Motor somatotopy impacts imagery strategy success in human intracortical brain-computer interfaces

Abstract

The notion of a somatotopically organized motor cortex, with movements of different body parts being controlled by spatially distinct areas of cortex, is well known. However, recent studies have challenged this notion and suggested a more distributed representation of movement control. This shift in perspective has significant implications, particularly when considering the implantation location of electrode arrays for intracortical brain-computer interfaces (iBCIs). We sought to evaluate whether the location of neural recordings from the precentral gyrus, and thus the underlying somatotopy, has any impact on the imagery strategies that can enable successful iBCI control. Three individuals with a spinal cord injury were enrolled in an ongoing clinical trial of an iBCI. Participants had two intracortical microelectrode arrays implanted in the arm and/or hand areas of the precentral gyrus based on presurgical functional imaging. Neural data were recorded while participants attempted to perform movements of the hand, wrist, elbow, and shoulder. We found that electrode arrays that were located more medially recorded significantly more activity during attempted proximal arm movements (elbow, shoulder) than did lateral arrays, which captured more activity related to attempted distal arm movements (hand, wrist). We also evaluated the relative contribution from the two arrays implanted in each participant to decoding accuracy during calibration of an iBCI decoder for translation and grasping tasks. For both task types, imagery strategy (e.g., reaching vs. wrist movements) had a significant impact on the relative contributions of each array to decoding. Overall, we found some evidence of broad tuning to arm and hand movements; however, there was a clear bias in the amount of information accessible about each movement type in spatially distinct areas of cortex. These results demonstrate that classical concepts of somatotopy can have real consequences for iBCI use, and highlight the importance of considering somatotopy when planning iBCI implantation.

Competing Interest Statement

N.H. has a consulting agreement with Blackrock Microsystems.

Clinical Trial

NCT01894802

Clinical Protocols

https://clinicaltrials.gov/study/NCT01894802

Funding Statement

This work was supported by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under Award Numbers UH3NS107714 and R01NS121079, as well as the Swiss National Science Foundation under Award Number P500PM_210800.

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The details of the IRB/oversight body that provided approval or exemption for the research described are given below:

This study was conducted under an Investigational Device Exemption from the Food and Drug Administration and approved by the Institutional Review Boards at the University of Pittsburgh and the University of Chicago. This study is registered on clinicaltrials.gov (NCT01894802). Informed consent was obtained from all participants before any study procedures were conducted. All research was conducted in accordance with the Declaration of Helsinki and with local statutory requirements.

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Data Availability

Data supporting the findings of this study will be available upon request and completion of a brief data use agreement at https://dabi.loni.usc.edu.

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