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  5. Morphology, connectivity, and encoding features of tactile and motor representations of the fingers in the human precentral and postcentral gyrus
 
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Morphology, connectivity, and encoding features of tactile and motor representations of the fingers in the human precentral and postcentral gyrus
File(s)
1572.full.pdf (3.79 MB)
Published version
Author(s)
Mastria, Giulio
Scaliti, Eugenio
Mehring, Carsten
Burdet, Etienne
Becchio, Cristina
more
Type
Journal Article
Abstract
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.
Date Issued
2023-03-01
Date Acceptance
2022-09-14
Citation
The Journal of Neuroscience, 2023, 43 (9), pp.1572-1589
URI
http://hdl.handle.net/10044/1/102236
URL
https://www.jneurosci.org/content/43/9/1572
DOI
https://www.dx.doi.org/10.1523/JNEUROSCI.1976-21.2022
ISSN
0270-6474
Publisher
Society for Neuroscience
Start Page
1572
End Page
1589
Journal / Book Title
The Journal of Neuroscience
Volume
43
Issue
9
Copyright Statement
Copyright © 2023 Mastria et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
License URL
https://creativecommons.org/licenses/by/4.0/
Identifier
https://www.ncbi.nlm.nih.gov/pubmed/36717227
PII: JNEUROSCI.1976-21.2022
Subjects
body representation
fMRI
perception
polidactility
representational similarity analysis
sensorimotor
Female
Humans
Somatosensory Cortex
Fingers
Touch
Hand
Magnetic Resonance Imaging
Polydactyly
Brain Mapping
Publication Status
Published
Coverage Spatial
United States
Date Publish Online
2023-03-01
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