Electrocorticography is superior to subthalamic local field potentials for movement decoding in Parkinson’s disease

Author:

Merk Timon1ORCID,Peterson Victoria23,Lipski Witold J4ORCID,Blankertz Benjamin5ORCID,Turner Robert S4ORCID,Li Ningfei1,Horn Andreas1ORCID,Richardson Robert Mark23ORCID,Neumann Wolf-Julian1ORCID

Affiliation:

1. Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt Universität zu Berlin

2. Brain Modulation Lab, Department of Neurosurgery, Massachusetts General Hospital

3. Harvard Medical School

4. Department of Neurobiology, University of Pittsburgh

5. Department of Computer Science, Technische Universität Berln

Abstract

Brain signal decoding promises significant advances in the development of clinical brain computer interfaces (BCI). In Parkinson’s disease (PD), first bidirectional BCI implants for adaptive deep brain stimulation (DBS) are now available. Brain signal decoding can extend the clinical utility of adaptive DBS but the impact of neural source, computational methods and PD pathophysiology on decoding performance are unknown. This represents an unmet need for the development of future neurotechnology. To address this, we developed an invasive brain-signal decoding approach based on intraoperative sensorimotor electrocorticography (ECoG) and subthalamic LFP to predict grip-force, a representative movement decoding application, in 11 PD patients undergoing DBS. We demonstrate that ECoG is superior to subthalamic LFP for accurate grip-force decoding. Gradient boosted decision trees (XGBOOST) outperformed other model architectures. ECoG based decoding performance negatively correlated with motor impairment, which could be attributed to subthalamic beta bursts in the motor preparation and movement period. This highlights the impact of PD pathophysiology on the neural capacity to encode movement vigor. Finally, we developed a connectomic analysis that could predict grip-force decoding performance of individual ECoG channels across patients by using their connectomic fingerprints. Our study provides a neurophysiological and computational framework for invasive brain signal decoding to aid the development of an individualized precision-medicine approach to intelligent adaptive DBS.

Funder

National Institutes of Health

Bundesministerium für Bildung und Forschung

Deutsche Forschungsgemeinschaft

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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