Somatotopic organization of inputs from the hand to the spinal gray and cuneate nucleus of monkeys with observations on the cuneate nucleus of humans

Abstract

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.

Hand/Face Border as a Limiting Boundary in the Body Representation in Monkey Somatosensory Cortex

“…Neurons responding to stimulation of the lower jaw and neck region have never been reported in V PM (Jones et al, 1986a;Rausell and Jones, 1991a); V PM receives only trigeminal inputs which do not overlap into V PL (Jones et al, 1986b;Rausell and Jones, 1991b). Studies of somatotopy in the dorsal column and principal trigeminal nuclei of monkeys (Kerr et al, 1968;Ferrington et al, 1988;Culbertson and Brushart, 1989;Florence et al, 1989) have not reported whether lower jaw and neck representations are found in both nuclei. There is, however, extensive overlap of upper cervical and trigeminal inputs in the caudal spinal trigeminal nucleus (Kerr, 1972).…”

Functional organization of tactile inputs from the hand in the cuneate nucleus and its relationship to organization in the somatosensory cortex

“…The central substrates that process these inputs include a substantial portion of the somatosensory area 3b cortex that, in turn, receives driving inputs from subcortical lemniscal substrates (e.g., Jones et al, , 1997Mountcastle, 1984;Florence et al, 1989Florence et al, , 1991Rausell et al, 1992a,b;Jain et al, 1997). These substrates originate in the main cuneate nucleus (CN) and subsequently project to area 3b by means of the ventroposterior lateral nucleus (VPL) of the thalamus.…”

Functional and Anatomical Features of the Dorsal Column Nuclei in Mammals and Lower Animals

“…The physiological studies of the Cu in galagos [56] and New and Old World monkeys [57,58,59,60,61,62,63] showed that the cell clusters in the main part of the nucleus (pars rotunda) is related to specific inputs from the hand. These cell clusters, identified as cytochrome oxidase (CO)-patches, receive inputs from digits 1-5 in a lateromedial sequence.…”