Somatosensory cortex and body representation: Updating the motor system during a visuo-proprioceptive cue conflict

ABSTRACT The brain’s representation of hand position is critical for voluntary movement. Representation is multisensory, combining visual and proprioceptive cues. When these cues conflict, the brain recalibrates its unimodal estimates, shifting them closer together to compensate. Converging evidence from research in perception, behavior, and neurophysiology suggest that such updates to body representation are communicated to the motor system to keep hand movements accurate. We hypothesized that primary somatosensory cortex (SI) is crucial in this updating process due to its role in proprioception and connections with primary motor cortex. We tested this hypothesis in two experiments. We predicted that proprioceptive, but not visual, recalibration would be associated with change in short latency afferent inhibition (SAI), a measure of sensorimotor integration (influence of sensory input on motor output) (Expt. 1). We further predicted that modulating SI activity with repetitive transcranial magnetic stimulation (TMS) should affect recalibration of the proprioceptive estimate of hand position, but have no effect on the visual estimate or on the normal inverse relationship between proprioceptive and visual recalibration (Expt. 2). Our results are consistent with these predictions, supporting the idea that (1) SI is indeed a key region in facilitating motor system updates based on changes in body representation, and (2) this function is mediated by unisensory (proprioceptive) processing, separate from multisensory visuo-proprioceptive computations. Other aspects of the body representation (visual and multisensory) may be conveyed to the motor system via separate pathways, e.g. from posterior parietal regions to motor cortex. Significance Statement Representation of the hand, which is critical for accurate control of movement, comes from weighting and combining available proprioceptive (position sense) and visual cues. Our results suggest that when the hand representation is modified by introducing a conflict between these cues, the motor system receives updates directly from the primary somatosensory cortex (SI). These updates are specific to the change in proprioceptive representation and are absent when cues are not in conflict. This may represent a unisensory pathway to the motor system that conveys information about hand representation, acting in parallel with multisensory pathways involving posterior parietal and premotor regions. Competing Interest Statement The authors have declared no competing interest. Footnotes The methods section has been expanded to provide more detail on the behavioral task and the reasoning behind specific methodological choices. The introduction has been revised, and a new conceptual figure added, to better explain how specific results support the conclusions reached. A control experiment has been added to resolve the question of whether participants undershoot the visual cue because they are minimizing their physical effort (a confound) or because they are recalibrating their visual estimate of its location. The control experiment clearly contradicts the idea of effort minimization. Other changes to the presentation of the data and methods have been made to improve clarity.