Retrograde analyses of spinothalamic projections in the macaque monkey: input to the ventral lateral nucleus. J Comp Neurol

Atkinson Research Laboratory, Barrow Neurological Institute, Phoenix, Arizona 85013, USA.
The Journal of Comparative Neurology (Impact Factor: 3.23). 06/2008; 508(2):315-28. DOI: 10.1002/cne.21672
Source: PubMed


The distribution of retrogradely labeled spinothalamic tract (STT) neurons was analyzed in monkeys following variously sized injections of cholera toxin subunit B (CTb) in order to determine whether different STT termination sites receive input from different sets of STT cells. This report focuses on STT input to the ventral lateral nucleus (VL), where prior anterograde tracing studies identified dense or moderately dense STT terminations. Large and very large injections in VL produced large numbers of labeled cells predominantly in laminae V and VII (more than half as many as from massive injections in the entire thalamus). Medium-sized and small injections in VL labeled STT cells almost exclusively in laminae V and VII, in segments consistent with the coarse mediolateral VL topography; few or no cells were labeled in lamina I. All injections labeled the deep cerebellar nuclei (see accompanying article: Evrard and Craig, 2008). Notably, even the most anterior injection in VL that produced dense pallidal labeling still labeled both STT and deep cerebellar cells. These observations indicate that VL receives STT input originating from laminae V and VII neurons that may be coextensive with its cerebellothalamic input. These findings support the role of laminae V and VII STT cells in sensorimotor integration and suggest a significant ongoing influence on both motor and premotor thalamocortical function. Together with the preceding observations of selective STT projections to other thalamic regions, these results provide compelling evidence that the primate STT consists of anatomically and functionally differentiable components.

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    • "Proprioceptive reafference to precentral motor cortex (not shown) is conveyed via the spinothalamic tract, which projects to the motor thalamus (the ventral lateral posterior thalamic nucleus, VLp) 3 and then to primary motor cortex (Stepniewska et al. 2003). Retrograde tracing techniques show that the origin of spinothalamic inputs to VLp are separate clusters of interneurons sited in layers V and VII of the spinal grey matter (Craig 2008). Both groups are thought to integrate primary afferent sensory signals with descending motor signals—layers V and VII processing cutaneous and proprioceptive signals, respectively—which Craig succinctly summarises as an ascending projection ''conveying activity that represents the state of the segmental interneuronal pools that are used for motor control''. "
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    ABSTRACT: The descending projections from motor cortex share many features with top-down or backward connections in visual cortex; for example, corticospinal projections originate in infragranular layers, are highly divergent and (along with descending cortico-cortical projections) target cells expressing NMDA receptors. This is somewhat paradoxical because backward modulatory characteristics would not be expected of driving motor command signals. We resolve this apparent paradox using a functional characterisation of the motor system based on Helmholtz's ideas about perception; namely, that perception is inference on the causes of visual sensations. We explain behaviour in terms of inference on the causes of proprioceptive sensations. This explanation appeals to active inference, in which higher cortical levels send descending proprioceptive predictions, rather than motor commands. This process mirrors perceptual inference in sensory cortex, where descending connections convey predictions, while ascending connections convey prediction errors. The anatomical substrate of this recurrent message passing is a hierarchical system consisting of functionally asymmetric driving (ascending) and modulatory (descending) connections: an arrangement that we show is almost exactly recapitulated in the motor system, in terms of its laminar, topographic and physiological characteristics. This perspective casts classical motor reflexes as minimising prediction errors and may provide a principled explanation for why motor cortex is agranular.
    Brain Structure and Function 11/2012; 218(3). DOI:10.1007/s00429-012-0475-5 · 5.62 Impact Factor
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    • "The motor cortex gives rise to the pyramidal tract, and like other descending systems, may receive modulating signals from the cerebellum via the ventrolateral thalamus (Beloozerova and Sirota, 1988, 2002). It may also receive information from limb afferents via the somatosensory cortex (Waters et al., 1982, Mori et al., 1989) and/or directly from thalamic relays (Asanuma et al., 1979; Yen et al., 1991, Craig, 2008). "
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    ABSTRACT: During locomotion, neurons in motor cortex exhibit profound step-related frequency modulation. The source of this modulation is unclear. The aim of this study was to reveal the contribution of different limb controllers (locomotor mechanisms of individual limbs) to the periodic modulation of motor cortex neurons during locomotion. Experiments were conducted in chronically instrumented cats. The activity of single neurons was recorded during regular quadrupedal locomotion (control), as well as when only one pair of limbs (fore, hind, right, or left) was walking while another pair was standing. Comparison of the modulation patterns in these neurons (their discharge profile with respect to the step cycle) during control and different bipedal locomotor tasks revealed several groups of neurons that receive distinct combinations of inputs from different limb controllers. In the majority (73%) of neurons from the forelimb area of motor cortex, modulation during control was determined exclusively by forelimb controllers (right, left, or both), while in the minority (27%), hindlimb controllers also contributed. By contrast, only in 30% of neurons from the hindlimb area was modulation determined exclusively by hindlimb controllers (right or both), while in 70% of them, the controllers of forelimbs also contributed. We suggest that such organization of inputs allows the motor cortex to contribute to the right-left limbs' coordination within each of the girdles during locomotion, and that it also allows hindlimb neurons to participate in coordination of the movements of the hindlimbs with those of the forelimbs.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 03/2011; 31(12):4636-49. DOI:10.1523/JNEUROSCI.6511-10.2011 · 6.34 Impact Factor
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    • "The view that ST input to the CMAd and CMAv is involved in sensorimotor integration fits with the concept that a portion of the ST system conveys information about the state of segmental interneurons involved in motor mechanisms such as spinal reflexes, locomotion and posture (e.g., Menétrey et al., 1984; Craig, 2008). Craig (2008) has proposed that a component of the ST system originates from neurons in laminae V and VII and primarily targets M1. However, our results suggest that the ST input to M1 is quite limited (see also Greenan and Strick, 1986; Stepniewska et al., 2003). "
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    ABSTRACT: Classically, the spinothalamic (ST) system has been viewed as the major pathway for transmitting nociceptive and thermoceptive information to the cerebral cortex. There is a long-standing controversy about the cortical targets of this system. We used anterograde transneuronal transport of the H129 strain of herpes simplex virus type 1 in the Cebus monkey to label the cortical areas that receive ST input. We found that the ST system reaches multiple cortical areas located in the contralateral hemisphere. The major targets are granular insular cortex, secondary somatosensory cortex and several cortical areas in the cingulate sulcus. It is noteworthy that comparable cortical regions in humans consistently display activation when subjects are acutely exposed to painful stimuli. We next combined anterograde transneuronal transport of virus with injections of a conventional tracer into the ventral premotor area (PMv). We used the PMv injection to identify the cingulate motor areas on the medial wall of the hemisphere. This combined approach demonstrated that each of the cingulate motor areas receives ST input. Our meta-analysis of imaging studies indicates that the human equivalents of the three cingulate motor areas also correspond to sites of pain-related activation. The cingulate motor areas in the monkey project directly to the primary motor cortex and to the spinal cord. Thus, the substrate exists for the ST system to have an important influence on the cortical control of movement.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 11/2009; 29(45):14223-35. DOI:10.1523/JNEUROSCI.3398-09.2009 · 6.34 Impact Factor
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