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Proprioceptive and tactile processing in individuals with Friedreich ataxia: an fMRI study

OBJECTIVE: Friedreich ataxia (FA) neuropathology affects dorsal root ganglia, posterior columns in the spinal cord, the spinocerebellar tracts, and cerebellar dentate nuclei. The impact of the somatosensory system on ataxic symptoms remains debated. This study aims to better evaluate the contributio...

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Autores principales: Destrebecq, Virginie, Rovai, Antonin, Trotta, Nicola, Comet, Camille, Naeije, Gilles
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10556689/
https://www.ncbi.nlm.nih.gov/pubmed/37808498
http://dx.doi.org/10.3389/fneur.2023.1224345
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author Destrebecq, Virginie
Rovai, Antonin
Trotta, Nicola
Comet, Camille
Naeije, Gilles
author_facet Destrebecq, Virginie
Rovai, Antonin
Trotta, Nicola
Comet, Camille
Naeije, Gilles
author_sort Destrebecq, Virginie
collection PubMed
description OBJECTIVE: Friedreich ataxia (FA) neuropathology affects dorsal root ganglia, posterior columns in the spinal cord, the spinocerebellar tracts, and cerebellar dentate nuclei. The impact of the somatosensory system on ataxic symptoms remains debated. This study aims to better evaluate the contribution of somatosensory processing to ataxia clinical severity by simultaneously investigating passive movement and tactile pneumatic stimulation in individuals with FA. METHODS: Twenty patients with FA and 20 healthy participants were included. All subjects underwent two 6 min block-design functional magnetic resonance imaging (fMRI) paradigms consisting of twelve 30 s alternating blocks (10 brain volumes per block, 120 brain volumes per paradigm) of a tactile oddball paradigm and a passive movement paradigm. Spearman rank correlation tests were used for correlations between BOLD levels and ataxia severity. RESULTS: The passive movement paradigm led to the lower activation of primary (cSI) and secondary somatosensory cortices (cSII) in FA compared with healthy subjects (respectively 1.1 ± 0.78 vs. 0.61 ± 1.02, p = 0.04, and 0.69 ± 0.5 vs. 0.3 ± 0.41, p = 0.005). In the tactile paradigm, there was no significant difference between cSI and cSII activation levels in healthy controls and FA (respectively 0.88 ± 0.73 vs. 1.14 ± 0.99, p = 0.33, and 0.54 ± 0.37 vs. 0.55 ± 0.54, p = 0.93). Correlation analysis showed a significant correlation between cSI activation levels in the tactile paradigm and the clinical severity (R = 0.481, p = 0.032). INTERPRETATION: Our study captured the difference between tactile and proprioceptive impairments in FA using somatosensory fMRI paradigms. The lack of correlation between the proprioceptive paradigm and ataxia clinical parameters supports a low contribution of afferent ataxia to FA clinical severity.
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spelling pubmed-105566892023-10-07 Proprioceptive and tactile processing in individuals with Friedreich ataxia: an fMRI study Destrebecq, Virginie Rovai, Antonin Trotta, Nicola Comet, Camille Naeije, Gilles Front Neurol Neurology OBJECTIVE: Friedreich ataxia (FA) neuropathology affects dorsal root ganglia, posterior columns in the spinal cord, the spinocerebellar tracts, and cerebellar dentate nuclei. The impact of the somatosensory system on ataxic symptoms remains debated. This study aims to better evaluate the contribution of somatosensory processing to ataxia clinical severity by simultaneously investigating passive movement and tactile pneumatic stimulation in individuals with FA. METHODS: Twenty patients with FA and 20 healthy participants were included. All subjects underwent two 6 min block-design functional magnetic resonance imaging (fMRI) paradigms consisting of twelve 30 s alternating blocks (10 brain volumes per block, 120 brain volumes per paradigm) of a tactile oddball paradigm and a passive movement paradigm. Spearman rank correlation tests were used for correlations between BOLD levels and ataxia severity. RESULTS: The passive movement paradigm led to the lower activation of primary (cSI) and secondary somatosensory cortices (cSII) in FA compared with healthy subjects (respectively 1.1 ± 0.78 vs. 0.61 ± 1.02, p = 0.04, and 0.69 ± 0.5 vs. 0.3 ± 0.41, p = 0.005). In the tactile paradigm, there was no significant difference between cSI and cSII activation levels in healthy controls and FA (respectively 0.88 ± 0.73 vs. 1.14 ± 0.99, p = 0.33, and 0.54 ± 0.37 vs. 0.55 ± 0.54, p = 0.93). Correlation analysis showed a significant correlation between cSI activation levels in the tactile paradigm and the clinical severity (R = 0.481, p = 0.032). INTERPRETATION: Our study captured the difference between tactile and proprioceptive impairments in FA using somatosensory fMRI paradigms. The lack of correlation between the proprioceptive paradigm and ataxia clinical parameters supports a low contribution of afferent ataxia to FA clinical severity. Frontiers Media S.A. 2023-09-22 /pmc/articles/PMC10556689/ /pubmed/37808498 http://dx.doi.org/10.3389/fneur.2023.1224345 Text en Copyright © 2023 Destrebecq, Rovai, Trotta, Comet and Naeije. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Destrebecq, Virginie
Rovai, Antonin
Trotta, Nicola
Comet, Camille
Naeije, Gilles
Proprioceptive and tactile processing in individuals with Friedreich ataxia: an fMRI study
title Proprioceptive and tactile processing in individuals with Friedreich ataxia: an fMRI study
title_full Proprioceptive and tactile processing in individuals with Friedreich ataxia: an fMRI study
title_fullStr Proprioceptive and tactile processing in individuals with Friedreich ataxia: an fMRI study
title_full_unstemmed Proprioceptive and tactile processing in individuals with Friedreich ataxia: an fMRI study
title_short Proprioceptive and tactile processing in individuals with Friedreich ataxia: an fMRI study
title_sort proprioceptive and tactile processing in individuals with friedreich ataxia: an fmri study
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10556689/
https://www.ncbi.nlm.nih.gov/pubmed/37808498
http://dx.doi.org/10.3389/fneur.2023.1224345
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