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
N1 - Publisher Copyright:
© 2015 Indovina, Riccelli, Chiarella, Petrolo, Augimeri, Giofrè, Lacquaniti, Staaband Passamonti.
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 - CSD
KW - Chronic subjective dizziness
KW - FMRI
KW - Hippocampus
KW - Insula
KW - STBs
KW - Sound-evoked vestibular stimulation
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
AN - SCOPUS:84957602220
SN - 1662-5153
VL - 9
JO - Frontiers in Behavioral Neuroscience
JF - Frontiers in Behavioral Neuroscience
IS - DEC
M1 - 334
ER -