Adult brains undergo large-scale plastic changes after peripheral and central injuries. Although it has been shown that both the cortical and thalamic representations can reorganize, uncertainties exist regarding the extent, nature, and time course of changes at each level. We have determined how cortical representations in the somatosensory area 3b and the ventroposterior (VP) nucleus of thalamus are affected by long standing unilateral dorsal column lesions at cervical levels in macaque monkeys. In monkeys with recovery periods of 22-23 months, the intact face inputs expanded into the deafferented hand region of area 3b after complete or partial lesions of the dorsal columns. The expansion of the face region could extend all the way medially into the leg and foot representations. In the same monkeys, similar expansions of the face representation take place in the VP nucleus of the thalamus, indicating that both these processing levels undergo similar reorganizations. The receptive fields of the expanded representations were similar in somatosensory cortex and thalamus. In two monkeys, we determined the extent of the brain reorganization immediately after dorsal column lesions. In these monkeys, the deafferented regions of area 3b and the VP nucleus became unresponsive to the peripheral touch immediately after the lesion. No reorganization was seen in the cortex or the VP nucleus. A comparison of the extents of deafferentation across the monkeys shows that even if the dorsal column lesion is partial, preserving most of the hand representation, it is sufficient to induce an expansion of the face representation.
In order to determine the relationship of superior colliculus inputs to thalamic neurons projecting to the middle temporal visual area (MT), injections of wheat germ agglutinin conjugated with horseradish peroxidase were placed in the superior colliculus of three owl monkeys, with injections of Fast Blue in the MT. The locations of labelled terminals and neurons in the posterior thalamus were related to four architectonically distinct nuclei of the inferior pulvinar (Stepniewska & Kaas, Vis. Neurosci. 14, pp.1043-1060, 1997). Fast Blue injections in the MT labelled neurons largely in the medial nucleus of the inferior pulvinar. A few labelled neurons were found in the adjoining central medial nucleus of the inferior pulvinar, as well as in the lateral pulvinar and the dorsal lateral geniculate nucleus. Superior colliculus inputs were most dense in the posterior and medial nuclei of the inferior pulvinar. There were sparser inputs to the central lateral nucleus of the inferior pulvinar, locations in the lateral and medial pulvinar, and the dorsal lateral geniculate nucleus. The results indicate that the medial nucleus of the inferior pulvinar, the major projection zone to the MT, does not receive a significant input from the superior colliculus.
Somatotopic maps in the cortex and the thalamus of adult monkeys and humans reorganize in response to altered inputs. After loss of the sensory afferents from the forelimb in monkeys because of transection of the dorsal columns of the spinal cord, therapeutic amputation of an arm or transection of the dorsal roots of the peripheral nerves, the deprived portions of the hand and arm representations in primary somatosensory cortex (area 3b), become responsive to inputs from the face and any remaining afferents from the arm. Cortical and subcortical mechanisms that underlie this reorganization are uncertain and appear to be manifold. Here we show that the face afferents from the trigeminal nucleus of the brainstem sprout and grow into the cuneate nucleus in adult monkeys after lesions of the dorsal columns of the spinal cord or therapeutic amputation of an arm. This growth may underlie the large-scale expansion of the face representation into the hand region of somatosensory cortex that follows such deafferentations.primate ͉ somatosensory ͉ sprouting ͉ plasticity ͉ dorsal columns I n adult monkeys and other mammals, a loss of afferents from the skin is followed by reorganization of the somatosensory cortex so that lost inputs are replaced by intact inputs in the representation (1, 2). Massive losses of inputs lead to large-scale reorganizations such that the somatotopic boundaries in the cortex may shift by more than 10 mm (3, 4). Such reorganizations in sensory representations probably depend on multiple mechanisms, including the potentiation of remaining synapses, the unmasking of latent connections by disinhibition, and possibly the growth of axon arbors and dendrites (5-10). However, there is little direct evidence for the mechanisms that mediate largescale reorganizations. We presumed that neuronal growth may play an important role in reorganizations where response to the face inputs expands into the hand region of area 3b because the expansion of the receptive fields is beyond any known limits of normal spread of thalamocortical or corticocortical arbors (11)(12)(13)(14)(15). Moreover, our experiments showed that the emergence of responses to the stimulation of the chin in the deprived hand cortex takes 6-8 mo (3), a time compatible with the growth of new connections. Finally, at the lower brainstem levels, the chin representation in the trigeminal nucleus lies adjacent to the hand representation in the cuneate nucleus. A limited growth of horizontal connections is known to occur within deprived visual cortex of adult cats (10) and deprived somatosensory cortex of monkeys (9). In addition, in monkeys with arm amputations, there is evidence that afferents from the stump of the arm can grow a short distance from their normal terminations in the dorsal part of the cuneate nucleus of the brainstem to the nearby ventral part, where digit inputs normally terminate (16). The question that we address here is whether the growth of new connections in the brain is a critical component of the massive cortical reorganizat...
Microelectrode mapping methods were used to define the parietal ventral somatosensory area (PV) on the upper bank of the lateral sulcus in five marmosets (Callithrix jacchus). In the same animals, neuroanatomical tracers were placed into electrophysiologically identified sites in PV and/or the second somatosensory area (S2). Foci of anterograde and retrograde label were related to electrophysiological maps of cortical areas and cortical and thalamic architecture. The results lead to the following conclusions: (1) Multiunit recordings from cortex on the upper bank of the lateral sulcus demonstrate that PV is somatotopically organized, with the face representation adjoining area 3b and the hindlimb and tail representations away from this border in cortex deep on the upper bank of the lateral sulcus. The forelimb representation is caudal in PV adjacent to the S2 forelimb representation. The body surface representation in PV approximates a mirror image of that in S2; (2) Areas PV and S2 are less myelinated and have less cytochrome oxidase enzyme activity than area 3b; (3) The ventroposterior inferior nucleus (VPI) of the thalamus provides the major somatosensory projections to PV. PV is reciprocally connected with VPI and anterior pulvinar; (4) PV has ipsilateral cortical connections with areas 3a, 3b, 1, and M1 and higher order somatosensory fields, and at least most of these connections are somatotopically matched; and (5) Callosal connections of PV are with S2 and PV of the other cerebral hemisphere. These results further establish PV as one of at least four somatosensory areas of the lateral sulcus of primates.
An incomplete lesion of the ascending afferents from the hand in the dorsal columns of the spinal cord in monkeys is followed after weeks of recovery by a reactivation of much of the territory of the hand representations in primary somatosensory cortex (area 3b). However, the relationship between the extent of the dorsal column lesion and the amount of cortical reactivation has not been clear. Largely, this is due to the uncertainties about axon sparing after spinal cord lesions. Here, we unilaterally sectioned dorsal column afferents in the cervical spinal cord (C4-C6) in adult squirrel monkeys. After weeks of recovery, cholera toxin subunit B (CTB) was injected into the distal phalanges to label normal and surviving afferents to the cuneate nuclei representing the hands. Days later, the responsiveness of neurons in cortical areas 3b and 1 to tactile stimulation on the hand was evaluated in a microelectrode mapping session. The sizes and densities of CTB-labeled patches in the cuneate nuclei of both sides were quantified and compared. The results indicate that extensive reactivations of the hand representations in cortical areas 3b and 1 occur contralateral to the spinal cord lesion, even when less than 1% of labeled dorsal column terminations in the cuneate nucleus remained. These results raise the possibilities that secondary afferents from innervated neurons in the spinal cord contribute to the reactivation, and that the reactivation of area 1 is not completely dependent on inputs from area 3b.
Patterns of terminals labeled after WGA-HRP injections in the superior colliculus (SC) in squirrel monkeys and macaque monkeys, and after DiI application in marmosets, were related to the architecture of the pulvinar and dorsal lateral geniculate nucleus (LGN). In all studied species, the SC projects densely to two architectonic subdivisions of the inferior pulvinar, the posterior inferior pulvinar nucleus (PIp) and central medial inferior pulvinar nucleus (PIcM). These projection zones expressed substance P. Thus, sections processed for substance P reveal SC termination zones in the inferior pulvinar. The medial subdivision of the inferior pulvinar, PIm, which is known to project to visual area MT, does not receive a significant collicular input. Injections in MT of a squirrel monkey revealed no overlap between SC terminals and neurons projecting to area MT. Thus, PIm is not the significant relay station of visual input from the SC to MT. The SC also sends an input to the LGN, however, this projection is sparser than the input directed to pulvinar.
We determined the somatotopy of the face and the oral cavity representation in cortical area 3b of New World owl monkeys and squirrel monkeys. Area 3b is apparent as a densely myelinated strip in brain sections cut parallel to the surface of flattened cortex. A narrow myelin-light septum that we have termed the "hand-face septum" separates the hand representation from the more lateral face and mouth representation. The face and oral cavity representation is further divided into a series of myelin-dense ovals. We show that three ovals adjacent to the hand representation correspond to the upper face, upper lip, and chin plus lower lip, whereas three or four more rostral ovals successively represent the contralateral teeth, tongue, and the ipsilateral teeth and tongue. Strips of cortex lateral and medial to the area 3b ovals, possibly corresponding to area 1 and area 3a, respectively, have similar somatotopic sequences. Although previous results suggest the existence of great variability within and across primate species, we conclude that the representations of the face and mouth are highly similar across individuals of the same species, and there are extensive overall similarities across these two species of New World monkeys.
The nodes of a parietal-frontal pathway that mediates grasping in primates are in anterior intraparietal area (AIP) and ventral premotor cortex (PMv). Nevertheless, multiple somatosensory and motor representations of the hand, respectively in parietal and frontal cortex, suggest that additional pathways remain unrealized. We explored this possibility in macaque monkeys by injecting retrograde tracers into grasp zones identified in M1, PMv, and area 2 with long train electrical stimulation. The M1 grasp zone was densely connected with other frontal cortex motor regions. The remainder of the connections originated from somatosensory areas 3a and S2/PV, and from the medial bank and fundus of the intraparietal sulcus (IPS). The PMv grasp zone was also densely connected with frontal cortex motor regions, albeit to a lesser extent than the M1 grasp zone. The remainder of the connections originated from areas S2/PV and aspects of the inferior parietal lobe such as PF, PFG, AIP, and the tip of the IPS. The area 2 grasp zone was densely connected with the hand representations of somatosensory areas 3b, 1, and S2/PV. The remainder of the connections was with areas 3a and 5 and the medial bank and fundus of the IPS. Connections with frontal cortex were relatively weak and concentrated in caudal M1. Thus, the three grasp zones may be nodes of parallel parietal-frontal pathways. Differential points of origin and termination of each pathway suggest varying functional specializations. Direct and indirect connections between those parietal-frontal pathways likely coordinate their respective functions into an accurate grasp.
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