Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys

Abstract

In an earlier study ( Neuroscience 8, 33–55, 1983), we found that the cortex representing the skin of the median nerve within parietal somatosensory fields 3b and 1 was completely occupied by ‘new’ inputs from the ulnar and radial nerves, 2–9 months after the median nerve was cut and tied in adult squirrel and owl monkeys. In this report, we describe the results of studies directed toward determining the time course and likely mechanisms underlying this remarkable plasticity. Highly detailed maps of the hand surface representation were derived in monkeys before, immediately after, and at subsequent short and intermediate time stages after median nerve section. In one monkey, maps were derived before nerve section, immediately after nerve section, and 11, 22 and 144 days later. Thus, direct comparisons in cortical map structure could be made over time in this individual monkey. In other experiments, single maps were derived at given post-section intervals. These studies revealed that: (1) large cortical sectors were ‘silenced’ by median nerve transection. (2) Significant inputs restricted to the dorsum of the radial hand and the dorsum of digits 1, 2 and 3 were immediately ‘unmasked’ by median nerve transection. (3) These immediately ‘unmasked’ regions were topographically crude, and represented only fragments of this dorsal skin. They were transformed, over time, into very large, highly topographic and complete representations of dorsal skin surfaces. (4) Representations of bordering glabrous skin surfaces progressively expanded to occupy larger and larger portions of the former median nerve cortical representational zone. (5) These ‘expanded’ representations of ulnar nerve-innervated skin surfaces sometimes moved, in entirety, into the former median nerve representational zone. (6) Almost all of the former median nerve zone was driven by new inputs in a map derived 22 days after nerve section. At shorter times (3, 6 and 11 days), ‘reoccupation’ was still incomplete. (7) Very significant changes in map dimensions within and outside of the former median skin cortical field were seen after the ‘reoccupation’ of the deprived cortex by ‘new’ inputs was initially completed. (8) Progressive changes were recorded within the original ulnar and radial nerve cortical representational zones, as skin surfaces originally overtly represented wholly within these regions expanded into the former median nerve zone. (9) Throughout the studied period, the cortical representational loci of many skin sites appeared to change continually and often markedly. (10) The locations of map discontinuities also shifted significantly over time. (11) Concommitant with changes in representational magnification over time, inverse changes in receptive field sizes were recorded. (12) Immediately ‘unmasked’ inputs had greater than normal receptive field overlap as a function of distance across the cortical surface. The normal ‘hypercolumn’ rule 67 was progressively re-established. (13) The topographical progression of reorganization and ultimate reorganizational patterns differed greatly in Areas 3b and 1. The evident capacity for change in and around the deprived cortical zone of: (a) cortical map dimensions; (b) cortical sites of representation of different skin surfaces (obversely, the skin surfaces represented at given cortical sites over time) (c) receptive field sizes and overlaps (d) of the locations of map discontinuities clearly demonstrates that details of cortical map structure in Areas 3b and 1 are dynamically maintained. The present studies indicate that nerve transection results in both immediate and progressively developing changes in the cortical maps of this skin surface. While some portions of the deprived cortex were not cutaneously responsive immediately after transection, other parts of this cortex were immediately activated by ‘new’ cutaneous inputs. The reoccupation of the deprived cortex gradually increased, and dramatic changes in somatotopic organization occurred even after initial complete reactivation. Changes in receptive field sizes were seen concurrent with changes in somatotopic organization. These results have important implications for consideration of the nature of reorganization processes. They provide further, strong evidence that the detailed structure of the manifest somatotopic cortical organization is dynamically maintained. They bear implications for consideration of the significance and of the nature of physiologically recorded topographic representations of sensory epithelia in normal monkeys.