Reorganization in cerebral and cerebellar cortices is not restricted by proximity between body-part representations

Abstract

A fundamental organizing principle in the somatosensory and motor systems is somatotopy, where specific body parts are represented separately and adjacently to other body parts, resulting in a body map. Different terminals of the sensorimotor network show varied somatotopic layouts, in which the relative position, distance and overlap between body-part representations differ. Since somatotopy is best characterized in the primary somatosensory (S1) and motor (M1) cortices, these terminals have been the main focus of research on somatotopic remapping following loss of sensory input (e.g. arm amputation). Cortical remapping is generally considered to be driven by the layout of the underlying somatotopy, such that neighboring body-part representations tend to activate the deprived brain region. Here, we challenge the assumption that somatotopic layout restricts remapping, by comparing patterns of remapping in humans born without one hand (hereafter, one-handers, n=26) across multiple terminals of the sensorimotor pathway. We first report that in the cerebellum of one-handers, the deprived hand region represents multiple body parts. Importantly, the representations of some of these body parts do not neighbor the deprived hand region. We further replicate our previous finding, showing a similar pattern of remapping in the deprived hand region of the cerebral cortex in one-handers. Finally, we report preliminary results of a similar remapping pattern in the putamen of one-handers. Since these three sensorimotor terminals (cerebellum, cerebrum, putamen) contain different somatotopic layouts, the parallel remapping they undergo demonstrates that the mere spatial layout of body-part representations may not exclusively dictate remapping in the sensorimotor systems.\n\nSignificance StatementWhen a hand is missing, the brain region that typically processes information from that hand may instead process information from other body-parts, a phenomenon termed remapping. It is commonly thought that only body-parts whose information is processed in regions neighboring the hand region could \"take up\" the resources of this now deprived region. Here we demonstrate that information from multiple body-parts is processed in the hand regions of both the cerebral cortex and cerebellum. The native brain regions of these body-parts have varying levels of overlap with the hand region across multiple terminals in the sensorimotor hierarchy, and do not necessarily neighbor the hand region. We therefore propose that proximity between brain regions does not limit brain remapping.