Oscillatory and transient mechanisms of muscle inhibition during anticipatory postural control in adults and in children with and without ASD

Overview & Synopsis

In motor networks, inhibition has been associated with oscillatory activity in the mu (8-12 Hz) and beta (13-30 Hz) bands, yet the mechanisms by which these rhythms exert inhibitory modulation at the muscular level remain unclear. In this project, we investigated such mechanisms by tracking anticipatory inhibition of the elbow flexors in the load-supporting arm during a naturalistic bimanual load-lifting task. Using magnetoencephalography, which combines high temporal and good spatial resolution, we examined the neural pathways and the oscillatory and transient dynamics underlying this muscle inhibition. The thesis comprises three conceptual parts: the first elucidates the mechanisms of mature anticipatory inhibition in adults; the second examines its developmental trajectory in typically developing children; and the third investigates alterations of this mechanism in children with Autism Spectrum Disorders (ASD), in whom altered anticipatory postural control has been reported. In the bimanual load-lifting task, anticipatory inhibition of the elbow flexors in the load-supporting arm stabilizes the forearm during voluntary lifting. This inhibition manifests as a suppression of muscle activity, which allows investigation of both anticipatory postural control and the neural mechanisms of motor inhibition, given its clear signature at the muscle level. We showed that, in adults, optimal postural stabilization occurred when Biceps brachii inhibition preceded unloading by ~30 ms. In contrast, children exhibited broad variability in inhibition timing, consistent with the ongoing maturation of anticipatory postural control. In both groups, stronger suppression of Biceps brachii activity was associated with reduced cortical excitability – indexed by high-gamma (90-130 Hz) power – and a transient increase of high-beta power (19-30 Hz) in the contralateral Supplementary Motor Area (SMA). Furthermore, in SMA, trials with high-frequency beta bursts exhibited high-gamma suppression locked to the burst peak. During these bursts, in both groups we observed directed connectivity from the lateral PFC (middle frontal gyrus) and from premotor/M1 cortex to the SMA, preceding SMA burst peak by ~30-40 ms, suggesting their involvement in SMA inhibition. In children, we further observed that SMA beta bursts at the highest frequency (24-30 Hz) were only indirectly related to SMA suppression, as evidenced by a high-gamma power decrease ~100 ms after the burst peak. The association with earlier onset and postural stabilization in these trials suggests that these bursts act as a compensatory mechanism when anticipatory control is less efficient. In contrast, ASD children showed inhibition onset ~25 ms later than in control children, and although the inhibition peak time was comparable, no SMA inhibition was observed in this group, suggesting that a different mechanism is implicated. Together, our findings suggest that during voluntary load-lifting, optimally timed anticipatory inhibition of the load-supporting elbow flexor is achieved through SMA suppression mediated by inhibitory beta bursts. Additional corrective mechanisms can support postural stabilization when anticipatory control is suboptimal during development. Evidence in children with ASD suggests that they utilize a different mechanism for postural control which lacks anticipatory component. To our knowledge, these results provide the first evidence that beta bursts can exert direct inhibitory control over muscle function, while revealing differences in this mechanism between children with and without ASD. Beyond advancing the understanding of anticipatory postural mechanisms, our findings also inform existing knowledge on motor inhibition and underscore the importance of capturing the true temporal variability of beta-band activity in transient bursts to elucidate the functional roles of beta oscillations.