Error-related modulations of the sensorimotor post-movement and foreperiod beta-band activities arise from distinct neural substrates and do not reflect efferent signal processing

Abstract

While beta activity has been extensively studied in relation to voluntary movement, its role in sensorimotor adaptation remains largely uncertain. Recently, it has been shown that the post-movement beta rebound as well as beta activity during movement-preparation are modulated by movement errors. However, there are critical functional differences between pre- and post-movement beta activities. Here, we addressed two related open questions. Do the pre- and post-movement error-related modulations arise from distinct neural substrates? Do these modulations relate to efferent signals shaping muscle-activation patterns or do they reflect integration of sensory information, intervening upstream of the motor output? For this purpose, first we exploited independent component analysis (ICA) which revealed a double dissociation suggesting that distinct neural substrates are recruited in error-related beta-power modulations observed before and after movement. Second, we compared error-related beta oscillation responses observed in two bimanual reaching tasks involving similar movements but different interlimb coordination, and in which the same mechanical perturbations induced different behavioral adaptive responses. While the task difference was not reflected in the post-movement beta rebound, the pre-movement beta activity was differently modulated according to the interlimb coordination. Critically, we show an uncoupling between the behavioral and the electrophysiological responses during the movement preparation phase, which demonstrates that the error-related modulation of the foreperiod beta activity does not reflect changes in the motor output from primary motor cortex. It seems instead to relate to higher level processing of sensory afferents, essential for sensorimotor adaptation.