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Superior semicircular canal dehiscence and subsequent closure induces reversible impaired decision-making

BACKGROUND: Vestibular loss and dysfunction has been associated with cognitive deficits, decreased spatial navigation, spatial memory, visuospatial ability, attention, executive function, and processing speed among others. Superior semicircular canal dehiscence (SSCD) is a vestibular-cochlear disord...

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Autores principales: Mowery, Todd M., Wackym, P. Ashley, Nacipucha, Jacqueline, Dangcil, Evelynne, Stadler, Ryan D., Tucker, Aaron, Carayannopoulos, Nicolas L., Beshy, Mina A., Hong, Sean S., Yao, Justin D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10613502/
https://www.ncbi.nlm.nih.gov/pubmed/37905188
http://dx.doi.org/10.3389/fneur.2023.1259030
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author Mowery, Todd M.
Wackym, P. Ashley
Nacipucha, Jacqueline
Dangcil, Evelynne
Stadler, Ryan D.
Tucker, Aaron
Carayannopoulos, Nicolas L.
Beshy, Mina A.
Hong, Sean S.
Yao, Justin D.
author_facet Mowery, Todd M.
Wackym, P. Ashley
Nacipucha, Jacqueline
Dangcil, Evelynne
Stadler, Ryan D.
Tucker, Aaron
Carayannopoulos, Nicolas L.
Beshy, Mina A.
Hong, Sean S.
Yao, Justin D.
author_sort Mowery, Todd M.
collection PubMed
description BACKGROUND: Vestibular loss and dysfunction has been associated with cognitive deficits, decreased spatial navigation, spatial memory, visuospatial ability, attention, executive function, and processing speed among others. Superior semicircular canal dehiscence (SSCD) is a vestibular-cochlear disorder in humans in which a pathological third mobile window of the otic capsule creates changes to the flow of sound pressure energy through the perilymph/endolymph. The primary symptoms include sound-induced dizziness/vertigo, inner ear conductive hearing loss, autophony, headaches, and visual problems; however, individuals also experience measurable deficits in basic decision-making, short-term memory, concentration, spatial cognition, and depression. These suggest central mechanisms of impairment are associated with vestibular disorders; therefore, we directly tested this hypothesis using both an auditory and visual decision-making task of varying difficulty levels in our model of SSCD. METHODS: Adult Mongolian gerbils (n = 33) were trained on one of four versions of a Go-NoGo stimulus presentation rate discrimination task that included standard (“easy”) or more difficult (“hard”) auditory and visual stimuli. After 10 days of training, preoperative ABR and c+VEMP testing was followed by a surgical fenestration of the left superior semicircular canal. Animals with persistent circling or head tilt were excluded to minimize effects from acute vestibular injury. Testing recommenced at postoperative day 5 and continued through postoperative day 15 at which point final ABR and c+VEMP testing was carried out. RESULTS: Behavioral data (d-primes) were compared between preoperative performance (training day 8–10) and postoperative days 6–8 and 13–15. Behavioral performance was measured during the peak of SSCD induced ABR and c + VEMP impairment and the return towards baseline as the dehiscence began to resurface by osteoneogenesis. There were significant differences in behavioral performance (d-prime) and its behavioral components (Hits, Misses, False Alarms, and Correct Rejections). These changes were highly correlated with persistent deficits in c + VEMPs at the end of training (postoperative day 15). The controls demonstrated additional learning post procedure that was absent in the SSCD group. CONCLUSION: These results suggest that aberrant asymmetric vestibular output results in decision-making impairments in these discrimination tasks and could be associated with the other cognitive impairments resulting from vestibular dysfunction.
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spelling pubmed-106135022023-10-30 Superior semicircular canal dehiscence and subsequent closure induces reversible impaired decision-making Mowery, Todd M. Wackym, P. Ashley Nacipucha, Jacqueline Dangcil, Evelynne Stadler, Ryan D. Tucker, Aaron Carayannopoulos, Nicolas L. Beshy, Mina A. Hong, Sean S. Yao, Justin D. Front Neurol Neurology BACKGROUND: Vestibular loss and dysfunction has been associated with cognitive deficits, decreased spatial navigation, spatial memory, visuospatial ability, attention, executive function, and processing speed among others. Superior semicircular canal dehiscence (SSCD) is a vestibular-cochlear disorder in humans in which a pathological third mobile window of the otic capsule creates changes to the flow of sound pressure energy through the perilymph/endolymph. The primary symptoms include sound-induced dizziness/vertigo, inner ear conductive hearing loss, autophony, headaches, and visual problems; however, individuals also experience measurable deficits in basic decision-making, short-term memory, concentration, spatial cognition, and depression. These suggest central mechanisms of impairment are associated with vestibular disorders; therefore, we directly tested this hypothesis using both an auditory and visual decision-making task of varying difficulty levels in our model of SSCD. METHODS: Adult Mongolian gerbils (n = 33) were trained on one of four versions of a Go-NoGo stimulus presentation rate discrimination task that included standard (“easy”) or more difficult (“hard”) auditory and visual stimuli. After 10 days of training, preoperative ABR and c+VEMP testing was followed by a surgical fenestration of the left superior semicircular canal. Animals with persistent circling or head tilt were excluded to minimize effects from acute vestibular injury. Testing recommenced at postoperative day 5 and continued through postoperative day 15 at which point final ABR and c+VEMP testing was carried out. RESULTS: Behavioral data (d-primes) were compared between preoperative performance (training day 8–10) and postoperative days 6–8 and 13–15. Behavioral performance was measured during the peak of SSCD induced ABR and c + VEMP impairment and the return towards baseline as the dehiscence began to resurface by osteoneogenesis. There were significant differences in behavioral performance (d-prime) and its behavioral components (Hits, Misses, False Alarms, and Correct Rejections). These changes were highly correlated with persistent deficits in c + VEMPs at the end of training (postoperative day 15). The controls demonstrated additional learning post procedure that was absent in the SSCD group. CONCLUSION: These results suggest that aberrant asymmetric vestibular output results in decision-making impairments in these discrimination tasks and could be associated with the other cognitive impairments resulting from vestibular dysfunction. Frontiers Media S.A. 2023-10-12 /pmc/articles/PMC10613502/ /pubmed/37905188 http://dx.doi.org/10.3389/fneur.2023.1259030 Text en Copyright © 2023 Mowery, Wackym, Nacipucha, Dangcil, Stadler, Tucker, Carayannopoulos, Beshy, Hong and Yao. 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
Mowery, Todd M.
Wackym, P. Ashley
Nacipucha, Jacqueline
Dangcil, Evelynne
Stadler, Ryan D.
Tucker, Aaron
Carayannopoulos, Nicolas L.
Beshy, Mina A.
Hong, Sean S.
Yao, Justin D.
Superior semicircular canal dehiscence and subsequent closure induces reversible impaired decision-making
title Superior semicircular canal dehiscence and subsequent closure induces reversible impaired decision-making
title_full Superior semicircular canal dehiscence and subsequent closure induces reversible impaired decision-making
title_fullStr Superior semicircular canal dehiscence and subsequent closure induces reversible impaired decision-making
title_full_unstemmed Superior semicircular canal dehiscence and subsequent closure induces reversible impaired decision-making
title_short Superior semicircular canal dehiscence and subsequent closure induces reversible impaired decision-making
title_sort superior semicircular canal dehiscence and subsequent closure induces reversible impaired decision-making
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10613502/
https://www.ncbi.nlm.nih.gov/pubmed/37905188
http://dx.doi.org/10.3389/fneur.2023.1259030
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