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Morphology, Connectivity, and Encoding Features of Tactile and Motor Representations of the Fingers in the Human Precentral and Postcentral Gyrus

Despite the tight coupling between sensory and motor processing for fine manipulation in humans, it is not yet totally clear which specific properties of the fingers are mapped in the precentral and postcentral gyrus. We used fMRI to compare the morphology, connectivity, and encoding of the motor an...

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Autores principales: Mastria, Giulio, Scaliti, Eugenio, Mehring, Carsten, Burdet, Etienne, Becchio, Cristina, Serino, Andrea, Akselrod, Michel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10008061/
https://www.ncbi.nlm.nih.gov/pubmed/36717227
http://dx.doi.org/10.1523/JNEUROSCI.1976-21.2022
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author Mastria, Giulio
Scaliti, Eugenio
Mehring, Carsten
Burdet, Etienne
Becchio, Cristina
Serino, Andrea
Akselrod, Michel
author_facet Mastria, Giulio
Scaliti, Eugenio
Mehring, Carsten
Burdet, Etienne
Becchio, Cristina
Serino, Andrea
Akselrod, Michel
author_sort Mastria, Giulio
collection PubMed
description Despite the tight coupling between sensory and motor processing for fine manipulation in humans, it is not yet totally clear which specific properties of the fingers are mapped in the precentral and postcentral gyrus. We used fMRI to compare the morphology, connectivity, and encoding of the motor and tactile finger representations (FRs) in the precentral and postcentral gyrus of 25 5-fingered participants (8 females). Multivoxel pattern and structural and functional connectivity analyses demonstrated the existence of distinct motor and tactile FRs within both the precentral and postcentral gyrus, integrating finger-specific motor and tactile information. Using representational similarity analysis, we found that the motor and tactile FRs in the sensorimotor cortex were described by the perceived structure of the hand better than by the actual hand anatomy or other functional models (finger kinematics, muscles synergies). We then studied a polydactyly individual (i.e., with a congenital 6-fingered hand) showing superior manipulation abilities and divergent anatomic-functional hand properties. The perceived hand model was still the best model for tactile representations in the precentral and postcentral gyrus, while finger kinematics better described motor representations in the precentral gyrus. We suggest that, under normal conditions (i.e., in subjects with a standard hand anatomy), the sensorimotor representations of the 5 fingers in humans converge toward a model of perceived hand anatomy, deviating from the real hand structure, as the best synthesis between functional and structural features of the hand. SIGNIFICANCE STATEMENT Distinct motor and tactile finger representations exist in both the precentral and postcentral gyrus, supported by a finger-specific pattern of anatomic and functional connectivity across modalities. At the representational level, finger representations reflect the perceived structure of the hand, which might result from an adapting process harmonizing (i.e., uniformizing) the encoding of hand function and structure in the precentral and postcentral gyrus. The same analyses performed in an extremely rare polydactyly subject showed that the emergence of such representational geometry is also found in neuromechanical variants with different hand anatomy and function. However, the harmonization process across the precentral and postcentral gyrus might not be possible because of divergent functional-structural properties of the hand and associated superior manipulation abilities.
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spelling pubmed-100080612023-03-12 Morphology, Connectivity, and Encoding Features of Tactile and Motor Representations of the Fingers in the Human Precentral and Postcentral Gyrus Mastria, Giulio Scaliti, Eugenio Mehring, Carsten Burdet, Etienne Becchio, Cristina Serino, Andrea Akselrod, Michel J Neurosci Research Articles Despite the tight coupling between sensory and motor processing for fine manipulation in humans, it is not yet totally clear which specific properties of the fingers are mapped in the precentral and postcentral gyrus. We used fMRI to compare the morphology, connectivity, and encoding of the motor and tactile finger representations (FRs) in the precentral and postcentral gyrus of 25 5-fingered participants (8 females). Multivoxel pattern and structural and functional connectivity analyses demonstrated the existence of distinct motor and tactile FRs within both the precentral and postcentral gyrus, integrating finger-specific motor and tactile information. Using representational similarity analysis, we found that the motor and tactile FRs in the sensorimotor cortex were described by the perceived structure of the hand better than by the actual hand anatomy or other functional models (finger kinematics, muscles synergies). We then studied a polydactyly individual (i.e., with a congenital 6-fingered hand) showing superior manipulation abilities and divergent anatomic-functional hand properties. The perceived hand model was still the best model for tactile representations in the precentral and postcentral gyrus, while finger kinematics better described motor representations in the precentral gyrus. We suggest that, under normal conditions (i.e., in subjects with a standard hand anatomy), the sensorimotor representations of the 5 fingers in humans converge toward a model of perceived hand anatomy, deviating from the real hand structure, as the best synthesis between functional and structural features of the hand. SIGNIFICANCE STATEMENT Distinct motor and tactile finger representations exist in both the precentral and postcentral gyrus, supported by a finger-specific pattern of anatomic and functional connectivity across modalities. At the representational level, finger representations reflect the perceived structure of the hand, which might result from an adapting process harmonizing (i.e., uniformizing) the encoding of hand function and structure in the precentral and postcentral gyrus. The same analyses performed in an extremely rare polydactyly subject showed that the emergence of such representational geometry is also found in neuromechanical variants with different hand anatomy and function. However, the harmonization process across the precentral and postcentral gyrus might not be possible because of divergent functional-structural properties of the hand and associated superior manipulation abilities. Society for Neuroscience 2023-03-01 /pmc/articles/PMC10008061/ /pubmed/36717227 http://dx.doi.org/10.1523/JNEUROSCI.1976-21.2022 Text en Copyright © 2023 Mastria et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Mastria, Giulio
Scaliti, Eugenio
Mehring, Carsten
Burdet, Etienne
Becchio, Cristina
Serino, Andrea
Akselrod, Michel
Morphology, Connectivity, and Encoding Features of Tactile and Motor Representations of the Fingers in the Human Precentral and Postcentral Gyrus
title Morphology, Connectivity, and Encoding Features of Tactile and Motor Representations of the Fingers in the Human Precentral and Postcentral Gyrus
title_full Morphology, Connectivity, and Encoding Features of Tactile and Motor Representations of the Fingers in the Human Precentral and Postcentral Gyrus
title_fullStr Morphology, Connectivity, and Encoding Features of Tactile and Motor Representations of the Fingers in the Human Precentral and Postcentral Gyrus
title_full_unstemmed Morphology, Connectivity, and Encoding Features of Tactile and Motor Representations of the Fingers in the Human Precentral and Postcentral Gyrus
title_short Morphology, Connectivity, and Encoding Features of Tactile and Motor Representations of the Fingers in the Human Precentral and Postcentral Gyrus
title_sort morphology, connectivity, and encoding features of tactile and motor representations of the fingers in the human precentral and postcentral gyrus
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10008061/
https://www.ncbi.nlm.nih.gov/pubmed/36717227
http://dx.doi.org/10.1523/JNEUROSCI.1976-21.2022
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