Cortical theta–gamma coupling governs the adaptive control of motor commands

Abstract

Abstract Motor control requires the adaptive updating of internal models to successfully target desired outcomes. This adaptive control can be proactive, such that imminent actions and corresponding sensorimotor programmes are anticipated prior to movement, or reactive, such that online error correction is necessary to adjust to sudden changes. While substantial evidence implicates a distributed cortical network serving adaptive control when behavioural changes are required (e.g. response inhibition), the neural dynamics serving such control when the target motor commands are to remain intact are poorly understood. To address this, we developed a novel proactive–reactive cued finger tapping paradigm that was performed during magnetoencephalography by 25 healthy adults. Importantly, to ensure condition-wise differences in adaptive cueing were not attributable to changes in movement kinematics, motor selection and planning processes were held constant despite changes in task demands. All data were imaged in the time-frequency domain using a beamformer to evaluate the effect of proactive and reactive cues on movement-related oscillations and subsequent performance. Our results indicated spectrally specific increases in low (i.e. theta) and high (i.e. gamma) frequency oscillations during motor execution as a function of adaptive cueing. Additionally, we observed robust cross-frequency coupling of theta and gamma oscillatory power in the contralateral motor cortex and further, the strength of this theta–gamma coupling during motor execution was differentially predictive of behavioural improvements and decrements during reactive and proactive trials, respectively. These data indicate that functional oscillatory coupling may govern the adaptive control of movement in the healthy brain and importantly, may serve as effective proxies for characterizing declines in motor function in clinical populations in the future.