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Cortical connections of the middle temporal and the middle temporal crescent visual areas in prosimian galagos (Otolemur garnetti)
The Anatomical Record
Abstract
While considerable progress has been made in understanding the organization of visual cortex in monkeys, less is known about the visual systems of prosimians. The middle temporal visual area (MT), an area involved in motion perception, is common to all primates. We placed injections of tracers in MT and just caudal to MT in cortex expected to be the MT crescent (MTc), an area previously identified in monkeys but not in prosimians. We analyzed the patterns of projections in sections of the flattened cortex and used sections stained for cytochrome oxidase (CO) and myelin to identify the borders of MT, MTc, middle superior temporal (MST), superior temporal sulcus (FST), and V1 and V2 and to identify possible subdivisions of these areas. As in owl monkeys, MTc is a belt around most of MT that consists of a single row of CO-dense patches in a CO-light surround. Injections placed in MT revealed connections with V1, V2, V3, FST, MST, MTc, dorsomedial, dorsolateral (DL), posterior parietal cortex, and inferotemporal (IT) cortex. Injections localized to MTc displayed a slightly different pattern of connections with more involvement of DL and IT cortex, though other aspects, including patchy connections with V1 and V2, were similar to MT connections. The results indicate that prosimian galagos have an MT area with connection patterns that are similar to those in New and Old World monkeys. The MTc, initially described in owl monkeys, is present in galagos and is likely to be a common component of primate visual cortex.
... As a result, the connections of MT with other areas of cortex have been extensively studied across a range of primate species, with considerable agreement across studies on the major MT connections with other cortical areas and regions. [15][16][17][18][19][20][21][22][23] The connections revealed by injections of tracers in MT are generally consistent with those MT connections revealed by injections in other areas of cortex. [24][25][26][27] We sought to add to this accumulation of evidence on the connections of MT in primates in several ways. ...
... For example, there is now considerable evidence for a single V3 with dorsal and ventral halves in primates, rather than a dorsal V3 and a ventral V3 (see Lyon and Connolly 28 ), and the relation of MT to adjoining areas including the middle temporal crescent (MTc or V4t), the middle superior temporal area (MST), and the dorsal and ventral fundal areas of the superior temporal sulcus (FSTd and FSTv, respectively) is better understood. 23,25 Furthermore, it is possible to inject several different retrograde tracers into different retinotopic locations in MT, thereby revealing the existence of retinotopic patterns of input connections, although this has not been done previously. Finally, strengths of MT connections have only been quantified in one previous study on marmosets, 21 and quantifications of connections are needed for comparison with other primates. ...
... Overall, the pattern of connections of MT with other areas of cortex revealed in the present study is in agreement with previous results from owl monkeys, 18,20,25,54 other New World monkeys, 15,[20][21][22]55 Old World macaques, 17,19 and prosimian galagos. 23 All studied primates appear to have neurons projecting to MT in visual areas V1, V2, and V3 (although V3 has not been consistently recognized), DM or a comparable region, parts of PPC that in macaques include LIP and VIP, frontal cortex in and near the expected locations of the FEF, areas of the MT complex (MTc, FST, and MST), DL, and parts of temporal cortex. Other regions have been variously reported (see Palmer and Rosa 21,55 for review). ...
We made eight retrograde tracer injections into the middle temporal visual area (MT) of three New World owl monkeys (Aotus nancymaae). These injections were placed across the representation of the retina in MT to allow us to compare the locations of labeled cells in other areas in order to provide evidence for any retinotopic organization in those areas. Four regions projected to MT: 1) early visual areas, including V1, V2, V3, the dorsolateral visual area, and the dorsomedial visual area, provided topographically organized inputs to MT; 2) all areas in the MT complex (the middle temporal crescent, the middle superior temporal area, and the fundal areas of the superior temporal sulcus) projected to MT. Somewhat variably across injections, neurons were labeled in other parts of the temporal lobe; 3) regions in the location of the medial visual area, the posterior parietal cortex, and the lateral sulcus provided other inputs to MT; 4) finally, projections from the frontal eye field, frontal visual field, and prefrontal cortex were also labeled by our injections. These results further establish the sources of input to MT, and provide direct evidence within and across cases for retinotopic patterns of projections from early visual areas to MT.
... For instance, subdivisions of frontal cortex have been defined, including the FEF (Wu et al., 2000), as have sensorimotor regions of posterior parietal cortex (Stepniewska et al., , 2009a. Additionally, recent evidence has shed light on the organization of some of the early visual areas, especially V3 (Lyon and Kaas, 2002) and areas that are part of the MT complex (Kaskan and Kaas, 2007). Yet, little is known about the connections of these areas with the SC. ...
... Cortical areas examined in this study within the occipital cortex are V1, V2, V3, DM, and DL (Fig. 1A). Area V1 was reliably identified in galagos by its characteristic CO blobinterblob pattern of staining and dark myelination (Condo and Casagrande, 1990;Kaskan and Kaas, 2007;Wong and Kaas, 2010). V2, rostral to V1, stains less darkly for myelin and, unlike anthropoid primates, has only a weak stripe-like pattern of CO staining at best (Condo and Casagrande, 1990;Kaskan and Kaas, 2007;Wong and Kaas, 2010). ...
... Area V1 was reliably identified in galagos by its characteristic CO blobinterblob pattern of staining and dark myelination (Condo and Casagrande, 1990;Kaskan and Kaas, 2007;Wong and Kaas, 2010). V2, rostral to V1, stains less darkly for myelin and, unlike anthropoid primates, has only a weak stripe-like pattern of CO staining at best (Condo and Casagrande, 1990;Kaskan and Kaas, 2007;Wong and Kaas, 2010). Thus, the rostral border of V2 was estimated by its known width. ...
The superior colliculus (SC) is a key structure within the extrageniculate pathway of visual information to cortex and is highly involved in visuomotor functions. Previous studies in anthropoid primates have shown that superficial layers of the SC receive direct inputs from various visual cortical areas such as V1, V2, and middle temporal (MT), while deeper layers receive direct inputs from visuomotor cortical areas within the posterior parietal cortex and the frontal eye fields. Very little is known, however, about the corticotectal projections in prosimian primates. In the current study we investigated the sources of cortical inputs to the SC in prosimian galagos (Otolemur garnetti) using retrograde anatomical tracers placed into the SC. The superficial layers of the SC in galagos received the majority of their inputs from early visual areas and visual areas within the MT complex. Yet, surprisingly, MT itself had relatively few corticotectal projections. Deeper layers of the SC received direct projections from visuomotor areas including the posterior parietal cortex and premotor cortex. However, relatively few corticotectal projections originated within the frontal eye fields. While prosimian galagos resemble other primates in having early visual areas project to the superficial layers of the SC, with higher visuomotor regions projecting to deeper layers, the results suggest that MT and frontal eye field projections to the SC were sparse in early primates, remained sparse in present-day prosimian primates, and became more pronounced in anthropoid primates.
... In myelin preparations, MT is densely myelinated ( Fig. 7B; 8B; 10B). Layer 4 of MT stains darkly for CO (Kaskan and Kaas, 2007), although this is not especially evident in figures 5C and 8C. Throughout the cortical layers, MT stains lighter for synaptic zinc than the surrounding areas ( Fig. 7D;8D). ...
... However, MT is more darkly stained for free synaptic zinc, especially in layer 4, than area 17. This is consistent with the evidence that MT receives a large amount of corticocortical inputs, a major portion of which originates from area 17 (Kaskan and Kaas, 2007). The PV immunostain is perhaps one of the best markers for MT, as MT stains darkly for PV immunopositive terminations and has a tri-banded appearance ( Fig. 7E;8E). ...
... In VGluT2 preparations, a thin, faintly stained band is present in layer 4 of MTc ( Fig. 7F; 8F), and MTc is lighter stained than MT (Fig. 9B). In sections cut tangentially to the pia, MTc contains several COdense puffs ( Fig. 9A; Kaskan and Kaas, 2007). ...
In the present study, galago brains were sectioned in the coronal, sagittal, or horizontal planes, and sections were processed with several different histochemical and immunohistochemical procedures to reveal the architectonic characteristics of the various cortical areas. The histochemical methods used included the traditional Nissl, cytochrome oxidase, and myelin stains, as well as a zinc stain, which reveals free ionic zinc in the axon terminals of neurons. Immunohistochemical methods include parvalbumin (PV) and calbindin (CB), both calcium-binding proteins, and the vesicle glutamate transporter 2 (VGluT2). These different procedures revealed similar boundaries between areas, which suggests that functionally relevant borders were being detected. These results allowed a more precise demarcation of previously identified areas. As thalamocortical terminations lack free ionic zinc, primary cortical areas were most clearly revealed by the zinc stain, because of the poor zinc staining of layer 4. Area 17 was especially prominent, as the broad layer 4 was nearly free of zinc stain. However, this feature was less pronounced in the primary auditory and somatosensory cortex. As VGluT2 is expressed in thalamocortical terminations, layer 4 of primary sensory areas was darkly stained for VGluT2. Primary motor cortex had reduced VGluT2 staining, and increased zinc-enriched terminations in the poorly developed granular layer 4 compared to the adjacent primary somatosensory area. The middle temporal visual (MT) showed increased PV and VGluT2 staining compared to the surrounding cortical areas. The resulting architectonic maps of cortical areas in galagos can usefully guide future studies of cortical organizations and functions.
... To localize injection sites most accurately in visual areas V1, V2, and MT in galagos, we artificially flattened cortex, cut sections parallel to the cortical surface, and processed sets of sections for myelin or CO. As demonstrated in previous studies with this approach (see, e.g., Cusick and Kaas, 1988;Krubitzer and Kaas, 1990;Collins et al., 2001;Lyon and Kaas, 2002;Xu et al., 2004;Kaskan and Kaas, 2007), area 17, or V1, is easily identified by its pattern of CO-dense blobs (Fig. 3C), as in other primates. In addition, a marked reduction in myelination is apparent rostral to the V1/V2 border in myelin-stained sections through the middle cortical layers (Fig. 3B). ...
... Finally, MT has been consistently identified in galagos and other primates as an oval of cortex that is CO and myelin dense (Fig. 3A,C). However, MST can also be CO dense (Kaskan and Kaas, 2007), and the most rostral one-third of the CO-dense region in Figure 3C is likely to be MST. All the injections were in the caudal two-thirds of the CO-dense oval and, thus, in MT. ...
... Although V1 appears to provide some projections to PIm in macaque monkeys (Gutierrez and Cusick, 1997), these terminations were revealed by large injections, and few labeled neurons were found. Overall, PIm in galagos likely corresponds to PIm or PIm plus PIcm of monkeys, as PIcm targets areas associated with MT (MTc, MST, and FST; Boussaoud et al., 1992;Weller et al., 2002;Kaskan and Kaas, 2007;Kaas and Lyon, 2007) and MT (Stepniewska et al., 1999(Stepniewska et al., , 2000. ...
The pulvinar complex of prosimian primates is not as architectonically differentiated as that of anthropoid primates. Thus, the functional subdivisions of the complex have been more difficult to determine. In the present study, we related patterns of connections of cortical visual areas (primary visual area, V1; secondary visual area, V2; and middle temporal visual area, MT) as well as the superior colliculus of the visual midbrain, with subdivisions of the pulvinar complex of prosimian galagos (Otolemur garnetti) that were revealed in brain sections processed for cell bodies (Nissl), cytochrome oxidase, or myelin. As in other primates, the architectonic methods allowed us to distinguish the lateral pulvinar (PL) and inferior pulvinar (PI) as major divisions of the visual pulvinar. The connection patterns further allowed us to divide PI into a large central nucleus (PIc), a medial nucleus (PIm), and a posterior nucleus (PIp). Both PL and PIc have separate topographic patterns of connections with V1 and V2. A third, posterior division of PI, PIp, does not appear to project to V1 and V2 and is further distinguished by receiving inputs from the superior colliculus. All these subdivisions of PI project to MT. The evidence suggests that PL of galagos contains a single, large nucleus, as in monkeys, and that PI may have only three subdivisions, rather than the four subdivisions of monkeys. In addition, the cortical projections of PI nuclei are more widespread than those in monkeys. Thus, the pulvinar nuclei in prosimian primates and anthropoid primates have evolved along somewhat different paths.
... The pattern of DL connections with PPCc in galagos, like the pattern of DL connections with V1 (Lyon and Kaas 2002a) and V2 (Collins et al. 2001), did not clearly identify rostral and caudal subdivisions of DL, which have been proposed for monkeys (Cusick and Kaas 1988;Steele et al. 1991;Weller et al. 1991;Stepniewska and Kaas 1996). Such subdivisions were also not architectonically apparent in galagos ( present study; Kaskan and Kaas 2007). The rostral division of DL in monkeys is thought to be more involved in dorsal stream processing, due to its connections with MT and DM areas. ...
... A clear retinotopic pattern of PPCc connections with MST-MT was not apparent in these cases. Tracing studies of MT connections in galagos (Krubitzer and Kaas 1990;Kaskan and Kaas 2007) revealed only sparsely distributed axon terminals around the posterior tip of the IPS and below the sulcus in the ventral PPCc. ...
Posterior parietal cortex (PPC) of prosimian galagos includes a rostral portion (PPCr) where electrical stimulation evokes different classes of complex movements from different subregions, and a caudal portion (PPCc) where such stimulation fails to evoke movements in anesthetized preparations ( Stepniewska, Fang et al. 2009). We placed tracer injections into PPCc to reveal patterns of its cortical connections. There were widespread connections within PPCc as well as connections with PPCr and extrastriate visual areas, including V2 and V3. Weaker connections were with dorsal premotor cortex, and the frontal eye field. The connections of different parts of PPCc with visual areas were roughly retinotopic such that injections to dorsal PPCc labeled more neurons in the dorsal portions of visual areas, representing lower visual quadrant, and injections to ventral PPCc labeled more neurons in ventral portions of these visual areas, representing the upper visual quadrant. We conclude that much of the PPCc contains a crude representation of the contralateral visual hemifield, with inputs largely, but not exclusively, from higher-order visual areas that are considered part of the dorsal visuomotor processing stream. As in galagos, the caudal half of PPC was likely visual in early primates, with the rostral PPC half mediating sensorimotor functions.
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... Among other areas, primary auditory (A1) and middle temporal visual (MT) areas were easily recognized by their dense myelination and CO-dark appearance (Krubitzer and Kaas, 1990). Visual areas V1 and V2 were also easily recognized by their characteristic CO and myelin patterns, demonstrating blobs in V1 and in most favorable sections stripes in V2 (Lyon and Kaas, 2002;Kaskan and Kaas, 2007). In favorable sections, area DM has been distinguished from PPC as more densely myelinated. ...
... The visual inputs to PPC come from visual areas well defined in galagos, including areas MT (Kaskan and Kaas, 2007), MST, V3, DM (Beck and Kaas, 1998), V2 (Collins et al., 2001), and other less well-understood and more associative areas. Based on our previous and unpublished observations, the caudal half of PPC that is unresponsive to ICMS receives most of the inputs from visual cortex and relays it to the anterior excitable PPC. ...
We studied cortical connections of functionally distinct movement zones of the posterior parietal cortex (PPC) in galagos identified by intracortical microstimulation with long stimulus trains ( approximately 500 msec). All these zones were in the anterior half of PPC, and each of them had a different pattern of connections with premotor (PM) and motor (M1) areas of the frontal lobe and with other areas of parietal and occipital cortex. The most rostral PPC zone has major connections with motor and visuomotor areas of frontal cortex as well as with somatosensory areas 3a and 1-2 and higher order somatosensory areas in the lateral sulcus. The dorsal part of anterior PPC region representing hand-to-mouth movements is connected mostly to the forelimb representation in PM, M1, 3a, 1-2, and somatosensory areas in the lateral sulcus and on the medial wall. The more posterior defensive and reaching zones have additional connections with nonprimary visual areas (V2, V3, DL, DM, MST). Ventral aggressive and defensive face zones have reciprocal connections with each other as well as connections with mostly face, but also forelimb representations of premotor areas and M1 as well as prefrontal cortex, FEF, and somatosensory areas in the lateral sulcus and areas on the medial surface of the hemisphere. Whereas the defensive face zone is additionally connected to nonprimary visual cortical areas, the aggressive face zone is not. These differences in connections are consistent with our functional parcellation of PPC based on intracortical long-train microstimulation, and they identify parts of cortical networks that mediate different motor behaviors.
... Presently, very little is known about the temporal cortex of strepsirrhine primates. There is only limited evidence for connections of visual areas DL (V4) and V2 with temporal cortex in galagos [206][207][208], and temporal areas project to frontal cortex, as in other primates [209]. But we don't yet know if strepsirrhine primates have functional domains in the temporal cortex that are similar to those in monkeys, and thus the organization of the ventral stream of visual processing in the ancestral primates remains uncertain. ...
Early mammals were small and nocturnal. Their visual systems had regressed and they had poor vision. After the extinction of the dinosaurs 66 mya, some but not all escaped the ‘nocturnal bottleneck’ by recovering high-acuity vision. By contrast, early primates escaped the bottleneck within the age of dinosaurs by having large forward-facing eyes and acute vision while remaining nocturnal. We propose that these primates differed from other mammals by changing the balance between two sources of visual information to cortex. Thus, cortical processing became less dependent on a relay of information from the superior colliculus (SC) to temporal cortex and more dependent on information distributed from primary visual cortex (V1). In addition, the two major classes of visual information from the retina became highly segregated into magnocellular (M cell) projections from V1 to the primate-specific temporal visual area (MT), and parvocellular-dominated projections to the dorsolateral visual area (DL or V4). The greatly expanded P cell inputs from V1 informed the ventral stream of cortical processing involving temporal and frontal cortex. The M cell pathways from V1 and the SC informed the dorsal stream of cortical processing involving MT, surrounding temporal cortex, and parietal–frontal sensorimotor domains.
This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.
... All extrastriate visual cortices including the posterior parietal and temporal cortex show a slightly higher CO density in deeper layer 3 and layer 4 compared to other layers, and the CO density gradually decreases along the ventral visual pathway (Tootell et al., 1985;Paxinos et al., 2009). The MT is reported to possess a slightly higher CO staining intensity, especially in deeper layer 3 and layer 4 (Tootell et al., 1985;Kaskan and Kaas, 2007). Although we did not include these areas in the present study, it is likely that the higher CO density in the middle layers of these cortical areas resides in afferent terminals that arise from the pulvinar. ...
Cytochrome oxidase (CO) histochemistry has been used to reveal the cytoarchitecture of the primate brain, including blobs/puffs/patches in the striate cortex (V1), and thick, thin and pale stripes in the middle layer of the secondary visual cortex (V2). It has been suggested that CO activity is coupled with the spiking activity of neurons, implying that neurons in these CO-rich subcompartments are more active than surrounding regions. However, we have discussed possibility that CO histochemistry represents the distribution of thalamo-cortical afferent terminals that generally use vesicular glutamate transporter 2 (VGLUT2) as their main glutamate transporter, and not the activity of cortical neurons. In this study, we systematically compared the labeling patterns observed between CO histochemistry and immunohistochemistry (IHC) for VGLUT2 from the system to microarchitecture levels in the visual cortex of squirrel monkeys. The two staining patterns bore striking similarities at all levels of the visual cortex, including the honeycomb structure of V1 layer 3Bβ (Brodmann's layer 4A), the patchy architecture in the deep layers of V1, the superficial blobs of V1, and the V2 stripes. The microarchitecture was more evident in VGLUT2 IHC, as expected. VGLUT2 protein expression that produced specific IHC labeling is thought to originate from the thalamus since the lateral geniculate nucleus (LGN) and the pulvinar complex both show high expression levels of VGLUT2 mRNA, but cortical neurons do not. These observations support our theory that the subcompartments revealed by CO histochemistry represent the distribution of thalamo-cortical afferent terminals in the primate visual cortex.
... The PPC has abundant reciprocal connections with sensory areas and is functionally parcellated such that the rostral portion of PPC is connected to somatosensory and motor regions, and the caudal portion of PPC has connections with visual and auditory regions (Stepniewska et al., 2009). The necessary inputs to PPC for sensorimotor processing needed for skilled hand movements include direct reciprocal inputs from the dorsomedial visual area that allows for continuous visual motion analysis necessary for interacting with the environment (Beck and Kaas, 1998;Kaskan and Kaas, 2007;Rosa et al., 2009; for review, see Kaas et al., 2011). Sensory inputs to BA 5 primarily come from somatosensory area S2 and the parietal ventral area, along with weaker inputs from S1 (Stepniewska et al., 2009). ...
Integration of sensory and motor information is one-step, among others, that underlies the successful production of goal-directed hand movements necessary for interacting with our environment. Disruption of sensorimotor integration is prevalent in many neurologic disorders, including stroke. In most stroke survivors, persistent paresis of the hand reduces function and overall quality of life. Current rehabilitative methods are based on neuroplastic principles to promote motor learning that focuses on regaining motor function lost due to paresis, but the sensory contributions to motor control and learning are often overlooked and currently understudied. There is a need to evaluate and understand the contribution of both sensory and motor function in the rehabilitation of skilled hand movements after stroke. Here, we will highlight the importance of integration of sensory and motor information to produce skilled hand movements in healthy individuals and individuals after stroke. We will then discuss how compromised sensorimotor integration influences relearning of skilled hand movements after stroke. Finally, we will propose an approach to target sensorimotor integration through manipulation of sensory input and motor output that may have therapeutic implications.
... Our results indicate that human visual cortex, as macaque cortex , includes a MT/V5 cluster consisting of four cortical areas sharing a central representation and housing polar maps that are mirror-symmetric with those of neighbors (Fig. 16). There is mounting evidence that New World monkeys, such as squirrel, titi, and owl monkeys (Kaas and Morel, 1993;Lyon and Kaas, 2002) or marmosets (Rosa and Tweedale, 2005), and even prosimians, such as galagos (Kaskan and Kaas, 2007), all possess a cluster including MT/V5, MST, FST, and a small region labeled the MT crescent, similar to V4t of macaques. Thus, the MT/V5 cluster may be a general primate feature. ...
... Visual cortex in primates is greatly expanded compared to most mammals, and in macaque monkeys, as many as 35 visual areas have been proposed (Felleman and Van Essen, 1991). The contributions to PPC primarily come from a collection of visual areas (Boussaoud et al., 1990; Morel, 1993, Born and Bradley, 2005; Kaskan and Kaas, 2007) that are especially involved in processing information about visual motion. The somatosensory areas that contribute to the dorsal stream involve subdivisions of anterior parietal cortex that are uniquely distinct in primates, and newly defined somatosensory areas of the cortex of the lateral sulcus (Qi et al., 2002; Disbrow et al., 2003; Coq et al., 2004 ). ...
In Prosimian primates, New World monkeys, and Old World monkeys microstimulation with half second trains of electrical pulses identifies separate zones in posterior parietal cortex (PPC) where reaching, defensive, grasping, and other complex movements can be evoked. Each functional zone receives a different pattern of visual and somatosensory inputs, and projects preferentially to functionally matched parts of motor and premotor cortex. As PPC is a relatively small portion of cortex in most mammals, including the close relatives of primates, we suggest that a larger, more significant PPC emerged with the first primates as a region where several ethologically relevant behaviors could be initiated by sensory and intrinsic signals, and mediated via connections with premotor and motor cortex. While several classes of PPC modules appear to be retained by all primates, elaboration and differentiation of these modules likely occurred in some primates, especially humans.
... Three related issues restrict this understanding. First, data available to address this issue have been dominated by studies that are anatomical in nature (Zeki 1970Zeki , 1974Zeki , 1976Zeki , 1980 Zeki and Sandeman 1976; Seltzer and Pandya 1978; Rockland and Pandya 1979; Maunsell and van Essen 1983; Miller 1985; Shipp and Zeki 1985 Gilbert and Wiesel 1989; Zeki and Shipp 1989; Bravo et al. 1990; Coogan and Burkhalter 1990; Felleman and Van Essen 1991; Lowenstein and Somogyi 1991; Scannell et al. 1995; Kaas 1996; McDonald and Mascagni 1996; Porter 1997; Beck and Kaas 1998; Shipp et al. 1998; Kaas and Collins 2001; Wu and Kaas 2003; Kaskan and Kaas 2007; Wong and Kaas 2009) with surprisingly little functional information about these connections. Thus, we lack a basic understanding of how these circuits actually function. ...
Little is known regarding the synaptic properties of corticocortical connections from one cortical area to another. To expand on this knowledge, we assessed the synaptic properties of excitatory projections from the primary to secondary auditory cortex and vice versa. We identified 2 types of postsynaptic responses. The first class of responses have larger initial excitatory postsynaptic potentials (EPSPs), exhibit paired-pulse depression, are limited to ionotropic glutamate receptor activation, and have larger synaptic terminals; the second has smaller initial EPSPs, paired-pulse facilitation, metabotropic glutamate receptor activation, and smaller synaptic terminals. These responses are similar to the driver and modulator properties previously identified for thalamic and thalamocortical circuitry, suggesting that the same classification may extend to corticocortical inputs and have an implication for the functional organization of corticocortical circuits.
... Our results indicate that human visual cortex, as macaque cortex (Kolster et al., 2009), includes a MT/V5 cluster consisting of four cortical areas sharing a central representation and housing polar maps that are mirror-symmetric with those of neighbors (Fig. 16). There is mounting evidence that New World monkeys, such as squirrel, titi, and owl monkeys (Kaas and Morel, 1993; Lyon and Kaas, 2002) or marmosets (Rosa and Tweedale, 2005), and even prosimians, such as galagos (Kaskan and Kaas, 2007), all possess a cluster including MT/V5, MST, FST, and a small region labeled the MT crescent, similar to V4t of macaques. Thus, the MT/V5 cluster may be a general primate feature. ...
Although there is general agreement that the human middle temporal (MT)/V5+ complex corresponds to monkey area MT/V5 proper plus a number of neighboring motion-sensitive areas, the identification of human MT/V5 within the complex has proven difficult. Here, we have used functional magnetic resonance imaging and the retinotopic mapping technique, which has very recently disclosed the organization of the visual field maps within the monkey MT/V5 cluster. We observed a retinotopic organization in humans very similar to that documented in monkeys: an MT/V5 cluster that includes areas MT/V5, pMSTv (putative ventral part of the medial superior temporal area), pFST (putative fundus of the superior temporal area), and pV4t (putative V4 transitional zone), and neighbors a more ventral putative human posterior inferior temporal area (phPIT) cluster. The four areas in the MT/V5 cluster and the two areas in the phPIT cluster each represent the complete contralateral hemifield. The complete MT/V5 cluster comprises 70% of the motion localizer activation. Human MT/V5 is located in the region bound by lateral, anterior, and inferior occipital sulci and occupies only one-fifth of the motion complex. It shares the basic functional properties of its monkey homolog: receptive field size relative to other areas, response to moving and static stimuli, as well as sensitivity to three-dimensional structure from motion. Functional properties sharply distinguish the MT/V5 cluster from its immediate neighbors in the phPIT cluster and the LO (lateral occipital) regions. Together with similarities in retinotopic organization and topological neighborhood, the functional properties suggest that MT/V5 in human and macaque cortex are homologous.
... At least most of the posterior half of PPC in galagos receives visual inputs from visual areas DM and V3 (Beck and Kaas, 1998a;Lyon and Kaas, 2002). Moreover, patterns of label after injections of tracers in the middle temporal visual area (MT) and narrow middle temporal crescent area (MTc) bordering MT suggest that both areas also have connections with posterior PPC (Wall et al., 1982;Krubitzer and Kaas, 1990;Kaskan and Kaas, 2007). Thus, there are probably four or more visual areas that distribute visual information to the posterior half of PPC in galagos. ...
We used half-second trains of intracortical microstimulation to study the functional organization of the posterior parietal cortex (PPC) in prosimian galagos. These trains of current pulses evoked meaningful behaviors from the anterior, but not posterior, half of PPC. Stimulation of dorsal PPC caused contralateral forelimb movements, including defensive, hand-to-mouth, and reaching movements. Defensive and hand-to-mouth movement territories overlapped, although hand-to-mouth movements were usually evoked from more rostrolateral sites than defensive movements. Reaching movement sites were typically more caudal than defensive or hand-to-mouth movement sites. Stimulation of the most medial PPC sites evoked complex movements of forelimbs and hindlimbs. Ventral PPC commonly represented defensive face movements. Similar defensive movements, with the addition of widely opening the mouth to expose the teeth, were elicited from a small area in front of the PPC defensive face zone. Sometimes defensive face movements occurred with forelimb movements. Thus, subregions of PPC relate to different ethologically relevant categories of behavior. Most movements were initiated within 33-100 msec after stimulus onset. Face, eye blink, and ear movements were generally less delayed than forelimb movements. The present results in galagos, together with those obtained from macaque monkeys by Graziano and coworkers (Graziano et al. [2002a] Neuron 34:841-851; Cooke et al., [2003] Proc. Natl. Acad. Sci. U.S.A. 100:6163-6168), suggest that the functional involvement of the PPC in specific types of sensorimotor behavior evolved early in the course of primate evolution and that networks for complex movements involving motor and posterior parietal areas are characteristic of all primate brains.
... Conversely, the SPARC mRNA expression was weak in V1 and gradually broadened in superficial layers and layer V along the visual pathway (brackets). WM/white matter; scale bar 5 1.0 mm. a distinct area of the primate visual system, the middle temporal visual area (MT), which is a highly myelinated compartment and the center of motion processing in the visual dorsal pathway (Kaskan and Kaas 2007). However, the expression patterns of occ1-related genes in MT were similar to those in extrastriate visual cortex and did not show clear demarcation with surrounding areas (Fig. 5). ...
We have previously revealed that occ1 is preferentially expressed in the primary visual area (V1) of the monkey neocortex. In our attempt to identify more area-selective genes in the macaque neocortex, we found that testican-1, an occ1-related gene, and its family members also exhibit characteristic expression patterns along the visual pathway. The expression levels of testican-1 and testican-2 mRNAs as well as that of occ1 mRNA start of high in V1, progressively decrease along the ventral visual pathway, and end of low in the temporal areas. Complementary to them, the neuronal expression of SPARC mRNA is abundant in the association areas and scarce in V1. Whereas occ1, testican-1, and testican-2 mRNAs are preferentially distributed in thalamorecipient layers including "blobs," SPARC mRNA expression avoids these layers. Neither SC1 nor testican-3 mRNA expression is selective to particular areas, but SC1 mRNA is abundantly observed in blobs. The expressions of occ1, testican-1, testican-2, and SC1 mRNA were downregulated after monocular tetrodotoxin injection. These results resonate with previous works on chemical and functional gradients along the primate occipitotemporal visual pathway and raise the possibility that these gradients and functional architecture may be related to the visual activity-dependent expression of these extracellular matrix glycoproteins.
This review summarizes our findings obtained from over 15 years of research on parietal-frontal networks involved in the dorsal stream of cortical processing. We have presented considerable evidence for the existence of similar, partially independent, parietal-frontal networks involved in specific motor actions in a number of primates. These networks are formed by connections between action-specific domains representing the same complex movement evoked by electrical microstimulation. Functionally matched domains in the posterior parietal (PPC) and frontal (M1-PMC) motor regions are hierarchically related. M1 seems to be a critical link in these networks, since the outputs of M1 are essential to the evoked behavior, whereas PPC and PMC mediate complex movements mostly via their connections with M1. Thus, lesioning or deactivating M1 domains selectively blocks matching PMC and PPC domains, while having limited impact on other domains. When pairs of domains are stimulated together, domains within the same parietal-frontal network (matching domains) are cooperative in evoking movements, while they are mainly competitive with other domains (mismatched domains) within the same set of cortical areas. We propose that the interaction of different functional domains in each cortical region (as well as in striatum) occurs mainly via mutual suppression. Thus, the domains at each level are in competition with each other for mediating one of several possible behavioral outcomes.
Previous studies in prosimian galagos (Otolemur garnetti) have demonstrated that posterior parietal cortex (PPC) is subdivided into several functionally distinct domains, each of which mediates a specific type of complex movements (e.g., reaching, grasping, hand‐to‐mouth) and has a different pattern of cortical connections. Here we identified a medially located domain in PPC where combined forelimb and hindlimb movements, as if climbing or running, were evoked by long‐train intracortical microstimulation (LT‐ICMS). We injected anatomical tracers in this climbing/running domain of PPC to reveal its cortical connections. Our results showed the PPC climbing domain had dense intrinsic connections within rostral PPC and reciprocal connections with forelimb and hindlimb region in primary motor cortex (M1) of the ipsilateral hemisphere. Fewer connections were with dorsal premotor cortex (PMd), supplementary motor (SMA) and cingulate motor (CMA) areas, as well as somatosensory cortex including areas 3a, 3b and 1‐2, secondary somatosensory (S2), parietal ventral (PV) and retroinsular (Ri) areas. The rostral portion of the climbing domain had more connections with primary somatosensory cortex than the caudal portion. Cortical projections were found in functionally matched domains in M1 and premotor cortex (PMC). Similar patterns of connections with fewer labeled neurons and terminals were seen in the contralateral hemisphere. These connection patterns are consistent with the proposed role of the climbing/running domain as part of a parietal‐frontal network for combined use of the limbs in locomotion as in climbing and running. The cortical connections identify this action‐specific domain in PPC as a more somatosensory driven domain.
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Considerable evidence supports the premise that the visual system of primates develops hierarchically, with primary visual cortex developing structurally and functionally first, thereby influencing the subsequent development of higher cortical areas. An apparent exception is the higher order middle temporal visual area, MT, which appears to be histologically distinct near the time of birth in marmosets. Here we used a number of histological and immunohistological markers to evaluate the maturation of cortical and subcortical components of the visual system in galagos ranging from newborns to adults. Galagos are representative of the large strepsirrhine branch of primate evolution, and studies of these primates help identify brain features that are broadly similar across primate taxa. The histological results support the view that MT is functional at or near the time of birth, as is primary visual cortex. Likewise, the superior colliculus, dorsal lateral geniculate nucleus, and the posterior nucleus of the pulvinar are well‐developed by birth. Thus, these subcortical structures likely provide visual information directly or indirectly to cortex in newborn galagos. We conclude that MT resembles a primary sensory area by developing early, and that the early development of MT may influence the subsequent development of dorsal stream visual areas. This article is protected by copyright. All rights reserved. The middle temporal visual area (MT) is revealed by parvalbumin (PV) immunoreactivity in early development (P3) of galagos, suggesting that MT resembles the primary sensory areas by developing early, and the early development of MT may influence the subsequent development of dorsal stream visual areas.
Primates and other mammals have at least three visual areas in common, V1, V2, and prostriata, as well as one or more subdivisions of visual temporal cortex. V1 of primates differs from other mammals in laminar and modular organization, and V2 has a modular organization that is unique to primates. Other areas, such as V3 and MT, appear to have emerged with the evolution of the first primates. Those areas and other extrastriate areas may have been modified or differentiated from areas in the nonprimate ancestor of primates. However, all primates have more visual areas than their nonprimate ancestors. Old World macaque monkeys have more visual areas than prosimian primates, and more areas have been identified in humans than in macaques.
The middle temporal (MT) and medial superior temporal (MST) areas of the macaque cortex have many cells that respond to straight movements in the frontoparallel plane with directional selectivity (D cells). We examined their responses to movements of a bar, of a wide dot pattern, and to combined movements of the two in anesthetized and immobilized animals. D cells in MT showed a wide variety in the strength of the inhibitory field surrounding the excitatory center field. Responses of SI+-type cells to a bar moving across the excitatory field were suppressed when a wide dot pattern moved over the surround field in the same direction and at the same speed as the bar. Inhibition was selective to the direction and speed of the surround movement, and the effective area for inhibition occupied a wide area, which expanded in all radial directions. Responses of SI- -type cells to a center bar movement were changed little by a conjoint movement over the surround field. Consequently, SI- -type cells responded to wide-field movement as well as to stimuli confined within the excitatory field. Although D cells in MST commonly had large excitatory fields, a proportion of them (Figure type) responded to bar movement much more strongly than to wide- field movement. Their responses to a bar movement were suppressed direction-selectively by a conjoint movement of a wide dot-pattern background. The effective area for inhibition coexisted with the excitatory field in these cells. MST cells of the Nonselective type responded comparably well to the two stimuli, and those of the Field type responded much more strongly to wide-field movement than to bar movement. It is thus suggested that MT cells of the SI+ type and MST cells of the Figure type can detect a difference between movements of an object and its wide background, whereas MST cells of the Field type can detect a conjoint movement of a wide field, neglecting the movements of a single object.
The cortical and subcortical connections of the middle temporal visual area (MT) of the macaque monkey were investigated using combined injections of [3H]proline and horseradish peroxidase within MT. Cortical connections were assigned to specific visual areas on the basis of their relationship to the pattern of interhemispheric connections, revealed by staining for degeneration following callosal transection. MT was shown to be reciprocally connected with many topographically organized cortical visual areas, including V1, V2, V3, and V4. These pathways link regions representing corresponding portions of the visual field in the different areas. In addition, MT has reciprocal connections with two previously unidentified cortical areas, which we have designated the medial superior temporal area (MST) and the ventral intraparietal area (VIP). The laminar distribution of terminals and cell bodies in cortical areas connected with MT follows a consistent pattern. In areas V1, V2, and V3, the projections to MT arise largely or exclusively from cells in supragranular layers, and the reciprocal connections from MT terminate mainly in supragranular and infragranular layers. In contrast, the projections to MST and VIP terminate mainly in layer IV, and the reciprocal pathways originate from cells in both superficial and deep layers. On the basis of this pattern, each connection can be designated as forward or feedback in nature, and a hierarchical arrangement of visual areas can be determined. In this hierarchy, MT is at a higher level than V1, V2, and V3, and at a lower level than MST and VIP. Subcortical projections were seen from MT to the claustrum, the putamen, the caudate nucleus, the inferior and lateral subdivisions of the pulvinar complex, the ventral lateral geniculate nucleus, the reticular nucleus of the thalamus, the superior colliculus, and the pontine nuclei.
The early stages of primate visual processing appear to be divided up into several component parts so that, for example, colour, form and motion are analysed by anatomically distinct streams. We have found that further subspecialization occurs within the motion processing stream. Neurons representing two different kinds of information about visual motion are segregated in columnar fashion within the middle temporal area of the owl monkey. These columns can be distinguished by labelling with 2-deoxyglucose in response to large-field random-dot patterns. Neurons in lightly labelled interbands have receptive fields with antagonistic surrounds: the response to a centrally placed moving stimulus is suppressed by motion in the surround. Neurons in more densely labelled bands have surrounds that reinforce the centre response so that they integrate motion cues over large areas of the visual field. Interband cells carry information about local motion contrast that may be used to detect motion boundaries or to indicate retinal slip during visual tracking. Band cells encode information about global motion that might be useful for orienting the animal in its environment.
In primate cortical tissue which has been stained for the mitochondrial enzyme cytochrome oxidase, a topographical pattern of regularly spaced blobs has been demonstrated in primary visual cortex (Hendrickson, A. E., S. P. Hunt, and J. -Y. Wu (1981) Nature 292: 605-607; Horton, J. C., and D. H. Hubel (1981) Nature 292: 762-764), and a pattern of stripes has been shown in secondary visual cortex (V2) as well (Livingstone, M. S., and D. H. Hubel (1982) Proc. Natl. Acad. Sci. U. S. A. 79: 6098-6101; Tootell, R. B. H., M. S. Silverman, E. Switkes, and R. L. De Valois (1982) Soc. Neurosci. Abstr. 8: 707). These regular cytoarchitectonic landmarks have proven extremely useful in parsing the functional and anatomical architecture of these two cortical areas. In order to look for similar landmarks in other cortical areas of a primate, we completely unfolded the cortical gray matter in the owl monkey (Aotus trivirgatus), sectioned it parallel with the flattened cortical surface, and stained the tissue for cytochrome oxidase. Distinctive cytochrome oxidase topographies were found in about seven different cortical areas. As in other primates, area V1 is characterized by blobs and area V2 is characterized by strips. In the owl monkey, area MT is characterized by an elaborate topography of dark staining in layers 1 to 4, interspersed with light blob-shaped regions, and partially surrounded by a dark ring. Many of these topographic inhomogeneities are also reflected in the lower layer myelination topography in MT. Visual area(s) VP/VA is characterized by an irregular or strip-like topography. In some animals, a distinctive topography can be seen in area DX, which is presumably equivalent to either area DM or DI. Primary auditory cortex stains very darkly, but the overall shape of area A is quite variable and the borders are indistinct. Somatosensory area 3B stains quite darkly with sharp borders, but again the overall shape of area 3B is different from that previously described.
We perceive the visual world as a unitary whole, yet one of the guiding principles of nearly a half century of neurophysiological research since the early recordings by Hartline (1938) has been that the visual system consists of neurons that are driven by stimulation within small discrete portions of the total visual field. These classical receptive fields (CRFs) have been mapped with the excitatory responses evoked by a flashed or moving stimulus, usually a spot or bar of light. Most of the visual neurons, in turn, are organized in a series of maps of the visual field, at least 10 of which exist in the visual cortex in primates as well as additional topographic representations in the lateral geniculate body, pulvinar and optic tectum (Allman 1977, Newsome & Allman 1980, Allman & Kaas 1984). It has been widely assumed that perceptual functions that require the integration of inputs over large portions of the visual field must be either collective properties of arrays of neurons representing the visual field, or features of those neurons at the highest processing levels in the visual system, such as the cells in inferotemporal or posterior parietal cortex that typically possess very large receptive fields and do not appear to be organized in visuotopic maps. These assumptions have been based on the results of the many studies in which receptive fields were mapped with conventional stimuli, presented one at a time, against a featureless background. However, unlike the neurophysiologist's tangent screen, the natural visual scene is rich in features, and there is a growing body of evidence that in many visual neurons stimuli presented outside the CRF strongly and selectively influence neural responses to stimuli presented within the CRF. These results suggest obvious mechanisms for local-global comparisons within visuotopically organized structures. Such broad and specific surround mechanisms could participate in many functions that require the integration of inputs over wide regions of the visual space such as the perceptual constancies, the segregation of figure from ground, and depth perception through motion parallax. In the first section of this paper, we trace the historical development of the evidence of response selectivity for visual stimuli presented beyond the CRF; in the second, examine the anatomical pathways that sub serve these far-reaching surround mechanisms; and in the third, explore the possible relationships between these mechanisms and perception.
An essential reference book for visual science. Visual science is the model system for neuroscience, its findings relevant to all other areas. This massive collection of papers by leading researchers in the field will become an essential reference for researchers and students in visual neuroscience, and will be of importance to researchers and professionals in other disciplines, including molecular and cellular biology, cognitive science, ophthalmology, psychology, computer science, optometry, and education.
Over 100 chapters cover the entire field of visual neuroscience, from its historical foundations to the latest research and findings in molecular mechanisms and network modeling. The book is organized by topic—different sections cover such subjects as the history of vision science; developmental processes; retinal mechanisms and processes; organization of visual pathways; subcortical processing; processing in the primary visual cortex; detection and sampling; brightness and color; form, shape, and object recognition; motion, depth, and spatial relationships; eye movements; attention and cognition; and theoretical and computational perspectives. The list of contributors includes leading international researchers in visual science.
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Nature 357, 497-499 (1992) IN experiments that used the 2-deoxyglucose technique to label the band/interband pattern in the middle temporal visual area of the owl monkey, animals were injected with 50 fig kg"1 of methamphetamine ~10min before infusion of 2-deoxyglucose. This was not included inthe reference cited in our paper as a description of the method (ref.
The dorsomedial visual area (DM) is an extrastriate area that was originally described in owl monkeys as a complete representation of the Visual hemifield in a heavily myelinated wedge of cortex just rostral to dorsomedial visual area V2. More recently, connections of DM in owl monkeys have been described (Krubitzer and Kaas [1993] J. Comp. Neurol 334:497-528). As part of an effort to determine whether DM exists in other primates, we compared the architecture, connections, and visual topography of DM in owl monkeys and the presumptive DM in squirrel monkeys. In both species of New World monkeys, the DM region was more heavily myelinated than adjacent cortex, and this region was connected with the fist and second visual areas, the middle temporal area (MT), the medial area: the ventral posterior parietal area, the dorsointermediate area, the dorsolateral area, the ventral posterior and ventral anterior areas, the medial superior temporal area, the fundal area of the superior temporal sulcus, the inferior temporal cortex: and frontal cortex in or near the frontal eye field. In squirrel monkeys, both blob and interblob regions of V1 contributed equally to DM, whereas the blob regions provided most of the projections to V1 in owl monkeys. In squirrel monkeys, connections were also found with cortex on the ventral surface in the ventral occipital temporal sulcus. In owl monkeys and squirrel monkeys, connections were with both the upper and lower visual field representations in V1, V2, and MT, demonstrating that DM contains a complete representation of the visual field. These similarities in architecture, connections, and retinotopy argue that DM is a visual area of both owl and squirrel monkeys. (C) 1998 Wiley-Liss, Inc.
In recent years, many new cortical areas have been identified in the macaque monkey. The number of identified connections between areas has increased even more dramatically. We report here on (1) a summary of the layout of cortical areas associated with vision and with other modalities, (2) a computerized database for storing and representing large amounts of information on connectivity patterns, and (3) the application of these data to the analysis of hierarchical organization of the cerebral cortex. Our analysis concentrates on the visual system, which includes 25 neocortical areas that are predominantly or exclusively visual in function, plus an additional 7 areas that we regard as visual-association areas on the basis of their extensive visual inputs. A total of 305 connections among these 32 visual and visual-association areas have been reported. This represents 31% of the possible number of pathways it each area were connected with all others. The actual degree of connectivity is likely to be closer to 40%. The great majority of pathways involve reciprocal connections between areas. There are also extensive connections with cortical areas outside the visual system proper, including the somatosensory cortex, as well as neocortical, transitional, and archicortical regions in the temporal and frontal lobes. In the somatosensory/motor system, there are 62 identified pathways linking 13 cortical areas, suggesting an overall connectivity of about 40%. Based on the laminar patterns of connections between areas, we propose a hierarchy of visual areas and of somato sensory/motor areas that is more comprehensive than those suggested in other recent studies. The current version of the visual hierarchy includes 10 levels of cortical processing. Altogether, it contains 14 levels if one includes the retina and lateral geniculate nucleus at the bottom as well as the entorhinal cortex and hippocampus at the top. Within this hierarchy, there are multiple, intertwined processing streams, which, at a low level, are related to the compartmental organization of areas V1 and V2 and, at a high level, are related to the distinction between processing centers in the temporal and parietal lobes. However, there are some pathways and relationships (about 10% of the total) whose descriptions do not fit cleanly into this hierarchical scheme for one reason or another. In most instances, though, it is unclear whether these represent genuine exceptions to a strict hierarchy rather than inaccuracies or uncertainties in the reported assignment.
It is now well established that monkey extrastriate cortex, the visual cortex beyond primary or striate cortex, contains many different areas (for review, see Van Essen et al., 1992; Felleman and Van Essen, 1991). Of these 30 or so extra-striate areas, a small group in the caudal superior temporal sulcus (STS) stands out because their neurons share the property of direction selectivity, suggesting that these areas might be involved in the analysis of retinal motion and in motion perception. A large number of studies have been devoted to substantiating and clarifying the role of the middle temporal (MT) area, also referred to as V5, and that of its satellites, the dorsal and ventral parts of the medial superior temporal (MST) visual area. Although area MT/V5 was discovered almost simultaneously in macaque monkeys (Zeki, 1969, 1971) and in owl monkeys (Allman and Kaas, 1971) and there are a number of similarities between these areas of the two species, this review will be restricted to the macaque monkey. Indeed, with the passage of time, differences between MT of the two species have become apparent (Sereno and Allman, 1991; Zeki, 1980) and the macaque as a species is closer to the human (Ciochon and Chiarelli, 1980). A further restriction will be that for the physiological studies preference will be given to the more recent, quantitative data. Since the physiology of macaque visual cortex, and particularly of area MT/V5 and its satellites, has been a major source of inspiration for recent human functional imaging work, the homologues of MT/V5 and MST in humans will be briefly discussed.
Because of its distinctive architecture, connections, and functions, primary visual cortex, area 17 or V1 of primates, can be easily identified in most mammals (Kaas, 1987). V1 (also referred to as striate cortex) is particularly distinctive in primates, and, as a result, it was the first cortical area identified histologically (see Gennari, 1782, in Fulton, 1937). V1 of most, if not all, primates has a number of conspicuous features that distinguish this structure from its homologue in other mammals. Unlike carnivores, such as cats and ferrets, almost all of the visual input relayed from the lateral geniculate nucleus (LGN) of primates terminates in V1 (Benevento and Standage, 1982; Bullier and Kennedy, 1983; see Henry, 1991, for review), and lesions of V1 produce a severe deficit known as cortical blindness (e.g., Cowey and Stoerig, 1989). In addition, visual cortex of all primates is activated by physiologically and morphologically distinguishable streams, or channels, of inputs that are relayed from the retina to V1 in a manner unique to primates (Kaas and Huerta, 1988; Casagrande and Norton, 1991). Furthermore, the intrinsic connections of V1 in primates exhibit both vertical (laminar) and areal (modular) distinctions that appear designed to create new output channels from input channels via features of internal circuitry. Finally, the output streams project to visual areas that seem to be organized in a manner unique to primates. In particular, the major cortical target of V1, the second visual area, V2, is composed of three morphologically distinct modules that are differentially activated from V1, and at least one other major target of V1, the middle temporal visual area or MT, appears to be a unique specialization of primates (Kaas and Preuss, 1993). These common features of visual cortex in primates are of particular interest because these specializations relate to vision in humans as well as other primates. In this review, we focus on common features that have been described for V1 across a variety of primate species, and therefore are most likely to be present in most or all primates. In addition, we describe differences in V1 organization across primate groups, since these differences may relate to functional specializations and adaptations in the greatly varied primate order. Features that vary across taxa, when related to behavioral niches, may provide clues as to the significance of variations. Finally, this review briefly compares V1 in primates with V1 in some nonprimates to emphasize the distinctiveness of V1 in primates.
The present review outlines and evaluates theories of how visual cortex is divided into areas in primates. Maps of cortical areas have long been used as guides for further research and they clearly have implications for how information is processed in the visual system. Early maps such as those of Brodmann (1909) and Von Economo (1929) have had great impact on current theories of visual cortex organization, and parts of these early theories remain in use. Yet early investigators disagreed on how extrastriate cortex is subdivided, and the usefulness of the architectonic methods used to formulate early proposals has been repeatedly questioned (e.g., Lashely and Clark, 1946). Current proposals are more complex and include many visual areas. In principle, current proposals should be more accurate because they are based on additional sorts of information, especially patterns of cortical connections and retinotopic organization. Indeed there is widespread agreement on the locations and extent of some proposed fields such as V2 and MT (V5). However, our maps of cortex also differ in many ways, suggesting that the supporting evidence is ambiguous and limited enough to allow different interpretations. As a reflection of this uncertainty, Felleman and Van Essen (1991), after an extensive review and synthesis, conclude that of 32 proposed visual areas, only five rate a high confidence level of 1 on a scale of 1–3. Possibly one might take an even more conservative view, since only three areas (V1, V2, and MT) are components of most proposals. In any case, it seems useful to review the progression from early to recent theories of cortical organization in an effort to see how they evolved and influenced each other, as well as determine both reliable features and those that require further study and evaluation.
One of the most striking aspects of the primate visual cortex is the remarkable extent of internal structure and organization within V 1, and the second visual area, V2. Architecturally, V2 is composed of an interleaved series of bands specialized for the processing of the visual submodalities of form, color, and depth, known as the V2 stripes. The unique position of V2 in the visual hierarchy at the juncture of the higher visual pathways suggests that its segregated functional architecture facilitates the channeling of visual input into these pathways for handling “what” and “where” visual information. Thus the organization and connectivity of V2 perhaps most clearly embodies the notion of parallel and integrated processing of form, color, motion, and stereopsis, as observed psychophysically in studies of human visual performance. In comparison to primary visual cortex V 1, the architecture and functional role of V2 has only recently been studied in earnest. This chapter reviews the current understanding of the modular organization within stripes, the functional properties of V2 stripes, the visual map with respect to the stripes, and the functional connectivity of V2 stripes with other cortical areas.
Area MT (middle temporal) is a well-defined visual representation common to all primates, which shows a clear selectivity to the analysis of visual motion. In the present study we examined the architecture of the intrinsic connections in area MT in an attempt to reveal its organizing principles and its potential relationship to the functional domains in area MT. Intrinsic connections were studied by placing small injections of the tracer biocytin in area MT of seven adult owl monkeys (Aotus nancymae). The injections were targeted at well-defined orientation domains revealed using optical imaging of intrinsic signals. The distribution of axons labeled by these injections was related both to the cytochrome oxidase histochemistry and to the layout of functional domains in area MT and surrounding tissue. Tracer injections in the superficial layers of area MT produced a complex network of extrinsic and intrinsic axonal connections. Clear instances of extrinsic connections were observed between area MT proper and the MT crescent situated postero-medially to it. The intrinsic connections were laterally spread and organized in patch-like clusters with an average distance from injection center to the furthest patch of 1.8 ± 0.55 mm (± SD, n = 9). The overall axonal distribution tended to be anisotropic, i.e. the patches were distributed within an elongated ellipse [average anisotropy ratio: 1.86 ± 0.66 (± SD)] and were asymmetrically distributed about either side of the injection site [average asymmetry ratio: 2.3 ± 0.7 (± SD)]. Finally, there was a tendency for the intrinsic connections to connect to functional domains of similar orientation preference in area MT. However, this tendency varied substantially between individual cases. The highly specific nature of MT lateral connections puts clear constraints on models of surround influences in the receptive fields of MT neurons.
edited by Kathleen S. Rockland, Jon H. Kaas and Alan Peters, 1997. $159.50 (xxi+844 pages) ISBN 0 306 45530 7
On the basis of extracellular recordings in marmoset monkeys, we report on the organisation of the middle temporal area (MT) and the surrounding middle temporal crescent (MTc). Area MT is approximately 5-mm long and 2-mm wide, whereas the MTc forms a crescent-shaped band of cortex 1-mm wide. Neurones in area MT form a first-order representation of the contralateral hemifield, whereas those in the MTc form a second-order representation with a field discontinuity near the horizontal meridian. The representation of the vertical meridian forms the border between area MT and the MTc. In both areas, the fovea is represented ventrocaudally, and the visual field periphery is represented dorsorostrally. Analysis of single units revealed that 86% of cells in area MT show a strong selectivity for the direction of motion of visual stimuli. The proportion of direction-selective cells in the MTc (53%), whereas lower than that in area MT, is much higher than that observed in most other visual areas. Neurones in the cortex immediately rostral to area MT and the MTc are direction selective, with receptive fields predominantly located in the visual field periphery. In contrast, only a minority of the cells in the cortex ventral to the MTc are direction selective, and their receptive fields emphasise central vision. The results suggest that the MTc is functionally closely related to area MT, and distinct from the areas forming the dorsolateral complex. The MTc may have a role in combining information about motion in the visual field, processed by area MT, with information about stimulus shape, processed by the dorsolateral complex. J. Comp. Neurol. 393:505–527, 1998. © 1998 Wiley-Liss, Inc.
The interhemispheric efferent and afferent connections of the V1/V2 border have been examined in the adult macaque monkey with the tracers horseradish peroxidase and horseradish peroxidase conjugated to wheat germ agglutinin. The V1/V2 border was found to have reciprocal connections with the contralateral visual area V1, as well as with three other cortical sites situated in the posterior bank of the lunate sulcus, the anterior bank of the lunate sulcus, and the posterior bank of the superior temporal sulcus.
Within V1, callosal projecting cells were found mainly in layer 4B with a few cells in layer 3. Anterograde labeled terminals were restricted to layers 2, 3, 4B, and 5. In extrastriate cortex, retrograde labeled cells were in layers 2 and 3 and only very rarely in infragranular layers. In the posterior bank of the lunate sulcus, labeled terminals were scattered throughout all cortical layers except layers 1 and 4. In the anterior bank of the lunate sulcus and in the superior temporal sulcus, anterograde labeled terminals were largely focused in layer 4.
Callosal connections in all contralateral regions were organized in a columnar fashion. Columnar organization of callosal connections was more apparent for anterograde labeled terminals than for retrograde labeled neurons. In the posterior bank of the lunate sulcus, columns of callosal connections were superimposed on regions of high cytochrome activity.
The tangential extent of callosal connections in V1 and V2 was found to be influenced by eccentricity in the visual field. Callosal connections were denser in the region of V1 subserving foveal visual field than in cortex representing the periphery. In V1 subserving the fovea, callosal connections extended up to 2 mm from the V1/V2 border and only up to 1 mm in more peripheral located cortex. In area V2 subserving the fovea, cortical connections extended up to 8 mm from the V1/V2 border and only up to 3 mm in peripheral cortex.
We have used physiological and anatomical techniques to address three general issues concerning the topographic organization of the middle temporal visual area (MT) of the macaque monkey. First, we carried out a quantitative analysis of irregularities and asymmetries in the visual representation in MT. This analysis revealed a striking overemphasis on a restricted portion of the visual field that runs obliquely through the inferior contralateral quadrant and largely avoids both the horizontal meridian and the inferior vertical meridian. This corresponds to the portion of the visual field that would be maximally stimulated during visually guided hand movements. Second, the physiologically determined topographic organization of MT was compared to the pattern of callosal inputs in the same hemisphere, which are known to be distributed irregularly within MT. Callosal inputs tended to be densest near the representation of the vertical meridian, but there were numerous exceptions to this trend. Thus, topographic irregularities account for only part of the irregularities in callosal inputs to MT. Finally, comparison of these data with previous reports shows a strong correlation between body weight and the average size of MT. The representation in myeloarchitectonically defined MT was found to include much of the visual periphery, although it is unclear from our data whether this representation is invariably complete.
Previous behavioral studies indicated that the inferior convexity of the temporal lobe in the rhesus monkey functions in relation to the visual system and that this function probably depends on corticocortical connections which link this area to the visual areas. Therefore, in an experimental anatomical study the corticocortical connections of some of the occipital, temporal and frontal areas were investigated in the monkey, by means of the Nauta-Gygax silver impregnation technique. The following findings were obtained. The striate cortex projects to certain parts of a “circumstriate cortical belt” which extends into the caudal bank of the superior temporal sulcus in its upper parts and into the caudal parts of the intraparietal sulcus. This circumstriate belt in turn projects to the inferior convexity of the temporal lobe and to the cortex around the arcuate sulcus of the frontal lobe. The inferior convexity of the temporal lobe in turn projects back to parts of the circumstriate belt and to the lateral and the ventrolateral surface of the frontal lobe.
For staining myelin with silver a physical development technique has been devised that can render visible the thinnest fibers in various animal species, including fishes and reptiles, even in the early phase of myelination and may be applied to both frozen and embedded materials. Its principle is as follows: Myelin can form and bind colloidal silver particles in a 0.1% ammoniacal silver nitrate solution of pH 7.5. The production of metallic silver by other tissue elements is suppressed by the sections pretreated with a 2:1 mixture of pyridine and acetic anhydride for 30 min. The colloidal silver particles bound in the myelin are enlarged to microscopic dimensions by a special physical developer.
Cortical connections within the occipital lobe (areas 17, 18 and 19) of the rhesus monkey are investigated with the autoradiographic and horseradish peroxidase procedures. Two efferent systems, each with a specific laminar organization, are observed. (1) Rostrally directed connections, from area 17 to 18, area 18 to 19 and area 19 to the inferotemporal region (area TE), originate from neurons in layer IIIc (and, in area 19, from a small complement of neurons in layer Va), and terminate in and around layer IV. (2) In contrast, connections in the reverse direction ('caudally directed' connections), from area TE to 19, area 19 to 18, and area 18 to 17, originate from neurons in layers Vb, VI and, to a lesser extent, IIIa, and terminate mainly in layer I. In addition, the laminar organization of several intrinsic and callosal connections are observed. In trinsic connections within areas 18 and 19 originate from neurons in layers IIIc and, to a lesser extent, Va, and terminate in vertical bands in layers I to IV. Callosal connections from areas 18, 19, and the caudal inferotemporal region originate from neurons mainly in layer IIIc. From areas 18 and 19, these callosal connections terminate in vertical bands in layers I through IV. Thus, different cortical projection systems are characterized by specific laminar distributions of efferent terminations as well as of their neurons of origin.
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.
Efferent cortical projections of posterior parietal cortex were determined by degeneration and autoradiographic methods in owl monkeys. Intraregional connections were to the immediate surround of the injection or lesion site, and to distinct foci within the posterior parietal region. The extraregional ipsilateral connections were with (1) previously established subdivisions of visual association cortex (the Dorsomedial Area, the Medial Area, the Dorsolateral Area, and the Middle Temporal Area), (2) other locations in caudal neocortex, and (3) frontal cortex. The callosal projections were to separate foci in posterior parietal cortex of the contralateral cerebral hemisphere. The separate foci of both ipsilateral and contralateral terminations in posterior parietal cortex raise the possibility that this region contains more than one functional subdivision. The connections with visual association cortex suggest a role for parietal cortex in visual behavior. Other foci in caudal neocortex indicate the possible locations of additional subdivisions of association cortex.
With the aid of the techniques of tracing axonal pathways by anterograde fiber degeneration, and by anterograde (autoradiography) and retrograde (HRP-histochemistry) axoplasmic transport, it could be shown that area 17 projects in a topographically and visuotopically organized manner onto the temporal visual area MT. The fibers of this association system originate from pyramidal cells in layer IIIc, and from the solitary cells of Meynert; they terminate in layers IV and III of area MT. A correspondingly organized system of countercurrent fibers originates from pyramidal cells in layers III/II and V/VI of area MT and terminates separately in layers VI, IIIc and I of area 17.
Efferent and afferent connections of primary visual cortex, Area 17, were determined in a prosimian, Galago senegalensis, by autoradiographic methods after injections of 3H-proline or 3H-HRP. The cortical connections of Area 17 with Areas 18 and MT were homotopic and reciprocal. Projections from Area 17 terminated largely in layer IV and somewhat in layer III of both Areas 18 and MT. Most of the cells projecting to Area 17 were located in layer V of Area 18 and layer VI of MT. Subcortical projections included the reticular nucleus of the thalamus, where columns of label corresponding to injection sites were found in the caudal fourth of the nucleus. Projections to the lateral geniculate nucleus were along lines of isorepresentation and were in register with the cells projecting back to the injection site. The parvocellular layers were less densely labeled than other layers by the transport of 3H-proline, while concentrations of label were noted on the dorsal and ventral margins of the nucleus and in interlaminar regions between the internal parvocellular and magnocellular layers and between the two magnocellular layers. The pattern of terminations in the pulvinar complex suggested functional subdivisions. We have divided the inferior pulvinar into a large central nucleus, IPc, with topologically organized input from Area 17; a smaller medial nucleus, IPm, with a second pattern of input from Area 17; and a dorso-posterior nucleus, IPp, without input from striate cortex. The superior pulvinar likewise appears to have several subdivisions. One of these, a "central" nucleus of the superior pulvinar, SPc, receives topologically organized projections from Area 17. SPc is about the same size as IPc and is organized as a mirror image of IPc. Thus, both IPc and SPc represent the lower visual quadrant medially and the upper visual quadrant laterally; central vision is represented along the common border for both nuclei, while peripheral vision is represented dorsorostrally in SPc and ventrocaudally in IPc. Finally, the superficial grey of the superior colliculus receives topologically organized input from Area 17.
Efferent projections from the dorsomedial visual area (DM) in the owl monkey to other portions of visually responsive cortex were determined by degeneration and autoradiograhic methods of demonstrating axon pathways. The most prominent ipsilateral pathway was to posterior parietal cortex (PP) just medial to the terminal portion of the Sylvian fissure. Other ipsilateral projections were to subdivisions of the temporal lobe, the middle temporal visual area (MT) and the surrounding dorsolateral crescent (DL), to regions just rostral to area 18 on the medial wall of the cerebral hemisphere, and to the upper bank of the Sylvian fissure. The callosal projections of DM were to DM, PP, and MT of the opposite cerebral hemisphere. The results support the notion that visual association cortex consists of a number of separate, but complexly interrelated, subdivisions. The efferents to posterior parietal cortex suggest the possibility of an area for the integration of somatosensory and visual information.
In the owl monkey, microelectrode mapping of Brodmann's area 19 indicates that this region contains part or all of at least 5 separate representations of the visual field, each of which adjoins the anterior border of V II and collectively are termed the third tier of cortical visual areas (V I is the first tier; V II is the second tier). Described in detail in this report is one of the third tier areas which is located on the dorsal surface and the adjacent medial wall of the occipital lobe and corresponds to a densely myelinated zone of cortex. In this dorsomedial area (DM), the representation of the horizontal meridian is partially split, and thus, like V II (see ref. 4) and the dorsolateral crescent5, DM is a second order transformation of the visual hemifield. In one abnormal owl monkey, a portion of the upper quadrant was represented twice in DM. This abnormal case may provide some clues as to how the normal pattern of visuotopic organization is established in the developing brain.
Investigations of monosynaptic connections in the central nervous system have been hindered by the lack of compatible markers that can be used at both light and electron microscopic levels. In attempts to determine synaptic contacts between fibers originating in the substantia nigra and neurons projecting to the spinal cord, we have developed a double immunolabeling technique using anterograde transport of Phaseolus vulgaris leucoagglutinin (PHA-L) and retrograde transport of unconjugated cholera toxin subunit B (CTB). In this report, we describe technical modifications which consistently produced superior labeling together with adequate ultrastructural preservation of the tissue and discuss the advantages of the two tracers.
A number of fluorescent dextrans were screened for axonal transport properties within the rat CNS. One compound, Fluoro-Ruby (FR), was found to be particularly sensitive for demonstrating retrograde and particularly anterograde axonal transport. The tracer may be either pressure or iontophoretically injected, and the fixed tissue can be examined without histochemical processing. The technique can be combined with a wide variety of other neuroanatomical methods.
A region of dorsal cortex along the rostral border of V II has been described as comprising a visual area or areas separate from more lateral cortex in both New and Old World primates. To evaluate these possibilities in squirrel monkeys, we studied patterns of cortical connections by injecting Fast Blue, Fluoro-Gold, horseradish peroxidase, and wheat germ agglutinin conjugated to horseradish peroxidase into the dorsal region and related results to distinctions in myeloarchitecture. Our major conclusions are as follows. 1) The dorsal region (D) has distinctly different connections from the area found laterally, the caudal subdivision of the dorsolateral area (DLC). These include major connections with the rostral subdivision of the dorsolateral area (DLR), ventral posterior parietal cortex in the Sylvian fissure, the middle temporal area (MT), the medial superior temporal area (MST), ventral cortex just rostral to V II, and cortex in the inferior temporal sulcus. Weaker connections are with V I, V II, DLC, the fundal superior temporal area (FST), and the frontal lobe. In contrast, DLC has strong connections with V II and inferior temporal (IT) cortex, weaker connections with DLR, and lacks connections with ventral posterior parietal cortex (Steele et al: J Comp Neurol 306:495-520, 1991). 2) Caudal and rostral aspects of dorsal cortex differ in the magnitude of connections with V I, V II, DLR, and FST. These differences are consistent with the previous proposal that at least two visual areas, caudal and rostral, occupy the dorsal region in squirrel monkeys (Krubitzer and Kaas: Visual Neurosci 5:165, 1990), but they could also reflect regional differences in the connections of a single visual area. 3) The dorsal region is more densely myelinated than surrounding cortex; however, rostral aspects of dorsal cortex are less myelinated than caudal aspects, again suggesting the existence of at least two areas. 4) The distinctiveness of connections between dorsal cortex and rostral as compared to caudal dorsolateral cortex provides further evidence for dividing the region of DL into two visual areas, DLC and DLR (Cusick and Kaas: Visual Neurosci 1:211, 1988; Steele et al: J Comp Neurol 306:495-520, 1991).
Evidence suggests that all primates have rostral and caudal subdivisions in the region of visual cortex identified as the dorsolateral area (DL) or V4. However, the connections of DL/V4 have not been examined in terms of these subdivisions. To determine the cortical connections of the caudal subdivision of DL (DL c ) in squirrel monkeys, injections of the neuroanatomical tracers wheat germ agglutinin conjugated to horseradish peroxidase, Diamidino Yellow, and Fluoro‐Gold were made in cortex rostral to V II. To aid in delineating the borders of DL C , cortex was also evaluated architectonically.
Based on similar patterns of connections, DL C extends from dorsolateral to ventrolateral cortex. DL C receives strong, feedforward input from V II and projects in a feedforward fashion to the rostral subdivision of DL (DL R ) and caudal inferior temporal (IT) cortex, including a separate location in the inferior temporal sulcus. DL C has weaker connections with V I, the middle temporal area (MT), cortex rostral to MT in the location of the fundal superior temporal area (FST), cortex dorsal to DL C , ventral cortex‐rostral to V II, and cortex in the frontal lobe, lateral to the inferior arcuate sulcus. Only lateral DL C has connections with V I, and only dorsolateral DL C has connections with cortex dorsal to DL C . The topographic organization of DL C was inferred from its connections with V II. Thus, dorsolateral DL C represents the lower field, lateral DL C represents central vision, and ventrolateral DL C represents the upper field.
Limited observations were made on DL R . Confirming earlier observations (Cusick and Kaas: Visual Neurosci. 1:211, 1988), DL R is paler than DL C myeloarchitectonically. DL R receives only sparse feedforward input from V II, but stronger input from DL C . DL R has strong connections with cortex just rostral to dorsal V II, ventral posterior parietal cortex in the sylvian fissure, MT, the medial superior temporal area, FST, and the inferior temporal sulcus. DL R also shares connections with IT cortex. Thus, while both DL C and DL R are involved in the pathway relaying visual information to IT cortex, an area specialized for object vision, DL R also projects densely to areas such as MT involved in the pathway relaying to posterior parietal cortex, a region specialized for spatial localization and motion perception.
In recent years, many new cortical areas have been identified in the macaque monkey. The number of identified connections between areas has increased even more dramatically. We report here on (1) a summary of the layout of cortical areas associated with vision and with other modalities, (2) a computerized database for storing and representing large amounts of information on connectivity patterns, and (3) the application of these data to the analysis of hierarchical organization of the cerebral cortex. Our analysis concentrates on the visual system, which includes 25 neocortical areas that are predominantly or exclusively visual in function, plus an additional 7 areas that we regard as visual-association areas on the basis of their extensive visual inputs. A total of 305 connections among these 32 visual and visual-association areas have been reported. This represents 31% of the possible number of pathways if each area were connected with all others. The actual degree of connectivity is likely to be closer to 40%. The great majority of pathways involve reciprocal connections between areas. There are also extensive connections with cortical areas outside the visual system proper, including the somatosensory cortex, as well as neocortical, transitional, and archicortical regions in the temporal and frontal lobes. In the somatosensory/motor system, there are 62 identified pathways linking 13 cortical areas, suggesting an overall connectivity of about 40%. Based on the laminar patterns of connections between areas, we propose a hierarchy of visual areas and of somatosensory/motor areas that is more comprehensive than those suggested in other recent studies. The current version of the visual hierarchy includes 10 levels of cortical processing. Altogether, it contains 14 levels if one includes the retina and lateral geniculate nucleus at the bottom as well as the entorhinal cortex and hippocampus at the top. Within this hierarchy, there are multiple, intertwined processing streams, which, at a low level, are related to the compartmental organization of areas V1 and V2 and, at a high level, are related to the distinction between processing centers in the temporal and parietal lobes. However, there are some pathways and relationships (about 10% of the total) whose descriptions do not fit cleanly into this hierarchical scheme for one reason or another. In most instances, though, it is unclear whether these represent genuine exceptions to a strict hierarchy rather than inaccuracies or uncertainities in the reported assignment.
The distribution and differential staining patterns of cytochrome oxidase (CO) activity in visual cortical areas have provided useful anatomical markers for the modular organization of area 17 (striate cortex) and area 18 in primates. In macaque and squirrel monkeys, previous studies have shown that the majority of cells that lie in areas of high CO activity are color selective, are nonoriented, and project to adjacent zones of high CO activity in area 17 and to stripes of high CO activity in area 18. By contrast, most cells in zones with weak CO activity in area 17 have relatively narrow orientation tuning and are not color selective (Livingstone and Hubel: J. Neurosci. 4:309‐356, 2830‐2835, '84; 7:3371‐3377, '87). The periodic organization of CO activity in area 17, the „blobs,”︁ and the stripe‐like organization in area 18 thus seem to define visual cortical processing modules and/or channels in primates. We have investigated the organization of CO activity in areas 17 and 18 in two species of nocturnal prosimian primates[ Galago crassicaudatus (GCC) and Galago senegalensis (GSS)] in order to evaluate CO staining patterns in primates that have been reported to possess almost exclusively rod retinae and no color vision.
In area 17 of both species, our results show that, as in diurnal and nocturnal simian primates, the darkest CO staining occurs in layers III and IV, with clear periodicity in layer III (i.e., CO blobs) and homogeneous staining in layer IVβ, the cortical recipient sublayer of the geniculate parvocellular layers. In GCC, individual blobs in layer III appear to be larger and less frequent than has been reported for the macaque monkey. Unlike simian primates, both galago species exhibit clear CO periodicities within layer IVα, the cortical recipient sublayer of the magnocellular geniculate layers. In addition, faint CO periodicities are apparent in layer VI and scattered large darkly CO stained pyramidal cells are visible throughout layer V.
Quantitative analysis suggests that CO periodicities are more frequent in GSS than in GCC, suggesting that there may be evolutionary pressure to maintain the same number of CO modules within the smaller striate cortex of the lesser galago, although this is not the trend found across distantly related species.
CO activity in area 18 is less well‐developed than reported in other primates. In fact, we could not reliably identify discontinuities in CO staining in area 18 of GSS. Instead, where present, discontinuities in CO staining in area 18 of GCC appear as faint regularly spaced patches.
Taken together, these results suggest underlying similarities in the basic features of primate cortical organization as revealed by CO staining. There are nonetheless some differences in the distribution of CO activity in visual cortex acros primate species. Thus, given species variation in visual niche requirements including differential dependence on color vision, it seems unlikely that CO blobs have evolved as a strictly color channel in all primates.
The visual receptive field physiology and anatomical connections of the lateral intraparietal area (area LIP), a visuomotor area in the lateral bank of the inferior parietal lobule, were investigated in the cynomolgus monkey ( Macaca fascicularis ). Afferent input and physiological properties of area 5 neurons in the medial bank of the intraparietal sulcus (i.e., area PEa) were also determined. Area LIP is composed of two myeloarchitectonic zones: a ventral zone (LIPv), which is densely myelinated, and a lightly myelinated dorsal zone (LIPd) adjacent to visual area 7a. Previous single‐unit recording studies in our laboratory have characterized visuomotor properties of area LIP neurons, including many neurons with powerful saccade‐related activity. In the first part of the present study, single‐unit recordings were used to map visual receptive fields from neurons in the two myeloarchitectonic zones of LIP. Receptive field size and eccentricity were compared to those in adjacent area 7a. The second part of the study investigated the cortico‐cortical connections of area LIP neurons using tritiated amino acid injections and fluorescent retrograde tracers placed directly into different rostrocaudal and dorsoventral parts of area LIP. The approach to area LIP was through somatosensory area 5, which eliminated the possibility of diffusion of tracers into area 7a.
Unlike many area 7a receptive fields, which are large and bilateral, area LIP receptive fields were much smaller and exclusively confined to the contralateral visual field. In area LIP, an orderly progression in visual receptive fields was evident as the recording electrode moved tangentially to the cortical surface and through the depths of area LIP. The overall visual receptive field organization, however, yielded only a rough topography with some duplications in receptive field representation within a given rostrocaudal or dorsoventral part of LIP. The central visual field representation was generally located more dorsally and the peripheral visual field more ventrally within the sulcus. The lower visual field was represented more anteriorly and the upper visual field more posteriorly. In LIP, receptive field size increased with eccentricity but with much variability within the sample.
Area LIPv was found to have reciprocal cortico‐cortical connections with many extrastriate visual areas, including the parieto‐occipital visual area PO; areas V3, V3A, and V4; the middle temporal area (MT); the middle superior temporal area (MST); dorsal prelunate area (DP); and area TEO (the occipital division of the intratemporal cortex). Area LIPv is also connected to area TF in the lateral posterior parahippocampal gyrus. Although area LIPd has many of the same cortico‐cortical connections as LIPv, some differences were apparent. Area LIPd and not LIPv has connections with visual areas TEa and TEm (anterior and medial divisions of the intratemporal cortex) and with multimodal area IPa (subdivision of association cortex in caudal bank of superior temporal cortex) in the superior temporal sulcus. A topographic relationship between rostrocaudal parts of area LIP (including both LIPv and LIPd) and the lateromedial parts of prefrontal cortex across areas 8a (frontal eye fields) and the medial portion of area 46 was also apparent. Intrinsic connections of LIP with other areas in the inferior parietal lobule included a feedforward projection to area 7a and connections with the bimodal ventral intraparietal area (VIP) as well as with somatosensory area 7b (PF). Some retrogradely labeled cells were seen in area 5, but this projection was not confirmed by control injections placed in the medial bank of the intraparietal sulcus (area PEa). An interesting observation was that the input into areas PEa and LIP from parieto‐occipital visual areas (medial dorsal parietal area (blDPl and area PO) was found to be topographically organized such that MDP and the dorsal part of PO project to area PEa, while ventral PO and a few MDP neurons project to the opposite bank in LIP. This “visual” input to area PEa was also seen in single‐unit recordings in area 5 in wlhich a small number of visually responsive cells were identified Le., 7 of 204 neurons). All remaining neurons mapped in area 5 were highly responsive to joint position, movement, and/or touch.
These anatomical and physiological data demonstrate that area LIP is a unique visual area in posterior parietal cortex, with histological, anatomical, and physiological properties different from other areas in the inferior parietal lobule. Analysis of feedforward and feedback projections suggests that area LIP occupies a high position in the overall hierarchy of extrastriate visual processing areas in the macaque brain.
Cortical connections were investigated by restricting injections of WGA-HRP to different parts of the middle temporal visual area, MT, in squirrel monkeys, owl monkeys, marmosets, and galagos. Cortex was flattened and sectioned tangentially to facilitate an analysis of the areal patterns of connections. In the experimental cases, brain sections reacted for cytochrome oxidase (CO) or stained for myelin were used to delimit visual areas of occipital and temporal cortex and visuomotor areas of the frontal lobe. Major findings are as follows: (1) The architectonic analysis suggests that in addition to the commonly recognized visual fields, area 17 (V-I), area 18 (V-II), and MT, all three New World monkeys and prosimian galagos have visual areas DL, DI, DM, MST, and FST. (2) Measurements of the size of these areas indicate that about a third of the neocortex in these primates is occupied by the eight visual areas, but they occupy a somewhat larger proportion of neocortex in the diurnal marmosets and squirrel monkeys than the nocturnal owl monkeys and galagos. The diurnal primates also have proportionally more neocortex devoted to areas 17, 18, and DL and less to MT. These differences are compatible with the view that diurnal primates are more specialized for detailed object and color vision. (3) In all four primates, restricted locations in MT receive major inputs from short meandering rows of neurons in area 17 and several bands of neurons in area 18. (4) Major feedforward projections of MT are to two visual areas adjoining the rostral half of MT, areas MST and FST. Other ipsilateral connections are with DL, DI, and in some cases DM, parts of inferotemporal (IT) cortex, and posterior parietal cortex. (5) In squirrel monkeys, where injection sites varied from caudal to rostral MT, caudal parts of MT representing central vision connect more densely to DL and IT than other parts. Both DL and IT cortex emphasize central vision. (6) In the frontal lobe, MT has dense connections with the frontal ventral area (FV), but not with the frontal eye field (FEF). (7) Callosal connections of MT are most dense with matched locations in MT of the other hemisphere, rather than with the outer boundary of MT representing the vertical meridian. Targets of sparser callosal connections include FST, MST, and DL.(ABSTRACT TRUNCATED AT 400 WORDS)
To identify the cortical connections of the medial superior temporal (MST) and fundus of the superior temporal (FST) visual areas in the extrastriate cortex of the macaque, we injected multiple tracers, both anterograde and retrograde, in each of seven macaques under physiological control. We found that, in addition to connections with each other, both MST and FST have widespread connections with visual and polysensory areas in posterior prestriate, parietal, temporal, and frontal cortex. In prestriate cortex, both areas have connections with area V3A. MST alone has connections with the far peripheral field representations of V1 and V2, the parieto-occipital (PO) visual area, and the dorsal prelunate area (DP), whereas FST alone has connections with area V4 and the dorsal portion of area V3. Within the caudal superior temporal sulcus, both areas have extensive connections with the middle temporal area (MT), MST alone has connections with area PP, and FST alone has connections with area V4t. In the rostral superior temporal sulcus, both areas have extensive connections with the superior temporal polysensory area (STP) in the upper bank of the sulcus and with area IPa in the sulcal floor. FST also has connections with the cortex in the lower bank of the sulcus, involving area TEa. In the parietal cortex, both the central field representation of MST and FST have connections with the ventral intraparietal (VIP) and lateral intraparietal (LIP) areas, whereas MST alone has connections with the inferior parietal gyrus. In the temporal cortex, the central field representation of MST as well as FST has connections with visual area TEO and cytoarchitectonic area TF. In the frontal cortex, both MST and FST have connections with the frontal eye field.
Subunit B of cholera toxin was used as a tracer substance in the central nervous system after being injected into various brain regions, mainly somatosensory relay structures. The tracer was localized with an immunoperoxidase technique, using monoclonal antibodies raised in mouse hybridomas. This method, which is applicable in both light and electron microscopic studies, is characterized by high contrast between specific labeling and unspecific background activity. It yields excellent retrograde labeling of the dendritic tree and is thus suitable for studying the neuronal cytoarchitecture and, on the ultrastructural level, the synaptic organization of identified projection neurons.
Patterns of cortical connections were studied in brain sections cut parallel to the surface of mechanically flattened cortex after single, double, or multiple injections of wheatgerm agglutinin conjugated to horseradish peroxidase (WGA-HRP) in area 17 of galagos (Galago crassicaudatus). Intrinsic connections of area 17 included a systematic pattern of patches of labeled cells and terminations associated with blobs of high cytochrome oxidase activity. The patches of connections extended with decreasing density for a distance of 2 mm or more from the margins of injection sites. Injections also revealed dense interconnections with area 18 (V-II) and the middle temporal visual area (MT). Single injections in area 17 produced several foci of label in both area 18 and MT, suggesting that a given location in area 17 is interconnected with subsets of processing modules in both of these fields. Injections including dorsolateral area 17 also labeled cortex between area 18 and MT. Finally, most injections in area in the temporal lobe.
The brain is composed of a heterogeneous population of neurons whose physiological characteristics often elude morphological identification. The tight coupling between neuronal activity and oxidative energy metabolism forms the basis for the use of cytochrome oxidase as an endogenous metabolic marker for neurons. In the past decade, cytochrome oxidase histo- and cytochemistry have provided a window to view the regional, cellular and subcellular functional diversity among neurons. These methods have shown that the entire neuron is often not metabolically homogeneous; most of the oxidative activity is usually found in dendrites. They have also revealed the dynamic metabolic responses of developing and mature neurons to altered functional demands.
The representation of the visual field in the dorsal portion of the superior temporal sulcus (ST) was studied by multiunit recordings in eight Cebus apella , anesthetized with N 2 O and immobilized with pancuronium bromide, in repeated recording sessions. On the basis of visuotopic organization, myeloarchitecture, and receptive field size, area MT was distinguished from its neighboring areas.
MT is an oval area of about 70 mm ² located mainly in the posterior bank of the superior temporal sulcus. It contains a visuotopically organized representation of at least the binocular visual field. The representation of the vertical meridian forms the dorsolateral, lateral, and ventrolateral borders of MT and that of the horizontal meridian runs across the posterior bank of ST. The fovea is represented at the lateralmost portion of MT, while the retinal periphery is represented medially.
The representation of the central visual field is magnified relative to that of the periphery in MT. The cortical magnification factor in MT decreases with increasing eccentricity following a negative power function. Receptive field size increases with increasing eccentricity. A method to evaluate the scatter of receptive field position in multiunit recordings based on the inverse of the magnification factor is described. In MT, multiunit receptive field scatter increases with increasing eccentricity.
As shown by the Heidenhain‐Woelcke method, MT is coextensive with two myeloarchitectonically distinct zones: one heavily myelinated, located in the posterior bank of ST, and another, less myelinated, located at the junction of the posterior bank with the anterior bank of ST.
At least three additional visual zones surround MT: DZ, MST, and FST. The areas of the dorsal portion of the superior temporal sulcus in the diurnal New World monkey Cebus are comparable to those described for the diurnal Old World monkey, Macaca. This observation suggests that these areas are ancestral characters of the simian lineage and that the differences observed in the owl monkey may be secondary adaptations to a nocturnal ecological niche.
1. Among the multiple extrastriate visual areas in monkey cerebral cortex, several areas within the superior temporal sulcus (STS) are selectively related to visual motion processing. In this series of experiments we have attempted to relate this visual motion processing at a neuronal level to a behavior that is dependent on such processing, the generation of smooth-pursuit eye movements. 2. We studied two visual areas within the STS, the middle temporal area (MT) and the medial superior temporal area (MST). For the purposes of this study, MT and MST were defined functionally as those areas within the STS having a high proportion of directionally selective neurons. MST was distinguished from MT by using the established relationship of receptive-field size to eccentricity, with MST having larger receptive fields than MT. 3. A subset of these visually responsive cells within the STS were identified as pursuit cells--those cells that discharge during smooth pursuit of a small target in an otherwise dark room. Pursuit cells were found only in localized regions--in the foveal region of MT (MTf), in a dorsal-medial area of MST on the anterior bank of the STS (MSTd), and in a lateral-anterior area of MST on the floor and the posterior bank of the STS (MST1). 4. Pursuit cells showed two characteristics in common when their visual properties were studied while the monkey was fixating. Almost all cells showed direction selectivity for moving stimuli and included the fovea within their receptive fields. 5. The visual response of pursuit cells in the several areas differed in two ways. Cells in MTf preferred small moving spots of light, whereas cells in MSTd preferred large moving stimuli, such as a pattern of random dots. Cells in MTf had small receptive fields; those in MSTd usually had large receptive fields. Visual responses of pursuit neurons in MST1 were heterogeneous; some resembled those in MTf, whereas others were similar to those in MSTd. This suggests that the pursuit cells in MSTd and MST1 belong to different subregions of MST.
We have identified the cortical connections of area MT and determined their topographic organization and relationship to myeloarchitectural fields. Efferents of MT were examined in seven macaques that had received injections of tritiated amino acids, and afferents were examined in one macaque that had received injections of two fluorescent dyes. The injection sites formed an orderly sequence from the representation of central to that of peripheral vision in the upper and lower visual fields.
In addition to connections with the striate cortex (V1), connections were found between MT and a variety of extrastriate areas, including V2, V3, V3A, V4, V4t, VIP, MST, FST, possibly PO, and, finally, the frontal eye field. The connections of MT with V1, V2, and the dorsal and ventral portions of V3 were topographically organized and consistent with the visuotopic arrangement reported previously in these areas. V2 could be distinguished from V3 by the distinctive myeloarchitectural appearance of the former.
Connections with areas V4 and V4t also displayed at least a coarse visuotopic organization, in that the central representation of MT projected laterally in these areas and the peripheral representation projected medially. The lower visual field representation of V4 was located dorsally, on the prelunate convexity, while the upper field representation was located primarily on the ventral aspect of the hemisphere. V4t had a distinctively light myeloarchitecture and received projections from only the lower field representation of MT.
The remaining connections of MT were with areas located entirely in the dorsal half of the hemisphere. There were widespread connections with areas MST and FST in the superior temporal sulcus, with some evidence for a crude visuotopic organization in MST. Connections were also found with area VIP in the intraparietal sulcus, with area V3A on the annectent gyrus, possibly with area PO in the dorsomedial prestriate cortex, and, finally, with the frontal eye field on the anterior bank of the lower limb of the arcuate sulcus. Area FST and parts of both MST and VIP had a distinctive myeloarchitecture.
The pattern of laminar connections with V1, V2, and V3 indicated that MT projects “back” to these areas and they project “forward” to MT. That is, the projections to these areas from MT terminated in both the supragranular and infragranular layers and the projections to MT from these areas originated predominantly from cells located above granular layer IV (above layer IVC in V1). The pattern of laminar connections with V3A, V4, V4t, and PO was of the “intermediate” type in that the projections from MT to these areas were spread almost evenly across the layers, including layer IV, and the projections to MT originated (in the case of area V4) from cells in both the infragranular and supragranular layers. Finally, the pattern of laminar connections with MST, FST, and VIP indicated that MT projects “forward” to these areas and they project “back” to MT. That is, the projections from MT terminated heavily in layer IV in these areas and the projections from these areas to MT originated primarily from cells in the infragranular layers. The connections of MT indicate that this area plays a major role in the relay of visual information from the striate cortex into the parietal lobe.
Anatomical and physiological evidence indicates that, in addition to area MT, much of the cortex in the caudal superior temporal sulcus (STS) of the macaque has visual functions. Yet the organization of areas outside of MT remains unclear, and there are even conflicting data on the boundaries of MT itself. To examine these issues, we recorded from neurons throughout this region in three monkeys. Anterograde or retrograde tracers were injected into MT at the conclusion of recording to identify its projection fields. Based on differences in their visuotopic organization, neuronal properties, receptive field size, myeloarchitecture, and pattern of connections with MT, several visual areas were distinguished within the caudal STS.
Area MT, defined as the heavily myelinated portion of the striate (VI) projection zone in STS, contained a systematic representation of only about the central 30°–40° of the contralateral field. The far peripheral field was represented medial to MT in MTp, which we had previously found receives projections from far peripheral V1 and V2 (Ungerleider and Desimone: J. Comp. Neurol 248 :147–163, 1986). Like MT, MTp contained a high proportion of directionally selective cells, and receptive field size in MTp was the size expected of MT fields if the latter were to extend into the periphery.
Areas MST (medial superior temporal) and PP (posterior parietal) were found medial to MT and MTp. Both MST and PP had a high proportion of directionally selective cells, but only MST received a direct projection from MT. Cells in MST had larger receptive fields than those in either MT or MTp butnonetheless displayed a crude visuotopic organization. Receptive fields of cells in PP were even larger, some including the entire contralateral visual field. Furthermore, unlike cells in MST, some in PP responded to auditoryor somesthetic stimuli in addition to visual stimuli.
Area FST, which has a distinctive myeloarchitecture, was found anterior to MT in the fundus of the STS, for which it is named. FST received a direct projection from MT, but only about a third of its cells were directionally selective. Receptive fields of cells in FST were large, often included the center of gaze, and often crossed into the ipsilateral visual field.
Area V4t (transitional V4) and a portion of V4 were found lateral to MT within the STS, and both received direct projections from MT. V4t has a distinctive, light myelination. Both areas had a low incidence of directionally selective cells, and both contained coarse representations of the lower visual field.
The neuronal properties of areas in the caudal STS suggest that MT, MTp, MST, and PP, together with the superior temporal polysensory area, constitute a cortical system for motion analysis. At successive stages in this system, neurons appear to integrate motion information over an increasingly large portion of the retina, respond selectively to more complex types of motion, and respond to inputs from additional sensory modalities.
The dorsolateral visual area (DL) is one of a number of visual areas that have been defined by electrophysiological mapping procedures and cortical architecture in the extrastriate cortex of owl monkeys. The projections of DL were determined by the intra-axonal transport of 3H-proline, 3H-acetyl-wheat germ agglutinin, and horseradish peroxidase after cortical injections. The major ipsilateral projection of DL defined a new subdivision of the visual cortex in owl monkeys, the caudal inferior temporal cortex. Single injections in DL sometimes produced label in two separate regions in the caudal inferior temporal cortex, suggesting that functional subdivisions exist in this projection zone. Other targets of DL included the region of the frontal eye fields, the dorsomedial visual area, the dorsointermediate visual area (DI), a region of the cortex rostral to DI which we call the temporoparietal cortex, and possibly the ventral (V) and posterior parietal areas. A major feedback projection of DL was to V-II. Projections from DL to V-II and the dorsomedial visual area were roughly retinotopic. Projections from DL to the contralateral cerebral hemisphere were to DL and the inferior temporal cortex. Overall, the results support the concept that a major relay of visual information proceeds from V-I to V-II to DL and then to the inferior temporal cortex. In addition, similarities in connection patterns of DL in owl monkeys and V4 in macaque monkeys suggest that DL and much or all of V4 are homologous.
Injections of the retrograde tracer HRP into the border region of the temporal visual area MT and adjoining cortex in Callithrix labeled pyramidal neurons in area 17 of the contralateral hemisphere. Evidence is presented that this newly discovered heterotopic callosal projection of the monkey striate cortex connects regions of representation of the zero vertical meridian of the visual field in a retinotopic order.