The “vestibular neuromatrix”: A proposed, expanded vestibular network from graph theory in post‐concussive vestibular dysfunction

Abstract

Convergent clinical and neuroimaging evidence suggests that higher vestibular function is subserved by a distributed network including visuospatial, cognitive–affective, proprioceptive, and integrative brain regions. Clinical vestibular syndromes may perturb this network, resulting in deficits across a variety of functional domains. Here, we leverage structural and functional neuroimaging to characterize this extended network in healthy control participants and patients with post‐concussive vestibular dysfunction (PCVD). Then, 27 healthy control subjects (15 females) and 18 patients with subacute PCVD (12 female) were selected for participation. Eighty‐two regions of interest (network nodes) were identified based on previous publications, group‐wise differences in BOLD signal amplitude and connectivity, and multivariate pattern analysis on affective tests. Group‐specific “core” networks, as well as a “consensus” network comprised of connections common to all participants, were then generated based on probabilistic tractography and functional connectivity between the 82 nodes and subjected to analyses of node centrality and community structure. Whereas the consensus network was comprised of affective, integrative, and vestibular nodes, PCVD participants exhibited diminished integration and centrality among vestibular and affective nodes and increased centrality of visual, supplementary motor, and frontal and cingulate eye field nodes. Clinical outcomes, derived from dynamic posturography, were associated with approximately 62% of all connections but best predicted by amygdalar, prefrontal, and cingulate connectivity. No group‐wise differences in diffusion metrics or tractography were noted. These findings indicate that cognitive, affective, and proprioceptive substrates contribute to vestibular processing and performance and highlight the need to consider these domains during clinical diagnosis and treatment planning.

Vestibular dysfunction is an important contributor to the aging of visuospatial ability in older adults–Data from a computerized test system

“…Numerous neuroimaging studies have further established the physiological basis for the connection between the vestibular system and cognition ( 3 , 18 ). A wider vestibular network in the brain has been identified.…”

Visuo‐vestibular and cognitive connections of the vestibular neuromatrix are conserved across age and injury populations

“…Preprocessing of rsfMRI data was completed similarly for both Site A and Site B. Data were preprocessed in the CONN Toolbox, version 19c, 43 as described in detail elsewhere 34 . Briefly, this preprocessing workflow consisted of a standard volume‐based preprocessing routine that includes SPM and aCompCor noise source removal, 44 registration of anatomical and rsfMRI data to the Montreal Neurological Institute (MNI) 152 standard space, and ordinary least‐squares regression of motion parameters and their first‐order derivatives, ART‐defined framewise outliers (i.e., censored if change in global signal exceeded 3 standard deviations or if motion was >0.5 mm), and mean signal from cerebrospinal fluid and white matter.…”

“…Eighty‐two ROI masks, defined as 8‐mm‐diameter spheres in MNI152 space, were provided by Site A and applied to both Site A and Site B data using the CONN Toolbox. As defined in Smith et al., 34 the ROIs were selected from previous publications (25 ROIs), groupwise differences between HC and ST participants (22 ROIs), and associations with depression, anxiety, or emotional regulation in HC and ST participants (35 ROIs). For the purposes of interpreting the results of the network analyses, these ROIs were divided into “vestibular/visual‐integrative” and “nonvestibular” (e.g., cognitive, affective) ROIs.…”

“…For the purposes of interpreting the results of the network analyses, these ROIs were divided into “vestibular/visual‐integrative” and “nonvestibular” (e.g., cognitive, affective) ROIs. Thus, the “vestibular/visual‐integrative” ROIs included right‐hemisphere parietoinsular vestibular cortex (PIVC/OP2) as well as left‐ and right‐hemisphere frontal eye fields, visual area V5/MT (subserving interoception and visual integration), posterior hippocampus (spatial orientation), putative multisensory orientation area and visual‐vestibular convergence zone (VVMCZ; composed of left middle frontal and right inferior frontal gyri), precuneus, supplementary eye fields, and inferior parietal sulcus (IPS) (subserving smooth pursuits and saccades) 34 …”

“…Thus, the overall goal of this study was to evaluate the generalizability of the previously identified vestibular neuromatrix in adults with and without PCVD to young athletes with and without SRC. To accomplish this, we sought to identify commonalities in the vestibular neuromatrix among two cohorts: (a) adult patients with PCVD and matched controls (previously published cross‐sectional data 34 ) and (b) young athletes aged 14‐17 (prospective longitudinal data consisting of preseason, postconcussion, and postseason time points).…”