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Malleability of the cortical hand map following a finger nerve block

View ORCID ProfileDaan B. Wesselink, Zeena-Britt Sanders, Laura R. Edmondson, Harriet Dempsey-Jones, Paulina Kieliba, Sanne Kikkert, Andreas C. Themistocleous, Uzay Emir, Jörn Diedrichsen, Hannes P. Saal, Tamar R. Makin
doi: https://doi.org/10.1101/2020.10.16.338640
Daan B. Wesselink
1Institute of Cognitive Neuroscience, University College London (UK)
2Wellcome Centre for Integrative Neuroimaging, University of Oxford (UK)
3Department of Neurobiology, Harvard Medical School (USA)
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  • ORCID record for Daan B. Wesselink
  • For correspondence: daan_wesselink@hms.harvard.edu
Zeena-Britt Sanders
2Wellcome Centre for Integrative Neuroimaging, University of Oxford (UK)
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Laura R. Edmondson
4Active Touch Laboratory, Department of Psychology, The University of Sheffield (UK)
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Harriet Dempsey-Jones
1Institute of Cognitive Neuroscience, University College London (UK)
2Wellcome Centre for Integrative Neuroimaging, University of Oxford (UK)
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Paulina Kieliba
1Institute of Cognitive Neuroscience, University College London (UK)
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Sanne Kikkert
2Wellcome Centre for Integrative Neuroimaging, University of Oxford (UK)
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Andreas C. Themistocleous
5Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK & Brain Function Research Group, University of the Witwatersrand, Johannesburg, South Africa
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Uzay Emir
2Wellcome Centre for Integrative Neuroimaging, University of Oxford (UK)
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Jörn Diedrichsen
6Brain and Mind Institute, University of Western Ontario (CA)
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Hannes P. Saal
4Active Touch Laboratory, Department of Psychology, The University of Sheffield (UK)
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Tamar R. Makin
1Institute of Cognitive Neuroscience, University College London (UK)
2Wellcome Centre for Integrative Neuroimaging, University of Oxford (UK)
7Wellcome Centre for Human Neuroimaging, University College London (UK)
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Abstract

Individual fingers in the primary somatosensory cortex (S1) are known to be represented separately and adjacently, forming a cortical hand map. Electrophysiological studies in monkeys show that finger amputation triggers increased selectivity to the neighbouring fingers within the deprived S1, causing local reorganisation. Neuroimaging research in humans, however, shows persistent S1 finger representation of the missing hand, even decades after amputation. We aimed to resolve these apparently contrasting evidence by examining finger representation in humans following pharmacological ‘amputation’ using single-finger nerve block and 7T neuroimaging. We hypothesised that beneath the apparent selectivity of individual fingers in the hand map, peripheral and central processing is distributed across fingers. If each finger contributes to the cortical representation of the others, then localised input loss will weaken finger representation across the hand map. For the same reason, the non-blocked fingers will stabilise the blocked finger’s representation, resulting in persistent representation of the blocked finger. Using univariate selectivity profiling, we replicated the electrophysiological findings of local S1 reorganisation. However, more comprehensive analyses confirmed that local blocking reduced representation of all fingers across the entire hand area. Importantly, multivariate analysis demonstrated that despite input loss, representation of the blocked finger remained persistent and distinct from the unblocked fingers. Computational modelling suggested that the observed findings are driven by distributed processing underlying the topographic map, combined with homeostatic mechanisms. Our findings suggest that the long-standing depiction of the somatosensory hand map is misleading. As such, accounts for map reorganisation, e.g. following amputation, need to be reconsidered.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 17, 2020.
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Malleability of the cortical hand map following a finger nerve block
Daan B. Wesselink, Zeena-Britt Sanders, Laura R. Edmondson, Harriet Dempsey-Jones, Paulina Kieliba, Sanne Kikkert, Andreas C. Themistocleous, Uzay Emir, Jörn Diedrichsen, Hannes P. Saal, Tamar R. Makin
bioRxiv 2020.10.16.338640; doi: https://doi.org/10.1101/2020.10.16.338640
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Malleability of the cortical hand map following a finger nerve block
Daan B. Wesselink, Zeena-Britt Sanders, Laura R. Edmondson, Harriet Dempsey-Jones, Paulina Kieliba, Sanne Kikkert, Andreas C. Themistocleous, Uzay Emir, Jörn Diedrichsen, Hannes P. Saal, Tamar R. Makin
bioRxiv 2020.10.16.338640; doi: https://doi.org/10.1101/2020.10.16.338640

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