Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss

  1. Victoria Root
  2. Dollyane Muret  Is a corresponding author
  3. Maite Arribas
  4. Elena Amoruso
  5. John Thornton
  6. Aurelie Tarall-Jozwiak
  7. Irene Tracey
  8. Tamar R Makin
  1. University of Oxford, United Kingdom
  2. University College London, United Kingdom
  3. King's College London, United Kingdom
  4. Queen Mary's Hospital, United Kingdom
  5. University of Cambridge, United Kingdom

Abstract

Cortical remapping after hand loss in the primary somatosensory cortex (S1) is thought to be predominantly dictated by cortical proximity, with adjacent body parts remapping into the deprived area. Traditionally, this remapping has been characterised by changes in the lip representation, which is assumed to be the immediate neighbour of the hand based on electrophysiological research in non-human primates. However, the orientation of facial somatotopy in humans is debated, with contrasting work reporting both an inverted and upright topography. We aimed to fill this gap in the S1 homunculus by investigating the topographic organisation of the face. Using both univariate and multivariate approaches we examined the extent of face-to-hand remapping in individuals with a congenital and acquired missing hand (hereafter one-handers and amputees, respectively), relative to two-handed controls. Participants were asked to move different facial parts (forehead, nose, lips, tongue) during fMRI scanning. We first confirmed an upright face organisation in all three groups, with the upper-face and not the lips bordering the hand area. We further found little evidence for remapping of both forehead and lips in amputees, with no significant relationship to the chronicity of their PLP. In contrast, we found converging evidence for a complex pattern of face remapping in congenital one-handers across multiple facial parts, where relative to controls, the location of the cortical neighbour - the forehead - is shown to shift away from the deprived hand area, which is subsequently more activated by the lips and the tongue. Together, our findings demonstrate that the face representation in humans is highly plastic, but that this plasticity is restricted by the developmental stage of input deprivation, rather than cortical proximity.

Data availability

The data generated and analysed during this study is available to the public on Open Science Framework (https://osf.io/xq3am/).

The following data sets were generated

Article and author information

Author details

  1. Victoria Root

    Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0500-3206
  2. Dollyane Muret

    University College London, London, United Kingdom
    For correspondence
    dollyane.muret@inserm.fr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2626-654X
  3. Maite Arribas

    Department of Psychosis Studies, King's College London, London, United Kingdom
    Competing interests
    No competing interests declared.
  4. Elena Amoruso

    University College London, London, United Kingdom
    Competing interests
    No competing interests declared.
  5. John Thornton

    University College London, London, United Kingdom
    Competing interests
    No competing interests declared.
  6. Aurelie Tarall-Jozwiak

    Queen Mary's Hospital, London, United Kingdom
    Competing interests
    No competing interests declared.
  7. Irene Tracey

    Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
  8. Tamar R Makin

    Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    Tamar R Makin, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5816-8979

Funding

European Research Council (715022)

  • Tamar R Makin

Wellcome Trust (215575/Z/19/Z)

  • Tamar R Makin

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

Reviewing Editor

  1. Olivier Collignon, Université Catholique de Louvain, Belgium

Ethics

Human subjects: Written Informed consent, and consent to publish, was obtained from all participants. Ethical approval was obtained from the NHS National Research Ethics Service approval (18/LO/0474).

Version history

  1. Preprint posted: July 5, 2021 (view preprint)
  2. Received: December 6, 2021
  3. Accepted: December 29, 2022
  4. Accepted Manuscript published: December 30, 2022 (version 1)
  5. Version of Record published: January 19, 2023 (version 2)

Copyright

© 2022, Root 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.

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  1. Victoria Root
  2. Dollyane Muret
  3. Maite Arribas
  4. Elena Amoruso
  5. John Thornton
  6. Aurelie Tarall-Jozwiak
  7. Irene Tracey
  8. Tamar R Makin
(2022)
Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss
eLife 11:e76158.
https://doi.org/10.7554/eLife.76158

Share this article

https://doi.org/10.7554/eLife.76158

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