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Sense of agency for intracortical brain–machine interfaces

Nature Human Behaviour volume 6, pages 565–578 (2022)Cite this article

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Abstract

Intracortical brain–machine interfaces decode motor commands from neural signals and translate them into actions, enabling movement for paralysed individuals. The subjective sense of agency associated with actions generated via intracortical brain–machine interfaces, the neural mechanisms involved and its clinical relevance are currently unknown. By experimentally manipulating the coherence between decoded motor commands and sensory feedback in a tetraplegic individual using a brain–machine interface, we provide evidence that primary motor cortex processes sensory feedback, sensorimotor conflicts and subjective states of actions generated via the brain–machine interface. Neural signals processing the sense of agency affected the proficiency of the brain–machine interface, underlining the clinical potential of the present approach. These findings show that primary motor cortex encodes information related to action and sensing, but also sensorimotor and subjective agency signals, which in turn are relevant for clinical applications of brain–machine interfaces.

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Fig. 1: Experimental setup.
Fig. 2: Agency judgements and confidence depends on sensory feedback.
Fig. 3: M1 activity depends on sensory feedback.
Fig. 4: Sense of agency in M1.
Fig. 5: Performance of BMI classifier as a function of sensory feedback and sense of agency.
Fig. 6: Somatosensory feedback changes firing rates of M1 neurons.

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Data availability

Behavioural data and processed data necessary to reproduce the figures in the main text can be found in the OSF repository accessible at: https://osf.io/7rma5/?view_only=9928bd8e32a748828f7ecfdbeb1f8baa.

Neural data and code for BMI control can be made available to qualified individuals for collaboration via a written agreement between Battelle Memorial Institute and the requester’s affiliated institution. Such enquiries or requests should be directed to: ganzer@battelle.org.

Code availability

Custom code for neural data analysis and BMI control can be obtained following a written agreement between Battelle Memorial Institute and the requester’s affiliated institution. Such inquiries or requests should be directed to: ganzer@battelle.org. Inquiries or requests concerning custom analysis code used for this study should be directed to A.S.

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Acknowledgements

The authors thank I. Burkhart for his dedication to the study and insightful conversations. A.S. is supported by the Swiss National Science Foundation (grant no. PP00P3_163951/1). M.B. is supported by the Craig H. Neilsen Foundation (grant no. 651289) and State of Ohio Research Incentive Third Frontier Fund. N.F. received funding from the European Research Council under the European Union Horizon 2020 research and innovation programme (grant no. 803122). O.B. is supported by two donors advised by CARIGEST SA (Fondazione Teofilo Rossi di Montelera e di Premuda and a second one wishing to remain anonymous), by the National Center of Competence in Research ‘Synapsy—The Synaptic Bases of Mental Diseases’ (grant no. 51NF40-185897), by the Swiss National Science Foundation (grant no. 320030-188798), by Parkinson Suisse and by the Empiris Foundation. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Author information

Author notes

  1. Marcia Bockbrader

    Present address: BEP Medical Group, Beavercreek Township, Beavercreek, OH, USA

  2. Sam Colachis IV, Collin Dunlap, Patrick Ganzer, Nick Annetta, Gaurav Sharma & David Friedenberg

    Present address: Medical Devices and Neuromodulation, Battelle Memorial Institute, Columbus, OH, USA

  3. Kaitie Eipel

    Present address: St. Elizabeth University, Morristown, NJ, USA

  4. Patrick Ganzer

    Present address: Department of Biomedical Engineering, University of Miami, Miami, FL, USA

  5. Gaurav Sharma

    Present address: Air Force Research Laboratory, Dayton, OH, USA

  6. These authors contributed equally: Andrea Serino, Marcia Bockbrader.

  7. These authors jointly supervised this work: Ali Rezai, Olaf Blanke.

Authors and Affiliations

  1. MySpace Lab, Department of Clinical Neuroscience, University Hospital Lausanne (CHUV), Lausanne, Switzerland

    Andrea Serino & Tommaso Bertoni

  2. Laboratory of Cognitive Neuroscience, Brain Mind Institute & Center for Neuroprosthetics, Ecole Polytechnique Fèdèrale de Lausanne (EPFL), Campus Biotech, Geneva, Switzerland

    Andrea Serino, Marco Solcà, Pavo Orepic, Nathan Faivre & Olaf Blanke

  3. Department of Physical Medicine and Rehabilitation, The Ohio State University, Columbus, OH, USA

    Marcia Bockbrader, Sam Colachis IV, Collin Dunlap, Kaitie Eipel & Ali Rezai

  4. Department of Psychology, University of Virginia, Charlottesville, VA, USA

    Per Sederberg

  5. Univ. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS, LPNC, Grenoble, France

    Nathan Faivre

  6. Rockefeller Neuroscience Institute, West Virginia University, Morgantown, WV, USA

    Ali Rezai

  7. Department of Neurology, University Hospital, Geneva, Switzerland

    Olaf Blanke

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Contributions

A.S.: conceptualization, formal analysis, methodology, writing; M.B.: methodology, investigation, project administration, review and editing; T.B.: data curation, formal analysis, software, visualization, review and editing; S.C.: methodology, data curation, formal analysis, investigation, software; M.S.: formal analysis, investigation, visualization, review and editing; C.D. and K.E.: investigation, data collection; P.G.: methodology, review and editing; G.S.: methodology, software and hardware development; N.A.: methodology, review and editing; P.O.: investigation, software and hardware development; D.F.: investigation, software and hardware development; P.S.: methodology, review and editing; N.F.: formal analysis, methodology, visualization, review and editing; A.R.: funding acquisition, resources, supervision, review and editing; O.B.: conceptualization, funding acquisition, methodology, supervision and writing.

Corresponding authors

Correspondence to Andrea Serino or Olaf Blanke.

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Competing interests

A.S. is head of Neuroscience at MindMaze SA. O.B. is cofounder and shareholder of Metaphysiks Engineering SA, as well as member of the board and shareholder of MindMaze SA. P.G., G.S., N.A. and D.F. hold patents for the BMI system. M.B, C.D., K.E., M.S., T.B., N.F., P.S. and A.R. declare no competing interests.

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Serino, A., Bockbrader, M., Bertoni, T. et al. Sense of agency for intracortical brain–machine interfaces. Nat Hum Behav 6, 565–578 (2022). https://doi.org/10.1038/s41562-021-01233-2

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