Abstract

A key factor in the clinical translation of brain-machine interfaces (BMIs) for restoring hand motor function will be their robustness to changes in a task. With functional electrical stimulation (FES) for example, the patient's own hand will be used to produce a wide range of forces in otherwise similar movements. To investigate the impact of task changes on BMI performance, we trained two rhesus macaques to control a virtual hand with their physical hand while we added springs to each finger group (index or middle-ring-small) or altered their wrist posture. Using simultaneously recorded intracortical neural activity, finger positions, and electromyography, we found that decoders trained in one context did not generalize well to other contexts, leading to significant increases in prediction error, especially for muscle activations. However, with respect to online BMI control of the virtual hand, changing either the decoder training task context or the hand's physical context during online control had little effect on online performance. We explain this dichotomy by showing that the structure of neural population activity remained similar in new contexts, which could allow for fast adjustment online. Additionally, we found that neural activity shifted trajectories proportional to the required muscle activation in new contexts. This shift in neural activity possibly explains biases to off-context kinematic predictions and suggests a feature that could help predict different magnitude muscle activations while producing similar kinematics.

Data availability

Neural, behavioral, EMG, and online BMI performance data has been deposited in the Dryad repository (https://doi.org/10.5061/dryad.p2ngf1vtn).

The following data sets were generated

Article and author information

Author details

  1. Matthew J Mender

    Department of Biomedical Engineering, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1562-3289
  2. Samuel R Nason-Tomaszewski

    Department of Biomedical Engineering, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Hisham Temmar

    Department of Biomedical Engineering, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4464-4911
  4. Joseph T Costello

    Department of Electrical Engineering and Computer Science, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Dylan M Wallace

    Department of Robotics, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Matthew S Willsey

    Department of Biomedical Engineering, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Nishant Ganesh Kumar

    Department of Surgery, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Theodore A Kung

    Department of Surgery, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Parag Patil

    Department of Biomedical Engineering, University of Michigan-Ann Arbor, Ann Arbor, United States
    For correspondence
    pgpatil@med.umich.edu
    Competing interests
    The authors declare that no competing interests exist.
  10. Cynthia A Chestek

    Department of Biomedical Engineering, University of Michigan-Ann Arbor, Ann Arbor, United States
    For correspondence
    cchestek@umich.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9671-7051

Funding

National Science Foundation (Grant Number 1926576)

  • Matthew J Mender
  • Hisham Temmar
  • Parag Patil
  • Cynthia A Chestek

National Institute of General Medical Sciences (Grant Number R01GM111293)

  • Parag Patil
  • Cynthia A Chestek

National Science Foundation (Graduate Research Fellowship Program)

  • Joseph T Costello

Eunice Kennedy Shriver National Institute of Child Health and Human Development (Grant Number F31HD098804)

  • Samuel R Nason-Tomaszewski

National Institute of Neurological Disorders and Stroke (Grant Number T32NS007222)

  • Matthew S Willsey

National Institute of Neurological Disorders and Stroke (Grant Number R01NS105132)

  • Nishant Ganesh Kumar
  • Theodore A Kung

The D. Dan and Betty Kahn Foundation (Grant AWD011321)

  • Dylan M Wallace

University of Michigan Robotics Institute (Graduate student fellowship)

  • Dylan M Wallace

A. Alfred Taubman Medical Research Institute

  • Parag Patil

Craig H. Neilsen Foundation (Project 315108)

  • Cynthia A Chestek

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All protocols were in accord with the National Institutes of Health guidelines and approved by the University of Michigan Institutional Animal Care and Use Committee (protocol numbers PRO00010076 and PRO00008138).

Copyright

© 2023, Mender et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 665
    views
  • 114
    downloads
  • 1
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Matthew J Mender
  2. Samuel R Nason-Tomaszewski
  3. Hisham Temmar
  4. Joseph T Costello
  5. Dylan M Wallace
  6. Matthew S Willsey
  7. Nishant Ganesh Kumar
  8. Theodore A Kung
  9. Parag Patil
  10. Cynthia A Chestek
(2023)
The impact of task context on predicting finger movements in a brain-machine interface
eLife 12:e82598.
https://doi.org/10.7554/eLife.82598

Share this article

https://doi.org/10.7554/eLife.82598

Further reading

    1. Neuroscience
    Jean-François Brunet
    Review Article

    Historically, the creation of the parasympathetic division of the autonomic nervous system of the vertebrates is inextricably linked to the unification of the cranial and sacral autonomic outflows. There is an intriguing disproportion between the entrenchment of the notion of a ‘cranio-sacral’ pathway, which informs every textbook schematic of the autonomic nervous system since the early XXth century, and the wobbliness of its two roots: an anatomical detail overinterpreted by Walter Holbrook Gaskell (the ‘gap’ between the lumbar and sacral outflows), on which John Newport Langley grafted a piece of physiology (a supposed antagonism of these two outflows on external genitals), repeatedly questioned since, to little avail. I retrace the birth of a flawed scientific concept (the cranio-sacral outflow) and the way in which it ossified instead of dissipated. Then, I suggest that the critique of the ‘cranio-sacral outflow’ invites, in turn, a radical deconstruction of the very notion of a ‘parasympathetic’ outflow, and a more realistic description of the autonomic nervous system.

    1. Immunology and Inflammation
    2. Neuroscience
    Rocio Vicario, Stamatina Fragkogianni ... Frédéric Geissmann
    Research Article

    Somatic genetic heterogeneity resulting from post-zygotic DNA mutations is widespread in human tissues and can cause diseases, however, few studies have investigated its role in neurodegenerative processes such as Alzheimer’s disease (AD). Here, we report the selective enrichment of microglia clones carrying pathogenic variants, that are not present in neuronal, glia/stromal cells, or blood, from patients with AD in comparison to age-matched controls. Notably, microglia-specific AD-associated variants preferentially target the MAPK pathway, including recurrent CBL ring-domain mutations. These variants activate ERK and drive a microglia transcriptional program characterized by a strong neuro-inflammatory response, both in vitro and in patients. Although the natural history of AD-associated microglial clones is difficult to establish in humans, microglial expression of a MAPK pathway activating variant was previously shown to cause neurodegeneration in mice, suggesting that AD-associated neuroinflammatory microglial clones may contribute to the neurodegenerative process in patients.