Microelectrode mapping methods were used to define and describe 3 representations of the body surface in somatosensory cortex of marmosets: S-I proper or area 3b of anterior parietal cortex, S-II, and the parietal ventral area (PV) of the upper bank of the lateral sulcus. In the same animals, injections of anatomical tracers were placed into electrophysiologically determined sites in area 3b or S-II. Mapping results and patterns of connections were later related to architectonic fields that were delimited in sections cut parallel to the surface of manually flattened cortex and stained for myelin. There were several major results. (1) Recordings from area 3b revealed a characteristic somatotopic organization of foot to face in a mediolateral sequence as previously reported in other members of the marmoset family (Carlson et al., 1986). (2) Multiple injections of WGA-HRP in area 3b demonstrated dense, patchy interconnections with ipsilateral S-II, PV, area 3a, and area 1, less dense interconnections with primary motor cortex (M-I), the supplementary motor area (SMA), limbic cortex of the medial wall (L), and rostrolateral parietal cortex of the lateral sulcus (PR), and callosal connections with areas 3b, S-II, and PV. Injections of 3 different tracers into the representation of 3 body regions in area 3b indicated that the connections with areas 3a, 3b, 1, S-II, and PV are topographically organized. (3) Recordings from cortex on the upper bank of the lateral sulcus demonstrated a somatotopic representation of the body surface that matches that of S-II of other mammals. S-II immediately adjoined areas 3b along the dorsal lip of the lateral sulcus. The face representation in S-II was adjacent to the face representation in 3b while the trunk, hindlimb, and forelimb were represented in a caudorostral sequence deeper in the sulcus. (4) Injections in S-II revealed ipsilateral connections with areas 3a, 3b, 1, a presumptive area 2, PV, PR, M-I, SMA, limbic cortex, the frontal eye fields, and the frontal ventral visual area. Dense callosal connections were with S-II and PV. (5) The recordings also revealed a systematic representation just rostral to S-II that has not been previously described in primates.(ABSTRACT TRUNCATED AT 400 WORDS)

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Reorganization of somatosensory cortex after peripheral nerve damage typically has been attributed to cortical plasticity. Here we provide evidence that much of the large-scale cortical reorganization that occurs after a major loss of peripheral inputs reflects the sprouting or expansion of afferents from the remaining forelimb into deprived territories of the spinal cord and brainstem. We examined sensory afferent terminations in the spinal cord and brainstem, and determined the somatotopic organization of cortical area 3b in three adult monkeys with previous hand or forearm amputation, as veterinary treatment of forelimb injuries. In each monkey, the distribution of labeled sensory afferent terminations from the remaining parts of the fore-limb was much more extensive than the normal distribution of inputs from the forelimb, and extended into portions of the dorsal horn of the spinal cord and the cuneate nucleus of the brainstem related to the amputated hand. In the same animals, tactile stimulation of the forelimb activated much of the deprived hand representation in area 3b of cortex; the lateral portion of the deprived region in area 3B appeared to be reactivated by inputs from the face. These data provide important new evidence that one of the mechanisms subserving large scale reorganization in cortex is a relay of topographic changes that occur subcortically. Presumably, the expanded primary sensory inputs activate postsynaptic neurons that are normally driven by inputs from the hand so that the neurons now have receptive fields on the forearm. Since the topographic representation of the body is greatly magnified in the relay to cortex, the subcortical changes can result in dramatic cortical map changes.

Central termination patterns of primary afferents from the hand and forelimb were studied following subdermal injections of HRP conjugates in macaque monkeys. In the middle layers of the dorsal horn of the spinal cord, afferents from digits 1-5 terminated in a rostrocaudal sequence in separate, elongated columns at cervical levels 5-7. Afferents from the glabrous digits extended to the medial margin of the dorsal gray, while afferents from the dorsal skin of the digits terminated more laterally. Afferents from the dorsal hand and palm terminated lateral to those from the digits, while inputs from the forearm occupied tissue rostral and caudal to the representation of the hand. In the cuneate nucleus, terminations from each digit formed an elongated column that was densely labelled in the central pars rotunda and sparsely labelled in both the rostral and caudal reticular poles. Within the pars rotunda, digits 1-5 were represented in order from lateral to medial. Inputs from the digit tips terminated ventral to inputs from the proximal digits. Afferents from the dorsal skin of the digits terminated in an even more dorsal position, while the most dorsal portion of the pars rotunda related to the glabrous and dorsal hand. Within the pars rotunda, terminations from specific parts of the hand overlapped parcellated clusters of neurons. These clusters were densely reactive for cytochrome oxidase (CO) and were surrounded by myelinated fibers. Much sparser label in the reticular poles was found consistently only after injections in the glabrous digits. Inputs to the poles appeared diffuse and overlapping while preserving some somatotopic order. When treated for CO or stained for Nissl substance or myelin, the pars rotunda of humans showed parcellation patterns that closely resembled the patterns seen in monkeys. From the relationship of inputs to the CO dense cell clusters in monkeys, it was possible to postulate in detail the somatotopic organization of inputs to pars rotunda of humans. The present results provide a comprehensive description of the somatotopic patterns of termination of afferents from the skin of the hand and forearm in the spinal cord and cuneate nucleus of macaque monkeys. A direct relationship of afferent somatotopy and identifiable cell clusters in the pars rotunda of the cuneate nucleus is further demonstrated. Finally, the patterns of cell clusters in the pars rotunda of macaque monkeys and humans suggest that the somatotopic organization of the cuneate nucleus may be very similar in human and nonhuman primates.

The owl monkey, as do other mammals, has X-and Y-cells in its lateral geniculate nucleus. X-cells are found in the parvocellular laminae; Y-cells, in the magnocellular laminae.