Role of the insula and vestibular system in patients with chronic subjective dizziness

An fMRI study using sound-evoked vestibular stimulation

Iole Indovina, Roberta Riccelli, Giuseppe Chiarella, Claudio Petrolo, Antonio Augimeri, Laura Giofrè, Francesco Lacquaniti, Jeffrey P Staab, Luca Passamonti

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

Chronic subjective dizziness (CSD) is a common vestibular disorder characterized by persistent non-vertiginous dizziness, unsteadiness, and heightened sensitivity to motion stimuli that may last for months to years after events that cause acute vestibular symptoms or disrupt balance. CSD is not associated with abnormalities of basic vestibular or oculomotor reflexes. Rather, it is thought to arise from persistent use of high-threat postural control strategies and greater reliance on visual cues for spatial orientation (i.e., visual dependence), long after triggering events resolve. Anxiety-related personality traits confer vulnerability to CSD. Anomalous interactions between the central vestibular system and neural structures related to anxiety may sustain it. Vestibular- and anxiety-related processes overlap in the brain, particularly in the insula and hippocampus. Alterations in activity and connectivity in these brain regions in response to vestibular stimuli may be the neural basis of CSD. We examined this hypothesis by comparing brain activity from 18 patients with CSD and 18 healthy controls measured by functional magnetic resonance imaging during loud short tone bursts, which are auditory stimuli that evoke robust vestibular responses. Relative to controls, patients with CSD showed reduced activations to sound-evoked vestibular stimulation in the parieto-insular vestibular cortex (PIVC) including the posterior insula, and in the anterior insula, inferior frontal gyrus, hippocampus, and anterior cingulate cortex. Patients with CSD also showed altered connectivity between the anterior insula and PIVC, anterior insula and middle occipital cortex, hippocampus and PIVC, and anterior cingulate cortex and PIVC. We conclude that reduced activation in PIVC, hippocampus, anterior insula, inferior frontal gyrus, and anterior cingulate cortex, as well as connectivity changes among these regions, may be linked to long-term vestibular symptoms in patients with CSD. Furthermore, altered connectivity between the anterior insula and middle occipital cortex may underlie the greater reliance on visual cues for spatial orientation in CSD patients relative to controls.

Original languageEnglish (US)
Article number334
JournalFrontiers in Behavioral Neuroscience
Volume9
Issue numberDEC
DOIs
StatePublished - Dec 9 2015

Fingerprint

Dizziness
Magnetic Resonance Imaging
Cerebral Cortex
Gyrus Cinguli
Occipital Lobe
Hippocampus
Anxiety
Prefrontal Cortex
Cues
Brain
Parahippocampal Gyrus
Reflex
Personality

Keywords

  • Chronic subjective dizziness
  • CSD
  • FMRI
  • Hippocampus
  • Insula
  • Sound-evoked vestibular stimulation
  • STBs

ASJC Scopus subject areas

  • Behavioral Neuroscience
  • Cognitive Neuroscience
  • Neuropsychology and Physiological Psychology

Cite this

Role of the insula and vestibular system in patients with chronic subjective dizziness : An fMRI study using sound-evoked vestibular stimulation. / Indovina, Iole; Riccelli, Roberta; Chiarella, Giuseppe; Petrolo, Claudio; Augimeri, Antonio; Giofrè, Laura; Lacquaniti, Francesco; Staab, Jeffrey P; Passamonti, Luca.

In: Frontiers in Behavioral Neuroscience, Vol. 9, No. DEC, 334, 09.12.2015.

Research output: Contribution to journalArticle

Indovina, Iole ; Riccelli, Roberta ; Chiarella, Giuseppe ; Petrolo, Claudio ; Augimeri, Antonio ; Giofrè, Laura ; Lacquaniti, Francesco ; Staab, Jeffrey P ; Passamonti, Luca. / Role of the insula and vestibular system in patients with chronic subjective dizziness : An fMRI study using sound-evoked vestibular stimulation. In: Frontiers in Behavioral Neuroscience. 2015 ; Vol. 9, No. DEC.
@article{cf8acb25f96c4edbac61d50b9d23a553,
title = "Role of the insula and vestibular system in patients with chronic subjective dizziness: An fMRI study using sound-evoked vestibular stimulation",
abstract = "Chronic subjective dizziness (CSD) is a common vestibular disorder characterized by persistent non-vertiginous dizziness, unsteadiness, and heightened sensitivity to motion stimuli that may last for months to years after events that cause acute vestibular symptoms or disrupt balance. CSD is not associated with abnormalities of basic vestibular or oculomotor reflexes. Rather, it is thought to arise from persistent use of high-threat postural control strategies and greater reliance on visual cues for spatial orientation (i.e., visual dependence), long after triggering events resolve. Anxiety-related personality traits confer vulnerability to CSD. Anomalous interactions between the central vestibular system and neural structures related to anxiety may sustain it. Vestibular- and anxiety-related processes overlap in the brain, particularly in the insula and hippocampus. Alterations in activity and connectivity in these brain regions in response to vestibular stimuli may be the neural basis of CSD. We examined this hypothesis by comparing brain activity from 18 patients with CSD and 18 healthy controls measured by functional magnetic resonance imaging during loud short tone bursts, which are auditory stimuli that evoke robust vestibular responses. Relative to controls, patients with CSD showed reduced activations to sound-evoked vestibular stimulation in the parieto-insular vestibular cortex (PIVC) including the posterior insula, and in the anterior insula, inferior frontal gyrus, hippocampus, and anterior cingulate cortex. Patients with CSD also showed altered connectivity between the anterior insula and PIVC, anterior insula and middle occipital cortex, hippocampus and PIVC, and anterior cingulate cortex and PIVC. We conclude that reduced activation in PIVC, hippocampus, anterior insula, inferior frontal gyrus, and anterior cingulate cortex, as well as connectivity changes among these regions, may be linked to long-term vestibular symptoms in patients with CSD. Furthermore, altered connectivity between the anterior insula and middle occipital cortex may underlie the greater reliance on visual cues for spatial orientation in CSD patients relative to controls.",
keywords = "Chronic subjective dizziness, CSD, FMRI, Hippocampus, Insula, Sound-evoked vestibular stimulation, STBs",
author = "Iole Indovina and Roberta Riccelli and Giuseppe Chiarella and Claudio Petrolo and Antonio Augimeri and Laura Giofr{\`e} and Francesco Lacquaniti and Staab, {Jeffrey P} and Luca Passamonti",
year = "2015",
month = "12",
day = "9",
doi = "10.3389/fnbeh.2015.00334",
language = "English (US)",
volume = "9",
journal = "Frontiers in Behavioral Neuroscience",
issn = "1662-5153",
publisher = "Frontiers Research Foundation",
number = "DEC",

}

TY - JOUR

T1 - Role of the insula and vestibular system in patients with chronic subjective dizziness

T2 - An fMRI study using sound-evoked vestibular stimulation

AU - Indovina, Iole

AU - Riccelli, Roberta

AU - Chiarella, Giuseppe

AU - Petrolo, Claudio

AU - Augimeri, Antonio

AU - Giofrè, Laura

AU - Lacquaniti, Francesco

AU - Staab, Jeffrey P

AU - Passamonti, Luca

PY - 2015/12/9

Y1 - 2015/12/9

N2 - Chronic subjective dizziness (CSD) is a common vestibular disorder characterized by persistent non-vertiginous dizziness, unsteadiness, and heightened sensitivity to motion stimuli that may last for months to years after events that cause acute vestibular symptoms or disrupt balance. CSD is not associated with abnormalities of basic vestibular or oculomotor reflexes. Rather, it is thought to arise from persistent use of high-threat postural control strategies and greater reliance on visual cues for spatial orientation (i.e., visual dependence), long after triggering events resolve. Anxiety-related personality traits confer vulnerability to CSD. Anomalous interactions between the central vestibular system and neural structures related to anxiety may sustain it. Vestibular- and anxiety-related processes overlap in the brain, particularly in the insula and hippocampus. Alterations in activity and connectivity in these brain regions in response to vestibular stimuli may be the neural basis of CSD. We examined this hypothesis by comparing brain activity from 18 patients with CSD and 18 healthy controls measured by functional magnetic resonance imaging during loud short tone bursts, which are auditory stimuli that evoke robust vestibular responses. Relative to controls, patients with CSD showed reduced activations to sound-evoked vestibular stimulation in the parieto-insular vestibular cortex (PIVC) including the posterior insula, and in the anterior insula, inferior frontal gyrus, hippocampus, and anterior cingulate cortex. Patients with CSD also showed altered connectivity between the anterior insula and PIVC, anterior insula and middle occipital cortex, hippocampus and PIVC, and anterior cingulate cortex and PIVC. We conclude that reduced activation in PIVC, hippocampus, anterior insula, inferior frontal gyrus, and anterior cingulate cortex, as well as connectivity changes among these regions, may be linked to long-term vestibular symptoms in patients with CSD. Furthermore, altered connectivity between the anterior insula and middle occipital cortex may underlie the greater reliance on visual cues for spatial orientation in CSD patients relative to controls.

AB - Chronic subjective dizziness (CSD) is a common vestibular disorder characterized by persistent non-vertiginous dizziness, unsteadiness, and heightened sensitivity to motion stimuli that may last for months to years after events that cause acute vestibular symptoms or disrupt balance. CSD is not associated with abnormalities of basic vestibular or oculomotor reflexes. Rather, it is thought to arise from persistent use of high-threat postural control strategies and greater reliance on visual cues for spatial orientation (i.e., visual dependence), long after triggering events resolve. Anxiety-related personality traits confer vulnerability to CSD. Anomalous interactions between the central vestibular system and neural structures related to anxiety may sustain it. Vestibular- and anxiety-related processes overlap in the brain, particularly in the insula and hippocampus. Alterations in activity and connectivity in these brain regions in response to vestibular stimuli may be the neural basis of CSD. We examined this hypothesis by comparing brain activity from 18 patients with CSD and 18 healthy controls measured by functional magnetic resonance imaging during loud short tone bursts, which are auditory stimuli that evoke robust vestibular responses. Relative to controls, patients with CSD showed reduced activations to sound-evoked vestibular stimulation in the parieto-insular vestibular cortex (PIVC) including the posterior insula, and in the anterior insula, inferior frontal gyrus, hippocampus, and anterior cingulate cortex. Patients with CSD also showed altered connectivity between the anterior insula and PIVC, anterior insula and middle occipital cortex, hippocampus and PIVC, and anterior cingulate cortex and PIVC. We conclude that reduced activation in PIVC, hippocampus, anterior insula, inferior frontal gyrus, and anterior cingulate cortex, as well as connectivity changes among these regions, may be linked to long-term vestibular symptoms in patients with CSD. Furthermore, altered connectivity between the anterior insula and middle occipital cortex may underlie the greater reliance on visual cues for spatial orientation in CSD patients relative to controls.

KW - Chronic subjective dizziness

KW - CSD

KW - FMRI

KW - Hippocampus

KW - Insula

KW - Sound-evoked vestibular stimulation

KW - STBs

UR - http://www.scopus.com/inward/record.url?scp=84957602220&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84957602220&partnerID=8YFLogxK

U2 - 10.3389/fnbeh.2015.00334

DO - 10.3389/fnbeh.2015.00334

M3 - Article

VL - 9

JO - Frontiers in Behavioral Neuroscience

JF - Frontiers in Behavioral Neuroscience

SN - 1662-5153

IS - DEC

M1 - 334

ER -