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February 15, 2022; 98 (7) Research Article

Intracortical Somatosensory Stimulation to Elicit Fingertip Sensations in an Individual With Spinal Cord Injury

Matthew S. Fifer, View ORCID ProfileDavid P. McMullen, View ORCID ProfileLuke E. Osborn, View ORCID ProfileTessy M. Thomas, View ORCID ProfileBreanne Christie, Robert W. Nickl, Daniel N. Candrea, View ORCID ProfileEric A. Pohlmeyer, Margaret C. Thompson, Manuel A. Anaya, View ORCID ProfileWouter Schellekens, View ORCID ProfileNick F. Ramsey, View ORCID ProfileSliman J. Bensmaia, William S. Anderson, View ORCID ProfileBrock A. Wester, View ORCID ProfileNathan E. Crone, Pablo A. Celnik, View ORCID ProfileGabriela L. Cantarero, View ORCID ProfileFrancesco V. Tenore
First published December 8, 2021, DOI: https://doi.org/10.1212/WNL.0000000000013173
Matthew S. Fifer
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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David P. McMullen
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Luke E. Osborn
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Tessy M. Thomas
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Breanne Christie
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Robert W. Nickl
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Daniel N. Candrea
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Eric A. Pohlmeyer
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Margaret C. Thompson
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Manuel A. Anaya
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Wouter Schellekens
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Nick F. Ramsey
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Sliman J. Bensmaia
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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William S. Anderson
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Brock A. Wester
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Nathan E. Crone
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Pablo A. Celnik
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Gabriela L. Cantarero
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Francesco V. Tenore
From the Research and Exploratory Development Department (M.S.F., L.E.O., B.P.C., E.A.P., M.C.T., F.V.T.), Johns Hopkins University Applied Physics Laboratory, Laurel; National Institute of Mental Health (D.P.M.), NIH, Bethesda; Department of Biomedical Engineering (T.M.T., D.N.C.), Department of Physical Medicine and Rehabilitation (R.W.N., M.A.A., P.A.C., G.L.C.), Department of Neurosurgery (W.S.A.), and Department of Neurology (B.A.W., N.E.C.), Johns Hopkins University, Baltimore, MD; UMC Utrecht Brain Center (W.S., N.F.R.), the Netherlands; and Department of Organismal Biology and Anatomy (S.J.B.), University of Chicago, IL.
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Citation
Intracortical Somatosensory Stimulation to Elicit Fingertip Sensations in an Individual With Spinal Cord Injury
Matthew S. Fifer, David P. McMullen, Luke E. Osborn, Tessy M. Thomas, Breanne Christie, Robert W. Nickl, Daniel N. Candrea, Eric A. Pohlmeyer, Margaret C. Thompson, Manuel A. Anaya, Wouter Schellekens, Nick F. Ramsey, Sliman J. Bensmaia, William S. Anderson, Brock A. Wester, Nathan E. Crone, Pablo A. Celnik, Gabriela L. Cantarero, Francesco V. Tenore
Neurology Feb 2022, 98 (7) e679-e687; DOI: 10.1212/WNL.0000000000013173

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Abstract

Background and Objectives The restoration of touch to fingers and fingertips is critical to achieving dexterous neuroprosthetic control for individuals with sensorimotor dysfunction. However, localized fingertip sensations have not been evoked via intracortical microstimulation (ICMS).

Methods Using a novel intraoperative mapping approach, we implanted electrode arrays in the finger areas of left and right somatosensory cortex and delivered ICMS over a 2-year period in a human participant with spinal cord injury.

Results Stimulation evoked tactile sensations in 8 fingers, including fingertips, spanning both hands. Evoked percepts followed expected somatotopic arrangements. The subject was able to reliably identify up to 7 finger-specific sites spanning both hands in a finger discrimination task. The size of the evoked percepts was on average 33% larger than a finger pad, as assessed via manual markings of a hand image. The size of the evoked percepts increased modestly with increased stimulation intensity, growing 21% as pulse amplitude increased from 20 to 80 µA. Detection thresholds were estimated on a subset of electrodes, with estimates of 9.2 to 35 µA observed, roughly consistent with prior studies.

Discussion These results suggest that ICMS can enable the delivery of consistent and localized fingertip sensations during object manipulation by neuroprostheses for individuals with somatosensory deficits.

ClinicalTrials.gov Identifier NCT03161067.

Glossary

BiCNS=
Investigation on the Bidirectional Cortical Neuroprosthetic System;
ECoG=
electrocorticographic;
FDA=
Food and Drug Administration;
ICMS=
intracortical microstimulation;
IQR=
interquartile range;
NHP=
nonhuman primate;
SCI=
spinal cord injury;
3D-1U=
3 down–1 up;
2AFC=
2-alternative forced-choice

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • ↵* These authors contributed equally to this work as first authors.

  • Editorial, page 261

  • Received May 24, 2021.
  • Accepted in final form November 19, 2021.
  • © 2021 American Academy of Neurology
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