The Differential Effects of Acute Right- vs. Left-Sided Vestibular Deafferentation on Spatial Cognition in Unilateral Labyrinthectomized Mice

This study aimed to investigate the disparity in locomotor and spatial memory deficits caused by left- or right-sided unilateral vestibular deafferentation (UVD) using a mouse model of unilateral labyrinthectomy (UL) and to examine the effects of galvanic vestibular stimulation (GVS) on the deficits...

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Main Authors: Thanh Tin Nguyen, Gi-Sung Nam, Jin-Ju Kang, Gyu Cheol Han, Ji-Soo Kim, Marianne Dieterich, Sun-Young Oh
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-12-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2021.789487/full
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author Thanh Tin Nguyen
Thanh Tin Nguyen
Gi-Sung Nam
Gi-Sung Nam
Jin-Ju Kang
Jin-Ju Kang
Gyu Cheol Han
Ji-Soo Kim
Marianne Dieterich
Marianne Dieterich
Marianne Dieterich
Sun-Young Oh
Sun-Young Oh
author_facet Thanh Tin Nguyen
Thanh Tin Nguyen
Gi-Sung Nam
Gi-Sung Nam
Jin-Ju Kang
Jin-Ju Kang
Gyu Cheol Han
Ji-Soo Kim
Marianne Dieterich
Marianne Dieterich
Marianne Dieterich
Sun-Young Oh
Sun-Young Oh
author_sort Thanh Tin Nguyen
collection DOAJ
description This study aimed to investigate the disparity in locomotor and spatial memory deficits caused by left- or right-sided unilateral vestibular deafferentation (UVD) using a mouse model of unilateral labyrinthectomy (UL) and to examine the effects of galvanic vestibular stimulation (GVS) on the deficits over 14 days. Five experimental groups were established: the left-sided and right-sided UL (Lt.-UL and Rt.-UL) groups, left-sided and right-sided UL with bipolar GVS with the cathode on the lesion side (Lt.-GVS and Rt.-GVS) groups, and a control group with sham surgery. We assessed the locomotor and cognitive-behavioral functions using the open field (OF), Y maze, and Morris water maze (MWM) tests before (baseline) and 3, 7, and 14 days after surgical UL in each group. On postoperative day (POD) 3, locomotion and spatial working memory were more impaired in the Lt.-UL group compared with the Rt.-UL group (p < 0.01, Tamhane test). On POD 7, there was a substantial difference between the groups; the locomotion and spatial navigation of the Lt.-UL group recovered significantly more slowly compared with those of the Rt.-UL group. Although the differences in the short-term spatial cognition and motor coordination were resolved by POD 14, the long-term spatial navigation deficits assessed by the MWM were significantly worse in the Lt.-UL group compared with the Rt.-UL group. GVS intervention accelerated the vestibular compensation in both the Lt.-GVS and Rt.-GVS groups in terms of improvement of locomotion and spatial cognition. The current data imply that right- and left-sided UVD impair spatial cognition and locomotion differently and result in different compensatory patterns. Sequential bipolar GVS when the cathode (stimulating) was assigned to the lesion side accelerated recovery for UVD-induced spatial cognition, which may have implications for managing the patients with spatial cognitive impairment, especially that induced by unilateral peripheral vestibular damage on the dominant side.
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spelling doaj.art-f966497b7a81402496bd7dbbe331b5ff2022-12-21T22:53:41ZengFrontiers Media S.A.Frontiers in Neurology1664-22952021-12-011210.3389/fneur.2021.789487789487The Differential Effects of Acute Right- vs. Left-Sided Vestibular Deafferentation on Spatial Cognition in Unilateral Labyrinthectomized MiceThanh Tin Nguyen0Thanh Tin Nguyen1Gi-Sung Nam2Gi-Sung Nam3Jin-Ju Kang4Jin-Ju Kang5Gyu Cheol Han6Ji-Soo Kim7Marianne Dieterich8Marianne Dieterich9Marianne Dieterich10Sun-Young Oh11Sun-Young Oh12Department of Neurology, Jeonbuk National University Hospital & School of Medicine, Jeonju, South KoreaDepartment of Pharmacology, Hue University of Medicine and Pharmacy, Hue University, Hue, VietnamDepartment of Otorhinolaryngology-Head and Neck Surgery, Chosun University College of Medicine, Gwangju, South KoreaResearch Institute of Clinical Medicine of Jeonbuk National University-Jeonbuk National University Hospital, Jeonju, South KoreaDepartment of Neurology, Jeonbuk National University Hospital & School of Medicine, Jeonju, South KoreaResearch Institute of Clinical Medicine of Jeonbuk National University-Jeonbuk National University Hospital, Jeonju, South KoreaDepartment of Otolaryngology-Head and Neck Surgery, Gachon University of Medicine and Science, Graduate School of Medicine, Incheon, South KoreaDepartment of Neurology, Seoul National University Bundang Hospital & School of Medicine, Seoul, South KoreaDepartment of Neurology, University Hospital, Ludwig-Maximilians-Universität, Munich, GermanyGerman Center for Vertigo and Balance Disorders-IFB, University Hospital, Ludwig-Maximilians-Universität, Munich, GermanyMunich Cluster for Systems Neurology (SyNergy), Munich, GermanyDepartment of Neurology, Jeonbuk National University Hospital & School of Medicine, Jeonju, South KoreaResearch Institute of Clinical Medicine of Jeonbuk National University-Jeonbuk National University Hospital, Jeonju, South KoreaThis study aimed to investigate the disparity in locomotor and spatial memory deficits caused by left- or right-sided unilateral vestibular deafferentation (UVD) using a mouse model of unilateral labyrinthectomy (UL) and to examine the effects of galvanic vestibular stimulation (GVS) on the deficits over 14 days. Five experimental groups were established: the left-sided and right-sided UL (Lt.-UL and Rt.-UL) groups, left-sided and right-sided UL with bipolar GVS with the cathode on the lesion side (Lt.-GVS and Rt.-GVS) groups, and a control group with sham surgery. We assessed the locomotor and cognitive-behavioral functions using the open field (OF), Y maze, and Morris water maze (MWM) tests before (baseline) and 3, 7, and 14 days after surgical UL in each group. On postoperative day (POD) 3, locomotion and spatial working memory were more impaired in the Lt.-UL group compared with the Rt.-UL group (p < 0.01, Tamhane test). On POD 7, there was a substantial difference between the groups; the locomotion and spatial navigation of the Lt.-UL group recovered significantly more slowly compared with those of the Rt.-UL group. Although the differences in the short-term spatial cognition and motor coordination were resolved by POD 14, the long-term spatial navigation deficits assessed by the MWM were significantly worse in the Lt.-UL group compared with the Rt.-UL group. GVS intervention accelerated the vestibular compensation in both the Lt.-GVS and Rt.-GVS groups in terms of improvement of locomotion and spatial cognition. The current data imply that right- and left-sided UVD impair spatial cognition and locomotion differently and result in different compensatory patterns. Sequential bipolar GVS when the cathode (stimulating) was assigned to the lesion side accelerated recovery for UVD-induced spatial cognition, which may have implications for managing the patients with spatial cognitive impairment, especially that induced by unilateral peripheral vestibular damage on the dominant side.https://www.frontiersin.org/articles/10.3389/fneur.2021.789487/fullhemispheric dominancelabyrinthectomyunilateral vestibular deafferentationhigher vestibular cognitiongalvanic vestibular stimulation
spellingShingle Thanh Tin Nguyen
Thanh Tin Nguyen
Gi-Sung Nam
Gi-Sung Nam
Jin-Ju Kang
Jin-Ju Kang
Gyu Cheol Han
Ji-Soo Kim
Marianne Dieterich
Marianne Dieterich
Marianne Dieterich
Sun-Young Oh
Sun-Young Oh
The Differential Effects of Acute Right- vs. Left-Sided Vestibular Deafferentation on Spatial Cognition in Unilateral Labyrinthectomized Mice
Frontiers in Neurology
hemispheric dominance
labyrinthectomy
unilateral vestibular deafferentation
higher vestibular cognition
galvanic vestibular stimulation
title The Differential Effects of Acute Right- vs. Left-Sided Vestibular Deafferentation on Spatial Cognition in Unilateral Labyrinthectomized Mice
title_full The Differential Effects of Acute Right- vs. Left-Sided Vestibular Deafferentation on Spatial Cognition in Unilateral Labyrinthectomized Mice
title_fullStr The Differential Effects of Acute Right- vs. Left-Sided Vestibular Deafferentation on Spatial Cognition in Unilateral Labyrinthectomized Mice
title_full_unstemmed The Differential Effects of Acute Right- vs. Left-Sided Vestibular Deafferentation on Spatial Cognition in Unilateral Labyrinthectomized Mice
title_short The Differential Effects of Acute Right- vs. Left-Sided Vestibular Deafferentation on Spatial Cognition in Unilateral Labyrinthectomized Mice
title_sort differential effects of acute right vs left sided vestibular deafferentation on spatial cognition in unilateral labyrinthectomized mice
topic hemispheric dominance
labyrinthectomy
unilateral vestibular deafferentation
higher vestibular cognition
galvanic vestibular stimulation
url https://www.frontiersin.org/articles/10.3389/fneur.2021.789487/full
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