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

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 as...

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Autores principales: Root, Victoria, Muret, Dollyane, Arribas, Maite, Amoruso, Elena, Thornton, John, Tarall-Jozwiak, Aurelie, Tracey, Irene, Makin, Tamar R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9851617/
https://www.ncbi.nlm.nih.gov/pubmed/36583538
http://dx.doi.org/10.7554/eLife.76158
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author Root, Victoria
Muret, Dollyane
Arribas, Maite
Amoruso, Elena
Thornton, John
Tarall-Jozwiak, Aurelie
Tracey, Irene
Makin, Tamar R
author_facet Root, Victoria
Muret, Dollyane
Arribas, Maite
Amoruso, Elena
Thornton, John
Tarall-Jozwiak, Aurelie
Tracey, Irene
Makin, Tamar R
author_sort Root, Victoria
collection PubMed
description 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 functional MRI (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 phantom limb pain (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.
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spelling pubmed-98516172023-01-20 Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss Root, Victoria Muret, Dollyane Arribas, Maite Amoruso, Elena Thornton, John Tarall-Jozwiak, Aurelie Tracey, Irene Makin, Tamar R eLife Neuroscience 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 functional MRI (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 phantom limb pain (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. eLife Sciences Publications, Ltd 2022-12-30 /pmc/articles/PMC9851617/ /pubmed/36583538 http://dx.doi.org/10.7554/eLife.76158 Text en © 2022, Root, Muret et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Root, Victoria
Muret, Dollyane
Arribas, Maite
Amoruso, Elena
Thornton, John
Tarall-Jozwiak, Aurelie
Tracey, Irene
Makin, Tamar R
Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss
title Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss
title_full Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss
title_fullStr Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss
title_full_unstemmed Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss
title_short Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss
title_sort complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9851617/
https://www.ncbi.nlm.nih.gov/pubmed/36583538
http://dx.doi.org/10.7554/eLife.76158
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