Abstract
Approximately half of the brain’s circuits are involved in vision and control of eye movements. Therefore, visual dysfunction is a common symptom of concussion, the mildest form of traumatic brain injury (TBI). Photosensitivity, vergence dysfunction, saccadic abnormalities, and distortions in visual perception have been reported as vision-related symptoms following concussion. Impaired visual function has also been reported in populations with a lifetime history of TBI. Consequently, vision-based tools have been developed to detect and diagnose concussion in the acute setting, and characterize visual and cognitive function in those with a lifetime history of TBI. Rapid automatized naming (RAN) tasks have provided widely accessible and quantitative measures of visual-cognitive function. Laboratory-based eye tracking approaches demonstrate promise in measuring visual function and validating results from RAN tasks in patients with concussion. Optical coherence tomography (OCT) has detected neurodegeneration in patients with Alzheimer’s disease and multiple sclerosis and may provide critical insight into chronic conditions related to TBI, such as traumatic encephalopathy syndrome. Here, we review the literature and discuss the future directions of vision-based assessments of concussion and conditions related to TBI.
摘要
将近一半的大脑回路参与视觉及眼球运动的控制。因此, 视觉障碍是脑震荡的常见症状, 是最轻微的脑部创伤 (TBI) ——。光敏度下降、辐辏功能失调、扫视运动异常和视物变形已被报道为脑震荡后的视觉相关体征。在有TBI终生病史的人群中, 也有视觉功能受损的报道。因此, 用于检测和诊断急性环境中的脑震荡的视觉工具已研发出来, 用以检测有TBI终生病史的患者的视觉和认知功能。快速自动命名 (RAN) 任务提供了视觉认知功能的广泛可及的定量测量。基于实验室的眼动追踪方法在测量脑震荡患者的视觉功能和验证RAN任务的结果方面大有前景。相干光断层扫描技术 (OCT) 已检测到阿尔茨海默病和多发性硬化症患者的神经元退行性变, 并可能提供与TBI相关的慢性疾病之间的关键性证据, 如创伤性脑病综合征。本文我们对文献进行了回顾性分析, 讨论了基于视觉的脑震荡评估和TBI相关研究的未来方向。
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References
Langlois JA, Rutland-Brown W, Wald MM. The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil. 2006;21:375–8.
Thurman DJ. The epidemiology of traumatic brain injury in children and youths: a review of research since 1990. J Child Neurol. 2016;31:20–7.
McCrory P, Meeuwisse W, Dvorak J, Aubry M, Bailes J, Broglio S, et al. Consensus statement on concussion in sport—the 5th international conference on concussion in sport held in Berlin, October 2016. Br J Sports Med. 2017;51:838–47.
McKee AC, Stern RA, Nowinski CJ, Stein TD, Alvarez VE, Daneshvar DH, et al. The spectrum of disease in chronic traumatic encephalopathy. Brain J Neurol. 2013;136:43–64.
McAllister T, McCrea M. Long-term cognitive and neuropsychiatric consequences of repetitive concussion and head-impact exposure. J Athl Train. 2017;52:309–17.
Manzanero S, Elkington LJ, Praet SF, Lovell G, Waddington G, Hughes DC. Post-concussion recovery in children and adolescents: a narrative review. J Concussion. 2017;1:2059700217726874.
Doroszkiewicz C, Gold D, Green R, Tartaglia MC, Ma J, Tator CH. Anxiety, depression, and quality of life: a long-term follow-up study of patients with persisting concussion symptoms. J Neurotrauma. 2021;38:493–505.
Felleman DJ, Van Essen DC. Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex. 1991;1:1–47.
Marinides Z, Galetta KM, Andrews CN, Wilson JA, Herman DC, Robinson CD, et al. Vision testing is additive to the sideline assessment of sports-related concussion. Neurol Clin Pract. 2015;5:25–34.
Master CL, Podolak OE, Ciuffreda KJ, Metzger KB, Joshi NR, McDonald CC, et al. Utility of pupillary light reflex metrics as a physiologic biomarker for adolescent sport-related concussion. JAMA Ophthalmol. 2020;138:1135–41.
Armstrong RA. Visual problems associated with traumatic brain injury. Clin Exp Optom. 2018;101:716–26.
Leong D, Morettin C, Messner LV, Steinmetz RJ, Pang Y, Galetta SL, et al. Visual structure and function in collision sport athletes. J Neuro-Ophthalmol. 2018;38:285–91.
Lempke LB, Schmidt JD, Lynall RC. Athletic trainers’ concussion-assessment and concussion-management practices: an update. J Athl Train. 2020;55:17–26.
Torres DM, Galetta KM, Phillips HW, Dziemianowicz EMS, Wilson JA, Dorman ES, et al. Sports-related concussion. Neurol Clin Pract. 2013;3:279–87.
May T, Foris LA, Donnally III CJ. Second impact syndrome. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2022. http://www.ncbi.nlm.nih.gov/books/NBK448119/.
Ventura RE, Jancuska JM, Balcer LJ, Galetta SL. Diagnostic tests for concussion: is vision part of the puzzle? J Neuroophthalmol. 2015;35:73–81.
Abusamak M, Alrawashdeh HM. Post-concussion syndrome light sensitivity: a case report and review of the literature. Neuro-Ophthalmol Aeolus Press. 2022;46:85–90.
Diel RJ, Mehra D, Kardon R, Buse DC, Moulton E, Galor A. Photophobia: shared pathophysiology underlying dry eye disease, migraine and traumatic brain injury leading to central neuroplasticity of the trigeminothalamic pathway. Br J Ophthalmol. 2021;105:751–60.
Ciuffreda KJ, Joshi NR, Truong JQ. Understanding the effects of mild traumatic brain injury on the pupillary light reflex. Concussion. 2017;2:CNC36.
Carrick FR, Azzolino SF, Hunfalvay M, Pagnacco G, Oggero E, D’Arcy RCN, et al. The pupillary light reflex as a biomarker of concussion. Life. 2021;11:1104.
Alkathiry AA, Kontos AP, Furman JM, Whitney SL, Anson ER, Sparto PJ. Vestibulo-ocular reflex function in adolescents with sport-related concussion: preliminary results. Sports Health. 2019;11:479–85.
Alvarez DTL. Functional mechanism of neural control in persistent post-concussion symptoms convergence insufficiency. clinicaltrials.gov; 2022. Report No.: NCT05262361. https://clinicaltrials.gov/ct2/show/NCT05262361.
Capó-Aponte JE, Urosevich TG, Temme LA, Tarbett AK, Sanghera NK. Visual dysfunctions and symptoms during the subacute stage of blast-induced mild traumatic brain injury. Mil Med. 2012;177:804–13.
Tyler CW, Likova LT, Mineff KN, Nicholas SC. Deficits in the activation of human oculomotor nuclei in chronic traumatic brain injury. Front Neurol. 2015;6:173. https://www.frontiersin.org/articles/10.3389/fneur.2015.00173.
Barnes GR. Cognitive processes involved in smooth pursuit eye movements. Brain Cogn. 2008;68:309–26.
Suh M, Kolster R, Sarkar R, McCandliss B, Ghajar J. Deficits in predictive smooth pursuit after mild traumatic brain injury. Neurosci Lett. 2006;401:108–13.
Maruta J, Suh M, Niogi SN, Mukherjee P, Ghajar J. Visual tracking synchronization as a metric for concussion screening. J Head Trauma Rehabil. 2010;25:293–305.
Drew AS, Langan J, Halterman C, Osternig LR, Chou LS, van Donkelaar P. Attentional disengagement dysfunction following mTBI assessed with the gap saccade task. Neurosci Lett. 2007;417:61–5.
Heitger MH, Jones RD, Macleod AD, Snell DL, Frampton CM, Anderson TJ. Impaired eye movements in post-concussion syndrome indicate suboptimal brain function beyond the influence of depression, malingering or intellectual ability. Brain 2009;132:2850–70.
Mucha A, Collins MW, Elbin RJ, Furman JM, Troutman-Enseki C, DeWolf RM, et al. A brief vestibular/ocular motor screening (VOMS) assessment to evaluate concussions: preliminary findings. Am J Sports Med. 2014;42:2479–86.
Ferris LM, Kontos AP, Eagle SR, Elbin RJ, Collins MW, Mucha A, et al. Predictive accuracy of the sport concussion assessment tool 3 and vestibular/ocular-motor screening, individually and in combination: A National Collegiate Athletic Association-Department of Defense Concussion Assessment, Research and Education Consortium Analysis. Am J Sports Med. 2021;49:1040–8.
Park G, Balcer MJ, Colcombe JR, Hasanaj L, Joseph B, Kenney R, et al. The MICK (Mobile integrated cognitive kit) app: Digital rapid automatized naming for visual assessment across the spectrum of neurological disorders. J Neurol Sci. 2022;434:120150.
Denckla MB, Rudel RG. Rapid ‘automatized’ naming (R.A.N.): dyslexia differentiated from other learning disabilities. Neuropsychologia. 1976;14:471–9.
Geschwind N, Fusillo M. Color-naming defects in association with alexia. Arch Neurol. 1966;15:137–46.
Norton ES, Wolf M. Rapid automatized naming (RAN) and reading fluency: implications for understanding and treatment of reading disabilities. Annu Rev Psychol. 2012;63:427–52.
Cobbs L, Hasanaj L, Amorapanth P, Rizzo JR, Nolan R, Serrano L, et al. Mobile Universal Lexicon Evaluation System (MULES) test: a new measure of rapid picture naming for concussion. J Neurol Sci. 2017;372:393–8.
Dahan N, Moehringer N, Hasanaj L, Serrano L, Joseph B, Wu S, et al. The SUN test of vision: Investigation in healthy volunteers and comparison to the mobile universal lexicon evaluation system (MULES). J Neurol Sci. 2020;415:116953.
Cummine J, Szepesvari E, Chouinard B, Hanif W, Georgiou GK. A functional investigation of RAN letters, digits, and objects: How similar are they? Behav Brain Res. 2014;275:157–65.
Gunasekaran P, Fraser CL, Hodge C. The learning effect of the King-Devick test in semi-professional rugby union athletes. J Neurol Sci. 2020;419:117168.
DiFabio M, Oldham J, DeWolf R, Kaminski T, Buckley T. Evaluating concussion recovery through oculomotor testing (I13.004). Neurology. 2016;86. https://n.neurology.org/content/86/16_Supplement/I13.004.
Akhand O, Galetta MS, Cobbs L, Hasanaj L, Webb N, Drattell J, et al. The new Mobile Universal Lexicon Evaluation System (MULES): A test of rapid picture naming for concussion sized for the sidelines. J Neurol Sci. 2018;387:199–204.
Stockbridge MD, Doran A, King K, Newman RS. The effects of concussion on rapid picture naming in children. Brain Inj. 2018;32:506–14.
Wu SZ, Nolan-Kenney R, Moehringer NJ, Hasanaj LF, Joseph BM, Clayton AM, et al. Exploration of rapid automatized naming and standard visual tests in prodromal Alzheimer disease detection. J Neuroophthalmol. 2022;42:79–87.
Galetta KM, Liu M, Leong DF, Ventura RE, Galetta SL, Balcer LJ. The King-Devick test of rapid number naming for concussion detection: meta-analysis and systematic review of the literature. Concussion. 2015;1:CNC8.
Galetta KM, Brandes LE, Maki K, Dziemianowicz MS, Laudano E, Allen M, et al. The King–Devick test and sports-related concussion: Study of a rapid visual screening tool in a collegiate cohort. J Neurol Sci. 2011;309:34–9.
Galetta KM, Barrett J, Allen M, Madda F, Delicata D, Tennant AT, et al. The King-Devick test as a determinant of head trauma and concussion in boxers and MMA fighters. Neurology. 2011;76:1456–62.
King D, Clark T, Gissane C. Use of a rapid visual screening tool for the assessment of concussion in amateur rugby league: A pilot study. J Neurol Sci. 2012;320:16–21.
Kyle Harrold G, Hasanaj L, Moehringer N, Zhang I, Nolan R, Serrano L, et al. Rapid sideline performance meets outpatient clinic: Results from a multidisciplinary concussion center registry. J Neurol Sci. 2017;379:312–7.
Cifu DX, Wares JR, Hoke KW, Wetzel PA, Gitchel G, Carne W. Differential eye movements in mild traumatic brain injury versus normal controls. J Head Trauma Rehabil. 2015;30:21–8.
Hunfalvay M, Roberts CM, Murray N, Tyagi A, Kelly H, Bolte T. Horizontal and vertical self-paced saccades as a diagnostic marker of traumatic brain injury. Concussion. 2019;4:CNC60.
Rizzo JR, Hudson TE, Dai W, Birkemeier J, Pasculli RM, Selesnick I, et al. Rapid number naming in chronic concussion: eye movements in the King–Devick test. Ann Clin Transl Neurol. 2016;3:801–11.
Hudson TE, Conway J, Rizzo JR, Martone J, Chou LT, Balcer LJ, et al. Rapid automatized picture naming in an outpatient concussion center: quantitative eye movements during the Mobile Universal Lexicon Evaluation System (MULES) Test. Clin. Transl Neurosci. 2022;6:18.
Rizzo JR, Hudson TE, Martone J, Dai W, Ihionu O, Chaudhry Y, et al. How sandbag-able are concussion sideline assessments? A close look at eye movements to uncover strategies. Brain Inj. 2021;35:426–35.
Moss HE, McCluskey L, Elman L, Hoskins K, Talman L, Grossman M, et al. Cross-sectional evaluation of clinical neuro-ophthalmic abnormalities in an amyotrophic lateral sclerosis population. J Neurol Sci. 2012;314:97–101.
Scheiman M, Mitchell GL, Cotter S, Cooper J, Kulp M, Rouse M, et al. A randomized clinical trial of treatments for convergence insufficiency in children. Arch Ophthalmol. 2005;123:14–24.
Fisher JB, Jacobs DA, Markowitz CE, Galetta SL, Volpe NJ, Nano-Schiavi ML, et al. Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis. Ophthalmology. 2006;113:324–32.
Wu SZ, Masurkar AV, Balcer LJ. Afferent and efferent visual markers of Alzheimer’s disease: a review and update in early stage disease. Front Aging Neurosci. 2020;12:572337. https://www.frontiersin.org/articles/10.3389/fnagi.2020.572337.
Seyer LA, Galetta K, Wilson J, Sakai R, Perlman S, Mathews K, et al. Analysis of the visual system in Friedreich ataxia. J Neurol. 2013;260:2362–9.
Galvin JE, Kleiman MJ, Walker M. Using optical coherence tomography to screen for cognitive impairment and dementia. J Alzheimers Dis. 2021;84:723–36.
Petzold A, de Boer JF, Schippling S, Vermersch P, Kardon R, Green A, et al. Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis. Lancet Neurol. 2010;9:921–32.
Gilmore CS, Lim KO, Garvin MK, Wang JK, Ledolter J, Fenske AL, et al. Association of optical coherence tomography with longitudinal neurodegeneration in veterans with chronic mild traumatic brain injury. JAMA Netw Open. 2020;3:e2030824.
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This study was supported in part by the NYU Grossman School of Medicine.
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The authors confirm contribution to the paper as follows: study conception and design: SLG; literature review: CAB; draft manuscript preparation: CAB; LJB, SLG, SNG, MB. All authors reviewed and approved the final version or the manuscript.
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LJB is editor-in-chief of the Journal of Neuro-Ophthalmology. The remaining authors have no disclosures.
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Bell, C.A., Grossman, S.N., Balcer, L.J. et al. Vision as a piece of the head trauma puzzle. Eye 37, 2385–2390 (2023). https://doi.org/10.1038/s41433-023-02437-8
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DOI: https://doi.org/10.1038/s41433-023-02437-8
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