Reorganization of the raccoon cuneate nucleus after peripheral denervation

Abstract

The effects of peripheral nerve transection on the cuneate nucleus were studied in anesthetized raccoons using extracellular, single-unit recordings. The somatotopic organization of the cuneate nucleus first was examined in intact, control animals. The cuneate nucleus in the raccoon is organized with the digits represented in separate cell clusters. The dorsal cap region of the cuneate nucleus contains a representation of the claws and hairy skin of the digits. Within the representation of the glabrous skin, neurons with rapidly adapting properties tended to be segregated from those with slowly adapting properties. The representations of the distal and proximal pads on a digit also were segregated. Electrical stimulation of two adjacent digits provided a detailed description of the responses originating from the digit that contains the tactile receptive field (the on-focus digit) and from the adjacent (off-focus) digit. Stimulation of the on-focus digit produced a short latency excitation in all 99 neurons tested, with a mean of 10.5 ms. These responses had a low threshold (426 microA). Stimulation of an off-focus digit activated 65% of these neurons. These responses had a significantly longer latency (15.3 ms) than on-focus responses and the threshold was more than twice as large. Two to five months after amputation of digit 4, 97 cells were tested with stimulation of digits 3 and 5. A total of 44 were in the intact regions of the cuneate nucleus. They had small receptive fields on intact digits and their responses to electrical stimulation did not differ from the control neurons. The remaining 53 neurons were judged to be deafferented and in the fourth digit region on the basis of their location with respect to intact neurons. All but two of these cells had receptive fields that were much larger than normal, often including more than one digit and part of the palm. When compared with the off-focus control neurons, their responses to electrical stimulation had lower thresholds and an increased response probability and magnitude. The latencies of these cells did not decrease, however, and were the same as the off-focus control values. The enhanced responses of the deafferented neurons to adjacent digit stimulation indicate that there is a strengthening of synapses that were previously ineffective. The increased proportion of neurons that could be activated after amputation suggests that there is also a growth of new connections. This experiment demonstrates that reorganization in the adult somatotopic system does occur at the level of the dorsal column nuclei. As a consequence, many of the changes reported at the cortex and thalamus may be due to the changes occurring at this first synapse in the somatosensory pathway.