Modulation Dynamics in the Orofacial Sensorimotor Cortex during Motor Skill Acquisition

Abstract

The orofacial sensorimotor cortex is known to play a role in motor learning. However, how motor learning changes the dynamics of neuronal activity and whether these changes differ between orofacial primary motor (MIo) and somatosensory (SIo) cortices remain unknown. To address these questions, we used chronically implanted microelectrode arrays to track learning-induced changes in the activity of simultaneously recorded neurons in MIo and SIo as two naive monkeys (Macaca mulatta) were trained in a novel tongue-protrusion task. Over a period of 8-12 d, the monkeys showed behavioral improvements in task performance that were accompanied by rapid and long-lasting changes in neuronal responses in MIo and SIo occurring in parallel: (1) increases in the proportion of task-modulated neurons, (2) increases in the mutual information between tongue-protrusive force and spiking activity, (3) reductions in the across-trial firing rate variability, and (4) transient increases in coherent firing of neuronal pairs. More importantly, the time-resolved mutual information in MIo and SIo exhibited temporal alignment. While showing parallel changes, MIo neurons exhibited a bimodal distribution of peak correlation lag times between spiking activity and force, whereas SIo neurons showed a unimodal distribution. Moreover, coherent activity between pairs of MIo neurons was higher and centered around force onset compared with pairwise coherence of SIo neurons. Overall, the results suggest that the neuroplasticity in MIo and SIo occurring in parallel serves as a substrate for linking sensation and movement during sensorimotor learning, whereas the differing dynamic organizations reflect specific ways to control movement parameters as learning progresses.