Functional reorganization in somatosensory cortical areas 3b and 1 of adult monkeys after median nerve repair: possible relationships to sensory recovery in humans

Abstract

Previous studies have shown that the primary somatosensory cortex of adult mammals undergoes somatotopic reorganization in response to peripheral nerve transection. The present study assesses how cortical organization is affected when a transected nerve subsequently regenerates. The median nerve to one hand of adult owl monkeys was transected and repaired. Following nerve regeneration, the representations of the hand in cortical areas 3b and 1 were studied with neurophysiological mapping methods. The major results were as follows: Peripherally, median nerve transection, repair, and regeneration resulted in reinnervation of the median nerve skin territory. Centrally, both the initial loss and subsequent regeneration of median nerve inputs caused reorganizational changes in cortex. Reorganizational changes were specifically restricted to regions of the hand cortex where inputs from the median nerve were normally represented. The functional features of cortical regions that recovered tactile responsiveness from reinnervated skin regions were abnormal in several respects. Most notably, these regions contained recording sites with abnormally located or multiple cutaneous receptive fields, and contained major topographical changes, such as reestablishment of palmar pad or digit representations in small, discontinuous patches of cortex. Normal organizational features were reestablished to a more limited extent. These features included recovery of delimited, discrete receptive fields and reestablishment of topographic representations for localized skin areas. Different transformations in topographical organization were seen in areas 3b and 1 of the same monkey. These results suggest that nerve regeneration reestablishes the cortical capacity to process tactile information from reinnervated skin via a prolonged reorganizational process that appears dependent on peripheral and central factors. Cortical recovery mechanisms clearly appear to have limitations, since preinjury patterns of cortical organization are not widely recovered even almost 1 year after repair. We suggest possible relationships between cortical reorganizational changes in these primates, and postrepair sensory changes in humans.

Redirection of cutaneous sensation from the hand to the chest skin of human amputees with targeted reinnervation

“…The large hand perceptions may result from the activation of anatomical connections between central pathways/cortical representations by a small number of randomly organized inputs from the skin surface (16)(17)(18)(19). Another possibility is that these large or disparate percepts appear because when normally separate skin surfaces are activated simultaneously it may cause the formerly distinct representative regions within the cortex to expand and merge (20).…”

Re-emergence of hand-muscle representations in human motor cortex after hand allograft

“…It has been shown in primates that complete peripheral nerve section followed by reconnection results in a reshuffling of primary somatosensory cortex (S1) digit representations, suggesting that the regrowth of severed peripheral sensory nerves is often an imprecise process (1). Therapeutic amputation of the hand in monkeys is followed by a large-scale reorganization of the somatosensory pathways (6), and an extensive sprouting of corticocortical connections is observed in S1 after peripheral injury (7), indicating that the somatosensory system is engaged in a massive reorganization after a peripheral lesion.…”

“…Evidence from human and animal models show that, when deprived of its afferent sensory input and/or its motor effectors, the primary sensory (S1) and motor (M1) cortical regions undergo plastic modifications (1)(2)(3)(4)(5)(6)(7)(8)(9)(10).…”

Functional Architecture of Spatial Attention in the Parietal Cortex of the Behaving Monkey

“…Third, the patches were consistently absent when the monkeys' attention was restricted on the fixation point. Although there are examples of variability of representations across time (Wall et al, 1986;Kaas et al, 1990;Wilson and McNaughton, 1993;Darian-Smith and Gilbert, 1995), these can have very different underlying causes and timescales. The variability and stability of these measurements was examined in three ways.…”