Precise cortical contributions to sensorimotor feedback control during reactive balance

The role of the cortex in shaping automatic whole-body motor behaviors such as walking and balance is poorly understood. Gait and balance are typically mediated through subcortical circuits, with the cortex becoming engaged as needed on an individual basis by task difficulty and complexity. However, we lack a mechanistic understanding of how increased cortical contribution to whole-body movements shapes motor output. Here we use reactive balance recovery as a paradigm to identify relationships between hierarchical control mechanisms and their engagement across balance tasks of increasing difficulty in young adults. We hypothesize that parallel sensorimotor feedback loops engaging subcortical and cortical circuits contribute to balance-correcting muscle activity, and that the involvement of cortical circuits increases with balance challenge. We decomposed balance-correcting muscle activity based on hypothesized subcortically- and cortically-mediated feedback components driven by similar sensory information, but with different loop delays. The initial balance-correcting muscle activity was engaged at all levels of balance difficulty. Its onset latency was consistent with subcortical sensorimotor loops observed in the lower limb. An even later, presumed, cortically-mediated burst of muscle activity became additionally engaged as balance task difficulty increased, at latencies consistent with longer transcortical sensorimotor loops. We further demonstrate that evoked cortical activity in central midline areas measured using electroencephalography (EEG) can be explained by a similar sensory transformation as muscle activity but at a delay consistent with its role in a transcortical loop driving later cortical contributions to balance-correcting muscle activity. These results demonstrate that a neuromechanical model of muscle activity can be used to infer cortical contributions to muscle activity without recording brain activity. Our model may provide a useful framework for evaluating changes in cortical contributions to balance that are associated with falls in older adults and in neurological disorders such as Parkinson's disease. Our goal is to gain a mechanistic understanding of how cortical and subcortical systems shape motor output in whole-body movements. Using novel neuromechanical models, we identify how cortical and subcortical control mechanisms differentially contribute to balance-correcting muscle activity across reactive balance task difficulty. Bursts of balance-correcting muscle activity in young adults were decomposed into parallel sensorimotor feedback components driven by balance error but acting at different loop latencies. Corroborating the transcortical nature of the longer latency loop, we showed that evoked cortical responses to perturbations were also driven by balance error. While the contributions of the faster subcortical loop to muscle activity was present in all perturbation levels, the slower cortically-mediated burst of muscle was increasingly engaged with difficulty level. Our computational framework thus dissociates cortical and subcortical muscle activity components of balance control which may be useful to inform balance training and rehabilitation.