Dominance for Vestibular Cortical Function in the Non-dominant Hemisphere

Abstract

The aim of this (15)O-labelled H(2)O bolus positron emission tomography (PET) study was to analyse the hemispheric dominance of the vestibular cortical system. Therefore, the differential effects of caloric vestibular stimulation (right or left ear irrigation with warm water at 44 degrees C) on cortical and subcortical activation were studied in 12 right-handed and 12 left-handed healthy volunteers. Caloric irrigation induces a direction-specific sensation of rotation and nystagmus. Significant regional cerebral blood flow increases were found in a network within both hemispheres, including the superior frontal gyrus/sulcus, the precentral gyrus and the inferior parietal lobule with the supramarginal gyrus. These areas correspond best to the cortical ocular motor centres, namely the prefrontal cortex, the frontal eye field and the parietal eye field, known to be involved in the processing of caloric nystagmus. Furthermore, distinct temporo-parietal activations could be separated in the posterior part of the insula with the adjacent superior temporal gyrus, the inferior parietal lobule and precuneus. These areas fit best to the human homologues of multisensory vestibular cortex areas identified in the monkey and correspond to the parieto-insular vestibular cortex (PIVC), the visual temporal sylvian area (VTS) and areas 7 and 6. Further cortical activations were seen in the anterior insula, the inferior frontal gyrus and anterior cingulum. The subcortical activation pattern in the putamen, thalamus and midbrain is consistent with the organization of efferent ocular motor pathways. Cortical and subcortical activation of the described areas was bilateral during monaural stimulation, but predominant in the hemisphere ipsilateral to the stimulated ear and exhibited a significant right hemispheric dominance for vestibular and ocular motor structures in right-handed volunteers. Similarly, a significant left hemispheric dominance was found in the 12 left-handed volunteers. Thus, this PET study showed for the first time that cortical and subcortical activation by vestibular caloric stimulation depends (i) on the handedness of the subjects and (ii) on the side of the stimulated ear. Maximum activation was therefore found when the non-dominant hemisphere was ipsilateral to the stimulated ear, i.e. in the right hemisphere of right-handed subjects during caloric irrigation of the right ear and in the left hemisphere of left-handed subjects during caloric irrigation of the left ear. The localization of handedness and vestibular dominance in opposite hemispheres might conceivably indicate that the vestibular system and its hemispheric dominance, which matures earlier during ontogenesis, determine right- or left-handedness.

A brief review of the clinical anatomy of the vestibular-ocular connections—how much do we know?

“…[14][15][16][17] These data have implicated a widespread distributed network in the frontal and tempo-parietal areas that strongly overlaps with the neural networks found for spatial attention, 18 with a right hemisphere dominance. 19,20 Behavioural observations in patients with posterior parietal cortical lesions provide further support for the suggested overlapping neural networks. Posterior parietal cortical lesions (particularly on the right) typically result in spatial neglect, a disorder of spatial attention.…”

Body ownership and embodiment: Vestibular and multisensory mechanisms

“…Congruently, epileptic patients with vestibular aurae suffer from lesions surrounding the superior temporal gyrus and the temporoparietal cortex [99,107]. This location has also been confirmed by functional neuroimaging studies in healthy subjects using caloric and galvanic stimulation of the peripheral vestibular system revealing unanimously predominant activations centered on the TPJ and insula [6,19,20,32,39,46,47,50,51,70,72,85,94,95,110,112,118] with activations in the superior temporal gyrus, posterior insula, inferior parietal lobule (angular and supramarginal gyri), and postcentral gyrus. Although many regions surrounding the TPJ/insula have been found activated, opinions concerning the exact location of the human homologue of the PIVC differ (Fig.…”

“…In healthy subjects, sense of body ownership and self-attribution of actions are also more specifically related to right posterior insula activity [49,115]. Also, there is an overall right hemispheric dominance for the vestibular cortex [39,46,50,51,112], and the integration of vestibular and proprioceptive cues seems to involve particularly the right TPJ (see Bottini et al [19]). In the case of autoscopic hallucinations, lesion sites are mostly located in right parieto-occipital and temporo-occipital cortex with less involvement of the TPJ [13,15].…”

“…Yen Pik Sang et al [120] reported that caloric vestibular stimulations in healthy subjects may induce transient symptoms of depersonalization and derealisation (''body feels strange/different in some ways'', ''feeling of detachment or separation from surroundings'') by a disintegration in personal space and/or disintegration between personal and extrapersonal space. In a PET study on depersonalization, Simeon et al [106] found brain activation changes related to embodiment in regions that have also been shown to be activated by caloric vestibular stimulation, such as the superior temporal gyrus, posterior insula and inferior parietal lobule [19,20,39,47,50,112]. Collectively, these findings suggest that caloric vestibular stimulation interferes with self-processing and embodiment, also inducing symptoms of depersonalization, which share several aspects with out-ofbody experiences [105].…”

Cerebral plasticity in acute vestibular deficit

“…There is vestibular dominance in the non-dominant hemisphere and stronger activation occurs in the hemisphere ipsilateral to the stimulated ear [23]. A subsequent human PET study on right-handed patients aVected by right-sided vestibular neuritis showed an activation of the primary vestibular cortex (parieto-insular vestibular cortex-PIVC) on the left side, contralateral to the aVected side, and a deactivation of the supposed "secondary" multisensory vestibular cortex areas on the right side, ipsilateral to the aVected ear [12].…”