Increased brain responsivity to galvanic vestibular stimulation in bilateral vestibular failure

Abstract

In this event-related functional magnetic resonance imaging (fMRI) study we investigated how the brain of patients with bilateral vestibular failure (BVF) responds to vestibular stimuli. We used imperceptible noisy galvanic vestibular stimulation (GVS) and perceptible bi-mastoidal GVS intensities and related the corresponding brain activity to the evoked motion perception. In contrast to caloric irrigation, GVS stimulates the vestibular organ at its potentially intact afferent nerve site. Motion perception thresholds and cortical responses were compared between 26 BVF patients to 27 age-matched healthy control participants. To identify the specificity of vestibular cortical responses we used a parametric design with different stimulus intensities (noisy imperceptible, low perceptible, high perceptible) allowing region-specific stimulus response functions. In a 2 × 3 flexible factorial design all GVS-related brain activities were contrasted with a sham condition that did not evoke perceived motion. Patients had a higher motion perception threshold and rated the vestibular stimuli higher than the healthy participants. There was a stimulus intensity related and region-specific increase of activity with steep stimulus response functions in parietal operculum (e.g. OP2), insula, superior temporal gyrus, early visual cortices (V3) and cerebellum while activity in the hippocampus and intraparietal sulcus did not correlate with vestibular stimulus intensity. Using whole brain analysis, group comparisons revealed increased brain activity in early visual cortices (V3) and superior temporal gyrus of patients but there was no significant interaction, i.e. stimulus-response function in these regions were still similar in both groups. Brain activity in these regions during (high)GVS increased with higher dizziness-related handicap scores but was not related to the degree of vestibular impairment or disease duration. nGVS did not evoke cortical responses in any group. Our data indicate that perceptible GVS-related cortical responsivity is not diminished but increased in multisensory (visual-vestibular) cortical regions despite bilateral failure of the peripheral vestibular organ. The increased activity in early visual cortices (V3) and superior temporal gyrus of BVF patients has several potential implications: (i) their cortical reciprocal inhibitory visuo-vestibular interaction is dysfunctional, (ii) it may contribute to the visual dependency of BVF patients, and (iii) it needs to be considered when BVF patients receive peripheral vestibular stimulation devices, e.g. vestibular implants or portable GVS devices. Imperceptible nGVS did not elicit cortical brain responses making it unlikely that the reported balance improvement of BVF by nGVS is mediated by cortical mechanisms.

Effects of galvanic vestibular stimulation on resting state brain activity in patients with bilateral vestibulopathy

“…They were recruited from the University Centre for Vertigo and Balance Disorders. The majority of subjects of this group participated in a related study examining the GVS‐evoked brain activity in an event‐related study design (Helmchen et al, ). Each participant provided informed oral and written consent in accordance with the Declaration of Helsinki.…”

“…Accordingly, clinical improvement, once it occurs, most likely comes from central compensatory mechanisms (Lacour, Helmchen, & Vidal, ), that is, by modifying the gain in the somatosensory (Strupp, Arbusow, Dieterich, Sautier, & Brandt, ), the proprioceptive (Cutfield et al, ) or visual system (Ahmad et al, ; Dieterich, Bauermann, Best, Stoeter, & Schlindwein, ; Kalla et al, ). This may be accomplished by changing the excitability in the brain (Ahmad et al, ; Cutfield et al, ; Helmchen, Rother, Spliethoff, & Sprenger, ) and its intra‐ and interhemispheric interactions (Cutfield et al, ), as well as alterations of network properties in the brain, that is, functional connectivity (Gottlich et al, ) and/or regional structural changes (Brandt et al, ; Cutfield et al, ; Gottlich et al, ; Kremmyda et al, ).…”

“…Visual motion coherence threshold is increased in BV and associated with decreased motion processing in the attempt to counteract involuntary oscillopsia during locomotion (Kalla et al, ). Moreover, thresholds of self‐motion perception following vestibular stimulation are also increased in BV (Helmchen et al, ). In PET brain imaging (H 2 O 15 ) during vestibular caloric stimulation the parietoinsular vestibular cortex showed decreased activation (Bense et al, ), that is, visuo‐vestibular interaction was reduced as deactivation of the visual cortex was concomitantly smaller compared to healthy controls.…”

“…This potentially bypasses the further peripheral damage in the sensory vestibular hair cells in BV. Using GVS in BV patients, we recently found pronounced neural activity with steep stimulus–response functions in cortical regions of vestibular processing, nearly indistinguishable from healthy controls, and even stronger activity in early visual cortex and superior temporal gyrus (STG) which was related to the level of dizziness‐related disability (Helmchen et al, ). This pronounced cortical responsivity potentially provides a physiological ground for artificial vestibular stimulation in BV, that is, by vestibular implants (Fornos et al, ; van de Berg et al, ) or portable GVS devices.…”

“…We pursued the following hypotheses concerning the influence of GVS on the disturbed cortical processing and visuo‐vestibular interactions in BV patients (see Figure for schematic illustration): We expected GVS to increase the reduced resting‐state brain activity in vestibular core regions of BV patients via stimulation of vestibular nerve afferents that transmit vestibular signals to the chronically deprived cortical areas engaged in vestibular processing. This change may be related to the severity of vestibular hypofunction. Due to the known abnormal visual–vestibular interaction in BV patients (Helmchen et al, ), the visual cortex is less suppressed by vestibular stimuli and, accordingly, resting state brain activity in the visual cortex should be increased in BV and related to the level of perceived dizziness of BV. After GVS, this increased activity in visual cortex is expected to be decreased since inhibitory visual–vestibular interaction are suspected to be partially resumed.…”