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 three-dimensional (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 video-radiography, we tracked implanted tongue markers in behaving rhesus macaques (<i>Macaca mulatta</i>) 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 at both individual and population levels 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. This study advances our understanding of single-neuron and population activity in OSMCx and their potential contributions to the sensorimotor control of complex naturalistic tongue movements. By extending current knowledge of orofacial control to 3D tongue movements, our findings demonstrate the specificity and adaptability of population activity in MIo and SIo in response to different behavioral contexts, providing important insights for understanding neural mechanisms underlying skilled tongue control.