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THE IMPACT OF CONCUSSION HISTORY ON THE NEAR REFLEX AND PUPILLARY LIGHT REFLEX IN VIRTUAL REALITY
Marchetto, Jonathan Dior
Marchetto, Jonathan Dior
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2024-08
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http://dx.doi.org/10.34944/dspace/10876
Abstract
Background: Mild traumatic brain injury (mTBI) is a major public health concern, with over 1 million concussions estimated to occur each year in the United States alone. TBI impacts a diverse array of brain regions, producing a wide range of cognitive, physical, and psychological symptoms. Notably, there is currently no agreed-upon gold-standard concussion assessment, as the type, severity, and duration of impairments can vary widely between patients. To establish a valid and reliable biomarker for concussions, oculomotor behavior has gained increased attention as a promising avenue for detecting post-injury deficits caused by mTBI. Importantly, numerous oculomotor functions, including convergence, accommodation, and pupillary response, are commonly found to be impacted by mTBI. Deficits in oculomotor responses produce significant impairments to a patient’s quality of life, such as difficulties reading, challenges driving, motion sickness, and sensitivity to light. These deficits also suggest that the near reflex triad, the joint response consisting of convergence, accommodation, and pupillary constriction associated with near vision, as well as the pupillary light reflex (PLR), hold promise as sensitive biomarkers. However, there has yet to be a comprehensive assessment of these reflexes in patients with a history of concussions.
Aims: Our primary aim was to determine whether differences in the near response and the PLR could be detected between healthy young adults (HCG) and patients with a history of concussions (CHX). It was hypothesized that the CHX group’s responses would be reduced, slowed, or delayed, across ocular metrics. Further, we aimed to establish the ability of our novel virtual reality (VR) assessments to elicit stimulus-specific changes in oculomotor behavior by determining whether responses were altered by manipulations in visual stimuli across test conditions. We hypothesized that differences would be found across PLR, vergence, and accommodation tests as a function of manipulations in the VR scene similar to the stimulus-dependent changes in oculomotor response found across commonly used clinical tests.
Methods: Forty-five young adults (29 females, 16 males; Age M = 26.18, SD 4.18 years [18-35 years]) were recruited to either a Concussion History Group, which included participants with a history of one or more diagnosed concussions (CHX; n = 24), or a Healthy Control Group (HCG; n = 21). Participants performed a novel suite of oculomotor assessments in an SensoMotoric Instruments (SMI) HTC Vive with built-in video oculography (VOG) eye-tracking, which recorded eye movements and pupillometry at 89.6 Hz while simultaneously presenting an immersive VR environment. Tests were divided into three primary categories, (1) PLR tests (VR_PLR) – participants fixated on a target while the intensity (dim vs bright) and duration (pulse vs step) of a light stimulus was manipulated in the visual scene, (2) Vergence tests (VR_VA) – participants performed four tasks which primarily assessed convergence (VR_NPC), divergence (Divergence Fusion), Vergence Tracking, and Vergence Holding, by manipulating the movement of a virtual target in depth during binocular viewing, (3) Accommodation tests (VR_AT) – participants viewed two targets (near vs far, 35 cm apart) with a blur filter randomly applied to either stimulus and were tasked with judging which had greater clarity across progressively more difficult trials in binocular and monocular assessments. Standard clinical oculomotor data outside of a VR environment was also collected using an accommodative slide ruler to establish near-point of convergence (NPC) scores and a Snellen chart to assess visual acuity.
Statistical Analysis: For the PLR tests, a mixed repeated measures ANOVA of four conditions (2 intensity x 2 duration) and two participant groups (CHX vs HCG) was used to analyze eleven standard pupillary response variables (minimum diameter, maximum diameter, baseline diameter, final diameter, amplitude, peak and average constriction velocity, peak and average dilation velocity, and latency). For the vergence tests, independent samples t-tests were used for the VR_NPC and Divergence Fusion tests to compare interpupillary distance (IPD) metrics between CHX and HCG (minimum IPD, maximum IPD, IPD amplitude, correlations between IPD and target position, subjective breakpoint, and target fusion position). Repeated measures ANOVAs were used for the Convergence Tracking and Holding tasks to further assess whether IPD metrics were altered through changes across target cycles or steps. For the accommodation tasks, repeated measures ANOVAs were also used to assess differences in response metrics (reaction time, accuracy, target distance, target blur) between groups and across binocular and monocular conditions. Additional repeated measures ANOVAs were conducted by subdividing the HCG based on the number of concussions to determine whether there was an additive effect of multiple concussions, single, or no concussions. Follow-up pairwise comparisons with Bonferroni adjusted alpha levels to account for multiple comparisons were conducted if significant main effects were found across experiments. Regression analyses were conducted using time since injury as a factor to determine whether recovery time impacted PLR and near response metrics.
Results: No differences were seen between the CHX and HCG groups across clinical visual and oculomotor tests. Limited significant differences in oculomotor metrics were found between the CHX and HCG groups, but they were inconsistent across tests. Similarly, follow-up analysis was unable to detect consistent differences based on time since injury or the number of concussions. Across assessments, significant differences within testing conditions were consistently found for VR_PLR, VR_VA, and VR_AT.
Conclusion: Our results demonstrated that VR technology is capable of eliciting and measuring the near reflex triad through manipulations in the virtual environment producing changes in VOG metrics that are stimulus-dependent. Our assessments produced expected response patterns which were similar to clinical tests (e.g., a brighter light produced greater pupil constriction). Limited significant differences as a result of a history of concussions conflict with past research but are likely attributed to notable heterogeneity in our patient population’s time since injury. Notably, the auditory pupil response, divergence fusion, and monocular accommodation tests appeared to be the most sensitive to potential deficits as a result of chronic mTBI. Our findings suggest that VR technology is capability of clinical oculomotor testing, but more research is needed to understand the utility of these tests among mTBI patients.
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