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Handedness‐dependent functional organizational patterns within the bilateral vestibular cortical network revealed by fMRI connectivity based parcellation

V. Kirsch,R. Boegle,D. Keeser,E. Kierig,B. Ertl-Wagner,T. Brandt,M. Dieterich

Published 2018 in NeuroImage

ABSTRACT

Abstract Current evidence points towards a vestibular cortex that involves a multisensory bilateral temporo‐parietal‐insular network with a handedness‐dependent hemispheric lateralization. This study aimed to identify handedness‐dependent organizational patterns of (lateralized and non‐lateralized) functional subunits within the human vestibular cortex areas. 60 healthy volunteers (30 left‐handed and 30 right‐handed) were examined on a 3T MR scanner using resting state functional MRI (fMRI). The data was analyzed in four major steps using a functional connectivity based parcellation (fCBP) approach: (1) independent component analysis (ICA) on a whole brain level to identify different resting state networks (RSN); (2) creation of a vestibular informed mask from four whole brain ICs that included reference coordinates of the vestibular network extracted from meta‐analyses of vestibular neuroimaging experiments; (3) Re‐ICA confined to the vestibular informed mask; (4) cross‐correlation of the activated voxels within the vestibular subunits (parcels) to each other (P‐to‐P) and to the whole‐brain RSN (P‐to‐RSN). This approach disclosed handedness‐dependency, inter‐hemispheric symmetry, the scale of connectedness to major whole brain RSN and the grade of spatial overlap of voxels within parcels (common/unique) as meaningful discriminatory organizational categories within the vestibular cortex areas. This network consists of multiple inter‐hemisphere symmetric (not lateralized), well‐connected (many RSN‐assignments) multisensory areas (or hubs; e.g., superior temporal gyrus, temporo‐parietal intersection) organized around an asymmetric (lateralized, “dominant”) and functionally more specialized (few RSN‐assignments) core region in the parieto‐insular cortex. The latter is in the middle, posterior and inferior insula. In conclusion, the bilateral cortical vestibular network contains not only a handedness‐dependent lateralized central region concentrated in the right hemisphere in right‐handers and left hemisphere in left‐handers, but also surrounding inter‐hemisphere symmetric multisensory vestibular areas that seem to be functionally influenced by their neighboring sensory systems (e.g., temporo‐parietal intersection by the visual system). One may speculate that the development of an asymmetrical organized vestibular subsystem reflects a more recent phylogenetic evolution of various multisensory vestibular functions. The right hemispheric dominance of spatial orientation and its disorders, spatial neglect and pusher syndrome, may serve as examples. HighlightsNon‐binary masked ICA addresses the non‐binary (multisensory) nature of the vestibular cortical network.Handedness‐dependent multiple symmetric integrative hub areas surround an asymmetric (lateralized, dominant) multisensory core region.The inferior insula is a target station for incoming lateralized vestibular information.Lateralized hemispheric function such as higher cortical vestibular functions might reflect most recent evolutionary developments.

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