Abstract
The contributions of the cerebral cortex to human balance control are clearly demonstrated by the profound impact of cortical lesions on the ability to maintain standing balance. The cerebral cortex is thought to regulate subcortical postural centers to maintain upright balance and posture under varying environmental conditions and task demands. However, the cortical mechanisms that support standing balance remain elusive. Here, we present an EEG-based analysis of cortical oscillatory dynamics during the preparation and execution of balance responses with distinct postural demands. In our experiment, participants responded to backward movements of the support surface either with one forward step or by keeping their feet in place. To challenge the postural control system, we applied participant-specific high accelerations of the support surface such that the postural demand was low for stepping responses and high for feet-in-place responses. We expected that postural demand modulated the power of intrinsic cortical oscillations.Independent component analysis and time-frequency domain statistics revealed stronger suppression of alpha (9–13 Hz) and low-gamma (31–34 Hz) rhythms in the supplementary motor area (SMA) when preparing for feet-in-place responses (i.e., high postural demand). Irrespective of the response condition, support-surface movements elicited broadband (3–17 Hz) power increase in the SMA and enhancement of the theta (3–7 Hz) rhythm in the anterior prefrontal cortex (PFC), anterior cingulate cortex (ACC), and bilateral sensorimotor cortices (M1/S1). Although the execution of reactive responses resulted in largely similar cortical dynamics, comparison between the bilateral M1/S1 showed that stepping responses corresponded with stronger suppression of the beta (13–17 Hz) rhythm in the M1/S1 contralateral to the support leg. Comparison between response conditions showed that feet-in-place responses corresponded with stronger enhancement of the theta (3–7 Hz) rhythm in the PFC. Our results provide novel insights into the cortical dynamics of SMA, PFC, and M1/S1 during the control of human balance.
Highlights
Balance control is a complex motor task controlled by neural ensembles in the spinal cord, brainstem, cerebellum, and cerebral cortex (Nutt et al, 2011; Takakusaki, 2017)
Early animal studies suggested limited participation of the cerebral cortex in controlling balance and posture (Magnus, 1926; Sherrington, 1910), recent evidence from human studies indicates that the cerebral cortex may regulate the excitability of subcortical postural centers to maintain balance and postural stability according to environmental demands (Bohnen and Jahn, 2013; Jahn and Zwergal, 2010; Peterson and Horak, 2016)
The distinct whole-body movements and postural demands of the stepping and feetin-place responses resulted in largely similar oscillatory dynamics during the response execution phase, with two notable differences: reactive feet-in-place responses corresponded with stronger theta enhancement in prefrontal cortex (PFC), and, during reactive stepping, asymmetric vertical load during single support corresponded with stronger beta suppression in M1/S1 contralateral to the support leg
Summary
Balance control is a complex motor task controlled by neural ensembles in the spinal cord, brainstem, cerebellum, and cerebral cortex (Nutt et al, 2011; Takakusaki, 2017). Analysis of scalp-level event-related potentials elicited by whole-body mechanical perturbations to standing balance (see Varghese et al (2017); Wittenberg et al (2017) for recent reviews), whereas only few studies have investigated the scalp-level spectral characteristics of cortical activity elicited by such perturbations (Mierau et al, 2017; Varghese et al, 2014). Time-frequency analysis of the EEG can reveal changes to specific cortical dynamics in relation to internal and external events (Makeig, 1993; Pfurtscheller and Lopes da Silva, 1999). Low-frequency cortical rhythms (13 Hz) are commonly associated with motor function (Engel and Fries, 2010; Muthukumaraswamy, 2010; Neuper and Pfurtscheller, 2001)
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