Cargando…

Changes in functional connectivity among vestibulo-visuo-somatosensory and spatial cognitive cortical areas in persistent postural-perceptual dizziness: resting-state fMRI studies before and after visual stimulation

INTRODUCTION: Persistent postural-perceptual dizziness (PPPD) is a functional chronic vestibular syndrome with symptom exacerbation by upright posture, motion, and complex visual stimuli. Among these exacerbating factors, visual exacerbation is the most specific characteristic of PPPD requiring furt...

Descripción completa

Detalles Bibliográficos
Autores principales: Yagi, Chihiro, Morita, Yuka, Yamagishi, Tatsuya, Ohshima, Shinsuke, Izumi, Shuji, Takahashi, Kuniyuki, Watanabe, Masaki, Itoh, Kosuke, Suzuki, Yuji, Igarashi, Hironaka, Horii, Arata
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10406134/
https://www.ncbi.nlm.nih.gov/pubmed/37554393
http://dx.doi.org/10.3389/fneur.2023.1215004
_version_ 1785085685576761344
author Yagi, Chihiro
Morita, Yuka
Yamagishi, Tatsuya
Ohshima, Shinsuke
Izumi, Shuji
Takahashi, Kuniyuki
Watanabe, Masaki
Itoh, Kosuke
Suzuki, Yuji
Igarashi, Hironaka
Horii, Arata
author_facet Yagi, Chihiro
Morita, Yuka
Yamagishi, Tatsuya
Ohshima, Shinsuke
Izumi, Shuji
Takahashi, Kuniyuki
Watanabe, Masaki
Itoh, Kosuke
Suzuki, Yuji
Igarashi, Hironaka
Horii, Arata
author_sort Yagi, Chihiro
collection PubMed
description INTRODUCTION: Persistent postural-perceptual dizziness (PPPD) is a functional chronic vestibular syndrome with symptom exacerbation by upright posture, motion, and complex visual stimuli. Among these exacerbating factors, visual exacerbation is the most specific characteristic of PPPD requiring further investigation. We hypothesized that stimulus-induced changes occur in the functional connectivity (FC) rather than simple neural activation that is involved in visual stimulation. The present study aimed to identify the neural basis of PPPD by investigating FC before and after visual stimulation. METHODS: Eleven patients with PPPD and 11 age- and sex-matched healthy controls (HCs) underwent resting-state fMRI (rs-fMRI) before and after task-based fMRI with visual stimuli. RESULTS: At pre-stimulus, FC between the vestibular cortex and visual areas was low, while that between the somatosensory and visual areas was high in PPPD compared with that in HCs. FC between the visuospatial (parahippocampal gyrus) and spatial cognitive areas (inferior parietal lobule) was elevated in PPPD even in the pre-stimulus condition, which no longer increased at post-stimulus as observed in HCs. In the post-stimulus condition, FC between the visual and spatial cognitive areas and that between the visual and prefrontal areas increased compared with that in the pre-stimulus condition in PPPD. Task-based fMRI demonstrated that no brain regions showed different activities between the HC and PPPD groups during visual stimulation. DISCUSSION: In PPPD, vestibular inputs may not be fully utilized in the vestibulo-visuo-somatosensory network. Given that the FC between visuospatial and spatial cognitive areas increased even in HCs after visual stimuli, elevated status of this FC in combination with the high FC between the somatosensory and visual areas would be involved in the visual exacerbation in PPPD. An increase in FC from the visual areas to spatial cognitive and prefrontal areas after visual stimuli may account for the prolonged symptoms after visual exacerbation and anxious status in PPPD.
format Online
Article
Text
id pubmed-10406134
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-104061342023-08-08 Changes in functional connectivity among vestibulo-visuo-somatosensory and spatial cognitive cortical areas in persistent postural-perceptual dizziness: resting-state fMRI studies before and after visual stimulation Yagi, Chihiro Morita, Yuka Yamagishi, Tatsuya Ohshima, Shinsuke Izumi, Shuji Takahashi, Kuniyuki Watanabe, Masaki Itoh, Kosuke Suzuki, Yuji Igarashi, Hironaka Horii, Arata Front Neurol Neurology INTRODUCTION: Persistent postural-perceptual dizziness (PPPD) is a functional chronic vestibular syndrome with symptom exacerbation by upright posture, motion, and complex visual stimuli. Among these exacerbating factors, visual exacerbation is the most specific characteristic of PPPD requiring further investigation. We hypothesized that stimulus-induced changes occur in the functional connectivity (FC) rather than simple neural activation that is involved in visual stimulation. The present study aimed to identify the neural basis of PPPD by investigating FC before and after visual stimulation. METHODS: Eleven patients with PPPD and 11 age- and sex-matched healthy controls (HCs) underwent resting-state fMRI (rs-fMRI) before and after task-based fMRI with visual stimuli. RESULTS: At pre-stimulus, FC between the vestibular cortex and visual areas was low, while that between the somatosensory and visual areas was high in PPPD compared with that in HCs. FC between the visuospatial (parahippocampal gyrus) and spatial cognitive areas (inferior parietal lobule) was elevated in PPPD even in the pre-stimulus condition, which no longer increased at post-stimulus as observed in HCs. In the post-stimulus condition, FC between the visual and spatial cognitive areas and that between the visual and prefrontal areas increased compared with that in the pre-stimulus condition in PPPD. Task-based fMRI demonstrated that no brain regions showed different activities between the HC and PPPD groups during visual stimulation. DISCUSSION: In PPPD, vestibular inputs may not be fully utilized in the vestibulo-visuo-somatosensory network. Given that the FC between visuospatial and spatial cognitive areas increased even in HCs after visual stimuli, elevated status of this FC in combination with the high FC between the somatosensory and visual areas would be involved in the visual exacerbation in PPPD. An increase in FC from the visual areas to spatial cognitive and prefrontal areas after visual stimuli may account for the prolonged symptoms after visual exacerbation and anxious status in PPPD. Frontiers Media S.A. 2023-07-24 /pmc/articles/PMC10406134/ /pubmed/37554393 http://dx.doi.org/10.3389/fneur.2023.1215004 Text en Copyright © 2023 Yagi, Morita, Yamagishi, Ohshima, Izumi, Takahashi, Watanabe, Itoh, Suzuki, Igarashi and Horii. 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
Yagi, Chihiro
Morita, Yuka
Yamagishi, Tatsuya
Ohshima, Shinsuke
Izumi, Shuji
Takahashi, Kuniyuki
Watanabe, Masaki
Itoh, Kosuke
Suzuki, Yuji
Igarashi, Hironaka
Horii, Arata
Changes in functional connectivity among vestibulo-visuo-somatosensory and spatial cognitive cortical areas in persistent postural-perceptual dizziness: resting-state fMRI studies before and after visual stimulation
title Changes in functional connectivity among vestibulo-visuo-somatosensory and spatial cognitive cortical areas in persistent postural-perceptual dizziness: resting-state fMRI studies before and after visual stimulation
title_full Changes in functional connectivity among vestibulo-visuo-somatosensory and spatial cognitive cortical areas in persistent postural-perceptual dizziness: resting-state fMRI studies before and after visual stimulation
title_fullStr Changes in functional connectivity among vestibulo-visuo-somatosensory and spatial cognitive cortical areas in persistent postural-perceptual dizziness: resting-state fMRI studies before and after visual stimulation
title_full_unstemmed Changes in functional connectivity among vestibulo-visuo-somatosensory and spatial cognitive cortical areas in persistent postural-perceptual dizziness: resting-state fMRI studies before and after visual stimulation
title_short Changes in functional connectivity among vestibulo-visuo-somatosensory and spatial cognitive cortical areas in persistent postural-perceptual dizziness: resting-state fMRI studies before and after visual stimulation
title_sort changes in functional connectivity among vestibulo-visuo-somatosensory and spatial cognitive cortical areas in persistent postural-perceptual dizziness: resting-state fmri studies before and after visual stimulation
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10406134/
https://www.ncbi.nlm.nih.gov/pubmed/37554393
http://dx.doi.org/10.3389/fneur.2023.1215004
work_keys_str_mv AT yagichihiro changesinfunctionalconnectivityamongvestibulovisuosomatosensoryandspatialcognitivecorticalareasinpersistentposturalperceptualdizzinessrestingstatefmristudiesbeforeandaftervisualstimulation
AT moritayuka changesinfunctionalconnectivityamongvestibulovisuosomatosensoryandspatialcognitivecorticalareasinpersistentposturalperceptualdizzinessrestingstatefmristudiesbeforeandaftervisualstimulation
AT yamagishitatsuya changesinfunctionalconnectivityamongvestibulovisuosomatosensoryandspatialcognitivecorticalareasinpersistentposturalperceptualdizzinessrestingstatefmristudiesbeforeandaftervisualstimulation
AT ohshimashinsuke changesinfunctionalconnectivityamongvestibulovisuosomatosensoryandspatialcognitivecorticalareasinpersistentposturalperceptualdizzinessrestingstatefmristudiesbeforeandaftervisualstimulation
AT izumishuji changesinfunctionalconnectivityamongvestibulovisuosomatosensoryandspatialcognitivecorticalareasinpersistentposturalperceptualdizzinessrestingstatefmristudiesbeforeandaftervisualstimulation
AT takahashikuniyuki changesinfunctionalconnectivityamongvestibulovisuosomatosensoryandspatialcognitivecorticalareasinpersistentposturalperceptualdizzinessrestingstatefmristudiesbeforeandaftervisualstimulation
AT watanabemasaki changesinfunctionalconnectivityamongvestibulovisuosomatosensoryandspatialcognitivecorticalareasinpersistentposturalperceptualdizzinessrestingstatefmristudiesbeforeandaftervisualstimulation
AT itohkosuke changesinfunctionalconnectivityamongvestibulovisuosomatosensoryandspatialcognitivecorticalareasinpersistentposturalperceptualdizzinessrestingstatefmristudiesbeforeandaftervisualstimulation
AT suzukiyuji changesinfunctionalconnectivityamongvestibulovisuosomatosensoryandspatialcognitivecorticalareasinpersistentposturalperceptualdizzinessrestingstatefmristudiesbeforeandaftervisualstimulation
AT igarashihironaka changesinfunctionalconnectivityamongvestibulovisuosomatosensoryandspatialcognitivecorticalareasinpersistentposturalperceptualdizzinessrestingstatefmristudiesbeforeandaftervisualstimulation
AT horiiarata changesinfunctionalconnectivityamongvestibulovisuosomatosensoryandspatialcognitivecorticalareasinpersistentposturalperceptualdizzinessrestingstatefmristudiesbeforeandaftervisualstimulation