Galvanic Vestibular Stimulation Improves Spatial Cognition After Unilateral Labyrinthectomy in Mice

Thanh Tin Nguyen; Gi-Sung Nam; Jin-Ju Kang; Gyu Cheol Han; Ji-Soo Kim; Marianne Dieterich; Sun-Young Oh

doi:10.3389/fneur.2021.716795

Galvanic Vestibular Stimulation Improves Spatial Cognition After Unilateral Labyrinthectomy in Mice

Front Neurol. 2021 Jul 29:12:716795. doi: 10.3389/fneur.2021.716795. eCollection 2021.

Authors

Thanh Tin Nguyen^{1

2

3}, Gi-Sung Nam^{2

4}, Jin-Ju Kang^{2

5}, Gyu Cheol Han⁶, Ji-Soo Kim⁷, Marianne Dieterich^{8

9

10}, Sun-Young Oh^{1

2

5}

Affiliations

¹ Jeonbuk National University College of Medicine, Jeonju, South Korea.
² Department of Neurology, Jeonbuk National University Hospital & School of Medicine, Jeonju, South Korea.
³ Department of Pharmacology, Hue University of Medicine and Pharmacy, Hue University, Hue, Vietnam.
⁴ Department of Otorhinolaryngology-Head and Neck Surgery, Chosun University College of Medicine, Kwangju, South Korea.
⁵ Research Institute of Clinical Medicine of Jeonbuk National University-Jeonbuk National University Hospital, Jeonju, South Korea.
⁶ Department of Otolaryngology-Head and Neck Surgery, Graduate School of Medicine, Gachon University of Medicine and Science, Incheon, South Korea.
⁷ Department of Neurology, Seoul National University Hospital & School of Medicine, Seoul, South Korea.
⁸ Department of Neurology, University Hospital, Ludwig-Maximilians-Universität, Munich, Germany.
⁹ German Center for Vertigo and Balance Disorders-IFB, University Hospital, Ludwig-Maximilians-Universität, Munich, Germany.
¹⁰ Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.

Abstract

Objectives: To investigate the deficits of spatial memory and navigation from unilateral vestibular deafferentation (UVD) and to determine the efficacy of galvanic vestibular stimulation (GVS) for recovery from these deficits using a mouse model of unilateral labyrinthectomy (UL). Methods: Thirty-six male C57BL/6 mice were allocated into three groups that comprise a control group and two experimental groups, UVD with (GVS group) and without GVS intervention (non-GVS group). In the experimental groups, we assessed the locomotor and cognitive behavioral function before (baseline) and 3, 7, and 14 days after surgical UL, using the open field (OF), Y maze, and Morris water maze (MWM) tests. In the GVS group, the stimulations were applied for 30 min daily from postoperative day (POD) 0-4 via the electrodes inserted subcutaneously close to both bony labyrinths. Results: Locomotion and spatial cognition were significantly impaired in the mice with UVD non-GVS group compared to the control group. GVS significantly accelerated recovery of locomotion compared to the control and non-GVS groups on PODs 3 (p < 0.001) and 7 (p < 0.05, Kruskal-Wallis and Mann-Whitney U tests) in the OF and Y maze tests. The mice in the GVS group were better in spatial working memory assessed with spontaneous alternation performance and spatial reference memory assessed with place recognition during the Y maze test than those in the non-GVS group on POD 3 (p < 0.001). In addition, the recovery of long-term spatial navigation deficits during the MWM, as indicated by the escape latency and the probe trial, was significantly better in the GVS group than in the non-GVS group 2 weeks after UVD (p < 0.01). Conclusions: UVD impairs spatial memory, navigation, and motor coordination. GVS accelerated recoveries in short- and long-term spatial memory and navigation, as well as locomotor function in mice with UVD, and may be applied to the patients with acute unilateral vestibular failure.

Keywords: galvanic vestibular stimulation; higher vestibular cognition; spatial navigation; unilateral labyrinthectomy; vestibular.