Functional MRI of Galvanic Vestibular Stimulation

Abstract

The cortical processing of vestibular information is not hierarchically organized as the processing of signals in the visual and auditory modalities. Anatomic and electrophysiological studies in the monkey revealed the existence of multiple interconnected areas in which vestibular signals converge with visual and/or somatosensory inputs. Although recent functional imaging studies using caloric vestibular stimulation (CVS) suggest that vestibular signals in the human cerebral cortex may be similarly distributed, some areas that apparently form essential constituents of the monkey cortical vestibular system have not yet been identified in humans. Galvanic vestibular stimulation (GVS) has been used for almost 200 years for the exploration of the vestibular system. By contrast with CVS, which mediates its effects mainly via the semicircular canals (SCC), GVS has been shown to act equally on SCC and otolith afferents. Because galvanic stimuli can be controlled precisely, GVS is suited ideally for the investigation of the vestibular cortex by means of functional imaging techniques. We studied the brain areas activated by sinusoidal GVS using functional magnetic resonance imaging (fMRI). An adapted set-up including LC filters tuned for resonance at the Larmor frequency protected the volunteers against burns through radio-frequency pickup by the stimulation electrodes. Control experiments ensured that potentially harmful effects or degradation of the functional images did not occur. Six male, right-handed volunteers participated in the study. In all of them, GVS induced clear perceptions of body movement and moderate cutaneous sensations at the electrode sites. Comparison with anatomic data on the primate cortical vestibular system and with imaging studies using somatosensory stimulation indicated that most activation foci could be related to the vestibular component of the stimulus. Activation appeared in the region of the temporo-parietal junction, the central sulcus, and the intraparietal sulcus. These areas may be analogous to areas PIVC, 3aV, and 2v, respectively, which form in the monkey brain, the "inner vestibular circle". Activation also occurred in premotor regions of the frontal lobe. Although undetected in previous imaging-studies using CVS, involvement of these areas could be predicted from anatomic data showing projections from the anterior ventral part of area 6 to the inner vestibular circle and the vestibular nuclei. Using a simple paradigm, we showed that GVS can be implemented safely in the fMRI environment. Manipulating stimulus waveforms and thus the GVS-induced subjective vestibular sensations in future imaging studies may yield further insights into the cortical processing of vestibular signals.

Influence of galvanic vestibular stimulation on egocentric and object-based mental transformations

“…A similar decrease in performance due to vestibular-spatial interaction eVects has been found in other studies that used vestibular stimulation in combination with speciWc cognitive tasks Mars et al 2005). Brain imaging studies suggest that areas in the posterior parietal cortex involved in mental transformation (Kosslyn et al 1998;Zacks et al 1999) are also activated during GVS-induced illusory body motion (Lobel et al 1998;Stephan et al 2005). Therefore, GVS activation of these areas presumably interferes and impairs mental transformation, corroborating Wndings of Mast et al (2006) who showed that caloric vestibular stimulation had a disruptive eVect on mental transformation but not on a cognitive control task not involving spatial imagery.…”

Vestibular stimulation attenuates unrealistic optimism

“…We speculate that anosognosia stems, at least in part (Orfei et al, 2007;Aimola Davies et al, 2009), from damage to a region of the brain that integrates undesirable information, and that vestibular stimulation abolishes anosognosia by restoring or augmenting this specific processing function. Converging evidence from lesion studies of anosognosia (Berti et al, 2005) and from fMRI investigations of unrealistic optimism and vestibular stimulation (Lobel et al, 1998;Fasold et al, 2002) implicates the pars opercularis in right IFG as the region in question. In putting forward this suggestion, we emphasise some limitations of our study.…”

“…Signals from the vestibular nuclei also project via the thalamus to (predominately contralateral) cortical and subcortical structures (Miller & Ngo, 2007). Notably, fMRI investigations have found that the cortical network activated during vestibular stimulation includes the pars opercularis region in the IFG (Lobel et al, 1998;Fasold et al, 2002). Remarkably, a number of studies have found that patients who previously have denied their left-sided hemisyndrome will transiently acknowledge it after left-ear irrigation with cold water (Cappa et al, 1987;Rode et al, 1992;Ramachandran, 1995).…”

Inducing out-of-body experiences

“…These are vestibular processing, multisensory integration as well as the perception of human bodies or body parts. The core region of the human vestibular cortex 25,26 is situated at the temporo-parietal junction including the posterior insula, and brain damage in this area has been associated with vestibular sensations and dysfunctions. 27,28 Several neuropsychological and neuroimaging studies suggest the implication of the temporo-parietal junction and cortical areas along the intraparietal sulcus in combining tactile, proprioceptive and visual information in a coordinated reference frame.…”