3D directional tuning in the orofacial sensorimotor cortex during natural feeding and drinking

Directional tongue movements are crucial for feeding and speech, ensuring proper food positioning for chewing and swallowing, as well as accurate sound production. While directional tuning in the arm region of the sensorimotor cortex during reaching tasks is well-studied, little is known about how 3D tongue direction is encoded in the orofacial sensorimotor cortex (OSMCx) during natural behaviors. Understanding this neural representation has important implications for rehabilitating individuals with orolingual dysfunctions. This study examines the directional tuning and population dynamics in OSMCx during naturalistic feeding and drinking, and how these are affected by sensory loss. Using biplanar videoradiography, we tracked implanted tongue markers in behaving rhesus macaques (Macaca mulatta) and simultaneously recorded 3D positional data with spiking activity from chronically implanted microelectrode arrays in primary motor (MIo) and somatosensory (SIo) areas of the orofacial cortex. In some sessions, tasks were preceded by bilateral nerve block injections to the sensory branches of the trigeminal nerve. Modulation to 3D tongue direction during feeding and drinking was found in most MIo and SIo neurons. Directional information in both individual- and population-level was higher in feeding and was more robust in MIo. Following sensory loss, alterations in tongue kinematics were accompanied by changes in directional information in MIo and SIo, manifesting as modifications in both individual neuron tuning characteristics and the broader dynamics of population-level neural activity. Overall, this study advances our understanding of how OSMCx contributes to complex, coordinated control of naturalistic tongue movements. It expands our current knowledge of orofacial control to three dimensions and demonstrates the specificity and adaptability of population activity in MIo and SIo in response to different behavioral contexts.