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

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: CSD; STBs; chronic subjective dizziness; fMRI; hippocampus; insula; sound-evoked vestibular stimulation.

Figures

Figure 1
Figure 1
Brain responses to sound evoked vestibular stimulation for the PIVC localizer group. Statistical parametric maps (p-corr < 0.05, cluster level corrected for multiple comparisons) for the contrast of STB100 vs. STB65 exclusively masked for white noise. PIVC, Parieto-Insular vestibular cortex; ReS, Right ear Stimulation; LeS, Left ear Stimulation. Mean activity profiles (±sem) show the activation is bilateral for ReS and LeS.
Figure 2
Figure 2
Brain responses to sound evoked vestibular stimulation for the whole sample of participants (18 healthy controls and 18 CSD patients). Statistical parametric maps (p-corr < 0.05, cluster level corrected for multiple comparisons) for the contrast of STB100 vs. STB65 exclusively masked for white noise (above threshold t-values in red). Response of the PIVC localizer group is outlined in white for comparison. Response is projected onto flat maps of the left (LH) and right (RH) hemisphere of the human PALS atlas (Caret, Washington University School of Medicine, Department of Anatomy and Neurobiology, http://brainmap.wustl.edu).
Figure 3
Figure 3
Decreased regional brain activity in response to short-tone burst vestibular stimulation in patients with chronic subjective dizziness (CSD) relative to healthy controls (HCs). The regions displayed are those that were consistently found either when including or excluding participants with psychiatric comorbidities (posterior insula, anterior insula/inferior frontal gyrus, and hippocampus). Note also that an additional region (anterior cingulate cortex) was found only when excluding people with psychiatric comorbidities (Table 4). The coordinates (X,Y,Z) are in mm in the Montreal Neurological Institute space. Color bars represent T-statistics. Plots report parameter estimates ± SE in arbitrary units.
Figure 4
Figure 4
A more negative functional connectivity change in response to short-tone burst vestibular stimulation was found in chronic subjective dizziness (CSD) patients relative to healthy controls (HCs) between the left anterior insula/inferior frontal gyrus (IFg) “seed” region and the right superior temporal gyrus (A). Likewise, more negative functional connectivity changes were found for the same comparison (i.e., HCs > CSD patients) between the left anterior insula/IFg and right middle occipital gyrus (B); the left hippocampus and right superior temporal gyrus (C); the left anterior cingulate cortex and right superior temporal gyrus (D). The coordinates (X,Y,Z) are in mm in the Montreal Neurological Institute space. Color bars represent T-statistics. Plots report parameter estimates ± SE in arbitrary units.
Figure 5
Figure 5
Summary of the regional results and connectivity findings. Patients with chronic subjective dizziness (CSD), relative to healthy controls, showed reduced brain responses to vestibular stimulation in the left anterior insula/inferior frontal gyrus, left hippocampus, left anterior cingulate cortex and right posterior insula. The left anterior insula more negative functional connectivity change with the right superior temporal gyrus [which is part of the Parieto-Insular Vestibular cortex (PIVC)], and with the middle occipital gyrus. Finally, the left anterior cingulate cortex and left hippocampus showed more negative functional connectivity changes with the right PIVC (superior temporal gyrus).

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