Oral somatosensation shapes lingual muscle maps in macaque orofacial primary motor cortex

Abstract

Oral behaviors such as chewing, swallowing, and speech depend on continuous sensory feedback from the tongue and oral tissues. Yet how oral somatosensation shapes motor cortical output to drive individual tongue muscles remains unknown. We combined electrical stimulation of 96 sites in the orofacial primary motor cortex (M1) with electromyographic (EMG) recordings from six tongue muscles in awake rhesus macaques (Macaca mulatta). Cortical motor maps of evoked muscle activity were evaluated under three oral sensory conditions: intact sensation, combined oral sensory nerve block, and selective preservation of tongue sensation. Orofacial M1 has a broadly distributed, strongly overlapping, and bilateral organization of individual tongue muscle representations. Under altered sensation, spatial reorganization, attenuation, and enhancement of cortical-to-muscle output emerged within a fast timescale. Selectively preserving tongue sensation neither restored the intact pattern, nor reproduced the combined nerve block pattern; instead, it generated a spatially distinct configuration of cortical-to-muscle outputs. Together, these findings demonstrate muscle-level, input-specific, and dynamic sensory shaping in orofacial M1, establishing oral somatosensory input as an active determinant of tongue-muscle output, rather than a peripheral modulator. The rapid reorganization suggests that altered sensation qualitatively reweights existing sensorimotor pathways, rather than merely scaling cortical output up or down, such that its disruption could immediately degrade tongue muscle coordination while enabling adaptation to sensory loss.