Delineating neural responses and functional connectivity changes during vestibular and nociceptive stimulation reveal the uniqueness of cortical vestibular processing

Judita Huber,Virginia Flanagin,Peter Zu Eulenburg,Maxine Ruehl

doi:10.1007/s00429-021-02394-6

Judita Huber, Virginia Flanagin + Show 2 more

Open Access

https://doi.org/10.1007/s00429-021-02394-6

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Abstract

Vestibular information is ubiquitous and often processed jointly with visual, somatosensory and proprioceptive information. Among the cortical brain regions associated with human vestibular processing, area OP2 in the parietal operculum has been proposed as vestibular core region. However, delineating responses uniquely to vestibular stimulation in this region using neuroimaging is challenging for several reasons: First, the parietal operculum is a cytoarchitectonically heterogeneous region responding to multisensory stimulation. Second, artificial vestibular stimulation evokes confounding somatosensory and nociceptive responses blurring responses contributing to vestibular perception. Furthermore, immediate effects of vestibular stimulation on the organization of functional networks have not been investigated in detail yet. Using high resolution neuroimaging in a task-based and functional connectivity approach, we compared two equally salient stimuli—unilateral galvanic vestibular (GVS) and galvanic nociceptive stimulation (GNS)—to disentangle the processing of both modalities in the parietal operculum and characterize their effects on functional network architecture. GNS and GVS gave joint responses in area OP1, 3, 4, and the anterior and middle insula, but not in area OP2. GVS gave stronger responses in the parietal operculum just adjacent to OP3 and OP4, whereas GNS evoked stronger responses in area OP1, 3 and 4. Our results underline the importance of considering this common pathway when interpreting vestibular neuroimaging experiments and underpin the role of area OP2 in central vestibular processing. Global network changes were found during GNS, but not during GVS. This lack of network reconfiguration despite the saliency of GVS may reflect the continuous processing of vestibular information in the awake human.

Highlights

The vestibular system monitors active and passive head movements in all translational and rotational directions while at the same time sensing gravity
Signal increases were found in area cingulate sulcus visual (CSv) bilaterally, and in the cerebellum including the dorsal oculomotor vermis, lobule VIIIb, IX and X of the vermis and right Crus II
No session effect was found when comparing the two resting-state datasets from the two experiments (U = 5608, p = 0.828). These results suggest that cortical nodes become more selective in their interaction during nociceptive stimulation, whilst no reorganisation occurs during vestibular stimulation

Summary

Introduction

The vestibular system monitors active and passive head movements in all translational and rotational directions while at the same time sensing gravity. Brain Structure and Function localization of a vestibular network in humans. Vestibular information is transmitted from the periphery to the cortex via posterior thalamic vestibular nuclei to the somatosensory cortex and to the parietoinsular vestibular cortex (PIVC) located in the lateral sulcus adjacent to the insula. In this area, primate studies localized the primary vestibular cortex taking into account the large amount of neurons responding to vestibular input (Guldin and Grüsser 1998) even in the absence of visual input in darkness (Chen et al 2010)

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Discussion

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