Experience-induced plasticity of cutaneous maps in the primary somatosensory cortex of adult monkeys and rats

Abstract

In a first study, the representations of skin surfaces of the hand in the primary somatosensory cortex, area 3b, were reconstructed in owl monkeys and squirrel monkeys trained to pick up food pellets from small, shallow wells, a task which required skilled use of the digits. Training sessions included limited manual exercise over a total period of a few hours of practice. From an early clumsy performance in which many retrieval attempts were required for each successful pellet retrieval, the monkeys exhibited a gradual improvement. Typically, the animals used various combinations of digits before developing a successful retrieval strategy. As the behavior came to be stereotyped, monkeys consistently engaged surfaces of the distal phalanges of one or two digits in the palpation and capture of food pellets from the smallest wells. Microelectrode mapping of the hand surfaces revealed that the glabrous skin of the fingertips predominantly involved in the dexterity task was represented over topographically expanded cortical sectors. Furthermore, cutaneous receptive fields which covered the most frequently stimulated digital tip surfaces were less than half as large as were those representing the corresponding surfaces of control digits. In a second series of experiments, Long-Evans rats were assigned to environments promoting differential tactile experience (standard, enriched, and impoverished) for 80 to 115 days from the time of weaning. A fourth group of young adult rat experienced a severe restriction of forepaw exploratory movement for either 7 or 15 days. Cortical maps derived in the primary somatosensory cortex showed that environmental enrichment induced a substantial enlargement of the cutaneous forepaw representation, and improved its spatial resolution (smaller glabrous receptive fields). In contrast, tactile impoverishment resulted in a degradation of the forepaw representation that was characterized by larger cutaneous receptive fields and the emergence of non-cutaneous responses. Cortical maps derived in the hemispheres contralateral to the immobilized forelimb exhibited a severe decrease of about 50% in the overall areal extent of the cutaneous representation of the forepaw, which resulted from the invasion of topographically organized cortical zones of non-cutaneous responses, and numerous discontinuities in the representation of contiguous skin territories. The size and the spatial arrangement of the cutaneous receptive fields were not significantly modified by the immobilization of the contralateral forelimb. Similar results were obtained regardless of whether the forelimb restriction lasted 7 or 15 days. These two studies corroborate the view that representational constructs are permanently reshaped by novel experiences through dynamic competitive processes. These studies also support the notion that subject-environment interactions play a crucial role in the maintenance of basic organizational features of somatosensory representations.