Plasticity of primary somatosensory cortex representations paralleling sensorimotor skill recovery from stroke in adult owl and squirrel monkeys. Christian Xerri, Michael M. Merzenich, Bret E. Peterson, William Jenkins. Keck Center and Coleman Laboratory, University of California at San Francisco, San Francisco, CA 94143-0732. Laboratoire de Neurobiologie des Restaurations Fonctionnelles, U.M.R 6562, CNRS/ Universite de Provence, Centre St-J_rome, Avenue E. Normandie-Niemen, 13397 Marseille Cedex 20, France.
APStracts 4:337N, 1997.
ABSTRACT
Adult owl and squirrel monkeys were initially trained to master a small-object retrieval sensorimotor skill (see Xerri et al., 1997). Behavioral observations along with positive changes in the cortical area 3b representations of specific skin surfaces directly implicated specific glabrous finger inputs as important contributors to skill acquisition. The small area 3b zones over which these behaviorally important surfaces were represented were destroyed by induction of a microlesion, which resulted in a marked degradation of the differentiated movements that were necessary for --- and had been progressively developed in --- the earlier acquisition of the skill. Monkeys were then retrained at the same behavioral task, with the knowledge that they could no longer receive critical feedback information from the zone of cortical area 3b that had earlier contributed important sensory feedback information to it. They could initially perform the task reasonably well using the stereotyped movements that they had learned in pre-lesion training, even though they commonly acted as if key finger surfaces were insensate. However, every monkey soon initiated alternative strategies for small object retrieval that resulted in a substantial drop in performance success. Over a subsequent several- to many-week-long period, every monkey again used the fingers for object retrieval that had been used successfully before the lesion, and very gradually re-acquired performance levels that were almost equal to those recorded before lesion induction. Detailed maps of the representations of the hands in SI cortical fields 3b, 3a and 1 were derived after this post-lesion functional recovery. Control maps were derived in the same hemispheres prior to lesion induction, and in the opposite (control) hemisphere. Among other findings, these studies revealed that: 1) There was a significant post-lesion re-emergence of the representation of the fingertips engaged in the behavior in novel locations in cortical area 3b in 2 of 5 monkeys, and a generally less substantial change in the representation of the hand in the intact parts of area 3b in 3 of 5 monkeys. 2) In contrast to the relatively modest post-lesion remodeling of area 3b, there was a striking emergence of a new representation of the cutaneous fingertips in cortical area 3a recorded in 4 of 5 monkeys, predominantly within cortical zones that had formerly been exclusively excited by proprioceptive inputs. This new cutaneous fingertip representation disproportionately represented behaviorally crucial fingertips. 3) There was an approximately 2X enlargement of the representation of the fingers recorded in cortical area 1 in post-lesion monkeys. In that remodeling, the specific finger surfaces employed in small-object retrieval (and that were selectively ablated within area 3b) were differentially enlarged in representation. Neurons at most emergent cutaneous sites were excited selectively by proprioceptive inputs prior to the lesion. 4) Multiple-digit receptive fields were recorded at a majority of emergent, cutaneous area 3a sites in all monkeys, and at a substantial number of area 1 sites in 3 of 5 post-lesion monkeys. Such fields were uncommon in area 1 in pre-lesion control maps. Single receptive fields and the component fields of multiple-digit fields in post-lesion representations were within normal receptive field size ranges. 5) Neurons in emergent or differentially enlarged representations of behaviorally engaged digits in area 1 were more strongly driven by cutaneous stimuli in chronic, post-lesion cases than in control maps. 6) No significant changes were recorded in the SI hand representations in the opposite (untrained, intact) control hemisphere. These findings are consistent with OsubstitutionO and OvicariationO (adaptive plasticity) models of recovery from brain damage and stroke. 

Received 8 April 1997; accepted in final form 25 November 1997.
APS Manuscript Number J281-7.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1997 The American Physiological Society.
Published in APStracts on 12 December 1997