Perception of microstimulation frequency in human somatosensory cortex

  1. Christopher L Hughes  Is a corresponding author
  2. Sharlene N Flesher
  3. Jeffrey M Weiss
  4. Michael L Boninger
  5. Jennifer Collinger
  6. Robert Gaunt  Is a corresponding author
  1. University of Pittsburgh, United States
  2. Stanford University, United States

Abstract

Microstimulation in the somatosensory cortex can evoke artificial tactile percepts and can be incorporated into bidirectional brain-computer interfaces (BCIs) to restore function after injury or disease. However, little is known about how stimulation parameters themselves affect perception. Here, we stimulated through microelectrode arrays implanted in the somatosensory cortex of two human participants with cervical spinal cord injury and varied the stimulus amplitude, frequency and train duration. Increasing the amplitude and train duration increased the perceived intensity on all tested electrodes. Surprisingly, we found that increasing the frequency evoked more intense percepts on some electrodes but evoked less intense percepts on other electrodes. These different frequency-intensity relationships were divided into three groups which also evoked distinct percept qualities at different stimulus frequencies. Neighboring electrode sites were more likely to belong to the same group. These results support the idea that stimulation frequency directly controls tactile perception and that these different percepts may be related to the organization of somatosensory cortex, which will facilitate principled development of stimulation strategies for bidirectional BCIs.

Data availability

Data and code for this paper are available at GitHub (https://github.com/chughes003r/FrequencyPaper)

The following data sets were generated

Article and author information

Author details

  1. Christopher L Hughes

    Bioengineering, University of Pittsburgh, Pittsburgh, United States
    For correspondence
    clh180@pitt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9257-8659
  2. Sharlene N Flesher

    Neurosurgery, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jeffrey M Weiss

    Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1332-674X
  4. Michael L Boninger

    Physical Medicine & Rehabilitation, Bioengineering, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6966-919X
  5. Jennifer Collinger

    Physical Medicine & Rehabilitation, Bioengineering, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4517-5395
  6. Robert Gaunt

    Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, United States
    For correspondence
    rag53@pitt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6202-5818

Funding

Defense Advanced Research Projects Agency (N66001-16-C4051)

  • Michael L Boninger
  • Jennifer Collinger
  • Robert Gaunt

National Institutes of Health (UH3NS107714)

  • Michael L Boninger
  • Jennifer Collinger
  • Robert Gaunt

National Institutes of Health (U01NS108922)

  • Michael L Boninger
  • Jennifer Collinger
  • Robert Gaunt

National Science Foundation (DGE-1247842)

  • Sharlene N Flesher

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

Ethics

Human subjects: This study was conducted under an Investigational Device Exemption from the U.S. Food and Drug administration, approved by the Institutional Review Boards at the University of Pittsburgh (Pittsburgh, PA) and the Space and Naval Warfare Systems Center Pacific (San Diego, CA), and registered at ClinicalTrials.gov (NCT0189-4802). Informed consent was obtained before any study procedures were conducted.

Reviewing Editor

  1. J Andrew Pruszynski, Western University, Canada

Publication history

  1. Preprint posted: July 17, 2020 (view preprint)
  2. Received: November 24, 2020
  3. Accepted: July 22, 2021
  4. Accepted Manuscript published: July 27, 2021 (version 1)
  5. Version of Record published: August 19, 2021 (version 2)
  6. Version of Record updated: July 5, 2022 (version 3)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Christopher L Hughes
  2. Sharlene N Flesher
  3. Jeffrey M Weiss
  4. Michael L Boninger
  5. Jennifer Collinger
  6. Robert Gaunt
(2021)
Perception of microstimulation frequency in human somatosensory cortex
eLife 10:e65128.
https://doi.org/10.7554/eLife.65128

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