Cortical responses to balance perturbations persist without active postural control

Abstract

Standing balance relies on rapid reflexes as well as longer-latency subcortical and cortical processes to generate corrective responses to postural disturbances. Electroencephalography (EEG) studies consistently identify two perturbation-evoked markers of cortical activity, the balance N1 and midfrontal theta power, associated with changes in body orientation and corrective actions. It remains unclear, however, whether these markers depend on the nervous systems active control of posture or reflect a more general evaluation of unexpected sensory input. We tested this by measuring cortical and muscle activity during support-surface perturbations while systematically manipulating whether participants actively controlled posture. In Experiment 1 (n = 10), participants experienced identical perturbations while either actively balancing or being passively moved through equivalent motion. Despite large reductions in balance-correcting muscle activity during passive trials ([~]30-60%), N1 and theta responses persisted with only modest amplitude reductions ([~]10%). In Experiment 2 (n = 16), we created passive conditions increasingly removed from balance by varying sensory feedback (footplate + whole-body vs footplate-only motion) and motor engagement (isometric contraction vs. relaxed posture). Relaxed postures markedly suppressed muscle responses, yet cortical responses persisted, showing only modest modulation with sensory feedback (larger during footplate-only rotations) and no dependence on motor engagement. Together, these results indicate that N1 and midfrontal theta are not dependent on active postural control and persist even without matching sensory feedback or motor engagement. Rather than reflecting the generation or scaling of corrective actions, they index the early detection and evaluation of unexpected sensory events, consistent with prediction error or surprise processing. Key pointsO_LIWhen standing balance is disturbed by a perturbation, the brain shows characteristic electrical responses called the balance N1 and theta activity, which are thought to contribute to balance-correcting actions. C_LIO_LIWe tested whether these cortical responses depend on actively controlling posture or instead reflect the detection of unexpected motion irrespective of balance conditions. C_LIO_LIParticipants stood in a robotic balance simulator and experienced identical perturbations while actively balancing or being passively moved, and when whole-body sensory feedback and muscle engagement were removed. C_LIO_LIThe balance N1 and theta activity persisted in conditions where participants were not controlling their movement and even when whole-body sensory feedback and motor engagement were removed, whereas balance-correcting muscle responses were strongly diminished. C_LIO_LIThis shows that cortical responses to balance perturbations are not specific to active balance control but likely represent the brains detection and evaluation of unexpected sensory events. C_LI