Alterations in Resting‐State Functional Brain Connectivity and Correlations with Vestibular/Ocular‐Motor Screening Measures in Postconcussion Vestibular Dysfunction

Abstract

BACKGROUND AND PURPOSE: Vestibular symptoms after concussion are common and associated with protracted recovery. The purpose of this study is to define resting-state functional MRI (rs-fMRI) brain connectivity alterations in patients with postconcussion vestibular dysfunction (PCVD) and correlations between rs-fMRI connectivity and symptoms provoked during Vestibular/Ocular-Motor Screening (VOMS) assessment. METHODS: Prospective IRB approved study. Study group: 12 subjects with subacute PCVD (2-10 weeks); control group: 10 agematched subjects without history of concussion or vestibular impairment. Both groups underwent clinical vestibular assessment. rs-fMRI was acquired on 3.0T Siemens Trio with a 12-channel head coil. rs-fMRI data analysis included independent component analysis-based functional connectivity group differences, graph theory analysis, and ROI-to-ROI connectivity correlation analysis with VOMS clinical derivatives. Group difference maps between resting-state networks were calculated using dual regression method and corrected for multiple comparisons. Correlation analysis between ROI-to-ROI rs-fMRI brain activation and VOMS assessment ratings was performed using Pearson correlation coefficient, with a significance threshold of P ≤ .05. RESULTS: Compared to controls, PCVD group demonstrated significantly increased rs-fMRI connectivity between the defaultmode network and right middle frontal gyrus and right postcentral gyrus; and between a vestibular-sensorimotor network and right prefrontal cortex. Significant positive correlations were found between clinical derivative VOMS scores and components of the vestibular, visual networks, and multisensory processing cortical representations. CONCLUSION: Altered rs-fMRI brain connectivity with increased connectivity of visual input, multisensory processing, and spatial memory in PCVD is correlative with clinical derivative VOMS scores, suggesting maladaptive brain plasticity underlying vestibular symptomatology.

Rethinking recovery in adolescent concussions: Network‐level functional connectivity alterations associated with motor deficits

“…Consistent with literature showing global hyper-connectivity patterns between brain networks (Churchill et al, 2017(Churchill et al, , 2019Manning, 2017) as well as previous findings specific to the motor network post-concussion (Schmidt et al, 2018;Trofimova et al, 2021), adolescents clinically recovered from concussion showed increased functional DMN-left lateral premotor cortex connectivity compared to controls. Regardless of the covariates included, there were cluster-level group differences in connectivity between DMN and right and left lateral premotor regions, suggesting that this is an important region bilaterally.…”

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

“…There is considerable interest and ongoing effort to characterize the cortical network subserving vestibular function and recent clinical and neuroimaging studies evince complex interactions between central vestibular substrates and cognitive, oculomotor, and emotional/affective domains (Indovina et al, 2020; Raiser et al, 2020). Brain regions involved in visuospatial, affective, and integrative functions also subserve vestibular processing, modulate oculomotor gain and visual attention, and may contribute to dysfunction in a subset of syndromes including PPPD and PCVD (Allen et al, 2021; Passamonti et al, 2018; Riccelli et al, 2017; Trofimova et al, 2021). This study is, to our knowledge, the first to situate these ancillary connections in the larger context of vestibular function and dysfunction.…”

“…Similarly, it was recently reported that control participants and patients with subacute post‐concussive vestibular dysfunction (PCVD) exhibit differential recruitment of the visual, parieto‐insular, parietal, frontal, and cingulate cortices and hippocampus in response to visual‐vestibular provocation, and noted that activity in the frontal eye field, posterior hippocampus, and middle temporal visual area (hMST/V5) was associated with Vestibular Ocular Motor Screening (VOMS: Mucha et al, 2014) scores across all control and PCVD participants (Allen et al, 2021). Subjects with higher resting‐state connectivity between the posterior hippocampus and ipsilateral V5, and among the left and right‐hemisphere MSO, PIVC, and right anterior insula, have also been shown to exhibit increased symptoms during VOMS testing (Trofimova et al, 2021). These results not only implicate visuospatial and integrative areas in vestibular function and dysfunction, but also suggest that, in some cases, dysfunction may arise from an overreliance on visual cues.…”

“…PCVD patients in particular appear to demonstrate greater recruitment of visual and visuospatial areas when provoked with visual stimuli containing high optic flow (Allen et al, 2021). They also exhibit richer, visuospatially directed networks, with “hubs” in the posterior hippocampus and anterior insula, and a greater number of intervening connections (longer path lengths) between the early visual areas V1/V2 and the posterior hippocampus (Trofimova et al, 2021).…”

Mild-to-Moderate Traumatic Brain Injury: A Review with Focus on the Visual System

“…Parietal regions are involved in processing vestibular information for the perception of self-motion [111]. In cases of post-concussion or mTBI vestibular dysfunction, vestibular impairment causes a myriad of symptoms related to imbalance and disorientation, which often manifests as dizziness/vertigo and/or lightheadedness and may be accompanied by nausea as well [112,113]. For non-hospitalized TBI patients, vestibular function testing detects abnormalities in somewhere between about 30 to 60% of those tested and symptoms may continue for in excess of one year in 10 to 15% of patients with a mild concussion [10,[114][115][116][117].…”