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.

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).

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.

Metrics

  • 1,120
    views
  • 143
    downloads
  • 10
    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. 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

Further reading

    1. Neuroscience
    Franziska Auer, Katherine Nardone ... David Schoppik
    Research Article

    Cerebellar dysfunction leads to postural instability. Recent work in freely moving rodents has transformed investigations of cerebellar contributions to posture. However, the combined complexity of terrestrial locomotion and the rodent cerebellum motivate new approaches to perturb cerebellar function in simpler vertebrates. Here, we adapted a validated chemogenetic tool (TRPV1/capsaicin) to describe the role of Purkinje cells — the output neurons of the cerebellar cortex — as larval zebrafish swam freely in depth. We achieved both bidirectional control (activation and ablation) of Purkinje cells while performing quantitative high-throughput assessment of posture and locomotion. Activation modified postural control in the pitch (nose-up/nose-down) axis. Similarly, ablations disrupted pitch-axis posture and fin-body coordination responsible for climbs. Postural disruption was more widespread in older larvae, offering a window into emergent roles for the developing cerebellum in the control of posture. Finally, we found that activity in Purkinje cells could individually and collectively encode tilt direction, a key feature of postural control neurons. Our findings delineate an expected role for the cerebellum in postural control and vestibular sensation in larval zebrafish, establishing the validity of TRPV1/capsaicin-mediated perturbations in a simple, genetically tractable vertebrate. Moreover, by comparing the contributions of Purkinje cell ablations to posture in time, we uncover signatures of emerging cerebellar control of posture across early development. This work takes a major step towards understanding an ancestral role of the cerebellum in regulating postural maturation.

    1. Neuroscience
    Zhujun Shao, Mengya Zhang, Qing Yu
    Research Article

    When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.