Distinct β Band Oscillatory Networks Subserving Motor and Cognitive Control during Gait Adaptation

Everyday locomotion and obstacle avoidance requires effective gait adaptation in response to sensory cues. Many studies have shown that efficient motor actions are associated with μ rhythm (8-13 Hz) and β band (13-35 Hz) local field desynchronizations in sensorimotor and parietal cortex, whereas a number of cognitive task studies have reported higher behavioral accuracy to be associated with increases in β band power in prefrontal and sensory cortex. How these two distinct patterns of β band oscillations interplay during gait adaptation, however, has not been established. Here we recorded 108 channel EEG activity from 18 participants (10 males, 22-35 years old) attempting to walk on a treadmill in synchrony with a series of pacing cue tones, and quickly adapting their step rate and length to sudden shifts in pacing cue tempo. Independent component analysis parsed each participant's EEG data into maximally independent component (IC) source processes, which were then grouped across participants into distinct spatial/spectral clusters. Following cue tempo shifts, mean β band power was suppressed for IC sources in central midline and parietal regions, whereas mean β band power increased in IC sources in or near medial prefrontal and dorsolateral prefrontal cortex. In the right dorsolateral prefrontal cortex IC cluster, the β band power increase was stronger during (more effortful) step shortening than during step lengthening. These results thus show that two distinct patterns of β band activity modulation accompany gait adaptations: one likely serving movement initiation and execution; and the other, motor control and inhibition.

Significance statement: Understanding brain dynamics supporting gait adaptation is crucial for understanding motor deficits in walking, such as those associated with aging, stroke, and Parkinson's. Only a few electromagnetic brain imaging studies have examined neural correlates of human upright walking. Here, application of independent component analysis to EEG data recorded during treadmill walking allowed us to uncover two distinct β band oscillatory cortical networks that are active during gait adaptation to shifts in the tempo of an auditory pacing cue: (8-13 Hz) μ rhythm and (13-35 Hz) β band power decreases in central and parietal cortex and (14-20 Hz) β band power increases in frontal brain areas. These results provide a fuller framework for electrophysiological studies of cortical gait control and its disorders.