Trial-by-trial source-resolved EEG responses to gait task challenges predict subsequent step adaptation

A growing body of evidence indicates a pivotal role of cognition and in particular executive function in gait control and fall prevention. In a recent gait study using electroencephalographic (EEG) imaging, we provided direct proof for cortical top-down inhibitory control in step adaptation. A crucial part of motor inhibition is recognizing stimuli that signal the need to inhibit or adjust motor actions such as steps during walking. One of the EEG signatures of performance monitoring in response to events signaling the need to adjust motor responses, are error-related potential (error-ERP) features. To examine whether error-ERP features may index executive control during gait adaptation, we analyzed high-density (108-channel) EEG data from an auditory gait pacing study. Participants (N = 18) walking on a steadily moving treadmill were asked to step in time to an auditory cue tone sequence, and then to quickly adapt their step length and rate, to regain step-cue synchrony following occasional unexpected shifts in the pacing cue train to a faster or slower cue tempo. Decomposition of the continuous EEG data by independent component analysis revealed a negative deflection in the source-resolved event-related potential (ERP) time locked to ‘late’ cue tones marking a shift to a slower cue tempo. This vertex-negative ERP feature, localized primarily to posterior medial frontal cortex (pMFC) and peaking 250 ms after the onset of the tempo-shift cue, we here refer to as the step-cue delay negativity (SDN). SDN source, timing, and polarity resemble other error-related ERP features, e.g., the Error-Related Negativity (ERN) and Feedback-Related Negativity (FRN) in (seated) button press response tasks. In single trials, SDN amplitude varied with the magnitude of the cue latency deviation (the time interval between the expected and actual cue onsets). Regression analysis also identified linear coupling between SDN amplitude and the subsequent speed of gait tempo adaptation (as measured by the increase in length of the ensuing adaptation step). The SDN in this paradigm thus seems both to index the perceived need for and the subsequent magnitude of the immediate gait adjustment, consistent with performance-monitoring models. Future research might investigate relationships of these control processes to the impairment of gait adjustment in motor disorders and cognitive decline, for example to develop a biomarker for fall risk prediction in early-stage Parkinson's.