and imaging data suggest that pain impulses are conveyed by specific sensory channels that ascend in a central homeostatic afferent pathway (Craig 2003a, b).
La percezione cosciente della sensibilità cutanea e propriocettiva e del gusto dipendono dalle vie di conduzione che connettono
i recettori periferici con i centri a livello del diencefalo e del telencefalo. La maggior parte di queste connessioni, a
eccezione delle vie per il gusto, è crociata. L’elaborazione iniziale dell’informazione sensoriale avviene nel midollo spinale
e nei nuclei delle colonne dorsali per le informazioni relative al tronco e alle estremità, e nei nuclei sensoriali del nervo
trigemino per quelle della faccia. Il primo relè per il gusto è situato nel nucleo del tratto solitario nel segmento inferiore
del tronco encefalico. Le vie di conduzione spinale sono costituite dal fascicolo anterolaterale e dalla via delle colonne
dorsali-lemnisco mediale. Entrambi questi sistemi sono crociati. Le vie corrispondenti traggono origine dai nuclei sensoriali
del nervo trigemino.
This account covers the cytoarchitecture and chemoarchitecture of the thalamus in representative prosimians and monkeys and in the human. Parcellations of the thalamus on the basis of histochemical staining patterns serve to confirm and extend those made on the basis of cyto- and myeloarchitecture alone, and help to reinforce the conviction that the thalamus of all primates is fundamentally similar. The major differences between prosimians and simians are in the relative reduction of the anterior nuclei and expansion of the ventral lateral, posterior intralaminar and pulvinar nuclei in the latter family. In humans, the enlargement of the thalamus parallels that of the cerebral cortex and is especially associated with expansions of the ventral lateral, posterior intralaminar and pulvinar nuclei. The nuclear divisions of the human thalamus are, nevertheless, fundamentally similar to those of the Old World monkey thalamus so that a common nomenclature, despite historical precedent to the contrary, is not only feasible but desirable in order to facilitate the exchange of experimental and clinical information. The basic circuitry of the thalamus is built up on the basis of glutamatergic thalamocortical relay neurons, divisible into subclasses with different immunocytochemical signatures, and two sets of inhibitory, GABAergic interneurons - those intrinsic to the relay nuclei and those in the reticular nucleus. Differential expression of calcium binding proteins is a major distinguishing feature of relay neurons. Those containing 28kDa calbindin form a small-celled matrix in many thalamic nuclei and project relatively diffusely to superficial layers of the cerebral cortex. Those expressing parvalbumin form the topographically-organized projection to middle layers. The afferent innervation of the thalamus comes from a variety of nucleus-specific input pathways. The nucleus- and subnucleus-specific terminations of these pathways form the basis of parallel, segregated channels through the thalamus to the cerebral cortex. These parallel pathways are especially evident in the motor and auditory nuclei of the thalamus. In the somatosensory and visual relay nuclei, further functional channels within a major thalamocortical projection are formed by subpopulations of neurons innervated by specific classes of cutaneous mechanoreceptor or retinal ganglion cell. The excitatory corticothalamic projection, especially acting in concert with the inhibitory reticular nucleus, is a major factor in inducing collective oscillations of large ensembles of thalamic neurons which underlie changes in conscious state. The synapses made by subcortical, cortical and reticular nucleus inputs to the dorsal thalamus are associated with the expression of a wide variety of genes encoding GABAAreceptor subunits and glutamate receptors. Many of these show nucleus-specific patterns of expression. The thalamus is also innervated in a relatively non-specific manner by cholinergic, noradrenergic, serotoninergic and peptidergic fibers of brainstem origin but by few or no dopaminergic fibers. Many of these inputs elicit effects upon the same set of membrane conductances while others have more specific effects related to interactions with particular classes of receptor. The dorsal thalamus projects not only to the cerebral cortex, including the neocortex, palaeocortex and archicortex, but also to the striatum and amygdala and related basal telencephalic structures. The cortical projection is based upon populations of cells, often with particular morphological and chemical identities, that project in an areal-specific or more diffuse manner to the cortex, their axons commonly terminating in different cortical layers. The striatal projection arises from the intralaminar nuclei and from certain other nuclei whose chemistry is identical to that of the intralaminar nuclei and should probably be included in the intralaminar system. Many aspects of thalamic function, such as the relay of sensory information and the relay of information in systems that do not form components of obvious sensory systems, are reflected in the organization of the specific relay nuclei of the dorsal thalamus. These are considered individually in Section 10. Other, more generalized functions of the thalamus, such as its role in state dependent activities of the whole forebrain, are best considered in relation to the intrinsic and transmitter-defined circuitry of the thalamus. These are recurrent themes throughout the whole chapter.
Ventral posterior nucleus of thalamus sends highly segregated inputs into each digit representation in area 3b of primary somatosensory cortex. However, the spatial organization of the connections that link digit representations of areas 3b with other somatosensory areas is less understood. Here we examined the cortical inputs to individual digit representations of area 3b in four squirrel monkeys and one prosimian galago. Retrograde tracers were respectively injected into neurophysiologically defined representations of individual digits of area 3b. Cortical tissues were cut in the horizontal plane in some cases and showed that feedback projections to individual digits overlapped extensively in the hand representations of areas 3b, 1, and parietal ventral (PV) and second somatosensory (S2) areas. Other regions with overlapping populations of labeled cells included area 3a and primary motor cortex (M1). The results were confirmed in other cases in which the cortical tissues were cut in the coronal plane. The same cases also showed that cells were primarily labeled in the infragranular layers and supragranular layers. Thus, feedback projections to individual digit representations in area 3b mainly originate from multiple digits and other portions of hand representations of areas 3b, 1, PV and S2. This organization is in stark contrast to the segregated thalamocortical inputs, which originate in single digit representations and terminate in the matching digit representation in the cortex. The organization of feedback connections could provide a substrate for the integration of information across the representations of adjacent digits in area 3b. J. Comp. Neurol., 2013. © 2013 Wiley Periodicals, Inc.
To determine the relative contributions of transthalamic cerebellar and pallidal projections to the primary motor cortex (M1) of owl monkeys, we examined the thalamic labeling resulting from injections of fluorescent tracers and wheatgerm agglutinin/horseradish peroxidase conjugate (WGA-HRP) into regions of M1 identified by intracortical microstimulation. Injections were placed in the major somatotopic divisions of M1 (the hindlimb, trunk, forelimb, and face representations) and in the caudal and rostral M1 subareas. In most cases, we injected several differentiable tracers into different parts of M1. Our results indicate that the strongest connections of M1 are with subdivisions of the ventral lateral thalamus (VL); other connections are mainly with intralaminar nuclei (the central lateral, paracentral, and center median nuclei) and the reticular nucleus. Most projections are reciprocal and topographically organized. M1 is strongly connected with the principal (VLp), medial (VLx), and anterior (VLa) subdivisions of the VL complex but has at most weak connections with the dorsal division (VLd). Each of the major somatotopic divisions of M1 is connected with an anteroposteriorly elongated territory within the VL complex. The connections are somatotopically organized such that the M1 hindlimb representation is connected with a band of cells in the lateral and anterior portions of the VL complex (spanning VLa and VLp), whereas the trunk, forelimb, and face representations are connected with successively more medially and posteriorly situated cell bands (spanning VLa, VLp, and VLx). There is some degree of overlap between the somatotopic territories within VL, although the absence of double-labeled cells in cases with injections of adjacent somatotopic divisions of M1 suggests that individual thalamic neurons project to single somatotopic regions.
This study examined anatomic pathways that are likely to transmit noxious and thermal cutaneous information to the primary somatosensory cortex. Anterograde and retrograde labeling techniques were combined to investigate the relationship between spinothalamic (STT) projections and thalamocortical neurons in the squirrel monkey (Saimiri sciureus). Large injections of diamidino yellow (DY) were placed in the physiologically defined hand region of primary somatosensory cortex (hSI), and wheat germ agglutinin-horseradish peroxidase (WGA-HRP) was injected in the contralateral cervical enlargement (C5T1). Both DY-labeled neuronal cell bodies and HRP-labeled STT terminal-like structures were visualized within single thalamic sections in each animal. Quantitative analysis of the positions and numbers of retrogradely labeled neurons and anterogradely labeled terminal fields reveal that: (1) ventral posterior lateral (VPL), ventral posterior inferior (VPI), and central lateral (CL), combined, receive 87% of spinothalamic inputs originating from the cervical enlargement; (2) these three nuclei contain over 91% of all thalamocortical neurons projecting to hSI that are likely to receive STT input; and (3) these putatively contacted neurons account for less than 24% of all thalamic projections to hSI. These results suggest that three distinct spinothalamocortical pathways are capable of relaying nociceptive information to the hand somatosensory cortex. Moreover, only a small portion of thalamocortical neurons are capable of relaying STT-derived nociceptive and thermal information to the primary somatosensory cortex.
There has been much controversy over the organization of the thalamocortical somatosensory networks, in particular, over the issue of serial versus parallel processing in the SI and SII cortical areas. Several reports have established unequivocally that, in non-primate species, there is a parallel scheme of processing in which inputs from the thalamus reach both SI and SII independently. However, observations that SII responsiveness was abolished in primate species (the macaque and marmoset monkey) following the surgical ablation of the SI area, led to the interpretation that in primates a serial scheme operated in which tactile information is conveyed from the thalamus to SI and thence to SII via intracortical connections (Pons et al., 1987; Garraghty et al., 1990). However, re-investigation of this issue in the marmoset monkey in experiments based on reversible inactivation of SI by means of localized cooling (Zhang et al., 1996; Rowe et al., 1996) show unequivocally that there is substantial direct thalamic input to SII in the marmoset.In conclusion, it appears that there is no longer justification for the hypothesis that there are fundamental differences in terms of serial and parallel organization of the SI and SII areas, between simian primates in general, and other mammals (Murray et al., 1992; Turman et al., 1992, Turman et al., 1995). Whether the serial scheme can be confirmed for the macaque monkey, the other primate in which SI ablation was reported to abolish SII responsiveness (Burton et al., 1990; Garraghty et al., 1990; Pons et al., 1987, Pons et al., 1992), will depend upon the application of refined reversible methods such as cooling, for SI inactivation, and quantitative evaluation of SII responsiveness in association with the reversible inactivation procedures.
Adult owl and squirrel monkeys were trained to master a small-object retrieval sensorimotor skill. Behavioral observations along with positive changes in the cortical area 3b representations of specific skin surfaces implicated specific glabrous finger inputs as important contributors to skill acquisition. The area 3b zones over which behaviorally important surfaces were represented were destroyed by microlesions, which resulted in a degradation of movements that had been developed in the earlier skill acquisition. Monkeys were then retrained at the same behavioral task. They could initially perform it reasonably well using the stereotyped movements that they had learned in prelesion training, although they acted as if key finger surfaces were insensate. However, monkeys soon initiated alternative strategies for small object retrieval that resulted in a performance drop. Over several- to many-week-long period, monkeys again used the fingers for object retrieval that had been used successfully before the lesion, and reacquired the sensorimotor skill. Detailed maps of the representations of the hands in SI somatosensory cortical fields 3b, 3a, and 1 were derived after postlesion functional recovery. Control maps were derived in the same hemispheres before lesions, and in opposite hemispheres. Among other findings, these studies revealed the following 1) there was a postlesion reemergence of the representation of the fingertips engaged in the behavior in novel locations in area 3b in two of five monkeys and a less substantial change in the representation of the hand in the intact parts of area 3b in three of five monkeys. 2) There was a striking emergence of a new representation of the cutaneous fingertips in area 3a in four of five monkeys, predominantly within zones that had formerly been excited only by proprioceptive inputs. This new cutaneous fingertip representation disproportionately represented behaviorally crucial fingertips. 3) There was an approximately two times enlargement of the representation of the fingers recorded in cortical area 1 in postlesion monkeys. The specific finger surfaces employed in small-object retrieval were differentially enlarged in representation. 4) Multiple-digit receptive fields were recorded at a majority of emergent, cutaneous area 3a sites in all monkeys and at a substantial number of area 1 sites in three of five postlesion monkeys. Such fields were uncommon in area 1 in control maps. 5) Single receptive fields and the component fields of multiple-digit fields in postlesion representations were within normal receptive field size ranges. 6) No significant changes were recorded in the SI hand representations in the opposite (untrained, intact) control hemisphere. These findings are consistent with "substitution" and "vicariation" (adaptive plasticity) models of recovery from brain damage and stroke.
This chapter reviews that brain imaging studies using positron emission tomography (PET), functional magnetic resonance imaging (fMRI), and magnetoencephalography (MEG) have greatly advanced the understanding of the way human brain processes pain. Despite a wide variability in experimental designs, imaging techniques, and types of pain, there is a relative good consistency across the results of different studies. It discusses that a set of brain areas, referred to as the pain-matrix is consistently activated in the large majority of the studies. Whereas early pain imaging studies mainly provided cartography of the areas activated by a painful stimulus, recent studies have used refined study designs that allow the respective roles of the different areas of the pain-matrix in the processing of pain to be disentangled. Brain imaging studies have provided compelling evidence that pain is not a bottom-up process, which is reliably driven by afferent sensory input. The relationship between neuronal activity and the signal measured in PET and fMRI studies is still not yet fully established. Therefore, brain imaging data should always be interpreted within the context of our knowledge about the neuroanatomy, neurochemistry, and neurophysiology of pain.
Thalamic connections of three subdivisions of somatosensory cortex in marmosets were determined by placing wheatgerm agglutinin conjugated with horseradish peroxidase and fluorescent dyes as tracers into electrophysiologically identified sites in S-I (area 3b), S-II, and the parietal ventral area, PV. The relation of the resulting patterns of transported label to the cytoarchitecture and cytochrome oxidase architecture of the thalamus lead to three major conclusions. 1) The region traditionally described as the ventroposterior nucleus (VP) is a composite of VP proper and parts of the ventroposterior inferior nucleus (VPi). Much of the VP region consists of groups of densely stained, closely packed neurons that project to S-I. VPi includes a ventral oval of pale, less densely packed neurons and finger-like protrusions that extend into VP proper and separate clusters of VP neurons related to different body parts. Neurons in both parts of VPi project to S-II rather than S-I. Connection patterns indicate that the proper and the embedded parts of VPi combine to form a body representation paralleling that in VP. 2) VPi also provides the major thalamic input into PV. 3) In architecture, location, and cortical connections, the region traditionally described as the anterior pulvinar (AP) of monkeys resembles the medial posterior nucleus, Pom, of other mammals and we propose that all or most of AP is homologous to Pom. AP caps VP dorsomedially, has neurons that are moderately dense in Nissl staining, and reacts moderately in CO preparations. AP neurons project to S-I, S-II, and PV in somatotopic patterns.
The afferent thalamic connections to cortical fields important for control of head movement in space were analysed by intracortical retrograde tracer injections. The proprioceptive/vestibular area 3aV, the neck‐trunk region of area 3a, receives two thirds of its thalamic projections from the oral and superior ventroposterior nucleus (VPO/VPS), which is considered as the proprioceptive relay of the ventroposterior complex (Kaas et al., J. Comp. Neurol. 226: 211–240, 1984). The parieto‐insular vestibular cortex (PIVC, area retroinsularis, Ri) receives its main thalamic input from posterior parts of the ventroposterior complex and from the medial pulvinar. Anatomical evidence is presented that the posterior region of the ventroposterior complex is a special compartment within this principal somatosensory relay complex. The parietotemporal association area T3, mainly involved in visual‐optokinetic signal processing, receives a substantial input from the medial, the lateral, and the inferior pulvinar.
Dual tracer experiments revealed that about 5% of the thalamic neurons projecting to 3aV were spatially intermingled with neurons projecting to areas PIVC or T3. This spatial intermingling was distributed over small but numerous, circumscribed thalamic regions, called “common patches,” which were found mainly in the intralaminar nuclei, the posterior group of thalamic nuclei, and the caudal parts of the ventroposterior complex. The “common patches” may indicate a functional coupling of area 3aV with the PIVC or area T3 on the thalamic level.
In control experiments thalamic projections to the granular insula Ig and the anterior part of area 7, two cerebral structures connected with the vestibular cortical areas, were studied. Some overlap in the thalamic relay structures projecting to these areas with these areas with those projecting to the vestibular cortices was found. A quantitative evaluation of thalamic regions projecting to different cortical structures was performed by constructing so‐called “thalamograms.” A scheme was developed that describes the afferent thalamic connections by which vestibular, visual‐optokinetic, and proprioceptive signals reach the vestibular cortical areas PIVC and 3aV. © 1992 Wiley‐Liss, Inc.
1. Adult owl monkeys were trained to detect differences in the frequency of a tactile flutter-vibration stimulus above a 20-Hz standard. All stimuli were delivered to a constant skin site restricted to a small part of a segment of one finger. The frequency-difference discrimination performance of all but one of these monkeys improved progressively with training. 2. The distributed responses of cortical neurons ("maps") of the hand surfaces were defined in detail in somatosensory cortical area 3b. Representations of trained hands were compared with those of the opposite, untrained hand, and to the area 3b representations of hands in a second set of monkeys that were stimulated tactually in the same manner while these monkeys were attending to auditory stimuli (passive stimulation controls). 3. The cortical representations of the trained hands were substantially more complex in topographic detail than the representations of unstimulated hands or of passively stimulated control hands. 4. In all well-trained monkeys the representations of the restricted skin location trained in the behavioral task were significantly (1.5 to greater than 3 times) greater in area than were the representations of equivalent skin locations on control digits. However, the overall extents of the representations of behaviorally stimulated fingers were not larger than those of control fingers in the same hemisphere, or in opposite hemisphere controls. 5. The receptive fields representing the trained skin were significantly larger than receptive fields representing control digits in all but one trained monkey. The largest receptive fields were centered in the zone of representation of the behaviorally engaged skin, but they were not limited to it. Large receptive fields were recorded in a 1- to 2-mm-wide zone in the area 3b maps of trained hands. 6. Receptive-field sizes were also statistically significantly larger on at least one adjacent, untrained digit when compared with the receptive fields recorded on the homologous digit of the opposite hand. 7. There was an increase in the percent overlaps of receptive fields in the cortical zone of representation of the trained skin. A significant number of receptive fields were centered on the behaviorally trained skin site. 8. The effects of increased topographic complexity, increased representation of the trained skin location, increased receptive-field size, and increased receptive-field overlap were not observed in the representations of the untrained hands in these same monkeys. Only modest increases in topographic complexity were recorded in the representations of passively stimulated hands, and no effects on receptive-field size or overlap were noted.(ABSTRACT TRUNCATED AT 400 WORDS)
Recent studies have led to a better understanding of the organization and connections of somatosensory and visual cortex in a number of mammalian species. Lesion studies have provided information on the significance of particular connections. The variable effectiveness of cortical lesions in deactivating target areas suggests that serial processing may be emphasized in higher primates.
In adult monkeys, peripheral nerve injuries induce dramatic examples of neural plasticity in somatosensory cortex. It has been suggested that a cortical distance limit exists and that the amount of plasticity that is possible after injury is constrained by this limit. We have investigated this possibility by depriving a relatively large expanse of cortex by transecting and ligating both the median and the ulnar nerves to the hand. Electrophysiological recording in cortical areas 3b and 1 in three adult squirrel monkeys no less than 2 months after nerve transection has revealed that cutaneous responsiveness is regained throughout the deprived cortex and that a roughly normal topographic order is reestablished for the reorganized cortex.
Excerpt
The purpose of this paper is to summarize our research progress in studies of the dynamic mechanisms of the cerebral cortex underlying its contributions to learning and nondeclarative memory in experiments conducted over the past five years. Five years ago, we and other workers (see below) had discovered that the details of cortical representations could be altered by peripheral lesions in adult primates. Furthermore, we argued that the cortical representational reorganization in somatosensory (SI) cortical fields following peripheral nerve injuries did not merely reflect the existence of aberrantly sprouted connections (see Merrill and Wall 1978), but must manifest normal dynamic cortical processes by which the selective, distributed responses of cortical neurons—cortical “maps”—are shaped by our experiences throughout life (Merzenich et al. 1983b, 1984a,b; Merzenich 1986). We set out to confirm and extend preliminary behavioral/physiological experiments in somatosensory cortical area 3b that supported this conclusion; to determine how such distributed representational...
Injections of WGA-HRP were made into somatosensory cortex to determine whether or not the cortex makes monosynaptic connections with neurons of the thalamic reticular nucleus. Two classes of synaptic profiles making asymmetric contacts onto small dendrites were labeled. The first class was small, and contained densely packed vesicles and few mitochondria. The second, larger class contained loosely packed vesicles, several mitochondria, and accounted for approximately one-third of labeled contacts.
Area 3a in the macaque monkey, located in the fundus of the central sulcus, separates motor and somatosensory cortical areas 4 and 3b. The known connections of areas 4 and 3b differ substantially, as does the information which they receive, process, and transfer to other parts of the central nervous system. In this analysis the thalamic projections to each of these three cortical fields were examined and compared by using retrogradely transported fluorescent dyes (Fast Blue, Diamidino Yellow, Rhodamine and Green latex microspheres) as neuron labels. Coincident labeling of projections to 2-3 cortical sites in each monkey allowed the direct comparison of the soma distributions within the thalamic space of the different neuron populations projecting to areas 3a, 3b, and 4, as well as to boundary zones between these cortical fields. The soma distribution of thalamic neurons projecting to a small circumscribed zone (diameter = 0.5-1.0 mm) strictly within cortical area 3a (in region of hand representation) filled out a "territory" traversing the dorsal half of the cytoarchitectonically defined thalamic nucleus, VPLc (abbreviations as in Olszewski [1952] The Thalamus of the Macaca mulatta. Basel: Karger). This elongate, rather cylindrical, territory extended caudally into the anterior pulvinar nucleus, but not forward into VPLo. The rostrocaudal extent of the thalamic territory defining the soma distribution of neurons projecting to small zones of cortical area 3b was similar, but typically extended into the ventral part of VPLc, filling out a medially concavo-convex laminar space. Two such territories projecting to adjacent zones of areas 3a and 3b, respectively, overlapped and shared thalamic space, but not thalamic neurons. Contrasting with the 3a and 3b thalamic territories, the soma distribution of thalamic neurons projecting to a circumscribed zone in the nearby motor cortex (area 4) did not penetrate into VPLc, but instead filled out a mediolaterally flattened territory extending from rostral VLo, VLm, VPLo to caudal and dorsal VLc, LP, and Pul.o. These territories skirted around VPLc. All three cortical areas 4, 3a, and 3b) also received input from distinctive clusters of cells in the intralaminar Cn.Md. It is inferred that, in combination, the thalamic territories enveloping those neuron somas projecting to, say, the sensorimotor hand representation in areas 3a, 3b, and 4 (and also areas 1 and 2), which would be coactive during the execution of a manual task, constituted a lamellar space extending from VLo rostrally to Pul.o caudally.(ABSTRACT TRUNCATED AT 400 WORDS)
The organization of the inferior pulvinar complex (PI) in squirrel monkeys was studied with histochemical localization of the calcium binding proteins calbindin‐D28k and parvalbumin, and of cytochrome oxidase. With each of these markers, the inferior pulvinar complex can be subdivided into four distinct regions. Calbindin‐D28k immunoreactivity is densely distributed in cells and neuropil within PI, except for a distinct centromedially located gap. This calbindin‐poor zone, termed the medial division of the inferior pulvinar (PI M ), corresponds precisely to a region that contains elevated cytochrome oxidase activity and parvalbumin immunostaining. The PI M extends slightly above and behind the classically defined limit of the inferior pulvinar, the corticotectal tract. Regions of inferior pulvinar with intense immunostaining for calbindin‐D28k were the posterior division of the inferior pulvinar (PI P , medial to PI M ) and the central division (PI C , lateral to PI M ). A newly recognized lateral region, PI L , adjoins the lateral geniculate nucleus and stains more lightly for calbindin and parvalbumin immunoreactivity and for cytochrome oxidase. Staining patterns for calbindin, parvalbumin, and cytochrome oxidase in the pulvinar of rhesus monkeys closely resemble those shown in squirrel monkey inferior pulvinar, suggesting that a common organization exists in all primates.
In order to examine cortical connection patterns of the histochemically defined compartments in the inferior pulvinar, injections of up to five neuroanatomical tracers (wheat germ agglutinin conjugated to horseradish peroxidase and fluorescent retrograde tracers) were placed in the same cerebral hemisphere. Single injection sites were in the middle temporal area (MT), and several separate injections were placed in a strip corresponding to the rostral subdivision of the dorsolateral area (DLr). Injections that involved only DLr and not MT labeled principally the PI C , and more sparsely PI P and PI L . DLr connections occupied a „shell”︁ region dorsal to PI M that extended from PI C into the lateral and medial divisions of the pulvinar, PL and PM. Injection sites that included MT or were largely restricted to MT produced dense label in PI M and moderate label in PI C and PI L .
The retinotopic organization within the inferior pulvinar was inferred from patterns of connections. Connections with cortex related most closely to central vision were found posteriorly in PI M and in adjacent portions of PI C as it wraps around the caudal pole of PI M . Cortex related to more peripheral locations in the lower visual field connected with more rostral PI M and PI C . Patterns of label within the portions of PL and PM that were immediately adjacent to PI M roughly paralleled those in PI M and PI C . Thus, a distinct chemoarchitectonic subdivision of the inferior pulvinar, PI M , is the major source of thalamic projections to MT in squirrel monkeys. Interestingly, the relative scarcity of calbindin immunostaining in PI M is characteristic of „primary”︁ thalamic relay nuclei, such as the ventroposterior and lateral geniculate nuclei. Thus, the PI M ‐MT pathway may share certain physiological charcteristics with primary sensory relays, such as those involving intracelluarl calcium buffering and, perhaps, rapid and secure impulse transmission. © 1993 Wiley‐Liss, Inc.
Our understanding of the functional organization of somatosensory cortex and thalamus in primates and other mammals has greatly increased over the last few years. It is now clear that higher primates have four strip-like representations of skin and muscle receptors corresponding to areas 3 a, 3b, 1 and 2 of anterior parietal cortex. Areas 3b and 1 receive cutaneous information from the ventroposterior nucleus, while a ventroposterior superior nucleus provides areas 3a and 2 with information from muscle receptors. Area 3b is the homolog of S-I in prosimians and non-primates and it provides most of the activating cutaneous inputs to areas 1 and 2. Most of the further processing that allows tactile recognition of objects involves somatosensory areas of the lateral sulcus, where both S-II and the parietal ventral area (PV) receive activating inputs from areas 3a, 3b, 1 and 2. S-II also projects to PV and to a parietal rostral area where further connections with the amygdala and hippocampus may occur to allow the formation of tactile memories. Areas of anterior parietal cortex also project to posterior parietal cortex, where regions of cortex are largely somatosensory, but the functional subdivisions remain uncertain. All of the somatosensory fields have access to motor areas of the frontal lobe, but the magnitude and targets of the projections differ.
The last decade has witnessed major changes in the experimental approach to the study of the thalamus and to the analysis of the anatomical and functional interrelations between thalamic nuclei and cortical areas. The present review focuses on the novel anatomical approaches to thalamo-cortical connections and thalamic functions in the historical framework of the classical studies on the thalamus. In the light of the most recent data it is here discussed that: a) the thalamus can subserve different functions according to functional changes in the cortical and subcortical afferent systems; b) the multifarious thalamic cellular entities play a crucial role in the different functional states.
The architecture of the pulvinar of rhesus monkeys was investigated by acetylcholinesterase (AChE) histochemistry, and by immunocytochemistry for calbindin-D28k and the SMI-32 antibody. The presence of four inferior subdivisions, comparable to those found in architectonic-connectional studies in squirrel monkeys (C.G. Cusick, J.L. Scripter, J.G. Darensbourg, and J.T. Weber, 1993, J. Comp. Neurol. 336:1-30), provided a basis for a proposed revised terminology for visual sectors of the macaque pulvinar. In the present study, the inferior pulvinar (PI) was identified as a neurochemically distinct region that included the traditional cytoarchitectonic nucleus PI and adjacent portions of the lateral and medial pulvinar nuclei, PL and PM. In calbindin-D28k stains, the lateral subdivision of the inferior pulvinar (PIL) had less intense neuropil staining than the adjacent central division, PIC. The PIL was characterized by large, intensely immunopositive neurons seldom found within PIC. PIL occupied the traditional PL and PI and exhibited a narrow shell zone, PIL-S, restricted to PL. The medial division of the inferior pulvinar (PIM) was in a location previously shown to be strongly connected with the middle temporal visual area (MT) in macaques. PIM was found in the medial one-half of the traditional PI and extended into adjacent portions of the traditional PM and PL. PIM was distinguished by less intense neuropil staining for calbindin and many cells stained with the SMI-32 antibody for neurofilament protein. In AChE stains, PIL was moderately dark, PIC appeared lighter, and PIM was characterized by small, intensely stained patches. The small posterior division (PIP) stained darkly for calbindin, lightly for AChE, and was unstained with the SMI-32 antibody. Thus, neurochemical, and perhaps connectional, subdivisions exist within PI, the region of the pulvinar that relays information to striate, "lower order" extrastriate, and inferotemporal visual cortex.
The aim of this study was to assess the distribution of neurons immunoreactive for parvalbumin (PV), calbindin (CaBP), glutamic acid decarboxylase (GAD), and gamma-aminobutyric acid (GABA) in the somatosensory thalamus of the raccoon and to compare these features to those of other species, especially primates. Immunohistochemistry was used to study the location of these neurons in the ventroposterior nucleus (VP), ventroposterior inferior nucleus (VPI), posterior group of nuclei (Po), and reticular nucleus (Rt). A consistent differential pattern of PV-positive (PV+) and CaBP-positive (CaBP+) cells was found in the somatosensory thalamus. Many PV+ neurons were observed in VP and Rt, but very few were found in VPI or Po. In contrast, CaBP+ neurons were distributed throughout VP, VPI, and Po but were very sparse or absent in Rt. In the VP nucleus, PV+ cells were distributed in clusters separated by interclusteral regions with a sparse distribution of PV+ cell bodies. The distributions of PV+ and CaBP+ cells tended to be complementary to each other in VP; regions with a high density of PV+ neurons had a low density of CaBP+ cell bodies. Double-labeling experiments revealed very few neurons in which PV and CaBP immunoreactivities were colocalized. Cells immunoreactive for GAD or GABA were found in PV-dense clusters of VP; fewer GABAergic neurons were present in the CaBP-dense interclusteral regions of VP and in VPI and Po. GAD+ and GABA+ neurons were most prominently distributed in Rt. We conclude that the distributions of PV+ and CaBP+ cell bodies in the raccoon somatosensory thalamus are very similar to those in primates. The density of GABAergic neurons in the somatosensory thalamus of the raccoon is less than that in the cat and monkey, but the relative distribution of GABAergic neurons in the different somatosensory nuclei is very similar to that in the cat and monkey. These results are discussed in relation to findings in other species and are related to the functions of lemniscal and nonlemniscal somatosensory pathways.
We obtained well-differentiated staining of thalamic subdivisions in rhesus macaques and squirrel monkeys using a lectin, Wisteria floribunda agglutinin (WFA), that labels extracellular matrix proteoglycans. Regional variations in staining were observed within the motor and somatosensory thalamic regions that bear on current interpretations of the organization of these regions. The pattern of WFA staining was generally similar to that obtained with Cat-301 antibody, which also stains proteoglycans. However, WFA reliably produced selective staining in both squirrel monkeys and macaques, whereas Cat-301 stained macaques more consistently than squirrel monkeys.
To investigate the organization of the dorsal pulvinar complex, patterns of neurochemical staining were correlated with cortico-pulvinar connections in macaques (Macaca mulatta). Three major neurochemical subdivisions of the dorsal pulvinar were identified by acetylcholinesterase (AChE) histochemistry, as well as immunostaining for calbindin-D(28K) and parvalbumin. The dorsal lateral pulvinar nucleus (PLd) was defined on histochemical criteria as a distinct AChE- and parvalbumin-dense, calbindin-poor wedge that was found to continue caudally along the dorsolateral edge of the pulvinar to within 1 mm of its caudal pole. The ventromedial border of neurochemical PLd with the rest of the dorsal pulvinar, termed the medial pulvinar (PM), was sharply defined. Overall, PM was lighter than PLd for AChE and parvalbumin and displayed lateral (PMl) and medial (PMm) histochemical divisions. PMm contained a central "oval" (PMm-c) that stained darker for AChE and parvalbumin than the surrounding region. The neurochemically defined PLd was labeled by tracer injections in the inferior parietal lobule (IPL) and dorsolateral prefrontal cortex but not the superior temporal gyrus (STG). Label within PMl was found after prefrontal and IPL and, to a lesser extent, after STG injections. The PMm was labeled after injections of the IPL and STG, but only sparsely following prefrontal injections. The histochemically distinct subregion or module of PMm, PMm-c, was labeled only by STG injections. Overlapping labeling was found in dorsal pulvinar divisions PMl and PLd following paired IPL/prefrontal, but not IPL/STG or these particular STG/prefrontal, injections. Thus, PLd may be a visuospatially related region whereas PM appears to contain several types of territories, some related to visual or auditory inputs, and others that receive directly converging input from posterior parietal and prefrontal cortex and may participate in a distributed cortical network concerned with visuospatial functions.
The representation of fingers in the first somatosensory cortex was studied in conscious monkeys by recording single neuronal activity, and the following results were obtained:(1)
In area 3a, most neurons responded to joint manipulation or other types of deep stimuli. The representation of five fingers was somatotopically arranged.
(2)
In area 3b, 77.7% and 20.9% of identified neurons responded to cutaneous and deep stimuli respectively.
(3)
Neurons responding to light mechanical stimuli and with receptive fields on the distal finger segment were found in the most anterior part of area 3b while those responding better to specific mechanical stimuli, such as rubbing, scraping, pinching, tapping, etc. of finger glabrous skin, were found in the more posterior part. The representation of the five fingers was somatotopically arranged.
(4)
Neurons responding to light or specific mechanical stimulation of the dorsal hairy skin of fingers were found in the posterior part of area 3b. The independent somatotopic representation of four fingers was recognized within this region.
(5)
Neurons responding to mechanical stimulation of the palmar skin were found in two separate regions, the medial one for the ulnar half and the lateral one for the radial half of the palm.
(6)
These results indicate that the representation of fingers in areas 3a and 3b of the conscious monkey is divided into multiple somatotopic subdivisions each representing a functional region of the hand and fingers.
(7)
Neurons with multi-finger receptive fields were occasionally found in area 3b, mostly in layer VI. Some of them had inhibitory receptive fields. Multifinger type receptive fields were more commonly found in area 1.
Retrogradely labeled neurons are observed in the posterior group of the thalamus (Po) after injection of wheatgerm agglutinin-horseradish peroxidase in the rat somatosensory cortex. These neurons are organized in rods elongated rostrocaudally, defining a clear somatotopic map. Injections of tritiated leucine in the somatosensory cortex indicate that these somatotopically organized connections are reciprocal. Injections of tritiated leucine in the dorsal column nuclei label afferent fibers in a small area dorsal to Po but not in the core of the nucleus. Po does not receive direct projections of ascending somatosensory afferents. It is hypothesized that this thalamic area participates in a thalamo-cortico-thalamic loop.
Multiunit microelectrode recordings were used to explore the responsiveness and somatotopic organization of the representation of the hand in area 3b of anesthetized macaque monkeys. Major findings were as follows: Recording sites throughout the hand representation were activated by low-threshold cutaneous stimulation. Simple, punctate mechanical stimuli were highly effective in activating neurons. Neurons had small, restricted receptive fields. Representations of nearly all skin surfaces of the hand were demonstrated in individual monkeys. The basic topographic pattern found in all monkeys included the following: a large sequential representation of the glabrous digits from thumb to little finger from lateral to medial in cortex, and from proximal to distal hand parts in cortex extending down the caudal bank of the central sulcus; moderately large representations of radial and ulnar pads of the palm in respective lateral and medial cortical locations in the hand representation; and a relatively small, fragmented representation of the dorsal hand and dorsal digits, with the fragments interspersed within the representation of the glabrous hand. The proportions of the proximal, middle, and distal glabrous digits varied, so that the representation of the distal phalanx sometimes approached the dorsal border of area 3b with area 1. A comparison of the present findings with previous results from macaque monkeys indicates that the above-described features have been revealed under a variety of recording and anesthetic conditions. Consistencies in previous and present results strongly support the conclusions that the hand representation in area 3b of macaque monkeys is activated by cutaneous receptors throughout; is composed of neurons with relatively simple, small, cutaneous receptive fields; includes all skin surfaces of the hand; and is somatotopic for the glabrous skin with small, discontinuous, intercalated representations of fragments of the dorsal skin.
The words “sensory-motor cortex” in this chapter’s title may appear unusual in these days of increasingly finer analysis when it would be more customary to devote individual chapters to each component of this large cortical region. The idea that somatosensory and motor cortex should form some kind of functional unit is now by no means a popular one. The reason for this is hard to determine, as it is difficult to conceive that any motor act is entirely without accompanying sensory phenomena [even allowing for the fact that a certain proportion of motor cortex neurons may not be subjected to immediate sensory feedback (Evarts and Fromm, 1977; see Evarts, this volume)]. Similarly, the involvement of parietal cortex in the analysis of spatial relations and the body image (Mountcastle, 1975) and of premotor cortex in planning movement strategies (Roland et al., 1980), including those into extrapersonal space, implies some kind of relationship between these two and associations between them and somatosensory and primary motor cortex. In view of all this, it does not seem inappropriate to ask: what are the pathways to and from sensory, motor, and premotor cortex; at what levels do they come together; what are the routes of intercommunication between the three cortical regions, and the routes of outflow from them; how does their intrinsic organization reflect the neural processing occurring within them? On account of the functional baseline alluded to above having its origins in human behavior, this chapter will be devoted entirely to the examination of connectivity in the monkey brain. Considerations of many of the comparable features of organization in the brains of cats and rats will be found in the chapters by Zarzecki, Wise and Donoghue, Dykes and Ruest, and Burton.
Walker in 1938 was able to end his book The Primate Thalamus with a lengthy chapter entitled “The Anatomical, Physiological and Clinical Significance of the Thalamus.” In this he concluded that the thalamus was composed of three fundamentally different groups of nuclei: midline and intralaminar nuclei projecting to other diencephalic structures; three relay nuclei (ventral posterior and the geniculate bodies); and a phylogenetically recent group including mediodorsal, lateral posterior, and pulvinar nuclei not receiving fibers from the principal afferent pathways. It was his viewpoint that these latter nuclei and the thalamus in general was an integrative center for all incoming stimuli, elaborating them before presentation “to the highest hierarchy of the central nervous system, the cerebral cortex, as complex and at least partially synthesized impulses.” His belief in the thalamus as a sensory integrative center seems to have derived from the clinical observation that lesions at upper levels of the neuraxis rarely lead to a disturbance of single sensory modalities. He recognized nevertheless that spatial relationships would be preserved through the thalamus because of the topographic ordering of inputs and of thalamocortical projections.
The connections of the cortical dysgranular “unresponsive zone” (UZ) (Sur et al.: J. Comp. Neurol. 179:425–450, '78) in the grey squirrel were studied with horseradish peroxidase and autoradiographic techniques. The results of these experiments show that the major subcortical connections of the unresponsive zone are in large part reciprocal. Connections are distributed within the thalamus in a poorly defined region including restricted portions of several nuclei that lie along the rostral, dorsal, and caudal borders of the ventral posterior nucleus. Additional thalamic connections of the UZ terminate in the reticular nucleus and are reciprocally related to the paralaminar and central median nuclei. Extrathalamic terminations were observed in the zona incerta, the intermediate and deep layers of the superior colliculus, the red nucleus, and several subdivisions of the pontine nuclei. The similarity between the pattern of subcortical connections of the UZ in the grey squirrel and patterns reported for the parietal septal region in rats (Chapin and Lin: J. Comp. Neurol. 229:199–213, '84) and for area 3a in primates (Friedman and Jones: J. Neurophysiol. 45:59–85, '81), suggests that the UZ in the grey squirrel may represent a counterpart of at least part of area 3a as described in primates. The results are further discussed with respect to a possible role of the thalamus in control or modulation of interhemispheric circuits and of the UZ in the modulation of nociceptive and kinesthetic pathways through the thalamus. Finally, the term parietal dysgranular cortex (PDC) is proposed as an alternative to denote the region currently called the unresponsive zone.
In the North American raccoon (Procyon lotor), representations of the glabrous surfaces of the hand digits are found within separate subnuclei of the thalamic ventrobasal complex (VB) and on separate subgyri of the somatosensory cortex (SmI). In the present study, the retrograde transport of horseradish peroxidase from SmI to VB was utilized to study relationships between physiologically identified cortical subgyri and somatotopically corresponding thalamic subnuclei.
Single large or multiple small injections confined to a single gyral crown led to retrograde labeling of large groupings of cells filling the entire VB subnucleus for the appropriate digit. In the aggregate, the regions of label appeared as thin, wedge-shaped sheets extended in the dorsoventral and anteroposterior dimensions, but flattened mediolaterally, and curving to form a laterally directed convexity; these appear to correspond to the lamellae of monkey VB described by others. These large injections led to labeling of approximately 80% of all large (18–30-μm diameter) cells within the lamella. Single, small, focal injections of a gyral crown led to variable amounts of labeling, ranging from an entire digital lamella to only a small focal cluster of cells. No evidence was obtained for the existence of anteroposteriorly extending “rods” of cells, as reported in primates. Finally, there was a sparse, but consistent labeling of cells of the posterior nuclear group (Po) following gyral crown injections.
These results are in agreement with expectations based on prior electrophysiological studies of raccoon VB and SmI, as well as prior anatomical studies of thalamocortical relationships.
Single and double retrograde tracer experiments were performed in cats in order to investigate the organization of thalamic neurons projecting to the primary (SI) and secondary (SII) somatosensory cortical areas. In one series of animals, horseradish peroxidase (HRP) was injected in either SI or SII, and the distribution of retrogradely labeled neurons was reconstructed in serial coronal and horizontal sections through the thalamus. In a second series of experiments, cats received injections of HRP in SI and tritiated, enzymatically inactive HRP ( ³ H‐apo‐HRP) in SII of the same hemisphere. The results from these experiments provide more exact information than can be obtained in single tracer experiments with regard to (1) the distribution and number of neurons projecting to both SI and SII by way of axon collaterals and (2) the topographical relationship among populations of thalamic neurons projecting to SI, SII, or both targets.
SI Single tracer experiments demonstrate, in agreement with previous findings, that, after injection of SI which are focused on the representations of the limbs, heavy retrograde labeling is present throughout VPL. Within this complex, densely and lightly labeled neurons are found consistently and show some preferential pattern of organization. Thus, while both types of neurons are uniformly distributed in VPLl, densely labeled neurons tend to be arranged in clusters, particularly in the ventral portion of VPLm. Outside VPL, moderate but unequivocal retrograde labeling is present in POm, even in cases in which the spread of injected tracer did not encroach upon area 5; labeling of intralaminar nuclei and of a transitional zone between VP and VL, known to receive ascending spinal afferents, is also a consistent feature of all cats with SI injections, although it cannot be excluded that this results from the spread of injected HRP into area 4.
SII From cases with injection of HRP in the anterior ectosylvian gyrus, it appears that as the injection site is shifted from posterior to anterior, labeling of neurons in the thalamus shifts from the lateral portion of the posterior group (POl) and the caudal region of the medial portion of this same group (POm) to involve progressively more rostral portions of this nucleus and also VP. Within VP, SII‐projecting neurons are confined primarily within the lateral portion (VPLl) and posterior cap, while in VPLm they are confined mainly to the periphery of this nuclear subdivision and are sparse within its core region. Labeled neurons are also present in the transitional VP‐VL zone.
Double tracer Simultaneous visualization of thalamic neurons projecting to SI, SII, or both targets shows that within VP these three neuronal populations are not distributed homogeneously. Rather, their differential distribution defines, on the basis of pattern of their cortical projections, three divisions of the thalamic somatosensory relay: (1) a central core region of VPLm, which contains predominantly neurons projecting to SI; (2) a shell of neurons within VPL, in which neurons projecting to SI are homogeneously distributed among neurons projecting to SII and neurons projecting to both SI and SII; and (3) a previously defined outer shell— outside VPL—which is characterized, as a whole, by widely divergent cortical connections. It is suggested that these three regions, distinguished from one another by their patterns of cortical projection, may correspond to similar differential sites of afferent projections, such that each zone‐core, inner and outer shells—would be dominated by a different ascending pathway.
Experiments using anterograde and retrograde tracing techniques have been used to identify projections to and from the region of mouse SmI cortex which contains the posteromedial barrel subfield (PMBSF, Woolsey and Van der Loos, '70). Microinjections containing horseradish peroxidase (HRP) and tritiated amino acids were placed unilaterally into the topographic center of the PMBSF. Brains were perfuse‐fixed and frozen sectioned. All sections were reacted for HRP and alternate sections were autoradiographed. Examination of sections cut tangential to the pial surface in the region of the injection site showed that diffusion of the injection was limited to cortex above and below the PMBSF in layer IV (i.e., PMBSF cortex). A “column” of HRP reaction product and developed silver grains was present in ipsilateral cortical area 40, in the face area of SmII. HRP positive cell bodies were mainly in layer III and VI of this “column.” A similar “column” was present in ipsilateral cortical area 6, in a region which in the rat corresponds to the vibrissal area of MsI (Hall and Lindholm, '74), but here HRF positive cells bodies were situated mainly in layer V. HRP labeled cells bodies were also present in layer V of ipsilateral cortical area 29c. The ipsilateral nucleus ventralis thalami pars lateralis and the nucleus posterior thalami contained many HRP positive cell bodies and were associated with dense aggregations of developed silver grains. Numerous silver grains were also present over portions of the ipsilateral caudate, reticular nucleus of the thalamus and ventral pontine nuclei, but no HRP positive cell bodies occurred in these regions.
HRP‐filled axons left the injection site and traveled via the corpus callosum to contralateral PMBSF cortex where HRF labeled cell bodies were present mainly in layers III and V. Usually only one or two labeled somata were located superficial or deep to a contralateral PMBSF barrel. A few HRF positive cell bodies were also present in layers II and III of contralateral pyriform cortex.
These results indicate that PMBSF cortex is reciprocally connected with ipsilateral cortical areas 6 and 40 and with the ipsilateral ventral and posterior nuclei of the thalamus. A small, homotopic callosal connection with contralateral PMBSF cortex has been demonstrated, and it is presumed that this projection is also reciprocal. PMBSF cortex projects to, but receives no projections from the ipsilateral caudate, reticular nucleus of the thalamus and the ventral pontine nuclei. Thus, many of the same projections of primary somatosensory cortex in higher animals, such as the monkey have been shown to occur in the mouse.
The results of the present anatomical study on macaque monkeys concern some aspects of the dorsal column nuclei, their projection to the thalamus and the cytoarchitecture and topography of the recipient areas in the thalamus for the somatosensory pathways. Some observations regarding the cytoarchitecture of the dorsal column nuclei are reported; the gracile nucleus differs cytoarchitectonically over the rostrocaudal dimension in a way similar to the feline nucleus; the cuneate nucleus has a distinct pars rotunda (Ferraro and Barrera, '35) which might be analogous to a similar structure in the raccoon shown to be activated by afferents from the volar side of the hand and digits (Johnson et al., '68). Cytoarchitectonic observations and other arguments suggesting the presence of the nucleus Z in the monkey are presented.
In Nissl stained frontal sections, cut in the stereotaxic frontal plane as well as in sections cut perpendicular to the long axis of the brain stem the cytoarchitecture and topography of the posteromedial, ventroposterior and centrolateral thalamic nuclei of the macaque were analysed. The posteromedial nucleus (POm) has been found to include portions of Olszewski's ('52) magnocellular medial geniculate, suprageniculate and pulvinar nuclei. The nucleus ventralis posterolateralis (VPL) corresponds to the main portion of Olszewski's VPLc, whereas most of his VPLo corresponds to the nucleus ventralis intermedius of Hassler ('59) and Mehler ('71).
Electrolytic lesions were used to study the projection from the gracile and cuneate nuclei to the thalamus. With postoperative survival periods of 6 to 14 days the resulting degeneration was studied in frontal sections stained according to the Wiitanen modification of the Fink‐Heimer method. Both the gracile and cuneate nuclei project profusely to the contralateral nucleus ventralis posterolateralis and more sparsely to the contralateral posteromedial nucleus and the zona incerta. A distinct somatotopic organization exists in the projection to the ventroposterior nucleus, but not in that to the other target areas. The projection to the ventroposterior nucleus is very dense and evenly distributed except rostrally and dorsally, where it is more scattered.
It is concluded that the posteromedial and the ventroposterior thalamic nuclei are very similar in monkeys and cats regarding cytoarchitecture, topography and afferent projections from the dorsal column nuclei.
In order to test the hypothesis that thalamic efferents of trigeminal nucleus caudalis (NC) are the cranial analogue of the spinothalamic system, lesion and autoradiographic studies were carried out in the squirrel monkey, and the terminal projection fields in thalamus were noted. Results showed that NC, including lateral reticular formation (LRF), projects to contralateral VPM, the VPM‐VPL border and medial VPL, and a region dorsal to ventroposterior nucleus (VP) proper which contains cells larger than those in VPM yet which stain as darkly as VPL neurons; this latter zone of termination may be homologous with VPL o (Vim) in other species, which is that area receiving lemniscal and cerebellar afferents (Mehler, '71; Walsh and Ebner, '73; Boivie, '74). In addition, a small projection is noted in an area intercalated between dorsomedial MG, limitans nucleus and posterior VP which closely agrees with the medial division of Posterior nucleus (Po) described in rhesus and squirrel monkey (Burton and Jones, '76). No terminations were observed in the gustatory nucleus medial to VPM.
Bilateral, terminal projection fields were observed in posterior mediodorsal nucleus (MD), and a paralaminar area (PL) which lies in the ventrolateral strip of MD and is particularly prominent in primates; other bilateral fields were noted in CL, particularly the more medial segment of the nucleus. A sparse projection was noted in contralateral CM. Ipsilateral, intratrigeminal connections between NC and main sensory nucleus (MSV) also were observed.
We conclude that, in the squirrel monkey, NC efferents, probably including LRF, may be considered analagous to the spinothalamic system by virtue of terminations in older medial and newer ventroposterior thalamus. Terminations in posterior MD may be specific to Primates . Moreover, projections to an area just dorsal to VP proper in squirrel monkey may be included within the broader definition of a neo‐spinothalamic area as reflected in spinothalamic tract projections to the ventrolateral complex in cat (Boivie, '71b; Jones and Burton, '74). The small NC projection to a part of Po is consistent with spinothalamic terminations to a “posterior” thalamic area in other primates (Mehler, '69), and with the suggestion that medial Po transmits pain information (Burton and Jones, '76).
Detailed microelectrode maps of the hand representation were derived in cortical areas 3b and 1 from a series of normal adult owl and squirrel monkeys. While overlap relationships were maintained, and all maps were internally topographic, many map features varied significantly when examined in detail. Variable features of the hand representations among different monkeys included (a) the overall shapes and sizes of hand surface representations; (b) the actual and proportional areas of representations of different skin surfaces and the cortical magnifications of representations of specific skin surfaces, which commonly varied severalfold in area 3b and manyfold in area 1; (c) the topographic relationships among skin surface representations, with skin surfaces that were represented adjacently in some monkeys represented in locations many hundreds of microns apart in others; (d) the internal orderliness of representations; (e) the completeness of representations of the dorsal hand surfaces; and (f) the skin surfaces represented along the borders of the hand representation.
Owl monkey maps were, in general, internally more strictly topographic than squirrel monkey maps. In both species, area 3b was more strictly topographic and less variable than was area 1.
The degree of individual variability revealed in these experiments is difficult to reconcile with the hypothesis that details of cortical maps are ontogenetically specified during a period in early life. Instead, we propose that differences in the details of cortical map structure are the consequence of individual differences in lifelong use of the hands. This conclusion is consistent with earlier studies of the consequences of peripheral nerve transection and digital amputation, which revealed that cortical maps are dynamically maintained and are alterable as a function of use or nerve injury in these monkeys (Merzenich et al., '83a, b, '84a; Merzenich, '86; Jenkins et al., '84; Jenkins and Merzenich, '87).
We have used single unit recording techniques to map the representation of cutaneous and joint somatosensory modalities in the primary somatosensory (SI) cortex of both anesthetized and awake rats. The cytoarchitectonic zones within the rat SI were divided into the following main categories: (1) granular zones (GZs)–areas exhibiting koniocortical cytoarchitecture (i.e., containing dense aggregates of layer IV granule cells), (2) perigranular zones (PGZs)–narrow strips of less granular cortex surrounding the GZs, and (3) dysgranular zones (DZs)–large areas of dysgranular cortex enclosed within the SI. The narrow strip between the SI and the rostrally adjacent frontal agranular cortex was termed the “transitional zone” (TZ).
Initial computer‐based studies of the properties of cutaneous receptive fields (RFs) in SI showed that, although there were differences in reponse threshold, adaptability, frequency response, and overall RF size and shape of adjacent neurons, the size and location of the “centers” of the RFs were quite constant and were similar to those seen in multiple unit recordings. The same was true of RFs of single neurons recorded through different anesthetic states.
The body representation in SI was first mapped by determining single unit and unit cluster RFs within a total of 2,170 microelectrode penetrations in barbiturate‐anesthetized rats. Cutaneous RFs in the GZs were quite discrete. Thus, a single, finely detailed, continuous map of the cutaneous periphery was definable within the GZs themselves. Only the forepaw had a double representation. RFs in the PGZs were larger and more diffuse, but since they covered roughly the same skin areas as the RFs in the most closely adjacent GZs, they fit into the same body map. Neurons in the DZs were unresponsive to any sensory stimuli in the anesthetized animal.
In chronically implanted, freely moving, awake animals cutaneous RFs were larger and more volatile than in the anesthetized, but the accuracy of the map was clearly preserved by the fact that the locations of the RF centers (which often must be defined quantitatively) were unchanged. The PGZs and DZs in the awake animals exhibited a multimodal convergence of cutaneous and joint movement RFs within single vertical penetrations, or even on single neurons. Directionally specific and bilateral cutaneous RFs were also observed in the DZs. It was concluded the DZs are more associational or integrative areas within the SI, but they could not be shown to comprise a distinct and separate body representation. The rat SI cortex therefore appears to contain, within a single overall body map, both granular and dysgranular cytoarchitectonic zones. Not only are different sensory modalities subserved within this map, but also different levels of physiological complexity and anesthesia sensitivity.
Corticothalamic connections of posterior parietal regions were studied in the rhesus monkey by using the autoradiographic technique. Our observations indicate that the rostral superior parietal lobule (SPL) is connected with the ventroposterolateral (VPL) thalamic nucleus. In addition, whereas the rostral SPL is connected with the ventrolateral (VL) and lateral posterior (LP) thalamic nuclei, the rostral IPL has connections with the ventroposteroinferior (VPI), ventroposteromedial parvicellular (VPMpc), and suprageniculate (SG) nuclei as well as the VL nucleus. The caudal SPL and the midportion of IPL show projections mainly to the lateral posterior (LP) and oral pulvinar (PO) nuclei, respectively. These areas also have minor projections to the medial pulvinar (PM) nucleus. Finally, the medial SPL and the caudal IPL project heavily to the PM nucleus, dorsally and ventrally, respectively. In addition, the medial SPL has some connections with the LP nucleus, whereas the caudal IPL has projections to the lateral dorsal (LD) nucleus. Furthermore, the caudal and medial SPL and the caudal IPL regions have additional projections to the reticular and intralaminar nuclei–the caudal SPL predominantly to the reticular, and the caudal IPL mainly to the intralaminar nuclei.
These results indicate that the rostral‐to‐caudal flow of cortical connectivity within the superior and inferior parietal lobules is paralleled by a rostral‐to‐caudal progression of thalamic connectivity. That is, rostral parietal association cortices project primarily to modality‐specific thalamic nuclei, whereas more caudal regions project most strongly to associative thalamic nuclei.
The efferent projections of the neocortex on the lateral convexity of the inferior parietal lobe (area 7 of Brodmann) were examined using the anterograde transport of tritiated amino acids. Multiple injections of 3H-leucine and 3H-proline were placed within the three cytoarchitecturally distinct zones that lie along the exposed surface of the inferior parietal lobe (IPL). The subcortical projections resulting from these injections were studied. Prominent projections were seen in the thalamus (medial and lateral pulvinar), brainstem (dorsolateral and ventral pontine nuclei), and basal ganglia (caudate and putamen) with less dense label over the thalamic intralaminar nuclei, pretectal complex, superior colliculus, reticular nucleus of the thalamus, suprageniculate nucleus, lateral posterior nucleus, oral pulvinar, and claustrum. In many of these cases there was a topographical relationship apparent with regard to the injections placed along the rostral-caudal dimension of the IPL. There is a striking reciprocal arrangement in the afferent and efferent projection systems of the IPL. The functional relevance of both the topography and the efferent projections of the IPL is discussed.
The thalamocortical and corticothalamic connections of the second somatic sensory area (SII) and adjacent cortical areas in the cat were studied with anterograde and retrograde tracers. Injections consisted of horseradish peroxidase conjugated to wheat germ agglutinin (HRP‐WGA) or a mixture of equal parts of tritiated leucine and proline. The cortical regions to be injected were electrophysiologically studied with microelectrodes to determine the localization of the selected components of the body representation in SII. The distribution of recording points was correlated in each case with the extent of the injection mass in the cortex. Distributions of retrograde and anterograde labeling in the thalamus were reconstructed from serial coronal sections. The results from cases with injections of tracers exclusively confined to separate parts of the body map in SII indicated a fairly precise topographical organization of projections from the ventrobasal complex (VB) to SII. The labeled cells and fibers were located within a series of lamella‐like rods that curved throughout the dorsoventral and rostrocaudal axis of VB. The position and extent of these lamellae shifted from medial and ventral, in the medial subdivision of ventral posterior lateral nucleus (VPLm) for radial forelimb digit zones of SII, to dorsal, Posterior, and lateral, in the lateral subdivision of ventral posterior lateral nucleus (VPLl) for proximal leg and trunk regions in SII. For every injected area in SII the densest clustering of labeled cells and fibers was usually more posteriorly represented in VB. The distribution in these dense zones of labeling often extended through the central core of VB. SII projecting neurons were also consistently noted in the extreme rostral portion of the medial subdivision of the posterior nuclei (Pom) that lies dorsal to VB. Corticothalamic and thalamocortical connections for SII Were entirely reciprocal.
Injections of tracers into cortical areas surrounding SII labeled other parts of the posterior complex but failed to label any part of VB except when the injection mass also diffused into SII. Injections into the somatic sensory cortex located lateral to SII, within the lips and depth of the upper bank of the anterior ectosylvian sulcus (AES), heavily labeled the central and posterior portions of Pom. Substantial labeling was noted in the lateral (Pol) and intermediate (Poi) divisions of Po only when the injections involved some part of the auditory area that occupies the most posterior part of the AEG and both banks of the immediately adjoining AES. The magnocellular nucleus of the medial geniculate (MGmc) was labeled only when some part of the auditory cortex was injected. The suprageniculate nucleus (SG) was labeled from the insula and lower bank of the AES. These results indicated that medial (rostral and caudal Pom) and lateral components (Poi, Pol, MGmc) of the Posterior complex have separate cortical projection zones to somatic sensory and auditory cortical regions, respectively.
SIV and the lateral extent of area 5a located in the medial bank of the anterior suprasylvian sulcus sent projections to the deep layers of the supe‐ rior colliculus and the ventrolateral periaqueductal gray. No cortico‐tectal projections were seen from SII.
Tetramethyl benzidine (TMB) is a presumptively non-carcinogenic chromogen which yields a blue reaction-product at sites of horseradish peroxidase activity. Sixty-six distinct procedures were performed in rats and monkeys in order to determine the optimal incubation parameters for TMB. As a result, a procedure is recommended whose sensitivity greatly surpasses that of a previously described benzidine dihydrochloride method. Indeed, the sensitivity of this new method in demonstrating retrograde transport is markedly superior to that of the previously described benzidine dihydrochloride method. Furthermore, as a consequence of this enhanced sensitivity, many efferent connections of the injection site are also visualized. The injection site demonstrated by this TMB procedure is significantly larger than the one demonstrated when benzidine dihydrochloride or diaminobenzidine is used as a chromogen. Finally, this TMB procedure has been compared to two other TMB procedures and found to provide superior morphology and sensitivity.
Descending connections from parietal cortex to pulvinar in squirrel monkey were investigated with the autoradiographic method. Somatosensory areas I (SI) and II (SII) were found to project to the oral (PuO) and medial (PuM) subdivisions of the pulvinar. Projections from the posterior parietal region were recorded in circumscribed areas of PuM and the lateral (PuL) and inferior (PuI) subdivisions of pulvinar. Retrograde labeling with horseradish peroxidase (HRP) demonstrated that rostral parietal cortex including the lateral cortex of SI and the rostral part of area 5 received reciprocal projections from PuO and rostral PuM. Injections of HRP into medial and lateral regions of SI also resulted in labeled cells in PuO and PuM. Within the limitations of the HRP technique, the latter results suggest a direct pathway from pulvinar to primary sensory cortex. The experimental results confirm the accepted view of projections from parieto-temporo-occipital "association" cortex to PuM, PuL and PuI. In addition, reciprocal connections of rostral parietal cortex with PuO and PuM were demonstrated.
1. An exploration of the occurrence of different functional cell types was made in the three cytoarchitectural subdivisions (areas 3, 1 and 2) of the hand area of the post-central gyrus of the monkey. The functional properties of 632 cells were studied using the transdural micro-electrode recording method. 2. Over half of the neurones studied (57%) belonged to the class of simple skin neurones that were related either to rapidly adapting (272 neurones) or slowly adapting (seventeen neurones) cutaneous receptors or to both (seventy-one neurones). The simple skin neurones were particularly common in the anterior part of S I where they constituted 60% of the cells. More complicated cutaneous neurones made up 10% of the total sample. They were more common in the posterior part of the gyrus. 3. Altogether ninety-two neurones (15%) were related to subcutaneous or deeper receptors. Another seventy-one neurones (11%) exhibited convergence of skin input and input from deep receptors. A smaller group of forty-seven undamaged neurones (7%) were unrelated to stimuli of the types described above. 4. In tangential electrode penetrations made along the anterior and posterior banks of the gyrus, functional columns were found to be 500 micrometers wide on the average; this width is comparable with that of ocular dominance columns and visual orientation hypercolumns. 5. Correlation of the functional types of cells with cytoarchitecture showed that the complexity of the functional properties of the neurones increased posteriorly. The receptive field size also increased toward posterior. The changes that take place in the functional properties of cells when moving across different cytoarchitectural areas suggests intracortical information processing which leads to handling of larger body regions and more complex combinations of information in the cellular elements of the posterior part of the post-central gyrus.
Previous electrophysiological mapping of somatic sensory (SI) and motor (MI) cortex in the rat has shown that these functional regions are completely overlapping in the hindlimb (HL) area. Partially separate in the forelimb area, and completel separate in the face area. The present studies were designed to show how the sensory and motor thalamic relay nuclei priject onto separate or overlapping subdivisions of SI and MI cortex. The experimental sequence involved physiological mapping of one subdivision of SI or MI cortex and then injecting horseradish peroxidase (HRP) as a retrograde cell marker to back‐fill the thalamic neurons that project to the identified area of cortex. The central issue was to compare the projection of the lemniscal‐recipient ventrobasal nucleus (VB) and the cerebellar‐recipient ventrolateral nucleus (VL) to the hindlimb and face subdivision of SI and MI cortex. Various authors, however have divided the ventral nucleus differently using Nisslstained transverse sections through the thalamus. Therefore, tritiated amino acids were also injected into the deep cerebellar nuclei and the distribution of cerebellar fiber terminals in the ventral nucleus was used as another criterion to identify the border between VB and VL.
Following HRP injections in physiologically identified HL cortex, labelled neurons were present in both VB an VL. Face area SI injections back‐filled cells in VB (but not VL), while face area MI injections back‐filled cells in VL (but not VB). Neurons in the intralminar nuclei and the posterior nuclear complex were labelled after all injections.
These results demonstrate that SI and MI cortex in the rat shows a combiation of overlapping and separated plans of organization. Other species, in which both the anatomical an physiological information is available, show other organizational plans. In the Virginia opssum, for example, overlap is present in all subregions of SI and MI cortex. While the Rhesus monkey shows separation of these areas. The result suggest that different mammals have evolved different degrees of separation of SI and MI cortex. Our results predict that in every case where there is evidence of sensory and motor overlap, there will be anatomical convergence of VB and VL projections to htat single cortical area.
The thalamic connectivity of areas 3b, 1 and 2 of the first somatic sensory cortex (SI) and of the adjacent areas 4, 3a and 5 has been studied in monkeys with anterograde and retrograde labeling techniques.
Anteroposterior sectors of the SI cortex are represented in the thalamic ventrobasal complex by curved lamellae of thalamocortical relay cells extending through the dorso‐ventral and anteroposterior dimensions of the ventrobasal complex. Within such a lamella there are clustered aggregations of cells each projecting to a punctate zone of SI. Such cortical zones are less than 1 mm in circumference and are interpreted as comparable to the “columns” of electrophysiological studies. Each clustered aggregation in the ventrobasal complex is of limited mediolateral and dorsoventral extent but extends through much of the anteroposterior dimension of the ventrobasal complex. Punctate zones lying adjacent to one another in the mediolateral dimension of the SI cortex are connected with aggregations of cells lying in adjacent lamellae of the ventrobasal complex. Punctate zones lying anterior or posterior to one another in the anteroposterior dimension of SI are connected with aggregations of cells lying ventral or dorsal to one another in a lamella of the ventrobasal complex.
Sectors of SI extending from posterior to anterior across areas 2 and 1 and others extending from posterior to anterior across area 3b, are each represented systematically across the full dorsal to ventral dimension of the ventrobasal complex. This implies at least two separate representations of the body surface: one in areas 2 and 1, and another in area 3b.
Within a lamella of the ventrobasal complex, aggregations of cells projecting to areas 2 and 1 are mingled with those projecting to area 3b. Measurements of the sizes of retrogradely labeled cells in brains in which areas 2 and 1 or area 3b were separately injected showed no distinction between cells projecting to the three areas on the basis of size. Experiments combining retrograde cell degeneration due to ablation of area 3b with retrograde labeling after injection of areas 1 and 2 indicated little possibility of collateral projections to the three areas from the same cell.
No part of SI, as defined by the most liberal anatomical criteria, is connected with any thalamic nucleus outside the confines of the ventrobasal complex (the caudal division of the ventroposterolateral nucleus and the large‐celled part of the ventroposteromedial nucleus) or of the intralaminar complex. Area 3a, as traditionally defined, has connectional relationships that strongly suggest it is a part of the motor cortex, area 4. However, short latency Group I evoked potentials could be elicited from a small part of area 3a lacking layer V giant cells and lying adjacent to area 3b. This part receives its thalamic input from the ventrobasal complex. The data indicate that area 4 is connected with the oral division of the ventroposterolateral nucleus and with the caudal nucleus of the ventral lateral complex. These cellular groupings, however, are only artificially separated and appear to form part of the same thalamic relay nucleus.
Experiments on area 5 not only suggest that the posterior boundary of SI should be placed further posterior than is customary, but also suggest that area 5 can be divided into an anterior field related to the anterior nucleus of the pulvinar and a posterior field related to the lateral posterior nucleus.
Anatomical tracers were injected into electrophysiologically defined sites in somatosensory cortical Area 3b (SI proper) and Area I (posterior cutaneous field) of owl monkeys after these cortical subdivisions had been extensively explored in microelectrode mapping experiments. These mapping experiments revealed that both Areas 3b and 1 contain complete and separate representations of the body surface (Merzenich et al., '78). Restricted injections of the retrograde tracer, horseradish peroxidase (HRP), into either Area 3b or Area 1 labeled neurons within a band of cells in the ventroposterior nucleus (VP). The location of the labeled band in VP varied with the location of the injection site in both representations, and the labeled region of VP was overlapping for injections in corresponding body parts in the two representations. Neurons projecting to the hand and foot cortical representations were in architectonically identified subnuclei. Because injections into either Area 3b or Area 1 labeled over half of the neurons in the appropriate regions of VP, it appears that some neurons in VP project to both cortical representations. Finally, injections of HRP combined with the anterograde tracer, 3H-proline, indicate that VP neurons are reciprocally interconnected with both Areas 3b and 1.
Microelectrode mapping experiments indicate that the classical primary somatosensory cortex of monkeys consists of as many as four separate body representations rather than just one. Two complete body surface representations occupy cortical fields 3b and 1. In addition, area 2 contains an orderly representation of predominantly "deep" body tissues. Area 3a may constitute a fourth representation.
The projections of the spinothalamic tract in the macaque monkey have been reinvestigated using the Wiitanen modification of the Fink‐Heimer technique. In agreement with previous studies in the monkey (Mehler, Bowsher, Kerr) it was found that the spinothalamic tract ascends outside the medial lemniscus, enters the thalamus just dorsal to this structure, and terminates in the posterior, intralaminar and ventral regions, as well as in the zona incerta.
The posteromedial nucleus (POm) receives a dense spinothalamic projection medially and ventromedially; elsewhere in the POm the projection is more scattered. The fibers to the intralaminar region terminate in the nucleus centralis laterials (CL) with a distinct pattern of the distribution. The nucleus centralis medialis (CeM) has a minute projection. There was no evidence for somatotopic organization in the projections to the POm or to the intralaminar region.
The distribution of the terminal degeneration in the ventral nuclear region was more complex. Although present in the whole nucleus ventralis posterolateralis (VPL), the degeneration was unevenly distributed and also extended beyond the VPL. So‐called clusters of dense degeneration lay in the outskirts of the forelimb and hindlimb representation areas, namely at its ventral, ventrolateral, dorsolateral, and medial borders. Centrally the degeneration was scattered. Thus, most of the VPL receives only a sparse spinothalamic projection, but a small portion contains dense networks of terminal spinal fibers. A somatotopic pattern was evident, for after low thoracic lesions most of the medial VPL lacked degeneration.
Spinothalamic fibers pass beyond the VPL to terminate in a zone of transition (nucleus ventralis intermedius or V.im of Hassler, '59; Mehler, '71) between the rostral pole of the VPL and the nucleus ventralis lateralis (VL). This zone also reportedly receives cerebellar and vestibular afferent fibers.
Observations suggesting that the evolution of the spinothalamic tract and the spino‐cervico‐thalamic pathway in carnivores and primates may be linked are discussed. The spinothalamic clusters in the monkey's VPL appear to be homologous to much of the cervicothalamic tract projection to the VPL in the cat.
In an attempt to understand the modifications which appears at the thalamic level when dorsal cord sections are performed, peripheral fields of thalamic units were studied in normal and dorsal-cord sectional monkeys, totally awake and implanted with glass micropipettes. Six normal Macaca cynomolgus and 7 having received spinal sections, were studied. Ventricular radiography was performed and all the coordinates were related to new stereotaxic coordinates using the posterior commissure as the origin. Cell-bodies and axon units were recognized on the basis of the shape of the spikes. In normal animals, 972 units were studied; 307 were thalamic units with peripheral fields and 177 were derived from cell bodies. Localization of these cells was studied as a function of their peripheral field and response characteristics. The majority of ventralis posterior (VP) cell bodies were only activated by contralateral stimulation, their peripheral field being frequently found on the extremities. Somatotopic organization consisted of concentric layers rather than zones in apposition. Dorsoventral segregation of afferent modality sensitivity (movement, pressure, light touch) was observed. Somatosensory convergence was found in VP inferior (VPi) as well as convergence of different types of afferents on a few VP cells. Units responding to bilateral or ipsilateral stimulations were found only in posterior VP and in surrounding nuclei. A particular somatotopy was shown to exist in n. reticularis. A total of 838 units were studied in animals having had dorsal columns and Morin's bundle served. Only a few cells (13) responded in VPl to contralateral hindlimb stimulation. Their characteristics recall those noted in layer V spinal cord cells. The other cells (55) still driven by a hindlimb were dispersed in the nuclei just adjacent to VPl. The majority of cells found in the VPl were activated from the forelimb. They were observed in their normal VPl localization as well as in areas where hindlimb representation was found in normal animals. This change of afferent input is attributed to a reinnervation of hindlimb cells (probably at the gracilis level) by sprouting from forelimb afferent.
Endogenous cytochrome oxidase activity within the mitochondria of neurons and neuropil was demonstrated histochemically under normal and experimental conditions. Since enzymatic changes were noted with chronic neuronal inactivity in the auditory system (Wong-Riley et al), the present study sought to examine functionally induced enzymatic changes in the visual system of kittens. Eight kittens were used experimentally: 5 had monocular lid suture for varying periods of time; one had binocular lid suture followed by monocular suture followed by binocular opening; two had monocular enucleation. All initial procedures were performed before eye opening. Materials from other normal kittens and cats were also used as controls. At the end of the experiments, the animals were perfused with aldehyde solutions and frozen sections of the brains were incubated for cytochrome oxidase activity (a detailed protocol was outlined). The results indicated that the deprivation caused by monocular suture produced a decrease in the cytochrome oxidase staining of the binocular segment of the deprived geniculate laminae. Enucleation yielded a greater decrease in the cytochrome oxidase activity in the affected geniculate laminae. However, the staining in the 'normal' lamina extended across the interlaminar border to include a row of surviving large cells in the 'denervated' lamina. The staining of the monocular segment appeared not to be affected by lid suture, but was decreased by enucleation. At the cortical level, lamina IV in area 17 of normal cats was stained darkly as a continuous band. Following lid suture, this pattern was replaced in part by alternating columns of light and dark staining, suggestive of ocular dominance columns. Thus, a decrease in neuronal activity due to reduced visual stimulation or destruction of the primary afferent nerves led to a significant decrease in the level of oxidative enzyme activity one to several synapses away.
Pulvinar-latero posterior afferents to the parietal cortical area 7 of the monkey have been demonstrated by means of horseradish peroxidase (HRP) tracing technique. Following HRP injection of area 7, labelled neurons have been found in the pulvinar medialis and the nucleus lateralis posterior. The role of these pulvinar projection fibers is discussed with reference to the "visual neurons" of area 7 recently recorded from.
The retrograde, horseradish peroxidase technique has been used to demonstrate the cells of origin of corticofugal fiber systems arising in the rat somatic sensory cortex and projecting to the striatum, diencephalon, brainstem, and spinal cord. Correlative experiments conducted with the anterograde, autoradiographic method have been used to confirm the terminal distribution of many of these fiber systems. Corticofugal pathways directed to subcortical structures arise in the first and second somatic sensory areas exclusively from pyramidal cells of the infragranular layers, V and VI. Fibers which descend to the midbrain, pons, medulla and spinal cord arise exclusively from the largest pyramidal cells, the somata of which are found in the deep part of layer V (layer VB). There is some evidence for a sublaminar organization of the different classes of efferent cells within this layer. Fibers projecting to the diencephalon arise from somata situated throughout layer VI and to a lesser extent in layer V. Corticostriatal fibers arise only from cells with somata in layer V, but the somata are more superficially situated than those of the other classes of corticofugal neurons. The laminar distribution of the somata of corticofugal neurons differs considerably from that of commissural and ipsilateral corticocortical neurons.
Recordings were obtained from 1,439 single neurons in the ventrobasal nuclear complex (VB) and in adjacent regions of the thalamus of macaque monkeys, in the absence of general anesthesia. Each neuron was classified as either cutaneous or deep on the basis of its responsiveness to light tactile stimulation, limb movement, or pressure on deep tissues. The location and extent of each neuron's receptive field was determined, using stimuli of uniform intensity. On the basis of qualitative criteria, each neuron was assigned to either the lemniscal or nonlemniscal category. The locations of all neurons in the sample were reconstructed histologically, thus permitting us to relate a neuron's position in VB to the location of its receptive field. The data show that VB neurons are segregated according to submodality class along the anteroposterior dimension of VB. At levels near the anterior and posterior ends of VB, neurons with deep receptive fields predominate, whereas neurons with cutaneous receptive fields predominate at intermediate levels. The body representation in VB can be viewed as a series of nearly identical horizontal two-dimensional maps stacked on top of one another. In any of these maps, over a rather wide vertical range, all body regions and submodalities are respresented. There are striking similarities between the characteristic organizational plan evident in reconstructions of horizontal cross sections of VB and the organizational plan of its projection field in the postcentral gyrus.
The inferior parietal lobule (IPL) of the monkey is the homologous region to the supramarginal and angular gyri in man, subserving language and related cortical functions. We have examined specific zones of the IPL by injecting eight monkeys with retrogradely transported HRP, and located the positive cells in the thalamic sections with the assistance of an X‐Y plotter and reference to the atlas of Olszewski ('52). Projections to the IPL were found in the following thalamic nuclei: Anterior (Anterior Medial, Anterior Ventral); Lateral (Ventral Anterior, Ventral Anterior magnocellularis, Ventral Lateral caudalis, Pulvinar oralis, medialis, lateralis and inferior, Lateral Posterior and Lateral Dorsal); Medial (Medialis Dorsalis densocellularis, parvocellularis, and multiformis); Midline and Intralaminar (Centralis densocellularis, Centralis lateralis, Centralis inferior, Centralis superior lateralis, Subfascicularis parvocellularis, Paracentralis and Parafascicularis); and Posterior (Limitans, Suprageniculatus and Geniculatus Medialis magnocellularis).
A major projection to the superior portion of the IPL was from the anterior nuclei and Paracentralis of the intralaminar group. Ventralis Lateralis and oral Pulvinar projected primarily to the anterior‐inferior portion of the IPL, whereas Lateral Posterior projected most strongly to the anterior and superior portion. The major projection of the lateral Pulvinar was to the mid‐superior portion of the IPL and to area 19. The projections of the inferior Fulvinar were heaviest to area 19, but there was some overlap in the mid‐superior portion of the IPL with the medial and lateral Pulvinar. The major projection from the posterior thalamic nuclear complex was to the mid‐IPL.
The heterogeneous input from the thalamus to the IPL was not anticipated on the basis of prior anterograde or retrograde degeneration studies, and suggests that classical subdivisions of specific and associational thalamic nuclei should be revised with the axonal transport methods of study.
The organization of thalamic input to functionally characterized zones in primary somatosensory cerebral cortex (S-I) of macaque monkeys (Macaca mulatta) was investigated using the method of labelling by retrograde transport of horseradish peroxidase (HRP). It was found that the cell columns positioned at the posterior margin of the band of cortex representing a given body region receive thalamic input from a posterior level of the ventroposterior thalamic nucleus (VP), and that cell columns at successively more anterior positions within that band receive input from successively more anterior levels of VP. The extreme posterior and anterior margins of the S-I hand, foot and face areas receive input from neuron populations which are not as widely separated in the anteroposterior dimension of VP as the neurons projecting to the extreme anterior and posterior margins of the proximal limb and trunk representations in S-I. These characteristics of the organization of the projections from VP to S-I are consistent with the view that the body representations in VP and S-I have the same connectivity and differential submodality distribution; and with the idea that thalamocortical conncetions only exist between functionally equivalent neuron populations in VP and S-I.
ABSTRACT: Lesions were made in parietal cortex, temporal operculum, and spinal cord of macaque monkeys. Connections were traced to the posterior thalamus using the Fink-Heimer I or Wiitanen methods. The postcentral gyrus projected strongly to n. ventralis posterior medialis and lateralis, with small projections to n. pulvinaris oralis, n. lateralis posterior, and n. ventralis posterior inferior. At the mesodiencephalic border degeneration was observed in n. geniculatus medialis (pars magnocellularis) and n. suprageniculatus. Parietal operculum projected mainly to n. ventralis posterior lateralis, medialis, and inferior, and to n. pulvinaris oralis and medialis, with lesser connections to n. medialis dorsalis, n. lateralis posterior, n. suprageniculatus, and n. geniculatus medialis (pars magnocellularis and parvocellularis). The superior parietal lobule projected mainly to n. lateralis posterior and n. pulvinaris oralis, with lesser connections to n. ventralis lateralis, n. suprageniculatus, and n. limitans. The rostral part of the inferior parietal lobule provided a small projection to n. lateralis posterior and dorsalis, whereas the caudal part projected heavily to these nuclei and less heavily to n. pulvinaris oralis and medialis, and n. suprageniculatus. The superior temporal gyrus projection to the posterior thalamus was to n. geniculatus medialis (pars magnocellularis and parvocellularis), n. suprageniculatus, and n. pulvinaris oralis and medialis. Spinothalamic fibers terminated in n. posterior lateralis, n. suprageniculatus, n. geniculatus medialis (pars magnocellularis), n. medialis dorsalis, and n. centralis lateralis. A few terminal ramifications were apparent in caudoventral n. pulvinaris oralis. The areas of overlap of ascending and descending connections in the posterior thalamus, exclusive of the primary sensory relay nuclei, were n. geniculatus medialis (pars magnocellularis), n. suprageniculatus, n. limitans, and the caudoventrai part of n. pulvinaris oralis. It is possible that these areas as well as the region of their poorly defined boundaries with n. ventralis posterior lateralis and medialis constitute a nuclear group comparable to the posterior nuclear group of the cat thalamus.
Experimental Neurology.
The posterior wall of the central sulcus in forelimb area of SI has been expolred with extracellular micro-electrodes in baboons lightyl anaesthetized with nitrous oxide and sodium thiopentone. 2. The excitatory responses of 130 single units to low intensity electrical stimulation of the deep radial (muscle) and the superficial radial (cutaneous) nerves have been investigated. 3. Units that responded only to muscle nerve stimulation were located in area 3a but overlapped into area 3b. Units that responded only to cutaneous nerve stimulation were found mainly in area 3b but a number occurred in area 3a. Units that responded to both muscle and nerve stimuli (convergent units) were found throughout area 3a and the rostral part of area 3b. 4. Latency analyses of all three response groups revealed a single population of units responding to low threshold muscle nerve stimulation (mean latency 8.5 msec), and both early and late populations responding to low threshold cutaneous nerve stimulation (mean latencies 9.5 and 13.6 msec respectively). A number of the convergent units had very similar latencies for both inputs. 5. Electrical stimulation within area 3a deminstrated a projection from areas 1 and 3b to area 3a; such a pathway may provide a route for excitation of the late skin population which was found mainly in area 3a. 6. In area 3a units commonly responded to light touch, local pressure or deep pressure but only rarely to movement of hairs. A number of the convergent units responded to natural stimulation of cutaneous receptors.
The posterior nuclear complex of the thalamus in rhesus, pigtailed and squirrel monkeys consists of the combined suprageniculate‐limitans nucleus and an ill defined region of heterogeneous cell types extending anteriorly from the dorsal lobe of the medial geniculate body towards the posterior pole of the ventral nuclear complex. This region is referred to as the posterior nucleus.
The cortical projections of each of these nuclei, together with those of the adjacent ventral, pulvinar and medial geniculate complexes, have been studied by means of the autoradiographic tracing technique. The suprageniculate‐limitans nucleus, the main input to which is the superior colliculus, projects upon the granular insular area of the cortex. The medial portion of the posterior nucleus projects to the retroinsular field lying posterior to the second somatic sensory area. There is clinical and electrophysiological evidence to suggest that the retroinsular area may form part of a central pain pathway. The lateral portion of the posterior nucleus which is closely related to certain elements of the medial geniculate complex, projects to the postaditory cortical field. The ventroposterioinferior nucleus, which may be involved in vestibular function, projects to the dysgranular insular field.
The principal medial geniculate nucleus can be subdivided into a ventral division that projects to field AI of the auditory cortex and a dorsal division that merges with the posterior nucleus; it is further subdivided into an anterodorsal component that projects to two fields on the superior temporal gyrus, together with a posterodorsal component in which separate cell populations project to areas lying anterior and medial to AI. The magnocellular medial geniculate nucleus, sometimes considered a part of the posterior complex, appears to project diffusely to layer I of all the auditory fields.
The Auditory fields are bounded on three sides by the projection field of the medial nucleus of the pulvinar which also extends into the upper end of the lateral sulcus to bound the fields receiving fibers from the posterior nucleus. The topography of the areas receiving fibers from the posterior, medial geniculate and pulvinar complexes, taken in conjunction with the rotation of the primate temporal lobe, permits all of these fields to be compared with similar, better known areas in the cat brain.
The anatomical tracer, wheat germ agglutinin, was used to determine the connections of electrophysiologically identified locations in three architectonically distinct representations of the body surface in the somatosensory cortex of gray squirrels. Injections in the first somatosensory area, S‐I, revealed reciprocal connections with the ventroposterior nucleus (VP), a portion of the thalamus just dorsomedial to VP, the posterior medial nucleus, Pom, and sometimes the ventroposterior inferior nucleus (VPI). As expected, injections in the representation of the face in S‐I resulted in label in ventroposterior medial (VPM), the medial subnucleus of VP, whereas injections in the representation of the body labeled ventroposterior lateral (VPL), the lateral subnucleus of VP. Furthermore, there was evidence from connections that the caudal face and head are represented dorsolaterally in VPM, and the forelimb is represented centrally and medially in VPL. The results also support the conclusion that a representation paralleling that in VP exists in Pom, so that the ventrolateral part of Pom represents the face and the dorsomedial part of Pom is devoted to the body. Because connections with VPI were not consistently revealed, the possibility exists that only some parts or functional modules of S‐I are interconnected with VPI.
Two separate small representations of the body surface adjoin the caudoventral border of S‐I. Both resemble the second somatosensory area, S‐II, enough to be identified as S‐II in the absence of evidence for the other. We term the more dorsal of the two fields S‐II because it was previously defined as S‐II in squirrels (Nelson et al., '79), and because it more closely resembles the S‐II identified in most other mammals. We refer to the other field as the parietal ventral area, PV (Krubitzer et al., '86). Injections in S‐II revealed reciprocal connections with VP, Pom, and a thalamic region lateral and caudal to Pom and dorsal to VP, the posterior lateral nucleus, Pol. Whereas major interconnections between S‐II and VPI have been reported for cats, raccoons, and monkeys, no such interconnections were found for S‐II in squirrels. The parietal ventral area, PV, was found to have prominent reciprocal interconnections with VP, VPI, and the internal (magnocellular) division of the medial geniculate complex (MGi). The pattern of connections conforms to the established somatotopic organization of VP and suggests a crude parallel somatotopic organization in VPI. Less prominent interconnections were with Pol. Sparse, fine label in part of the ventral (principal) nucleus of the medial geniculate complex (MGv) suggests the existence of some input from PV.
The connections demonstrated in the present study help characterize three somatosensory areas in squirrels. Such information is essential for identifying homologous areas of cortex across species, and several possibilities are outlined in the Discussion. In addition to VP, the results suggest the presence of two somatic nuclei, the medial and lateral nucleus of the Po group; and evidence is provided for the existence of VPI in rodents. Furthermore, consistent with many recent reports, we found that each cortical area has interconnections with more than one thalamic nuclei, and each thalamic nucleus has interconnections with more than one cortical field. Finally, in keeping with the responsiveness of neurons in PV to both somatic and auditory stimuli (Krubitzer et al., '86), PV was found to have interconnections with both somatic and auditory thalamic nuclei.
We provide evidence that the thalamic projections originating from the medial portion of the posterior thalamic complex to the somatosensory cortex of the rat are distributed in a detailed pattern which is complementary to the pattern of projections which originate in the ventral posterior nucleus.
Axonal tracing techniques were used to examine the distribution of corticothalamic projection neurons in relation to the organization of the thalamocortical recipient zones in the whisker representation of the rat first somatic sensory cortex. Following injection of horseradish peroxidase into the physiologically defined vibrissa area in the ventrobasal complex of the thalamus, labeling in the cortex had a columnar appearance. Dense patches of anterograde labeling were located within the centers of the layer IV barrels and extended superficially through lamina III; the septa between barrels contained considerably less reaction product. Retrogradely labeled neurons were observed in lower layer V and layer VI where they were concentrated preferentially deep to the barrel centers. Regions deep to the septa displayed less overall labeling and a lower relative number of thalamic projecting neurons. Zones having the larger numbers of retrogradely labeled cells also contained terminallike labeling of either corticothalamic or thalamocortical origin. Following an injection that included the posterior group medial to the ventrobasal complex, anterograde labeling in layer IV was located largely in the septa. In conjunction with previous findings concerning the origin and termination of other projection systems in the barrel cortex, these results suggest that a vibrissal column contains a central core zone intimately linked with the ventrobasal thalamus that is bounded by narrower regions of more diverse inputs and outputs that form an interface between adjacent cortical columns.
In order to elucidate the geometric organization of projections from the barrel cortex to the thalamus, iontophoretic injections of the anterograde tracer Phaseolus vulgaris-leucoagglutinin were made. The injections were confined to one barrel column (i.e. barrel in layer IV + cortical tissue above and below it). Axonal terminations could be demonstrated in three thalamic nuclei: reticularis (RT), ventrobasalis (VB) and posterior (PO). Anterograde terminal labelling was obtained in RT + VB; in PO only; or in RT + VB + PO. The terminals labelled in PO were much larger than those in RT and VB. The termination areas in RT, VB and PO were shaped like rods which have a rostro-caudal orientation. These cortico-thalamic projections are discretely and topographically organized. The clearest such arrangement was found in VB. Here, projections from the A row of barrels in BF terminate dorsally, whereas those from the C row end ventrally. Barrel A1 projects to the lateral part of VB, whereas A4, to more medial parts; other rows are arranged similarly. These results were compared with the distribution of thalamo-cortical projection neurons that were labelled after iontophoretic HRP injections in individual barrels. We concluded that the corticothalamic projections originating from one barrel column contact an are of barreloids in VB.
The fluorescent dye retrograde tracing technique was used to examine the projection from ventroposterior lateral thalamus to primary somatosensory cortex in the raccoon. Results are presented from fifteen experiments using Fast Blue in combination with either Nuclear Yellow or Diamidino Yellow Dihydrochloride. Injections of two dyes into adjacent but separate digit regions of cortex produced single-labeling of thalamic neurons, suggesting that projections for each digit are separate and independent with no branching to adjacent parts of the somatotopic map. Double-labeling was only seen when the cortical injection sites were overlapping. Similar results were seen in six cases in which amputation of the 5th digit of the contralateral forepaw was carried out four months earlier. These results suggest that neither the strengthening of existing collaterals nor growth of new collaterals in the thalamocortical projection are likely to be responsible for the physiological reorganization that is seen in raccoon cortex after peripheral deafferentation.
The adequate stimulus and body site that excited neurons in cat cortical somatosensory areas 3a and 3b were recorded using low-impedance tungsten microelectrodes. Horizontal penetrations provided a good correlation between the electrophysiological and cytoarchitectonic data. Responses best driven by cutaneous stimuli were replaced with responses driven by manipulation of deep tissue at, or very near, the border between areas 3a and 3b. Following functional identification of these areas horseradish peroxidase was injected into one of them. Injections into area 3a labeled neurons in a rostral and dorsal cap of the ventroposterior thalamus. It was suggested that this region is a distinct nucleus termed the ventroposterior oralis nucleus (VPO). Injections into the forelimb portion of area 3b labeled neurons in the ventroposterior lateral nucleus (VPL). With both vertical and horizontal microelectrode trajectories through the ventroposterior thalamic nuclei, inputs from deep structures presumed to be muscles were consistently located in the VPO nucleus and cutaneous inputs activated neurons in the VPL. The existence of several functionally-distinct subdivisions within the somatosensory nuclei of the thalamus supports the hypothesis of parallel processing and relay of somatosensory information at this level of the pathway.
The somatotopic organization of low threshold inputs from the face and head was determined in the lateral portion of areas 3b and 1 in squirrel monkeys. A complete, topographically organized representation was found in area 3b, and a separate, roughly parallel representation was found in adjacent area 1. In addition, there was evidence for remarkable individual variability in the representation of the lips in area 3b.
The intracortical arborizations of thalamocortical fibers arising from the ventroposterolateral (VPL) nucleus in the cat were studied following intra-axonal injections of horseradish peroxidase (HRP). The axons were impaled 1.5 to 3 mm below the surface of the cortex, identified electrophysiologically by stimulating the VPL nucleus and functionally by stimulating the somatic receptive field with natural stimuli. Many of the results obtained in a previous study using similar techniques (Landry and Deschênes 1981) were confirmed by the present experiments. Fibers activated by cutaneous stimulation arborized either in area 3b or 1 but some did send branches to both areas. Also, the intracortical arborization of a rapidly adapting cutaneous afferent fiber in area 2 is described. The size and tangential extent of the fiber in area 2 are similar to those arborizing in other areas of the primary somatosensory cortex and consist of multiple patches separated by uninvaded gaps. One fiber activated by stimulation of deep tissue receptors gave rise to two bushes that arborized along a rostrocaudal axis exclusively in area 3b. Terminal boutons and varicosities were found mostly in layers VI, IV, the bottom third of III and the upper portion of V, but some fibers did send a few collateral branches to layer II and the bottom part of layer I. The results suggest that in the forebrain representation, the same modality and submodality can be recorded in more that one cytoarchitectonic area but that areas 3b, 1 and 2 should not be considered as a single functionally homogeneous area. Counts of terminals suggest that a single fiber arborizing in area 1 makes as many as 3 times the number of synapses made in area 2 or 3b. Since fibers appear to be modality and submodality specific, if convergence of modality, submodality and/or body areas occur in the cortex, then this must be preferentially, but not exclusively, done by thalamic fibers of different functions which arborize in the same cytoarchitectonic area and synapse upon a shared postsynaptic target. In the same experiments intra-axonal recordings revealed the presence of two hyperpolarizing after potentials elicited by a preceding action potential. The first after potential was associated with a decrease in excitability of the fiber and an increase in membrane resistance.(ABSTRACT TRUNCATED AT 400 WORDS)
Experiments were performed on adult albino rats, using single-labeling (free horseradish peroxidase [HRP] or wheatgerm agglutinin conjugated to HRP [WGA:HRP]) and double-labeling (fluorescent dyes) techniques to investigate the thalamic projections to the secondary somatosensory cortex (SII) and to demonstrate the presence and location of thalamic neurons projecting to both the primary somatosensory cortex (SI) and SII by way of branching axons. In single-labeling experiments, the tracer was injected in SI or SII with or without electrophysiological control; in double-labeling experiments, fast blue and diamidino yellow were injected into the electrophysiologically identified forelimb areas of SI and SII. Single-tracer experiments showed that after injections in SI, focused in the forelimb representation area, retrogradely labeled neurons were present mainly in the ventral third of the nucleus ventralis posterolateralis (VPL) and in the anterior part of the posterior nuclear complex (PO); labeled neurons were also present consistently in the caudal portion of PO. Injection of tracers in the forelimb or forelimb and hindlimb representation areas of SII resulted in labeling of neurons in the posterior part of PO and in the caudal part of VPL. Double-labeling experiments confirmed the distribution of neurons projecting to SI or to SII, as observed in single-labeling experiments. Some neurons labeled with both tracers were also present. These neurons are interpreted as projecting to both SI and SII by means of axon collaterals and were observed in areas of overlap of the two single-labeled population of neurons--that is, at the border between PO and the ventroposterior complex, and in the medial part of caudal PO. Comparison of these data with those obtained after injections of tracers in SI and SII of cats (Spreafico et al., 1981b) suggests that in both species thalamic neurons projecting to these two areas are largely segregated, though partially overlapping; and that thalamic neurons projecting simultaneously to SI and SII, modest in number in cats, are even sparser in rats.
Multiunit microelectrode recording techniques were used to study the location and organization of the third somatosensory area (SIII) in cats. Representations of all major contralateral body parts were found in a small region of cortex along the lateral wing of the ansate sulcus and between the lateral sulcus and the suprasylvian sulcus. The systematic map of the body surface included forepaw and face regions previously identified as parts of SIII. The forepaw representation was generally buried on the rostral bank of the lateral wing of the ansate sulcus. The representations of the face and mystacial vibrissae were largely exposed on the rostral suprasylvian gyrus, but part of the representation of the face was also buried in the lateral wing of the ansate sulcus. Representations of the trunk and hindlimb extended from the suprasylvian gyrus onto the medial bank of the suprasylvian sulcus. We had expected to find these latter body parts in more medial cortex just caudal to the representation of these parts in the first somatosensory area (SI). Instead, neurons in penetrations in cortex caudal to the SI trunk and hindlimb representations were unresponsive to tactile stimulation. The unexpected location of the hindlimb in SIII led us to determine whether the proposed parts of SIII had similar cortical and thalamic connections. Injected anatomical tracers revealed that the representations of both the forelimb and hindlimb were interconnected with SI and a region of the thalamus just dorsal to the ventroposterior nucleus. Similarities in patterns of connections of forelimb and hindlimb portions of SIII supported the conclusion that SIII as presented here is a functional unit of cortex. We conclude that SIII has a somatotopic organization that does not parallel that in SI, and that SIII is not entirely coextensive with either area 5 or area 5a of Hassler and Muhs-Clement (1964).
Thalamic and corticocortical connections of the second somatic sensory area (SII) in the mouse cerebral cortex were investigated by means of the retrograde transport of horseradish peroxidase. Focal injections of the enzyme were made in physiologically determined locations within the parietal cortex. Results show that SII receives substantial inputs from topographically appropriate regions within the ipsilateral ventrobasal nucleus and from the ipsilateral posterior group. The limb representation, which was previously found to be responsive to auditory stimulation, received inputs also from the medial division of the medial geniculate body. The SII face representation, which is largely unresponsive to auditory stimuli, received little or no input from the medial geniculate body. SII injections yielded retrograde labeling in the topographically appropriate region in the first somatic sensory area (SI), and SI injections retrogradely labeled cells in SII in a pattern consistent with previous electrophysiological maps. Homotypical regions within SI and SII therefore appear to be reciprocally interconnected. SII also receives inputs from the ipsilateral motor cortex and from contralateral SI and SII. Finally, injections into the SI paw but not face regions yielded retrograde labeling in the thalamic ventrolateral nucleus. Thus, the distal limb representations in SI and SII each receive inputs from a third major relay nucleus (i.e., medial geniculate to SII, ventrolateral nucleus to SI) whereas the face representations do not. These results indicate a close functional interrelationship between homotypical areas in SI and SII, though the two areas differ in several important respects. It is proposed that SII in mice may complement the function of SI by helping to define the overall sensory context in which detailed tactile discriminations are made.
The cortex adjacent to and along the upper bank of the lateral sulcus (UB-LS) of a prosimian primate, Galago crassicaudatus, was explored to determine the topographical representation of low-threshold cutaneous inputs to this region. The somatic sensory projections to this cortex were considered homologous to those defined in other species as the second somatosensory cortical area (SII). Multiple and single neuron recordings were obtained with tungsten microelectrodes in animals anesthetized with sodium pentobarbital or ketamine hydrochloride; receptive fields were determined by means of manually applied tactile stimuli. The area of SII was located approximately 1-1.5 mm rostral to the posterior limit of LS, extended rostrally approximately 4 mm, and occupied nearly all of the upper bank of the sulcus throughout this region. Receptive fields (RFs) in SII were primarily contralateral except for some bilateral input in the cortex representing portions of the trunk, head, and face. The boundaries of RFs were well defined, especially where recordings were located in the middle layers of the cortex. The distribution of RFs across SII was somatotopically organized into a single, relatively erect representation of the body that involved inputs from the face rostral and medial (superficially along the UB-LS) surrounding an enlarged forelimb area; the latter, in turn, lies rostral and medial to the hindlimb zone. Projections from the tail and sacrum are located furthest caudal and lateral (deeper along UB-LS). Separate regions that were devoted to the glabrous skin surfaces of the distal limbs formed the rostral and lateral boundaries of the distal fore- and hindlimb representations, respectively. In the zone for the glabrous surfaces of the forelimb digits, individual digits dominated discrete components of the SII map, especially medially where digit 1 was represented. The glabrous tip of digit 5 was represented caudal and lateral to the tip of digit 1. A similar radial to ulnar medial to lateral sequence was noted in the area representing the palm. Except for a possible medially located toe 1 zone in the hindlimb representation, separated representations for the glabrous skin of individual toes were not noted. The dorsal hairy surfaces of the digits and toes were, respectively, amalgamated within the representations for the dorsal surfaces of the hand and foot. In these regions, which were found superficial and slightly caudal to their respective glabrous zones, some RFs were found that were devoted only to the distal extremities, but most RFs included more proximal portions of the hand or foot dorsum.(ABSTRACT TRUNCATED AT 400 WORDS)