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      Eye Tracking Detects Disconjugate Eye Movements Associated with Structural Traumatic Brain Injury and Concussion

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          Abstract

          Disconjugate eye movements have been associated with traumatic brain injury since ancient times. Ocular motility dysfunction may be present in up to 90% of patients with concussion or blast injury. We developed an algorithm for eye tracking in which the Cartesian coordinates of the right and left pupils are tracked over 200 sec and compared to each other as a subject watches a short film clip moving inside an aperture on a computer screen. We prospectively eye tracked 64 normal healthy noninjured control subjects and compared findings to 75 trauma subjects with either a positive head computed tomography (CT) scan ( n=13), negative head CT ( n=39), or nonhead injury ( n=23) to determine whether eye tracking would reveal the disconjugate gaze associated with both structural brain injury and concussion. Tracking metrics were then correlated to the clinical concussion measure Sport Concussion Assessment Tool 3 (SCAT3) in trauma patients. Five out of five measures of horizontal disconjugacy were increased in positive and negative head CT patients relative to noninjured control subjects. Only one of five vertical disconjugacy measures was significantly increased in brain-injured patients relative to controls. Linear regression analysis of all 75 trauma patients demonstrated that three metrics for horizontal disconjugacy negatively correlated with SCAT3 symptom severity score and positively correlated with total Standardized Assessment of Concussion score. Abnormal eye-tracking metrics improved over time toward baseline in brain-injured subjects observed in follow-up. Eye tracking may help quantify the severity of ocular motility disruption associated with concussion and structural brain injury.

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          Most cited references22

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          Impaired eye movements in post-concussion syndrome indicate suboptimal brain function beyond the influence of depression, malingering or intellectual ability.

          Post-concussion syndrome (PCS) can affect up to 20%-30% of patients with mild closed head injury (mCHI), comprising incomplete recovery and debilitating persistence of post-concussional symptoms. Eye movements relate closely to the functional integrity of the injured brain and eye movement function is impaired post-acutely in mCHI. Here, we examined whether PCS patients continue to show disparities in eye movement function at 3-5 months following mCHI compared with patients with good recovery. We hypothesized that eye movements might provide sensitive and objective functional markers of ongoing cerebral impairment in PCS. We compared 36 PCS participants (adapted World Health Organization guidelines) and 36 individually matched controls (i.e. mCHI patients of similar injury severity but good recovery) on reflexive, anti- and self-paced saccades, memory-guided sequences and smooth pursuit. All completed neuropsychological testing and health status questionnaires. Mean time post-injury was 140 days in the PCS group and 163 days in the control group. The PCS group performed worse on anti-saccades, self-paced saccades, memory-guided sequences and smooth pursuit, suggesting problems in response inhibition, short-term spatial memory, motor-sequence programming, visuospatial processing and visual attention. This poorer oculomotor performance included several measures beyond conscious control, indicating that subcortical functionality in the PCS group was poorer than expected after mCHI. The PCS group had poorer neuropsychological function (memory, complex attention and executive function). Analysis of covariance showed oculomotor differences to be practically unaffected by group disparities in depression and estimated intellectual ability. Compared with neuropsychological tests, eye movements were more likely to be markedly impaired in PCS cases with high symptom load. Poorer eye movement function, and particularly poorer subcortical oculomotor function, correlated more with post-concussive symptom load and problems on activities of daily living whilst poorer neuropsychological function exhibited slightly better correlations with measures of mental health. Our findings that eye movement function in PCS does not follow the normal recovery path of eye movements after mCHI are indicative of ongoing cerebral impairment. Whilst oculomotor and neuropsychological tests partially overlapped in identifying impairment, eye movements showed additional dysfunction in motor/visuospatial areas, response inhibition, visual attention and subcortical function. Poorer subconscious oculomotor function in the PCS group supports the notion that PCS is not merely a psychological entity, but also has a biological substrate. Measurement of oculomotor function may be of value in PCS cases with a high symptom load but an otherwise unremarkable assessment profile. Routine oculomotor testing should be feasible in centres with existing access to this technology.
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            Occurrence of oculomotor dysfunctions in acquired brain injury: a retrospective analysis.

            The purpose of this retrospective study was to determine the frequency of occurrence of oculomotor dysfunctions in a sample of ambulatory outpatients who have acquired brain injury (ABI), either traumatic brain injury (TBI) or cerebrovascular accident (CVA), with associated vision symptoms. Medical records of 220 individuals with either TBI (n = 160) or CVA (n = 60) were reviewed retrospectively. This was determined by a computer-based query spanning the years 2000 through 2003, for the frequency of occurrence of oculomotor dysfunctions including accommodation, version, vergence, strabismus, and cranial nerve (CN) palsy. The majority of individuals with either TBI (90%) or CVA (86.7%) manifested an oculomotor dysfunction. Accommodative and vergence deficits were most common in the TBI subgroup, whereas strabismus and CN palsy were most common in the CVA subgroup. The frequency of occurrence of versional deficits was similar in each diagnostic subgroup. These new findings should alert the clinician to the higher frequency of occurrence of oculomotor dysfunctions in these populations and the associated therapeutic, rehabilitative, and quality-of-life implications.
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              Visual tracking synchronization as a metric for concussion screening.

              Our goal was to determine whether performance variability during predictive visual tracking can provide a screening measure for mild traumatic brain injury (mTBI). Seventeen subjects with chronic postconcussive syndrome and 9 healthy control subjects were included in this study. Eye movements were recorded with video-oculography as the subject visually tracked a target that moved through a circular trajectory. We compared the variability of gaze positional errors relative to the target with the microstructural integrity of white matter tracts as measured by the fractional anisotropy (FA) parameter of diffusion tensor imaging. Gaze error variability was significantly correlated with the mean FA values of the right anterior corona radiata (ACR) and the left superior cerebellar peduncle, tracts that support spatial processing and sustenance of attention, and the genu of the corpus callosum. Because the ACR and the genu are among the most frequently damaged white matter tracts in mTBI, the correlations imply that gaze error variability during visual tracking may provide a useful screening tool for mTBI. Gaze error variability was also significantly correlated with attention and working memory measures in neurocognitive testing; thus, measurement of visual tracking performance is promising as a fast and practical screening tool for mTBI.
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                Author and article information

                Journal
                J Neurotrauma
                J. Neurotrauma
                neu
                Journal of Neurotrauma
                Mary Ann Liebert, Inc. (140 Huguenot Street, 3rd FloorNew Rochelle, NY 10801USA )
                0897-7151
                1557-9042
                15 April 2015
                15 April 2015
                : 32
                : 8
                : 548-556
                Affiliations
                [ 1 ]Steven and Alexandra Cohen Veterans Center for Post-Traumatic Stress and Traumatic Brain Injury at NYU Langone Medical Center, New York University School of Medicine , New York, New York.
                [ 2 ]Department of Neurosurgery, New York Harbor Health Care System , New York, New York.
                [ 3 ]Department of Neurosurgery, New York University School of Medicine , New York, New York.
                [ 4 ]Department of Ophthalmology, New York University School of Medicine , New York, New York.
                [ 5 ]Department of Neurosurgery, Baylor Scott & White Neuroscience Institute , Temple, Texas.
                [ 6 ]Department of Emergency Medicine, New York University School of Medicine , New York, New York.
                [ 7 ]Department of Trauma Surgery, New York University School of Medicine , New York, New York.
                Author notes
                Address correspondence to: Uzma Samadani, MD, PhD, Department of Neurosurgery, New York University School of Medicine 423 East 23rd Street, MC 112, New York, NY 10012, E-mail: uzma.samadani@ 123456nyumc.org
                Article
                10.1089/neu.2014.3687
                10.1089/neu.2014.3687
                4394159
                25582436
                3ceac929-9bb3-4813-9032-e39f2f28775d
                © Uzma Samadani, Robert Ritlop M. Eng, Marleen Reyes, Elena Nehrbass, Meng Li, Elizabeth Lamm, Julia Schneider, David Shimunov, Maria Sava, Radek Kolecki, Paige Burris, Lindsey Altomare, Talha Mehmood, Theodore Smith, Jason H. Huang, Christopher McStay, S. Rob Todd, Meng Qian, Douglas Kondziolka, Stephen Wall, and Paul Huang 2015; Published by Mary Ann Liebert, Inc.

                This Open Access article is distributed under the terms of the Creative Commons License Attribution-Non-Commercial Share Alike ( http://creativecommons.org/licenses/by-nc-sa/4.0/).

                History
                Page count
                Figures: 4, Tables: 7, Equations: 3, References: 23, Pages: 9
                Categories
                Original Articles

                concussion,cranial nerve palsy,disconjugate,eye movement tracking,ocular motility

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