Abstract
Human’s ability to coordinate stereotyped, alternating movements between the two legs during bipedal walking is a complex motor behavior that requires precisely timed activities across multiple nodes of the supraspinal network. Understanding of the neural network dynamics that underlie natural walking in humans is limited. We investigated cortical and subthalamic neural activities during overground walking and evaluated spectral biomarkers to decode the gait cycle in three patients with Parkinson’s disease without gait disturbances. Patients were implanted with chronic bilateral deep brain stimulation leads in the subthalamic nucleus (STN) and electrocorticography paddles overlaying the primary motor (M1) and somatosensory (S1) cortices. Local field potentials (LFP) were recorded from these areas while the participants performed overground walking and synchronized to external gait kinematic sensors. We found that the STN displays increased low frequency (4-12 Hz) spectral power during the period prior to contralateral leg swing. Furthermore, STN shows increased theta frequency (4-8 Hz) coherence with the primary motor through the initiation and early phase of contralateral leg swing. Additional analysis revealed that each patient had specific frequency bands which could detect a significant difference between left and right initial leg-swing. Our findings indicate that there is alternating spectral changes between the two hemispheres in accordance with the gait cycle. In addition, we identified patient-specific, gait-related biomarkers in both the STN and cortical areas at discrete frequency bands that may be used to drive adaptive DBS to improve gait dysfunction in patients with Parkinson’s disease.
Significance Statement
By recording from chronically implanted electrodes from the subthalamic nucleus and sensorimotor cortex in patients with Parkinson's disease, we found power modulations across multiple frequency bands (4-30 Hz) during specific phases of the gait cycle. The coherence between subthalamic-cortical areas of each brain hemisphere also increases prior to contralateral leg swing. The data supports the hypothesis that the basal ganglia and cortex coordinate alternating power and coherence fluctuations between hemispheres, which may indicate a mechanism to regulate continuous bipedal locomotion in humans. Lastly, we show that these putative biomarkers for gait can decode left and right gait events, implicating a potential use to drive future adaptive DBS algorithms.
Footnotes
The Authors report no conflict of interest.
This study was sponsored by NIH/NINDS K12 (NS080223), Burroughs Wellcome Fund Career Award for Medical Scientist, and Michael J Fox Foundation (MNS135499A). All funding was acquired by DDW.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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