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The “vestibular neuromatrix”: A proposed, expanded vestibular network from graph theory in post‐concussive vestibular dysfunction

Convergent clinical and neuroimaging evidence suggests that higher vestibular function is subserved by a distributed network including visuospatial, cognitive–affective, proprioceptive, and integrative brain regions. Clinical vestibular syndromes may perturb this network, resulting in deficits acros...

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Autores principales: Smith, Jeremy L., Trofimova, Anna, Ahluwalia, Vishwadeep, Casado Garrido, Jose J., Hurtado, Julia, Frank, Rachael, Hodge, April, Gore, Russell K., Allen, Jason W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8886666/
https://www.ncbi.nlm.nih.gov/pubmed/34862683
http://dx.doi.org/10.1002/hbm.25737
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author Smith, Jeremy L.
Trofimova, Anna
Ahluwalia, Vishwadeep
Casado Garrido, Jose J.
Hurtado, Julia
Frank, Rachael
Hodge, April
Gore, Russell K.
Allen, Jason W.
author_facet Smith, Jeremy L.
Trofimova, Anna
Ahluwalia, Vishwadeep
Casado Garrido, Jose J.
Hurtado, Julia
Frank, Rachael
Hodge, April
Gore, Russell K.
Allen, Jason W.
author_sort Smith, Jeremy L.
collection PubMed
description Convergent clinical and neuroimaging evidence suggests that higher vestibular function is subserved by a distributed network including visuospatial, cognitive–affective, proprioceptive, and integrative brain regions. Clinical vestibular syndromes may perturb this network, resulting in deficits across a variety of functional domains. Here, we leverage structural and functional neuroimaging to characterize this extended network in healthy control participants and patients with post‐concussive vestibular dysfunction (PCVD). Then, 27 healthy control subjects (15 females) and 18 patients with subacute PCVD (12 female) were selected for participation. Eighty‐two regions of interest (network nodes) were identified based on previous publications, group‐wise differences in BOLD signal amplitude and connectivity, and multivariate pattern analysis on affective tests. Group‐specific “core” networks, as well as a “consensus” network comprised of connections common to all participants, were then generated based on probabilistic tractography and functional connectivity between the 82 nodes and subjected to analyses of node centrality and community structure. Whereas the consensus network was comprised of affective, integrative, and vestibular nodes, PCVD participants exhibited diminished integration and centrality among vestibular and affective nodes and increased centrality of visual, supplementary motor, and frontal and cingulate eye field nodes. Clinical outcomes, derived from dynamic posturography, were associated with approximately 62% of all connections but best predicted by amygdalar, prefrontal, and cingulate connectivity. No group‐wise differences in diffusion metrics or tractography were noted. These findings indicate that cognitive, affective, and proprioceptive substrates contribute to vestibular processing and performance and highlight the need to consider these domains during clinical diagnosis and treatment planning.
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spelling pubmed-88866662022-03-04 The “vestibular neuromatrix”: A proposed, expanded vestibular network from graph theory in post‐concussive vestibular dysfunction Smith, Jeremy L. Trofimova, Anna Ahluwalia, Vishwadeep Casado Garrido, Jose J. Hurtado, Julia Frank, Rachael Hodge, April Gore, Russell K. Allen, Jason W. Hum Brain Mapp Research Articles Convergent clinical and neuroimaging evidence suggests that higher vestibular function is subserved by a distributed network including visuospatial, cognitive–affective, proprioceptive, and integrative brain regions. Clinical vestibular syndromes may perturb this network, resulting in deficits across a variety of functional domains. Here, we leverage structural and functional neuroimaging to characterize this extended network in healthy control participants and patients with post‐concussive vestibular dysfunction (PCVD). Then, 27 healthy control subjects (15 females) and 18 patients with subacute PCVD (12 female) were selected for participation. Eighty‐two regions of interest (network nodes) were identified based on previous publications, group‐wise differences in BOLD signal amplitude and connectivity, and multivariate pattern analysis on affective tests. Group‐specific “core” networks, as well as a “consensus” network comprised of connections common to all participants, were then generated based on probabilistic tractography and functional connectivity between the 82 nodes and subjected to analyses of node centrality and community structure. Whereas the consensus network was comprised of affective, integrative, and vestibular nodes, PCVD participants exhibited diminished integration and centrality among vestibular and affective nodes and increased centrality of visual, supplementary motor, and frontal and cingulate eye field nodes. Clinical outcomes, derived from dynamic posturography, were associated with approximately 62% of all connections but best predicted by amygdalar, prefrontal, and cingulate connectivity. No group‐wise differences in diffusion metrics or tractography were noted. These findings indicate that cognitive, affective, and proprioceptive substrates contribute to vestibular processing and performance and highlight the need to consider these domains during clinical diagnosis and treatment planning. John Wiley & Sons, Inc. 2021-12-03 /pmc/articles/PMC8886666/ /pubmed/34862683 http://dx.doi.org/10.1002/hbm.25737 Text en © 2021 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Research Articles
Smith, Jeremy L.
Trofimova, Anna
Ahluwalia, Vishwadeep
Casado Garrido, Jose J.
Hurtado, Julia
Frank, Rachael
Hodge, April
Gore, Russell K.
Allen, Jason W.
The “vestibular neuromatrix”: A proposed, expanded vestibular network from graph theory in post‐concussive vestibular dysfunction
title The “vestibular neuromatrix”: A proposed, expanded vestibular network from graph theory in post‐concussive vestibular dysfunction
title_full The “vestibular neuromatrix”: A proposed, expanded vestibular network from graph theory in post‐concussive vestibular dysfunction
title_fullStr The “vestibular neuromatrix”: A proposed, expanded vestibular network from graph theory in post‐concussive vestibular dysfunction
title_full_unstemmed The “vestibular neuromatrix”: A proposed, expanded vestibular network from graph theory in post‐concussive vestibular dysfunction
title_short The “vestibular neuromatrix”: A proposed, expanded vestibular network from graph theory in post‐concussive vestibular dysfunction
title_sort “vestibular neuromatrix”: a proposed, expanded vestibular network from graph theory in post‐concussive vestibular dysfunction
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8886666/
https://www.ncbi.nlm.nih.gov/pubmed/34862683
http://dx.doi.org/10.1002/hbm.25737
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