Phase-dependent modulation of the vestibular–cerebellar network via combined alternating current stimulation influences human locomotion and posture
BackgroundHuman locomotion induces rhythmic movements of the trunk and head. Vestibular signaling is relayed to multiple regions in the brainstem and cerebellum, and plays an essential role in maintaining head stability. However, how the vestibular–cerebellar network contributes to the rhythmic loco...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-12-01
|
| Series: | Frontiers in Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2022.1057021/full |
| _version_ | 1811294824064614400 |
|---|---|
| author | Hisato Nakazono Hisato Nakazono Takanori Taniguchi Tsubasa Mitsutake Akinori Takeda Emi Yamada Katsuya Ogata |
| author_facet | Hisato Nakazono Hisato Nakazono Takanori Taniguchi Tsubasa Mitsutake Akinori Takeda Emi Yamada Katsuya Ogata |
| author_sort | Hisato Nakazono |
| collection | DOAJ |
| description | BackgroundHuman locomotion induces rhythmic movements of the trunk and head. Vestibular signaling is relayed to multiple regions in the brainstem and cerebellum, and plays an essential role in maintaining head stability. However, how the vestibular–cerebellar network contributes to the rhythmic locomotor pattern in humans is unclear. Transcranial alternating current stimulation (tACS) has been used to investigate the effects of the task-related network between stimulation regions in a phase-dependent manner. Here, we investigated the relationship between the vestibular system and the cerebellum during walking imagery using combined tACS over the left cerebellum and alternating current galvanic vestibular stimulation (AC-GVS).MethodsIn Experiment 1, we tested the effects of AC-GVS alone at around individual gait stride frequencies. In Experiment 2, we then determined the phase-specificity of combined stimulation at the gait frequency. Combined stimulation was applied at in-phase (0° phase lag) or anti-phase (180° phase lag) between the left vestibular and left cerebellar stimulation, and the sham stimulation. We evaluated the AC-GVS-induced periodic postural response during walking imagery or no-imagery using the peak oscillatory power on the angular velocity signals of the head in both experiments. In Experiment 2, we also examined the phase-locking value (PLV) between the periodic postural responses and the left AC-GVS signals to estimate entrainment of the postural response by AC-GVS.ResultsAC-GVS alone induced the periodic postural response in the yaw and roll axes, but no interactions with imagery walking were observed in Experiment 1 (p > 0.05). By contrast, combined in-phase stimulation increased yaw motion (0.345 ± 0.23) compared with sham (−0.044 ± 0.19) and anti-phase stimulation (−0.066 ± 0.18) during imaginary walking (in-phase vs. other conditions, imagery: p < 0.05; no-imagery: p ≥ 0.125). Furthermore, there was a positive correlation between the yaw peak power of actual locomotion and in-phase stimulation in the imagery session (imagery: p = 0.041; no-imagery: p = 0.177). Meanwhile, we found no imagery-dependent effects in roll peak power or PLV, although in-phase stimulation enhanced roll motion and PLV in Experiment 2.ConclusionThese findings suggest that combined stimulation can influence vestibular–cerebellar network activity, and modulate postural control and locomotion systems in a temporally sensitive manner. This novel combined tACS/AC-GVS stimulation approach may advance development of therapeutic applications. |
| first_indexed | 2024-04-13T05:23:13Z |
| format | Article |
| id | doaj.art-bf1ade6757584d578168ca6dfe5c493d |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-04-13T05:23:13Z |
| publishDate | 2022-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-bf1ade6757584d578168ca6dfe5c493d2022-12-22T03:00:41ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2022-12-011610.3389/fnins.2022.10570211057021Phase-dependent modulation of the vestibular–cerebellar network via combined alternating current stimulation influences human locomotion and postureHisato Nakazono0Hisato Nakazono1Takanori Taniguchi2Tsubasa Mitsutake3Akinori Takeda4Emi Yamada5Katsuya Ogata6Department of Occupational Therapy, Faculty of Medical Science, Fukuoka International University of Health and Welfare, Fukuoka, JapanDepartment of Health Sciences, Graduate School of Medical Sciences, Kyushu University, Fukuoka, JapanDepartment of Physical Therapy, Faculty of Medical Science, Fukuoka International University of Health and Welfare, Fukuoka, JapanDepartment of Physical Therapy, Faculty of Medical Science, Fukuoka International University of Health and Welfare, Fukuoka, JapanResearch Center for Brain Communication, Research Institute, Kochi University of Technology, Kochi, JapanDepartment of Linguistics, Faculty of Humanities, Kyushu University, Fukuoka, JapanDepartment of Pharmaceutical Sciences, School of Pharmacy at Fukuoka, International University of Health and Welfare, Fukuoka, JapanBackgroundHuman locomotion induces rhythmic movements of the trunk and head. Vestibular signaling is relayed to multiple regions in the brainstem and cerebellum, and plays an essential role in maintaining head stability. However, how the vestibular–cerebellar network contributes to the rhythmic locomotor pattern in humans is unclear. Transcranial alternating current stimulation (tACS) has been used to investigate the effects of the task-related network between stimulation regions in a phase-dependent manner. Here, we investigated the relationship between the vestibular system and the cerebellum during walking imagery using combined tACS over the left cerebellum and alternating current galvanic vestibular stimulation (AC-GVS).MethodsIn Experiment 1, we tested the effects of AC-GVS alone at around individual gait stride frequencies. In Experiment 2, we then determined the phase-specificity of combined stimulation at the gait frequency. Combined stimulation was applied at in-phase (0° phase lag) or anti-phase (180° phase lag) between the left vestibular and left cerebellar stimulation, and the sham stimulation. We evaluated the AC-GVS-induced periodic postural response during walking imagery or no-imagery using the peak oscillatory power on the angular velocity signals of the head in both experiments. In Experiment 2, we also examined the phase-locking value (PLV) between the periodic postural responses and the left AC-GVS signals to estimate entrainment of the postural response by AC-GVS.ResultsAC-GVS alone induced the periodic postural response in the yaw and roll axes, but no interactions with imagery walking were observed in Experiment 1 (p > 0.05). By contrast, combined in-phase stimulation increased yaw motion (0.345 ± 0.23) compared with sham (−0.044 ± 0.19) and anti-phase stimulation (−0.066 ± 0.18) during imaginary walking (in-phase vs. other conditions, imagery: p < 0.05; no-imagery: p ≥ 0.125). Furthermore, there was a positive correlation between the yaw peak power of actual locomotion and in-phase stimulation in the imagery session (imagery: p = 0.041; no-imagery: p = 0.177). Meanwhile, we found no imagery-dependent effects in roll peak power or PLV, although in-phase stimulation enhanced roll motion and PLV in Experiment 2.ConclusionThese findings suggest that combined stimulation can influence vestibular–cerebellar network activity, and modulate postural control and locomotion systems in a temporally sensitive manner. This novel combined tACS/AC-GVS stimulation approach may advance development of therapeutic applications.https://www.frontiersin.org/articles/10.3389/fnins.2022.1057021/fulltranscranial alternating current stimulationcerebellumgalvanic vestibular stimulationlocomotionphase synchronization |
| spellingShingle | Hisato Nakazono Hisato Nakazono Takanori Taniguchi Tsubasa Mitsutake Akinori Takeda Emi Yamada Katsuya Ogata Phase-dependent modulation of the vestibular–cerebellar network via combined alternating current stimulation influences human locomotion and posture Frontiers in Neuroscience transcranial alternating current stimulation cerebellum galvanic vestibular stimulation locomotion phase synchronization |
| title | Phase-dependent modulation of the vestibular–cerebellar network via combined alternating current stimulation influences human locomotion and posture |
| title_full | Phase-dependent modulation of the vestibular–cerebellar network via combined alternating current stimulation influences human locomotion and posture |
| title_fullStr | Phase-dependent modulation of the vestibular–cerebellar network via combined alternating current stimulation influences human locomotion and posture |
| title_full_unstemmed | Phase-dependent modulation of the vestibular–cerebellar network via combined alternating current stimulation influences human locomotion and posture |
| title_short | Phase-dependent modulation of the vestibular–cerebellar network via combined alternating current stimulation influences human locomotion and posture |
| title_sort | phase dependent modulation of the vestibular cerebellar network via combined alternating current stimulation influences human locomotion and posture |
| topic | transcranial alternating current stimulation cerebellum galvanic vestibular stimulation locomotion phase synchronization |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2022.1057021/full |
| work_keys_str_mv | AT hisatonakazono phasedependentmodulationofthevestibularcerebellarnetworkviacombinedalternatingcurrentstimulationinfluenceshumanlocomotionandposture AT hisatonakazono phasedependentmodulationofthevestibularcerebellarnetworkviacombinedalternatingcurrentstimulationinfluenceshumanlocomotionandposture AT takanoritaniguchi phasedependentmodulationofthevestibularcerebellarnetworkviacombinedalternatingcurrentstimulationinfluenceshumanlocomotionandposture AT tsubasamitsutake phasedependentmodulationofthevestibularcerebellarnetworkviacombinedalternatingcurrentstimulationinfluenceshumanlocomotionandposture AT akinoritakeda phasedependentmodulationofthevestibularcerebellarnetworkviacombinedalternatingcurrentstimulationinfluenceshumanlocomotionandposture AT emiyamada phasedependentmodulationofthevestibularcerebellarnetworkviacombinedalternatingcurrentstimulationinfluenceshumanlocomotionandposture AT katsuyaogata phasedependentmodulationofthevestibularcerebellarnetworkviacombinedalternatingcurrentstimulationinfluenceshumanlocomotionandposture |