What determines the role of brain regions and their plasticity when typical inputs or experience is not provided? To what extent can extreme compensatory use affect brain organization? We tested the reorganization of primary and association sensorimotor cortex hand-selective areas in people born without hands, who use their feet for everyday tasks. We found that their primary sensorimotor hand area is preferentially activated for nearby body parts that cannot serve as effectors. In contrast, foot-selective compensatory plasticity was found in the association cortex, in an area typically involved in manual tool use. This shows limitations of compensatory plasticity and experience in modifying brain organization of early topographical cortex, as compared with association cortices where function-based organization is the driving factor.Abstract
What forces direct brain organization and its plasticity? When brain regions are deprived of their input, which regions reorganize based on compensation for the disability and experience, and which regions show topographically constrained plasticity? People born without hands activate their primary sensorimotor hand region while moving body parts used to compensate for this disability (e.g., their feet). This was taken to suggest a neural organization based on functions, such as performing manual-like dexterous actions, rather than on body parts, in primary sensorimotor cortex. We tested the selectivity for the compensatory body parts in the primary and association sensorimotor cortex of people born without hands (dysplasic individuals). Despite clear compensatory foot use, the primary sensorimotor hand area in the dysplasic subjects showed preference for adjacent body parts that are not compensatorily used as effectors. This suggests that function-based organization, proposed for congenital blindness and deafness, does not apply to the primary sensorimotor cortex deprivation in dysplasia. These findings stress the roles of neuroanatomical constraints like topographical proximity and connectivity in determining the functional development of primary cortex even in extreme, congenital deprivation. In contrast, increased and selective foot movement preference was found in dysplasics’ association cortex in the inferior parietal lobule. This suggests that the typical motor selectivity of this region for manual actions may correspond to high-level action representations that are effector-invariant. These findings reveal limitations to compensatory plasticity and experience in modifying brain organization of early topographical cortex compared with association cortices driven by function-based organization.