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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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-12-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/76158 |
| _version_ | 1797947426010562560 |
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| author | Victoria Root Dollyane Muret Maite Arribas Elena Amoruso John Thornton Aurelie Tarall-Jozwiak Irene Tracey Tamar R Makin |
| author_facet | Victoria Root Dollyane Muret Maite Arribas Elena Amoruso John Thornton Aurelie Tarall-Jozwiak Irene Tracey Tamar R Makin |
| author_sort | Victoria Root |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-10T21:27:39Z |
| format | Article |
| id | doaj.art-d2209e55103e4688af0920e0dd62531e |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-10T21:27:39Z |
| publishDate | 2022-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-d2209e55103e4688af0920e0dd62531e2023-01-19T16:23:47ZengeLife Sciences Publications LtdeLife2050-084X2022-12-011110.7554/eLife.76158Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand lossVictoria Root0https://orcid.org/0000-0002-0500-3206Dollyane Muret1https://orcid.org/0000-0002-2626-654XMaite Arribas2Elena Amoruso3John Thornton4Aurelie Tarall-Jozwiak5Irene Tracey6Tamar R Makin7https://orcid.org/0000-0002-5816-8979WIN Centre, University of Oxford, Oxford, United Kingdom; Institute of Cognitive Neuroscience, University College London, London, United Kingdom; Medical Research Council Cognition and Brain Sciences Unit (CBU), University of Cambridge, Cambridge, United KingdomInstitute of Cognitive Neuroscience, University College London, London, United KingdomInstitute of Cognitive Neuroscience, University College London, London, United Kingdom; Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, United KingdomInstitute of Cognitive Neuroscience, University College London, London, United Kingdom; Medical Research Council Cognition and Brain Sciences Unit (CBU), University of Cambridge, Cambridge, United KingdomWellcome Trust Centre for Neuroimaging, University College London, London, United KingdomQueen Mary’s Hospital, London, United KingdomWIN Centre, University of Oxford, Oxford, United KingdomInstitute of Cognitive Neuroscience, University College London, London, United Kingdom; Medical Research Council Cognition and Brain Sciences Unit (CBU), University of Cambridge, Cambridge, United Kingdom; Wellcome Trust Centre for Neuroimaging, University College London, London, United KingdomCortical 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.https://elifesciences.org/articles/76158primary somatosensory cortexcortical remappingfMRIface somatotopoyphantom limb pain |
| spellingShingle | Victoria Root Dollyane Muret Maite Arribas Elena Amoruso John Thornton Aurelie Tarall-Jozwiak Irene Tracey Tamar R Makin Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss eLife primary somatosensory cortex cortical remapping fMRI face somatotopoy phantom limb pain |
| 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 | primary somatosensory cortex cortical remapping fMRI face somatotopoy phantom limb pain |
| url | https://elifesciences.org/articles/76158 |
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