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

  • 589
    views
  • 106
    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
    Friedrich Schuessler, Francesca Mastrogiuseppe ... Omri Barak
    Research Article

    The relation between neural activity and behaviorally relevant variables is at the heart of neuroscience research. When strong, this relation is termed a neural representation. There is increasing evidence, however, for partial dissociations between activity in an area and relevant external variables. While many explanations have been proposed, a theoretical framework for the relationship between external and internal variables is lacking. Here, we utilize recurrent neural networks (RNNs) to explore the question of when and how neural dynamics and the network’s output are related from a geometrical point of view. We find that training RNNs can lead to two dynamical regimes: dynamics can either be aligned with the directions that generate output variables, or oblique to them. We show that the choice of readout weight magnitude before training can serve as a control knob between the regimes, similar to recent findings in feedforward networks. These regimes are functionally distinct. Oblique networks are more heterogeneous and suppress noise in their output directions. They are furthermore more robust to perturbations along the output directions. Crucially, the oblique regime is specific to recurrent (but not feedforward) networks, arising from dynamical stability considerations. Finally, we show that tendencies toward the aligned or the oblique regime can be dissociated in neural recordings. Altogether, our results open a new perspective for interpreting neural activity by relating network dynamics and their output.

    1. Neuroscience
    Ji Eun Ryu, Kyu-Won Shim ... Eun Young Kim
    Research Article

    The circadian clock, an internal time-keeping system orchestrates 24 hr rhythms in physiology and behavior by regulating rhythmic transcription in cells. Astrocytes, the most abundant glial cells, play crucial roles in CNS functions, but the impact of the circadian clock on astrocyte functions remains largely unexplored. In this study, we identified 412 circadian rhythmic transcripts in cultured mouse cortical astrocytes through RNA sequencing. Gene Ontology analysis indicated that genes involved in Ca2+ homeostasis are under circadian control. Notably, Herpud1 (Herp) exhibited robust circadian rhythmicity at both mRNA and protein levels, a rhythm disrupted in astrocytes lacking the circadian transcription factor, BMAL1. HERP regulated endoplasmic reticulum (ER) Ca2+ release by modulating the degradation of inositol 1,4,5-trisphosphate receptors (ITPRs). ATP-stimulated ER Ca2+ release varied with the circadian phase, being more pronounced at subjective night phase, likely due to the rhythmic expression of ITPR2. Correspondingly, ATP-stimulated cytosolic Ca2+ increases were heightened at the subjective night phase. This rhythmic ER Ca2+ response led to circadian phase-dependent variations in the phosphorylation of Connexin 43 (Ser368) and gap junctional communication. Given the role of gap junction channel (GJC) in propagating Ca2+ signals, we suggest that this circadian regulation of ER Ca2+ responses could affect astrocytic modulation of synaptic activity according to the time of day. Overall, our study enhances the understanding of how the circadian clock influences astrocyte function in the CNS, shedding light on their potential role in daily variations of brain activity and health.