2,324
Views
11
CrossRef citations to date
0
Altmetric
Articles

Saccadic impairment in chronic traumatic brain injury: examining the influence of cognitive load and injury severity

ORCID Icon, , &
Pages 1740-1748 | Received 20 Apr 2018, Accepted 26 Jul 2018, Published online: 05 Sep 2018

References

  • McMahon PJ, Hricik A, Yue JK, Puccio AM, Inoue T, Lingsma HF, Beers SR, Gordon WA, Valadka AB, Manley GT. Symptomatology and functional outcome in mild traumatic brain injury: results from the prospective TRACK-TBI study. J Neurotrauma. 2014;31(1):26–33. doi:10.1089/neu.2013.2984.
  • Vanderploeg RD, Belanger HG, Curtiss G. Mild traumatic brain injury and posttraumatic stress disorder and their associations with health symptoms. Arch Phys Med Rehabil. 2009;90(7):1084–93. doi:10.1016/j.apmr.2009.01.023.
  • Alexander MP. Mild traumatic brain injury: pathophysiology, natural history, and clinical management. Neurology. 1995;45(7):1253–60.
  • Binder LM, Rohling ML, Larrabee GJ. A review of mild head trauma. Part I: meta-analytic review of neuropsychological studies. J Clin Exp Neuropsychol. 1997;19(3):421–31. doi:10.1080/01688639708403870.
  • Wong JL, Regennitter RP, Barrios F. Base rate and simulated symptoms of mild head injury among normals. Arch Clinical Neuropsychol. 1994;9(5):411–25. doi:10.1093/arclin/9.5.411.
  • Boyle E, Cancelliere C, Hartvigsen J, Carroll LJ, Holm LW, Cassidy JD. Systematic review of prognosis after mild traumatic brain injury in the military: results of the International Collaboration on mild traumatic brain injury prognosis. Arch Phys Med Rehabil. 2014;95(3):S230–S7. doi:10.1016/j.apmr.2013.08.297.
  • Belanger HG, Spiegel E, Vanderploeg RD. Neuropsychological performance following a history of multiple self-reported concussions: a meta-analysis. J Int Neuropsychol Soc. 2010;16(2):262–67. doi:10.1017/S1355617709991287.
  • Rohling ML, Binder LM, Demakis GJ, Larrabee GJ, Ploetz DM, Langhinrichsen-Rohling J. A meta-analysis of neuropsychological outcome after mild traumatic brain injury: re-analyses and reconsiderations of Binder et al. (1997), Frencham et al. (2005), and Pertab et al. (2009). Clin Neuropsychol. 2011;25(4):608–23. doi:10.1080/13854046.2011.565076.
  • Schretlen DJ, Shapiro AM. A quantitative review of the effects of traumatic brain injury on cognitive functioning. Int Rev Psychiatry. 2003;15(4):341–49. doi:10.1080/09540260310001606728.
  • Bigler ED, Maxwell WL. Neuropathology of mild traumatic brain injury: relationship to neuroimaging findings. Brain Imaging Behav. 2012;6(2):108–36. doi:10.1007/s11682-011-9145-0.
  • Johnson VE, Stewart W, Smith DH. Axonal pathology in traumatic brain injury. Exp Neurol. 2013;246:35–43. doi:10.1016/j.expneurol.2012.01.013.
  • Kwok FY, Lee TM, Leung CH, Poon WS. Changes of cognitive functioning following mild traumatic brain injury over a 3-month period. Brain Inj. 2008;22(10):740–51. doi:10.1080/02699050802336989.
  • Binder LM. Persisting symptoms after mild head injury: a review of the postconcussive syndrome. J Clin Exp Neuropsychol. 1986;8(4):323–46. doi:10.1080/01688638608401325.
  • Kinsella G, Murtagh D, Landry A, Homfray K, Hammond M, O’beirne L, Dwyer L, Lamont M, Ponsford J. Everyday memory following traumatic brain injury. Brain Inj. 1996;10(7):499–508.
  • Vanderploeg RD, Crowell TA, Curtiss G. Verbal learning and memory deficits in traumatic brain injury: encoding, consolidation, and retrieval. J Clin Exp Neuropsychol. 2001;23(2):185–95. doi:10.1076/jcen.23.2.185.1210.
  • Vanderploeg RD, Curtiss G, Belanger HG. Long-term neuropsychological outcomes following mild traumatic brain injury. J Int Neuropsychol Soc. 2005;11(3):228–36. doi:10.1017/S1355617705050289.
  • Deary IJ, Der G, Ford G. Reaction times and intelligence differences: A population-based cohort study. Intell. 2001;29(5):389–99. doi:10.1016/S0160-2896(01)00062-9.
  • Sheppard LD, Vernon PA. Intelligence and speed of information-processing: A review of 50 years of research. Pers Individ Dif. 2008;44(3):535–51. doi:10.1016/j.paid.2007.09.015.
  • Ettenhofer ML, Hershaw JN, Barry DM. Multimodal assessment of visual attention using the Bethesda Eye & Attention Measure (BEAM). J Clin Exp Neuropsychol. 2016;38(1):96–110. doi:10.1080/13803395.2015.1089978.
  • Binder LM, Iverson GL, Brooks BL. To err is human:“abnormal” neuropsychological scores and variability are common in healthy adults. Arch Clinl Neuropsychol. 2009;24(1):31–46. doi:10.1093/arclin/acn001.
  • Schretlen DJ, Testa SM, Winicki JM, Pearlson GD, Gordon B. Frequency and bases of abnormal performance by healthy adults on neuropsychological testing. J Int Neuropsychol Soc. 2008;14(3):436–45. doi:10.1017/S1355617708080387.
  • 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(Pt 10):2850–70. doi:10.1093/brain/awp181.
  • Klein C, Rauh R, Biscaldi M. Cognitive correlates of anti-saccade task performance. Exp Brain Res. 2010;203(4):759–64. doi:10.1007/s00221-010-2276-5.
  • Heitger MH, Anderson TJ, Jones RD, Dalrymple-Alford JC, Frampton CM, Ardagh MW. Eye movement and visuomotor arm movement deficits following mild closed head injury. Brain. 2004;127(Pt 3):575–90. doi:10.1093/brain/awh066.
  • Heitger MH, Jones RD, Anderson TJ. A new approach to predicting postconcussion syndrome after mild traumatic brain injury based upon eye movement function. Conf Proc IEEE Eng Med Biol Soc. 2008;2008:3570–73. doi:10.1109/IEMBS.2008.4649977.
  • Heitger MH, 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 Inj. 2006;20(8):807–24. doi:10.1080/02699050600676354.
  • Heitger MH, Jones RD, Dalrymple-Alford JC, Frampton CM, Ardagh MW, Anderson TJ. Mild head injury–a close relationship between motor function at 1 week post-injury and overall recovery at 3 and 6 months. J Neurol Sci. 2007;253(1–2):34–47. doi:10.1016/j.jns.2006.11.007.
  • Heitger MH, Macaskill MR, Jones RD, Anderson TJ. The impact of mild closed head injury on involuntary saccadic adaptation: evidence for the preservation of implicit motor learning. Brain Inj. 2005;19(2):109–17.
  • Suh M, Basu S, Kolster R, Sarkar R, McCandliss B, Ghajar J. Increased oculomotor deficits during target blanking as an indicator of mild traumatic brain injury. Neurosci Lett. 2006;410(3):203–07. doi:10.1016/j.neulet.2006.10.001.
  • Suh M, Kolster R, Sarkar R, McCandliss B, Ghajar J. Deficits in predictive smooth pursuit after mild traumatic brain injury. Neurosci Lett. 2006;401(1–2):108–13. doi:10.1016/j.neulet.2006.02.074.
  • Contreras R, Kolster R, Voss HU, Ghajar J, Suh M, Bahar S. Eye-Target Synchronization in mild traumatic brain-injured patients. J Biol Phys. 2008;34(3–4):381–92. doi:10.1007/s10867-008-9092-1.
  • Rizzo JR, 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.
  • Caplan B, Bogner J, Brenner L, 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(1):21–28. doi:10.1097/HTR.0000000000000036.
  • Samadani U, Ritlop R, Reyes M, Nehrbass E, Li M, Lamm E, Schneider J, Shimunov D, Sava M, Kolecki R. Eye tracking detects disconjugate eye movements associated with structural traumatic brain injury and concussion. J Neurotrauma. 2015;32(8):548–56. doi:10.1089/neu.2014.3687.
  • Ettenhofer ML, Barry DM. Saccadic impairment associated with remote history of mild traumatic brain injury. J Neuropsychiatry Clin Neurosci. 2016;28(3):223–31. doi:10.1176/appi.neuropsych.15100243.
  • Kraus MF, Little DM, Wojtowicz SM, Sweeney JA. Procedural learning impairments identified via predictive saccades in chronic traumatic brain injury. Cogn Behav Neurol. 2010;23(4):210–17. doi:10.1097/WNN.0b013e3181cefe2e.
  • 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(4):293–305. doi:10.1097/HTR.0b013e3181e67936.
  • Kraus MF, Little DM, Donnell AJ, Reilly JL, Simonian N, Sweeney JA. Oculomotor function in chronic traumatic brain injury. Cogn Behav Neurol. 2007;20(3):170–78. doi:10.1097/WNN.0b013e318142badb.
  • Barker F, Cuiuffreda K, Jacobs J, Kardon R, Scheiman M, Schuchard R, Walsh D Traumatic brain injury detection using oculomotor and eye movement tracking: A Technical working group critical review. U.S. Army Medical Research & Materiel Command; 2013.
  • De Haan B, Morgan PS, Rorden C. Covert orienting of attention and overt eye movements activate identical brain regions. Brain Res. 2008;1204:102–11. doi:10.1016/j.brainres.2008.01.105.
  • Rizzolatti G, Riggio L, Dascola I, Umiltá C. Reorienting attention across the horizontal and vertical meridians: evidence in favor of a premotor theory of attention. Neuropsychologia. 1987;25(1):31–40.
  • Kahneman D. Attention and Effort. 1973 ed. Englewood Cliffs, New Jersey: Prentice-Hall Inc.; 1973. p. 253.
  • Wickens CD. Processing resources in attention. In: Parasuraman R, Davies DR, editors. Varieties of Attention. New York, NY: Academic Press; 1984. p. 63–102.
  • McDowell S, Whyte J., D’Esposito M. Working memory impairments in traumatic brain injury: evidence from a dual-task paradigm. Neuropsychologia. 1997;35(10):1341–53. doi: 10.1016/S0028-3932(97)00082-1.
  • Cicerone KD. Attention deficits and dual task demands after mild traumatic brain injury. Brain Inj. 1996;10(2):79–90. doi:10.1080/026990596124566.
  • Leclercq M, Couillet J, Azouvi P, Marlier N, Martin Y, Strypstein E, Rousseaux M. Dual task performance after severe diffuse traumatic brain injury or vascular prefrontal damage. J Clin Exp Neuropsychol. 2000;22(3):339–50. doi:10.1076/1380-3395(200006)22:3;1-V;FT339.
  • Dockree PM, Bellgrove MA, O’Keeffe FM, Moloney P, Aimola L, Carton S, Robertson IH. Sustained attention in traumatic brain injury (TBI) and healthy controls: enhanced sensitivity with dual-task load. Exp Brain Res. 2006;168(1–2):218–29. doi:10.1007/s00221-005-0079-x.
  • Azouvi P, Couillet J, Leclercq M, Martin Y, Asloun S, Rousseaux M. Divided attention and mental effort after severe traumatic brain injury. Neuropsychologia. 2004;42(9):1260–68. doi:10.1016/j.neuropsychologia.2004.01.001.
  • Bogner J, Corrigan JD. Reliability and predictive validity of the Ohio State University TBI identification method with prisoners. J Head Trauma Rehabil. 2009;24(4):279–91. doi:10.1097/HTR.0b013e3181a66356.
  • Corrigan JD, Bogner J. Initial reliability and validity of the Ohio State University TBI Identification Method. J Head Trauma Rehabil. 2007;22(6):318–29. doi:10.1097/01.HTR.0000300227.67748.77.
  • Holdnack JA. Wechsler Test of Adult Reading: manual. San Antonio, TX: Pearson, Inc.; 2001.
  • Reitan RM. The relation of the trail making test to organic brain damage. J Consult Psychol. 1955;19(5):393–94. doi:10.1037/h0044509.
  • Benedict RH, Schretlen D, Groninger L, Dobraski M, Shpritz B. Revision of the brief visuospatial memory test: studies of normal performance, reliability, and validity. Psychol Assess. 1996;8(2):145–53. doi:10.1037/1040-3590.8.2.145.
  • Wechsler D. Wechsler adult intelligence scale - Fourth Edition: administration and scoring manual. San Antonio, TX: Pearson, Inc.; 2008.
  • Wechsler D. WAIS-IV: technical and interpretive manual. San Antonio, TX: Pearson, Inc.; 2008.
  • Larrabee GJ. Detection of malingering using atypical performance patterns on standard neuropsychological tests. Clin Neuropsychol: 2003; Aug 1;17(3):410–25.
  • Schutte C, Axelrod BN. Use of embedded cognitive symptom validity measures in mild traumatic brain injury cases. In: Carone DA, Bush SS, editors. Mild traumatic brain injury: symptom validity assessment and malingering. New York, NY: Springer Publishing Company; 2013. p. 159–81.
  • Wilson JL, Pettigrew LE, Teasdale GM. Structured interviews for the glasgow outcome scale and the extended glasgow outcome scale: guidelines for their use. J Neurotrauma. 1998;15(8):573–85. doi:10.1089/neu.1998.15.573.
  • Cicerone KD, Kalmar K. Persistent postconcussion syndrome: the structure of subjective complaints after mild traumatic brain injury. J Head Trauma Rehabil. 1995;10(3):1–17. doi:10.1097/00001199-199510030-00002.
  • Safford A, Kegel J, Hershaw J, Girard D, Ettenhofer M, editors. Eye-Tracking technology for estimation of cognitive load after traumatic brain injury. International Conference on Augmented Cognition; 2015: Springer.
  • Kirchner WK. Age differences in short-term retention of rapidly changing information. J Exp Psychol. 1958;55(4):352. doi:10.1037/h0043688.
  • Fan J, McCandliss BD, Sommer T, Raz A, Posner MI. Testing the efficiency and independence of attentional networks. J Cogn Neurosci. 2002;14(3):340–47. doi:10.1162/089892902317361886.
  • Diwakar M, Harrington DL, Maruta J, Ghajar J, El-Gabalawy F, Muzzatti L, Corbetta M, Huang M-X, Lee RR. Filling in the gaps: anticipatory control of eye movements in chronic mild traumatic brain injury. Neuroimage Clin. 2015;8:210–23. doi:10.1016/j.nicl.2015.04.011.
  • Contreras R, Ghajar J, Bahar S, Suh M. Effect of cognitive load on eye-target synchronization during smooth pursuit eye movement. Brain Res. 2011;1398:55–63. doi:10.1016/j.brainres.2011.05.004.
  • Mitchell JP, Macrae CN, Gilchrist ID. Working memory and the suppression of reflexive saccades. J Cogn Neurosci. 2002;14(1):95–103. doi:10.1162/089892902317205357.
  • Stuyven E, van der Goten K, Vandierendonck A, Claeys K, Crevits L. The effect of cognitive load on saccadic eye movements. Acta Psychol. 2000;104(1):69–85. doi:10.1016/S0001-6918(99)00054-2.
  • C, Milea DMuri RM. Eye movement control by the cerebral cortex. Curr Opin Neurol. 2004;17(1):17–25. doi: 10.1097/01.wco.0000113942.12823.e0.
  • Pierrot-Deseilligny C, Muri RM, Nyffeler T, Milea D. The role of the human dorsolateral prefrontal cortex in ocular motor behavior. Ann N Y Acad Sci. 2005;1039:239–51. doi:10.1196/annals.1325.023.
  • Osaka M, Osaka N. Neural bases of focusing attention in working memory: an fMRI study based on indiviudal differences. In: Osaka N, Logie RH, D’Esposito M, editors. Cognitive neuroscience of working memory. New York, NY: Oxford University Press; 2007. p. 99–117.
  • Unsworth N, Schrock JC, Engle RW. Working memory capacity and the antisaccade task: individual differences in voluntary saccade control. J Exp Psychol Learn Mem Cogn. 2004;30(6):1302–21. doi:10.1037/0278-7393.30.6.1302.
  • Rizzo J-R, Hudson TE, Abdou A, Lui YW, Rucker JC, Raghavan P, Landy MS. Disrupted saccade control in chronic cerebral injury: upper motor neuron-like disinhibition in the ocular motor system. Front Neurol. 2017;8:12. doi:10.3389/fneur.2017.00012.
  • Ettenhofer ML, Abeles N. The significance of mild traumatic brain injury to cognition and self-reported symptoms in long-term recovery from injury. J Clin Exp Neuropsychol. 2009;31(3):363–72. doi:10.1080/13803390802175270.
  • Dikmen SS, Corrigan JD, Levin HS, Machamer J, Stiers W, Weisskopf MG. Cognitive outcome following traumatic brain injury. J Head Trauma Rehabil. 2009;24(6):430–38. doi:10.1097/HTR.0b013e3181c133e9.