Plasticity of cortical function related to voluntary movement motor learning and compensation following brain dysfunction

Abstract

Processes of motor learning and of compensation after localized brain dysfunction were studied in the monkey tasked with conditioned (visually-initiated, reaction-time) hand movements. Field potentials in various cortical areas of the cerebral hemisphere were recorded successively for many months with electrodes implanted on the surface and in the depth of the cortex. The potentials associated with the conditioned movement were found to change during processes of learning the movement and during courses of degradation as well as recovery after the brain dysfunction. Motor learning of the reaction-time movement can be categorized into "recognition" and "skill" learnings. The former is the process for associating the visual stimulus with the movement and accompanied mainly by increasing activities of prefrontal, premotor and prestriate cortices. The latter is attaining better performances in executing the movement, particularly with shorter and more fixed reaction time, and is accompanied by recruitment of the cerebro-cerebellar interaction. The conditioned movements which had been well established were experimentally disturbed by transient, local cooling of different cortical areas or by cerebellar hemispherectomy. Three possible mechanisms of compensation are proposed as follow: 1. Substitution: Compensation occurring immediately through substitutional neuronal circuits. On transient cooling of the forelimb motor cortex, the somatosensory cortex became predominant in motor function and replaced the disabled motor cortex in executing the reaction-time movement, although activity was weak and slow (paretic but not paralytic). Resection of the cerebellar hemisphere also induced the compensatory motor function of the somatosensory cortex so that the movement could be performed although it was weak, slow and clumsy. 2. Relearning: Compensation by relearning through normally unused neuronal circuits. Prolonged and variable reaction times after cerebellar hemispherectomy persisted when the operation included both dentate and interpositus nuclei but recovered within about three weeks when the interpositus nucleus was preserved. It is suggested that the information processing for the well accomplished reaction-time movement is mainly mediated by the cerebro-cerebellar neuronal circuit including the dentate nucleus but is gradually relearned through the normally unused circuits involving the interpositus nucleus after the dentate nucleus lesion. 3. Rebuilding: Compensation by rebuilt neuronal circuits, e.g., by sprouting and/or regeneration (see S. Kawaguchi in this book).