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

Neuroimage. 2018 Sep:178:224-237. doi: 10.1016/j.neuroimage.2018.05.018. Epub 2018 May 19.

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.

Keywords: Asymmetry; Functional parcellation; Hemisphere dominance; Lateralization; Multisensory; Vestibular cortical network.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Brain / diagnostic imaging
  • Brain / physiology*
  • Brain Mapping / methods*
  • Cerebral Cortex / diagnostic imaging
  • Cerebral Cortex / physiology*
  • Female
  • Functional Laterality / physiology*
  • Humans
  • Magnetic Resonance Imaging / methods*
  • Male
  • Middle Aged
  • Nerve Net / diagnostic imaging
  • Nerve Net / physiology*
  • Orientation, Spatial / physiology
  • Postural Balance / physiology
  • Proprioception / physiology
  • Reflex, Vestibulo-Ocular / physiology
  • Vestibule, Labyrinth / physiology*
  • Young Adult