Altered Processing of Complex Visual Stimuli in Patients with Postconcussive Visual Motion Sensitivity

Abstract

BACKGROUND AND PURPOSE: Vestibular symptoms are common after concussion. Vestibular Ocular Motor Screening identifies vestibular impairment, including postconcussive visual motion sensitivity, though the underlying functional brain alterations are not defined. We hypothesized that alterations in multisensory processing are responsible for postconcussive visual motion sensitivity, are detectable on fMRI, and correlate with symptom severity. MATERIALS AND METHODS:Twelve patients with subacute postconcussive visual motion sensitivity and 10 healthy control subjects underwent vestibular testing and a novel fMRI visual-vestibular paradigm including 30-second "neutral" or "provocative" videos. The presence of symptoms/intensity was rated immediately after each video. fMRI group-level analysis was performed for a "provocative-neutral" condition. Z-statistic images were nonparametrically thresholded using clusters determined by Z . 2.3 and a corrected cluster significance threshold of P ¼ .05. Symptoms assessed on Vestibular Ocular Motor Screening were correlated with fMRI mean parameter estimates using Pearson correlation coefficients.RESULTS: Subjects with postconcussive visual motion sensitivity had significantly more Vestibular Ocular Motor Screening abnormalities and increased symptoms while viewing provocative videos. While robust mean activation in the primary and secondary visual areas, the parietal lobe, parietoinsular vestibular cortex, and cingulate gyrus was seen in both groups, selective increased activation was seen in subjects with postconcussive visual motion sensitivity in the primary vestibular/adjacent cortex and inferior frontal gyrus, which are putative multisensory visual-vestibular processing centers. Moderate-to-strong correlations were found between Vestibular Ocular Motor Screening scores and fMRI activation in the left frontal eye field, left middle temporal visual area, and right posterior hippocampus.CONCLUSIONS: Increased fMRI brain activation in visual-vestibular multisensory processing regions is selectively seen in patients with postconcussive visual motion sensitivity and is correlated with Vestibular Ocular Motor Screening symptom severity, suggesting that increased visual input weighting into the vestibular network may underlie postconcussive visual motion sensitivity.

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.…”

“…An association between vestibular provocation and insular recruitment in controls, but not in PPPD participants, was reported in the same study (Riccelli et al, 2017). 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

“…Altered vestibular function has been hypothesized to cause postconcussive visual motion sensitivity. Allen et al found that post-concussion patients with subacute vestibular impairment symptoms showed exaggerated activation in the multisensory processing centers involved in visual-vestibular sensory processing [119]. They hypothesize that these patients developed overreliance on visual stimuli to compensate for vestibular impairment and that this may lead to difficulty in recovering after TBI.…”

Multisensory integration and white matter pathology: Contributions to cognitive dysfunction

“…Moreover, multimodal sensory management requirements incur a greater processing demand for persons with prior mTBI ( 110 – 112 ). Compromised multimodal sensory management of visual-vestibular stimuli is commonly found in persons with mTBI ( 110 – 113 ). The added processing challenges of multimodal signals often leads to impaired cognition well past the onset of mTBI.…”