Volitional control of single-electrode high gamma local field potentials by people with paralysis

Author:

Milekovic Tomislav123ORCID,Bacher Daniel24,Sarma Anish A.245,Simeral John D.245,Saab Jad24,Pandarinath Chethan678,Yvert Blaise129,Sorice Brittany L.10,Blabe Christine6,Oakley Erin M.10,Tringale Kathryn R.10,Eskandar Emad1112,Cash Sydney S.1012,Shenoy Krishna V.78131415,Henderson Jaimie M.6816,Hochberg Leigh R.2451012,Donoghue John P.125

Affiliation:

1. Department of Neuroscience, Brown University, Providence, Rhode Island

2. Carney Institute for Brain Science, Brown University, Providence, Rhode Island

3. Department of Fundamental Neuroscience, Faculty of Medicine, University of Geneva, Geneva, Switzerland

4. School of Engineering, Brown University, Providence, Rhode Island

5. Center for Neurorestoration and Neurotechnology, Rehabilitation Research & Development Service, Department of Veterans Affairs, Providence, Rhode Island

6. Department of Neurosurgery, Stanford University, Stanford, California

7. Department of Electrical Engineering, Stanford University, Stanford, California

8. Stanford Neurosciences Institute, Stanford University, Stanford, California

9. Inserm, University of Grenoble, Clinatec-Lab U1205, Grenoble, France

10. Department of Neurology, Massachusetts General Hospital, Boston, Massachusetts

11. Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts

12. Harvard Medical School, Boston, Massachusetts

13. Neurosciences Program, Stanford University, Stanford, California

14. Department of Neurobiology, Stanford University, Stanford, California

15. Department of Bioengineering, Stanford University, Stanford, California

16. Department of Neurology and Neurological Sciences, Stanford University, Stanford, California

Abstract

Intracortical brain-computer interfaces (BCIs) can enable individuals to control effectors, such as a computer cursor, by directly decoding the user’s movement intentions from action potentials and local field potentials (LFPs) recorded within the motor cortex. However, the accuracy and complexity of effector control achieved with such “biomimetic” BCIs will depend on the degree to which the intended movements used to elicit control modulate the neural activity. In particular, channels that do not record distinguishable action potentials and only record LFP modulations may be of limited use for BCI control. In contrast, a biofeedback approach may surpass these limitations by letting the participants generate new control signals and learn strategies that improve the volitional control of signals used for effector control. Here, we show that, by using a biofeedback paradigm, three individuals with tetraplegia achieved volitional control of gamma LFPs (40–400 Hz) recorded by a single microelectrode implanted in the precentral gyrus. Control was improved over a pair of consecutive sessions up to 3 days apart. In all but one session, the channel used to achieve control lacked distinguishable action potentials. Our results indicate that biofeedback LFP-based BCIs may potentially contribute to the neural modulation necessary to obtain reliable and useful control of effectors. NEW & NOTEWORTHY Our study demonstrates that people with tetraplegia can volitionally control individual high-gamma local-field potential (LFP) channels recorded from the motor cortex, and that this control can be improved using biofeedback. Motor cortical LFP signals are thought to be both informative and stable intracortical signals and, thus, of importance for future brain-computer interfaces.

Funder

Morton Cure Paralysis Fund (MCPF)

U.S. Department of Veterans Affairs (VA)

HHS | NIH | NICHD | National Center for Medical Rehabilitation Research (NCMRR)

HHS | NIH | National Institute on Deafness and Other Communication Disorders (NIDCD)

Doris Duke Charitable Foundation (DDCF)

Stanford Institute for Neuro-Innovation and Translational Neuroscience

Craig H. Neilsen Foundation

MGH-Deane Institute

Katie Samson Foundation

Bio-X NeuroVentures

The Garlick Fund

Institute National de la sante et de la recherche medicale

French-American Fulbright Commision

Publisher

American Physiological Society

Subject

Physiology,General Neuroscience

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