A primate genesis model of focal dystonia and repetitive strain injury: I. Learning-induced dedifferentiation of the representation of the hand in the primary somatosensory cortex in adult monkeys

Abstract

In this study we tested a neuroplasticity/learning origins hypothesis for repetitive strain injuries (RSIs), including occupationally induced focal dystonia. Repetitive movements produced in a specific form and in an appropriate behavioral context cause a degradation of the sensory feedback information controlling fine motor movements, resulting in the "learned" genesis of RSIs. Two adult New World owl monkeys were trained at a behavioral task that required them to maintain an attended grasp on a hand grip that repetitively and rapidly (20 msec) opened and closed over short distances. The monkeys completed 300 behavioral trials per day (1,100 to 3,000 movement events) with an accuracy of 80 to 90%. A movement control disorder was recorded in both monkeys. Training was continued until the performance accuracy dropped to below 50%. We subsequently conducted an electrophysiologic mapping study of the representations of the hand within the primary somatosensory (SI) cortical zone. The hand representation in the true primary somatosensory cortical field, SI area 3b, was found to be markedly degraded in these monkeys, as characterized by (1) a dedifferentiation of cortical representations of the skin of the hand manifested by receptive fields that were 10 to 20 times larger than normal, (2) the emergence of many receptive fields that covered the entire glabrous surface of individual digits or that extended across the surfaces of two or more digits, (3) a breakdown of the normally sharply segregated area 3b representations of volar glabrous and dorsal hairy skin of the hand, and (4) a breakdown of the local shifted-overlap receptive field topography of area 3b, with many digital receptive fields overlapping the fields of neurons sampled in cortical penetrations up to more than four times farther apart than normal. Thus, rapid, repetitive, highly stereotypic movements applied in a learning context can actively degrade cortical representations of sensory information guiding fine motor hand movements. This cortical plasticity/learning-based dedifferentiation of sensory feedback information from the hand contributes to the genesis of occupationally derived repetitive strain injuries, including focal dystonia of the hand. Successful treatment of patients with RSI will plausibly require learning-based restoration of differentiated representations of sensory feedback information from the hand.