How sandbag-able are concussion sideline assessments? A close look at eye movements to uncover strategies

References

• Davis GA, Ellenbogen RG, Bailes J, Cantu RC, Johnston KM, Manley GT, Nagahiro S, Sills A, Tator CH, McCrory P.The berlin international consensus meeting on concussion in sport. Neurosurgery. 2018;82(2):232–36.doi:10.1093/neuros/nyx344.
   PubMed Web of Science ®Google Scholar
• Langlois JA, Rutland-Brown W, Wald MM.The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil. 2006;21(5):375–78.doi:10.1097/00001199-200609000-00001.
   PubMed Web of Science ®Google Scholar
• SL Z, Kerr ZY, Yengo-Kahn A, Wasserman E, Covassin T, Solomon GS.Epidemiology of sports-related concussion in NCAA athletes from 2009-2010 to 2013-2014: incidence, recurrence, and mechanisms. Am J Sports Med. 2015;43(11):2654–62.doi:10.1177/0363546515599634.
   PubMed Web of Science ®Google Scholar
• Fallon S, Akhand O, Hernandez C, Galetta MS, Hasanaj L, Martone J, Webb N, Drattell J, Amorapanth P, Rizzo JR, et al. MULES on the sidelines: a vision-based assessment tool for sports-related concussion. J Neurol Sci. 2019;402:52–56.
   PubMed Web of Science ®Google Scholar
• Cobbs L, Hasanaj L, Amorapanth P, Rizzo JR, Nolan R, Serrano L, Raynowska J, Rucker JC, Jordan BD, Galetta SL, et al. Mobile Universal Lexicon Evaluation System (MULES) test: a new measure of rapid picture naming for concussion. J Neurol Sci. 2017;372:393–98.
   PubMed Web of Science ®Google Scholar
• Mucha A, Collins MW, Elbin RJ, Furman JM, Troutman-Enseki C, DeWolf RM, Marchetti G, Kontos AP.A brief Vestibular/Ocular Motor Screening (VOMS) assessment to evaluate concussions: preliminary findings. Am J Sports Med. 2014;42(10):2479–86.doi:10.1177/0363546514543775.
   PubMed Web of Science ®Google Scholar
• RN M, Covassin T, Elbin RJ, Gould D, Nogle S.Reliability and normative reference Values for the Vestibular/Ocular Motor Screening (VOMS) tool in youth athletes. Am J Sports Med. 2018;46(6):1475–80.doi:10.1177/0363546518756979.
   PubMed Web of Science ®Google Scholar
• RJ E, Meeuwisse W, McCrory P, Davis GA, Putukian M, Leddy J, Makdissi M, Sullivan SJ, Broglio SP, Raftery M, et al. The Sport Concussion Assessment Tool 5th Edition (SCAT5): background and rationale. Br J Sports Med. 2017;51(11):848–50.doi:10.1136/bjsports-2017-097506.
   PubMed Web of Science ®Google Scholar
• KM G, 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. 2016;1(2):CNC8.doi:10.2217/cnc.15.8.
   PubMedGoogle Scholar
• McCrory P, Johnston K, Meeuwisse W, Aubry M, Cantu R, Dvorak J, Graf-Baumann T, Kelly J, Lovell M, Schamasch P.Summary and agreement statement of the 2nd international conference on concussion in sport, Prague 2004. Br J Sports Med. 2005;39(4):196–204.doi:10.1136/bjsm.2005.018614.
   PubMed Web of Science ®Google Scholar
• McCrea M, Kelly JP, Kluge J, Ackley B, Randolph C.Standardized assessment of concussion in football players. Neurology. 1997;48(3):586–88.doi:10.1212/WNL.48.3.586.
   PubMed Web of Science ®Google Scholar
• McCrory P, Meeuwisse W, Johnston K, Dvorak J, Aubry M, Molloy M, Cantu R. Consensus statement on concussion in sport: the 3rd international conference on concussion in sport held in Zurich. Br J Sports Med. 2009;43(Suppl 1):i76–90. November 2008. doi:10.1136/bjsm.2009.058248.
   PubMed Web of Science ®Google Scholar
• DM T, Galetta KM, Phillips HW, Dziemianowicz EM, Wilson JA, Dorman ES, Laudano E, Galetta SL, Balcer LJ.Sports-related concussion: anonymous survey of a collegiate cohort. Neurol Clin Pract. 2013;3(4):279–87.doi:10.1212/CPJ.0b013e3182a1ba22.
   PubMedGoogle Scholar
• JD S, Register-Mihalik JK, Mihalik JP, Kerr ZY, Guskiewicz KM.Identifying impairments after concussion: normative data versus individualized baselines. Med Sci Sports Exerc. 2012;44(9):1621–28.doi:10.1249/MSS.0b013e318258a9fb.
   PubMed Web of Science ®Google Scholar
• CT G, Johnson LG.Reliability and validity of a computerized neurocognitive test battery, CNS vital signs. Arch Clin Neuropsychol. 2006;21(7):623–43.doi:10.1016/j.acn.2006.05.007.
   PubMed Web of Science ®Google Scholar
• Schatz P, Glatts C.“Sandbagging” baseline test performance on imPACT, without detection, is more difficult than it appears. Arch Clin Neuropsychol. 2013;28(3):236–44.doi:10.1093/arclin/act009.
   PubMed Web of Science ®Google Scholar
• Erdal K.Neuropsychological testing for sports-related concussion: how athletes can sandbag their baseline testing without detection. Arch Clin Neuropsychol. 2012;27(5):473–79.doi:10.1093/arclin/acs050.
   PubMed Web of Science ®Google Scholar
• Gaudet CE, Weyandt LL.Immediate Post-Concussion and Cognitive Testing (ImPACT): a systematic review of the prevalence and assessment of invalid performance. Clin Neuropsychol. 2017;31(1):43–58.doi:10.1080/13854046.2016.1220622.
   PubMed Web of Science ®Google Scholar
• MN A, Lempke LB, Bell DH, Lynall RC, Schmidt JD.The ability of CNS vital signs to detect coached sandbagging performance during concussion baseline testing: a randomized control trial. Brain Inj. 2020;34(3):369–74.doi:10.1080/02699052.2020.1724332.
   PubMed Web of Science ®Google Scholar
• Schatz P, Elbin RJ, Anderson MN, Savage J, Covassin T.Exploring sandbagging behaviors, effort, and perceived utility of the imPACT baseline assessment in college athletes.. Sport Exerc Perform Psychol. 2017;6(3):243–51.doi:10.1037/spy0000100.
   Web of Science ®Google Scholar
• AJ S, Alosco ML, Fedor A, Gunstad J.Invalid performance and the imPACT in national collegiate athletic association division I football players. J Athl Train. 2013;48(6):851–55.doi:10.4085/1062-6050-48.6.20.
   PubMed Web of Science ®Google Scholar
• Akhand O, Rizzo JR, Rucker JC, Hasanaj L, Galetta SL, Balcer LJ.History and future directions of vision testing in head trauma. J Neuroophthalmol. 2019;39(1):68–81.doi:10.1097/WNO.0000000000000726.
   PubMed Web of Science ®Google Scholar
• Akhand O, Galetta MS, Cobbs L, Hasanaj L, Webb N, Drattell J, Amorapanth P, Rizzo JR, Nolan R, Serrano L, 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.
   PubMed Web of Science ®Google Scholar
• Dahan N, Moehringer N, Hasanaj L, Serrano L, Joseph B, Wu S, Nolan-Kenney R, Rizzo JR, Rucker JC, Galetta SL, 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):116953.doi:10.1016/j.jns.2020.116953.
   PubMed Web of Science ®Google Scholar
• JR R, Hudson TE, Dai W, Desai N, Yousefi A, Palsana D, Seelesnick I, Balcer LJ, Galetta SL, Rucker JC. Objectifying eye movements during rapid number naming: methodology for assessment of normative data for the king–devick test. J Neurol Sci. 2016;362:232–39.doi:10.1016/j.jns.2016.01.045.
   PubMed Web of Science ®Google Scholar
• MK O, Marutani JK, Rouse MW, DeLand PN.Reliability study of the pierce and king-devick saccade tests. Am J Optom Physiol Opt. 1986;63(6):419–24.doi:10.1097/00006324-198606000-00005.
   PubMedGoogle Scholar
• KM G, Barrett J, Allen M, Madda F, Delicata D, Tennant AT, Branas CC, Maguire MG, Messner LV, Devick S, et al. The king-devick test as a determinant of head trauma and concussion in boxers and MMA fighters. Neurology. 2011;76(17):1456–62.doi:10.1212/WNL.0b013e31821184c9.
   PubMed Web of Science ®Google Scholar
• Dai W, Selesnick I, Rizzo JR, Rucker J, Hudson T.A nonlinear generalization of the savitzky-golay filter and the quantitative analysis of saccades. J Vis. 2017;17(9):10.doi:10.1167/17.9.10.
   PubMed Web of Science ®Google Scholar
• RH C, Williams ML.Neural computation of log likelihood in control of saccadic eye movements. Nature. 1995;377(6544):59–62.doi:10.1038/377059a0.
   PubMed Web of Science ®Google Scholar
• DM G, Swets JA. Signal detection theory and psychophysics. New York: Wiley; 1954.
   Google Scholar
• Jamali M, Carriot J, Cullen KE, Cullen KE. Coding strategies in the otolith system differ for translational head motion vs. static orientation relative to gravity. eLife. 2019;8:e45573.doi:10.7554/eLife.45573.
   PubMed Web of Science ®Google Scholar
• TE H. Bayesian data analysis for the behavioral and neural sciences. Cambridge: Cambridge University Press; 2021.
   Google Scholar
• Gelman A, Carlin JB, Stern HS, Dunson DB, Vehtari A, Rubin DB. Bayesian data analysis. Boca Raton, Florida: Chapman & Hall; 2013.
   Google Scholar
• KM G, Morganroth J, Moehringer N, Mueller B, Hasanaj L, Webb N, Civitano C, Cardone DA, Silverio A, Galetta SL, et al. Adding vision to concussion testing: a prospective study of sideline testing in youth and collegiate athletes. J Neuroophthalmol. 2015;35(3):235–41.doi:10.1097/WNO.0000000000000226.
   PubMed Web of Science ®Google Scholar
• KM G, Brandes LE, Maki K, Dziemianowicz MS, Laudano E, Allen M, Lawler K, Sennett B, Wiebe D, Devick S, 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(1–2):34–39.doi:10.1016/j.jns.2011.07.039.
   PubMed Web of Science ®Google Scholar
• JR R, Hudson TE, Dai W, Birkemeier J, Pasculli RM, Selesnick I, Balcer LJ, Galetta SL, Rucker JC.Rapid number naming in chronic concussion: eye movements in the king–devick test. Ann Clin Transl Neurol. 2016;3(10):801–11.doi:10.1002/acn3.345.
   PubMed Web of Science ®Google Scholar
• Ohtsuka K, Noda H.The effect of microstimulation of the oculomotor vermis on discharges of fastigial neurons and visually-directed saccades in macaques. Neurosci Res. 1991;10(4):290–95.doi:10.1016/0168-0102(91)90086-E.
   PubMed Web of Science ®Google Scholar
• EF K, Kenney DV, Gooley SG, Pratt SE, McGillis SL.Targeting errors and reduced oculomotor range following ablations of the superior colliculus or pretectum/thalamus. Behav Brain Res. 1986;22(3):191–210.doi:10.1016/0166-4328(86)90064-1.
   PubMed Web of Science ®Google Scholar
• Pierrot-Deseilligny C, Rosa A, Masmoudi K, Rivaud S, Gaymard B.Saccade deficits after a unilateral lesion affecting the superior colliculus. J Neurol Neurosurg Psychiatry. 1991;54:1106–09.doi:10.1136/jnnp.54.12.1106.
   PubMed Web of Science ®Google Scholar
• RJ L, Kennard C.Using saccades as a research tool in the clinical neurosciences. Brain. 2004;127(Pt 3):460–77.doi:10.1093/brain/awh035.
   PubMed Web of Science ®Google Scholar
• JC R, Calandrini DM, Carpenter RH.A single mechanism for the timing of spontaneous and evoked saccades. Exp Brain Res. 2008;187(2):283–93.doi:10.1007/s00221-008-1304-1.
   PubMed Web of Science ®Google Scholar
• MT K, Schmidt PP.Effect of oculomotor and other visual skills on reading performance: a literature review. Optom Vis Sci. 1996;73(4):283–92.doi:10.1097/00006324-199604000-00011.
   PubMed Web of Science ®Google Scholar
• AK H, Buttner-Ennever JA, Suzuki Y, Henn V.Histological identification of premotor neurons for horizontal saccades in monkey and man by parvalbumin immunostaining. J Comp Neurol. 1995;359(2):350–63.doi:10.1002/cne.903590212.
   PubMed Web of Science ®Google Scholar
• AK H, Helmchen C, Wahle P.GABAergic neurons in the rostral mesencephalon of the macaque monkey that control vertical eye movements. Ann N Y Acad Sci. 2003;1004(1):19–28.doi:10.1196/annals.1303.003.
   PubMed Web of Science ®Google Scholar
• MH H, Anderson TJ, Jones RD, Dalrymple-Alford JC, Frampton CM, Ardagh MW.Eye movement and visuomotor arm movement deficits following mild closed head injury. Brain: A Journal of Neurology. 2004;127(Pt 3):575–90.doi:10.1093/brain/awh066.
   PubMed Web of Science ®Google Scholar
• MH H, Jones RD, Dalrymple-Alford JC, Frampton CM, Ardagh MW, Anderson TJ.Motor deficits and recovery during the first year following mild closed head injury. Brain Injury. 2006;20(8):807–24.doi:10.1080/02699050600676354.
   PubMed Web of Science ®Google Scholar
• MF K, Little DM, Donnell AJ, Reilly JL, Simonian N, Sweeney JA.Oculomotor function in chronic traumatic brain injury. Cognitive and Behavioral Neurology: Official Journal of the Society for Behavioral and Cognitive Neurology. 2007;20(3):170–78.doi:10.1097/WNN.0b013e318142badb.
   PubMed Web of Science ®Google Scholar
• MH H, 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: A Journal of Neurology. 2009;132(Pt 10):2850–70.doi:10.1093/brain/awp181.
   PubMed Web of Science ®Google Scholar