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 tongueprotrusion 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 taskmodulated 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.

Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies

“…Similar patterns were observed for the mean MS coherence across neuronal pairs with significant modulation of coherence (Fig. 2D, shuffle test, P < 0.01), consistent with the task modulation of theta coherence previously found within MIo and within SIo (16). Out of all of the possible combinations of paired signals (n = 44,152) from 10 datasets, the proportion of neuronal pairs that showed significant task modulation of MS coherence (i.e., "functional network") was highest in theta and was significantly lower in the higher frequency bands (Fig.…”

“…To investigate cortico-cortical interactions between these areas, we measured coherence of spiking and local field potentials (LFPs) recorded simultaneously from MIo and SIo of the left hemisphere as monkeys learned a simple and controlled tongue protrusion task. Several studies using this behavioral paradigm have reported neuroplasticity and modulation of neuronal activity related to tongue protrusion separately in MIo and SIo (13)(14)(15)(16)(17). Here, we show that interactions between MIo and SIo involve coherent networks at multiple frequencies.…”

“…2A) These measures of coherence are presumed to represent the correlation of the outputs from both areas (MS) and the correlation of the outputs from one area with the inputs in the other (MSf and SMf). For each of the 5 sampled training days, D1-D5, we estimated coherence by using a 0.5-s sliding window with 0.01-s steps to show a time-resolved coherence profile in the theta (2-6 Hz), alpha (6-13 Hz), beta (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30), and gamma (30-50 Hz) bands. Coherence in these frequency bands is believed to play a role in attention, memory, motor control, and plasticity (16,(18)(19)(20).…”

“…For each of the 5 sampled training days, D1-D5, we estimated coherence by using a 0.5-s sliding window with 0.01-s steps to show a time-resolved coherence profile in the theta (2-6 Hz), alpha (6-13 Hz), beta (15-30 Hz), and gamma (30-50 Hz) bands. Coherence in these frequency bands is believed to play a role in attention, memory, motor control, and plasticity (16,(18)(19)(20). As Significance Sensorimotor integration is important for the acquisition and performance of motor skills.…”

Chronic recordings reveal tactile stimuli can suppress spontaneous activity of neurons in somatosensory cortex of awake and anesthetized primates

“…2B. These changes in neuronal recordings, based on characteristics of the extracellular recordings over weeks of time, are consistent with other examinations of the recording stability (Arce-McShane et al 2014;Dickey et al 2009). …”