Cortical midfrontal theta dynamics following foot strike may index response adaptation during reactive stepping

Abstract

Reactive balance recovery often requires stepping responses to regain postural stability following a sudden change in posture. The monitoring of postural stability has been linked to neuroelectrical markers such as the N1 potential and midfrontal theta frequency dynamics. Here, we investigated the role of cortical midfrontal theta dynamics during balance monitoring following foot landing of a reactive stepping response to recover from whole-body balance perturbations. We hypothesized that midfrontal theta dynamics reflect the engagement of a behavioral monitoring system, and therefore that theta would increase time-locked to the moment of foot strike after a stepping response, coinciding with a re-assessment of postural balance to determine if an additional step is necessary. We recorded high-density EEG and kinematic data of 15 healthy young participants while they stood on a platform that delivered multi-directional balance perturbations. Participants were instructed to recover balance with a single step utilizing either their left or right leg (in separate blocks). We used targeted spatial filtering (generalized eigen decomposition) in combination with time–frequency analysis of the EEG data to investigate whether theta dynamics increase following foot strike event. In line with our hypothesis, the results indicate that the foot strike event elicits a midfrontal theta power increase, though only for backward stepping. Counter to our expectations, however, this theta power increase was positively correlated with the margin of stability at foot strike, suggesting a different role of foot strike related theta from monitoring stability. Post-hoc analysis suggests that midfrontal theta dynamics following foot landing may instead facilitate adaptation of stability margins at subsequent stepping responses. We speculate that increase of theta power following foot strikes was not related to stability monitoring but instead may indicate cortical dynamics related to performance monitoring of the balance response.

Exploring Electrocortical Signatures of Gait Adaptation: Differential Neural Dynamics in Slow and Fast Gait Adapters

“…We quantified electrocortical activity during locomotor adaptation to a split-belt treadmill perturbation and examined differences in gait-related spectral power between two groups, sorted based on how quickly they restored their gait symmetry. Evidence from EEG recorded during locomotor adaptation suggests that alpha (8-12 Hz), beta (13-30 Hz), and theta (4-7 Hz) oscillations may be related to motor error monitoring (Sipp et al, 2013;Tan et al, 2014), standing postural stability (Solis-Escalante et al, 2021;Stokkermans et al, 2022), and balance perturbations during walking (Peterson & Ferris, 2018). Gait-related spectral perturbation data from the posterior parietal, sensorimotor, and anterior cingulate cortices under the same conditions have been published previously.…”

“…Given the association between midfrontal electrocortical dynamics, error awareness (Ficarella et al, 2019), and balance ability (Payne & Ting, 2020;Sipp et al, 2013;Solis-Escalante et al, 2020;Stokkermans et al, 2022), it is surprising there were no significant group differences in this brain region.…”

Unraveling the threads of stability: A review of the neurophysiology of postural control in Parkinson's disease

“…More specifically, different brain regions seem to display task-related frequency changes during reactive postural control challenges. At the fronto-central cortical regions, increased delta and theta power have been associated with the maintenance of standing balance during progressively more difficult tasks and reactive stepping responses following perturbation, suggesting their roles in situations requiring higher attention and cognitive demands when conditions become unstable [ 57 , [61] , [62] , [63] , [64] , [65] , [66] ].…”

“…In these same regions, increased alpha power was found to be associated with perturbation onset [ 57 , 62 ] and altered by one's attentional focus under conflicting visual input [ 67 ], while trends in alpha modulation appear sub-band dependent and largely decrease during progressively more difficult reactive balance tests [ 64 , 66 , 68 ]. These findings support hypotheses that alpha power reflects perhaps complementary, higher-level sensory processing and/or inhibitory mechanisms to control the degrees of freedom available for reactive balance responses [ 64 , 66 ].…”