Multisensory gaze stabilization in response to subchronic alteration of vestibular type I hair cells

The functional complementarity of the vestibulo-ocular reflex (VOR) and optokinetic reflex (OKR) allows for optimal combined gaze stabilization responses (CGR) in light. While sensory substitution has been reported following complete vestibular loss, the capacity of the central vestibular system to...

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Autores: Llorens Llacuna, Joan, Schenberg, Louise, Palou Miranda, Aida, Simon, François, Bonnard, Tess, Barton, Charles-Elliot, Fricker, Desdemona, Tagliabue, Michele, Beraneck, Mathieu
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Universidad de Barcelona
Repositorio:Dipòsit Digital de la UB
OAI Identifier:oai:diposit.ub.edu:2445/208298
Acceso en línea:https://hdl.handle.net/2445/208298
Access Level:acceso abierto
Palabra clave:Cabells
Cèl·lules acústiques
Neurociències
Hair
Hair cells
Neurosciences
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repository_id_str
spelling Multisensory gaze stabilization in response to subchronic alteration of vestibular type I hair cellsLlorens Llacuna, JoanSchenberg, LouisePalou Miranda, AidaSimon, FrançoisBonnard, TessBarton, Charles-ElliotFricker, DesdemonaTagliabue, MicheleBeraneck, MathieuCabellsCèl·lules acústiquesNeurociènciesHairHair cellsNeurosciencesThe functional complementarity of the vestibulo-ocular reflex (VOR) and optokinetic reflex (OKR) allows for optimal combined gaze stabilization responses (CGR) in light. While sensory substitution has been reported following complete vestibular loss, the capacity of the central vestibular system to compensate for partial peripheral vestibular loss remains to be determined. Here, we first demonstrate the efficacy of a 6-week subchronic ototoxic protocol in inducing transient and partial vestibular loss which equally affects the canal- and otolith-dependent VORs. Immunostaining of hair cells in the vestibular sensory epithelia revealed that organ-specific alteration of type I, but not type II, hair cells correlates with functional impairments. The decrease in VOR performance is paralleled with an increase in the gain of the OKR occurring in a specific range of frequencies where VOR normally dominates gaze stabilization, compatible with a sensory substitution process. Comparison of unimodal OKR or VOR versus bimodal CGR revealed that visuo-vestibular interactions remain reduced despite a significant recovery in the VOR. Modeling and sweep-based analysis revealed that the differential capacity to optimally combine OKR and VOR correlates with the reproducibility of the VOR responses. Overall, these results shed light on the multisensory reweighting occurring in pathologies with fluctuating peripheral vestibular malfunction.eLife Sciences2023info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfhttps://hdl.handle.net/2445/208298Articles publicats en revistes (Ciències Fisiològiques)reponame:Dipòsit Digital de la UBinstname:Universidad de BarcelonaInglésReproducció del document publicat a: https://doi.org/10.7554/eLife.88819.3eLife, 2023, vol. 12, p. RP88819https://doi.org/10.7554/eLife.88819.3cc-by (c) Schenberg, L. et al., 2023http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:diposit.ub.edu:2445/2082982026-05-27T06:46:51Z
dc.title.none.fl_str_mv Multisensory gaze stabilization in response to subchronic alteration of vestibular type I hair cells
title Multisensory gaze stabilization in response to subchronic alteration of vestibular type I hair cells
spellingShingle Multisensory gaze stabilization in response to subchronic alteration of vestibular type I hair cells
Llorens Llacuna, Joan
Cabells
Cèl·lules acústiques
Neurociències
Hair
Hair cells
Neurosciences
title_short Multisensory gaze stabilization in response to subchronic alteration of vestibular type I hair cells
title_full Multisensory gaze stabilization in response to subchronic alteration of vestibular type I hair cells
title_fullStr Multisensory gaze stabilization in response to subchronic alteration of vestibular type I hair cells
title_full_unstemmed Multisensory gaze stabilization in response to subchronic alteration of vestibular type I hair cells
title_sort Multisensory gaze stabilization in response to subchronic alteration of vestibular type I hair cells
dc.creator.none.fl_str_mv Llorens Llacuna, Joan
Schenberg, Louise
Palou Miranda, Aida
Simon, François
Bonnard, Tess
Barton, Charles-Elliot
Fricker, Desdemona
Tagliabue, Michele
Beraneck, Mathieu
author Llorens Llacuna, Joan
author_facet Llorens Llacuna, Joan
Schenberg, Louise
Palou Miranda, Aida
Simon, François
Bonnard, Tess
Barton, Charles-Elliot
Fricker, Desdemona
Tagliabue, Michele
Beraneck, Mathieu
author_role author
author2 Schenberg, Louise
Palou Miranda, Aida
Simon, François
Bonnard, Tess
Barton, Charles-Elliot
Fricker, Desdemona
Tagliabue, Michele
Beraneck, Mathieu
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Cabells
Cèl·lules acústiques
Neurociències
Hair
Hair cells
Neurosciences
topic Cabells
Cèl·lules acústiques
Neurociències
Hair
Hair cells
Neurosciences
description The functional complementarity of the vestibulo-ocular reflex (VOR) and optokinetic reflex (OKR) allows for optimal combined gaze stabilization responses (CGR) in light. While sensory substitution has been reported following complete vestibular loss, the capacity of the central vestibular system to compensate for partial peripheral vestibular loss remains to be determined. Here, we first demonstrate the efficacy of a 6-week subchronic ototoxic protocol in inducing transient and partial vestibular loss which equally affects the canal- and otolith-dependent VORs. Immunostaining of hair cells in the vestibular sensory epithelia revealed that organ-specific alteration of type I, but not type II, hair cells correlates with functional impairments. The decrease in VOR performance is paralleled with an increase in the gain of the OKR occurring in a specific range of frequencies where VOR normally dominates gaze stabilization, compatible with a sensory substitution process. Comparison of unimodal OKR or VOR versus bimodal CGR revealed that visuo-vestibular interactions remain reduced despite a significant recovery in the VOR. Modeling and sweep-based analysis revealed that the differential capacity to optimally combine OKR and VOR correlates with the reproducibility of the VOR responses. Overall, these results shed light on the multisensory reweighting occurring in pathologies with fluctuating peripheral vestibular malfunction.
publishDate 2023
dc.date.none.fl_str_mv 2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2445/208298
url https://hdl.handle.net/2445/208298
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a: https://doi.org/10.7554/eLife.88819.3
eLife, 2023, vol. 12, p. RP88819
https://doi.org/10.7554/eLife.88819.3
dc.rights.none.fl_str_mv cc-by (c) Schenberg, L. et al., 2023
http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv cc-by (c) Schenberg, L. et al., 2023
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv eLife Sciences
publisher.none.fl_str_mv eLife Sciences
dc.source.none.fl_str_mv Articles publicats en revistes (Ciències Fisiològiques)
reponame:Dipòsit Digital de la UB
instname:Universidad de Barcelona
instname_str Universidad de Barcelona
reponame_str Dipòsit Digital de la UB
collection Dipòsit Digital de la UB
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15.300719

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