The Neural Correlates of Chronic Symptoms of Vertigo Proneness in Humans

Ola Alsalman, Jan Ost, Robby Vanspauwen, Catherine Blaivie, Dirk De Ridder, Sven Vanneste, Zoi Kapoula
2016 PLoS ONE  
Vestibular signals are of significant importance for variable functions including gaze stabilization, spatial perception, navigation, cognition, and bodily self-consciousness. The vestibular network governs functions that might be impaired in patients affected with vestibular dysfunction. It is currently unclear how different brain regions/networks process vestibular information and integrate the information into a unified spatial percept related to somatosensory awareness and whether people
more » ... h recurrent balance complaints have a neural signature as a trait affecting their development of chronic symptoms of vertigo. Pivotal evidence points to a vestibular-related brain network in humans that is widely distributed in nature. By using resting state source localized electroencephalography in non-vertiginous state, electrophysiological changes in activity and functional connectivity of 23 patients with balance complaints where chronic symptoms of vertigo and dizziness are among the most common reported complaints are analyzed and compared to healthy subjects. The analyses showed increased alpha2 activity within the posterior cingulate cortex and the precuneues/cuneus and reduced beta3 and gamma activity within the pregenual and subgenual anterior cingulate cortex for the subjects with balance complaints. These electrophysiological variations were correlated with reported chronic symptoms of vertigo intensity. A region of interest analysis found reduced functional connectivity for gamma activity within the vestibular cortex, precuneus, frontal eye field, intra-parietal sulcus, orbitofrontal cortex, and the dorsal anterior cingulate cortex. In addition, there was a positive correlation between chronic symptoms of vertigo intensity and increased alpha-gamma nesting in the left frontal eye field. When compared to healthy subjects, there is evidence of electrophysiological changes in the brain of patients with balance complaints even outside chronic symptoms of vertigo episodes. This suggests that these patients have a neural signature or trait that makes them prone to developing chronic balance problems. Funding: The authors have no support or funding to report. whether there exists a neural signature of this proneness in their resting state brain activity and connectivity in between their symptoms. Vestibular processing occurs in different brain regions, implying a multimodal impairment of sensory integration that involves multiple regions [13] . All natural vestibular stimuli are multimodal, and multiple sensory inputs converge at all levels of the central vestibular system [14]. The vestibular percept of body position and motion is always relative to the subject's surrounding (i.e. exocentric), whereas the visual and auditory percepts are always relative to the subject within that space (i.e. egocentric) [14]. Furthermore, the vestibular cortical areas are represented in both hemispheres, with an ipsilateral predominance for processing ipsilateral input and clear lateralization: in right handed people the right vestibular cortex is dominant, and the left vestibular cortex is in left handed people [14, 15] . A core vestibular network has been described based on an ALE-meta-analysis, which involves the posterior insula, retroinsular cortex, and parietal operculum. In other words, the superior temporal and inferior parietal cortex are where vestibular afferents converge [16] . The posterior insula and temporo-parietal cortex core area receive input from the thalamus and vestibular stimuli often co-activating the frontal operculum, anterior insula [15, [17] [18] [19] , the intraparietal sulcus, frontal eye fields, hippocampus and parahippocampal area, anterior cingulate gyrus, and precuneus [16, 20, 21 ]. These reports demonstrate the level of uncertainty with regard to the exact anatomical identification of a vestibular network, which is likely widely distributed in nature. In addition, in healthy subjects functional connections exist between the abovementioned vestibular areas. For example, research exists supporting a joint vestibular network between the opercullum, temporo-parietal regions, premotor cortex, and the anterior cingulate cortex, according to a concept from animal literature termed the inner vestibular circle [22] . Moreover, combined structural and functional connectivity mapping using diffusion tensor imaging and functional connectivity magnetic resonance in healthy subjects describes a link between the vestibular nuclei and parieto-insular-vestibular cortex [23] . At present, it is neither clear how different regions in the brain process vestibular information, nor how they integrate this information into a global unified vestibular percept. Most of our current understanding of the human vestibular network has been derived from human lesion studies [24, 25] as well as studies in healthy controls [22, 26, 27] including PET studies comparing healthy controls to a patient population [28], complemented by tracer and electrophysiological studies in animals [29] [30] [31] [32] . Therefore, the aim of this paper is to verify whether there exists a neural signature of proneness to chronic vestibular symptoms characterized by a pattern of vestibular activation and connectivity in the resting brain (i.e. in-between vestibular spells).
doi:10.1371/journal.pone.0152309 pmid:27089185 pmcid:PMC4835222 fatcat:gw7iq6bucvfadhlwjpdq7tjhee