Peripheral Somatosensory Entrainment Modulates the Cross-Frequency Coupling of Movement-Related Theta-Gamma Oscillations

Abstract

Introduction:

Motor control requires a reciprocal volley between somatosensory and motor systems, with somatosensory feedback being essential for the online updating of motor commands to achieve behavioral outcomes. However, this dynamic interplay among sensorimotor brain systems serving motor control remains poorly understood.

Methods:

To address this, we designed a novel somatosensory entrainment-movement task, which 25 adults completed during magnetoencephalography (MEG). Specifically, participants completed a quasi-paced finger-tapping paradigm while subthreshold electrical stimulation was applied to the right median nerve at a sensorimotor-relevant frequency (15 Hz) and during a second condition where no electrical stimulation was applied. The MEG data were transformed into the time-frequency domain and imaged by using a beamformer to evaluate the effect of somatosensory feedback (i.e., entrainment) on movement-related oscillations and motor performance at the single trial level.

Results:

Our results indicated spectrally specific reductions in movement-related oscillatory power (i.e., theta, gamma) during 15 Hz stimulation in the contralateral motor cortex during motor execution. In addition, we observed robust cross-frequency coupling within the motor cortex and further, stronger theta-gamma coupling was predictive of faster reaction times, irrespective of condition (i.e., stim vs. no stim). Finally, in the presence of electrical stimulation, cross-frequency coupling of movement-related oscillations was reduced, and the stronger the entrained neuronal populations (i.e., increased oscillatory power) were before movement onset, the weaker the inherent theta-gamma coupling became in the motor cortex.

Discussion:

This novel exogenous manipulation paradigm provides key insights on how the somatosensory system modulates the motor cortical oscillations required for volitional movement in the normative sensorimotor system.

Impact statement

Functional coupling of neural oscillations has been proposed as a mechanism for neuronal communication both locally and across the cortex. Although the nested coupling of disparate rhythms governs higher-order cognitive processes, its role in the sensorimotor interactions serving motor control remains poorly understood. Herein, we provide evidence for a robust coupling of theta and gamma oscillations during motor execution in the presence and absence of continuous somatosensory feedback, with stronger functional coupling predictive of behavioral improvements. Further, stronger entrainment of neuronal populations led to substantially weakened motor cortical theta-gamma coupling, indicative of a dynamic interplay among sensorimotor cortices during movement.