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Verbal learning differences in chronic mild traumatic brain injury

Published online by Cambridge University Press:  01 March 2010

ELIZABETH K. GEARY
Affiliation:
Department of Neurology, The University of Illinois College of Medicine, Chicago, Illinois Center for Stroke Research, The University of Illinois College of Medicine, Chicago, Illinois
MARILYN F. KRAUS
Affiliation:
Department of Neurology, The University of Illinois College of Medicine, Chicago, Illinois Department of Psychiatry, The University of Illinois College of Medicine, Chicago, Illinois Center for Cognitive Medicine, The University of Illinois College of Medicine, Chicago, Illinois
NEIL H. PLISKIN
Affiliation:
Department of Neurology, The University of Illinois College of Medicine, Chicago, Illinois Department of Psychiatry, The University of Illinois College of Medicine, Chicago, Illinois Center for Cognitive Medicine, The University of Illinois College of Medicine, Chicago, Illinois
DEBORAH M. LITTLE*
Affiliation:
Department of Neurology, The University of Illinois College of Medicine, Chicago, Illinois Center for Stroke Research, The University of Illinois College of Medicine, Chicago, Illinois Center for Cognitive Medicine, The University of Illinois College of Medicine, Chicago, Illinois Departments of Anatomy, Ophthalmology, and Psychology, The University of Illinois College of Medicine, Chicago, Illinois
*
*Correspondence and reprint requests to: Deborah M. Little, Department of Neurology, MC 796, 912 South Wood Street 855 N, Chicago, Illinois 60612. E-mail: little@uic.edu

Abstract

Following mild traumatic brain injury (TBI), a percentage of individuals report chronic memory and attention difficulties. Traditional neuropsychological assessments often fail to find evidence for such complaints. We hypothesized that mild TBI patients may, in fact, experience subtle cognitive deficits that reflect diminished initial acquisition that can be explained by changes in cerebral white matter microstructure. In the data presented here, a sample of nonlitigating and gainfully employed mild TBI patients demonstrated statistically significant differences from age and education matched control participants in performance on the first trial of a verbal learning task. Performance on this trial was associated with reduced fractional anisotropy in the uncinate fasciculus and the superior longitudinal fasciculus providing an anatomical correlate for the cognitive findings. Mild TBI patients were not impaired relative to control participants on total learning or memory composite variables. Performance on the first learning trial was not related to any psychological variables including mood. We concluded that patients with mild TBI demonstrate diminished verbal learning that is not often interpreted in standard neuropsychological assessment. (JINS, 2010, 16, 506–516.)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2010

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References

REFERENCES

American Congress on Rehabilitation Medicine. (1993). Definition of mild traumatic brain injury. Journal of Head Trauma Rehabilitation, 8, 8687.Google Scholar
Anderson, J. (1982). Acquisition of a cognitive skill. Psychological Review, 89, 369406.Google Scholar
Bauer, R., Grande, L., & Valenstein, E. (2003). Amnesic disorders (4th ed.). Oxford: Oxford University Press.Google Scholar
Bay, E., & Bergman, K. (2006). Symptom experience and emotional distress after traumatic brain injury. Care Management Journal, 7, 39.Google ScholarPubMed
Bazarian, J., Zhong, J., Blyth, B., Zhu, T., Kavcic, V., & Peterson, D. (2007). Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: A pilot study. Journal of Neurotrauma, 24, 14471459.Google Scholar
Belanger, H., & Vanderploeg, R. (2005). The neuropsychological impact of sports-related concussion: A meta-analysis. Journal of the International Neuropsychological Society, 11, 345357.Google Scholar
Bendlin, B., Ries, M., Lazar, M., Alexander, A., Dempsey, R., Rowley, H., et al. (2008). Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage, 42, 503514.Google Scholar
Bigler, E. (2008). Neuropsychology and clinical neuroscience of persistent post-concussive syndrome. Journal of the International Neuropsychological Society, 14, 122.CrossRefGoogle ScholarPubMed
Breier, J., Hasan, K., Zhang, W., Men, D., & Papanicolaou, A. (2008). Language dysfunction after stroke and damage to white matter tracts evaluated using diffusion tensor imaging. American Journal of Neuroradiology, 29, 483487.Google Scholar
Carroll, L., Cassidy, J., Peloso, P., Borg, J., Von Holst, H., Holm, L., et al. (2004). Prognosis for mild traumatic brain injury: Results of the who collaborating centre task force on mild traumatic brain injury. Journal Rehabilitation Medicine, 43(Suppl.), 84105.CrossRefGoogle Scholar
Cassidy, J., Carroll, L., Peloso, P., Borg, J., von Holst, H., Holm, L., et al. ; WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. (2004). Incidence, risk factors and prevention of mild traumatic brain injury: Results of the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. Journal of Rehabilitation Medicine, 43(Suppl.), 2860.Google Scholar
Chamelian, L., & Feinstein, A. (2006). The effect of major depression on subjective and objective cognitive deficits in mild to moderate traumatic brain injury. Journal Neuropsychiatry and Clinical Neurosciences, 18, 3338.CrossRefGoogle ScholarPubMed
Chan, A., Kwoka, I., Chiub, H., Lamb, L., Pangb, A., & Chow, L. (2000). Memory and organizational strategies in chronic and acute schizophrenic patients. Schizophrenia Research, 41, 431445.Google Scholar
Cho, H., Yang, D.W., Shon, Y., Kim, B., Kim, Y., Choi, Y., et al. (2008). Abnormal integrity of corticocortical tracts in mild cognitive impairment: A diffusion tensor imaging study. Journal Korean Medical Science, 23, 477483.Google Scholar
Delis, D., Kramer, J., Kaplan, E., & Obers, B. (2000). California Verbal Learning Test-II (2nd ed.). San Antonio, TX: Psychological Corporation.Google Scholar
Ettenhofer, M., & Abeles, N. (2009). The significance of mild traumatic brain injury to cognition and self-reported symptoms in long-term recovery from injury. Journal of Clinical and Experimental Neuropsychology, 31, 363372.Google Scholar
Gentilini, M., Nichelli, P., Schoenhuber, R., Bortolotti, P., Tonelli, L., Falasca, A., et al. (1985). Neuropsychological evaluation of mild head injury. Journal of Neurology, Neurosurgery, and Psychiatry, 48, 137140.Google Scholar
Gioia, G., & Isquith, P. (2004). Ecological assessment of executive function in traumatic brain injury. Developmental Neuropsychology, 25, 135158.Google Scholar
Gold, B., Powell, D., Xuan, L., Jiang, Y., & Hardy, P. (2007). Speed of lexical decision correlates with diffusion anisotropy in left parietal and frontal white matter: Evidence from diffusion tensor imaging. Neuropsychologia, 45, 24392446.CrossRefGoogle ScholarPubMed
Gongvatana, A., Woods, S., Taylor, M., Vigil, O., Grant, I., & Group, T.H. (2007). Semantic clustering inefficiency in HIV associated dementia. The Journal of Neuropsychiatry and Clinical Neurosciences, 19, 3642.Google Scholar
Gouvier, W., Cubic, B., Jones, G., Phillip, B., & Cutlip, Q. (1992). Postconcussion symptoms and daily stress in normal and head-injured college populations. Archives of Clinical Neuropsychology, 7, 193211.Google Scholar
Hollingshead, A. (1975). Four factor index of social status. Unpublished manuscript. New Haven, CT: Yale University.Google Scholar
Inglese, M., Makani, S., Johnson, G., Cohen, B.A., Silver, J.A., Gonen, O., et al. (2005). Diffuse axonal injury in mild traumatic brain injury: A diffusion tensor imaging study. Journal of Neurosurgery, 103, 298303.CrossRefGoogle ScholarPubMed
Iverson, G., Lovell, M., & Smith, S. (2000). Does brief loss of consciousness affect cognitive functioning after mild head injury? Archives of Clinical Neuropsychology, 15, 643648.CrossRefGoogle ScholarPubMed
Ivory, S., Knight, R., Longmore, B., & Caradoc-Davie, T. (1999). Verbal memory in non-demented patients with idiopathic Parkinson’s disease. Neuropsychologia, 37, 817828.CrossRefGoogle ScholarPubMed
Jacobson, R. (1995). The post-concussional syndrome: Physiogenesis, psychogenesis and malingering. An integrative model. Journal of Psychosomatic Research, 39, 675693.CrossRefGoogle ScholarPubMed
Jorge, R., Acion, L., Starkstein, S., & Magnotta, V. (2007). Hippocampal volume and mood disorders after traumatic brain injury. Biological Psychiatry, 62, 332338.CrossRefGoogle ScholarPubMed
Karzmark, P., Hall, K., & Englander, J. (1995). Late-onset post-concussion symptoms after mild brain injury: The role of premorbid, injury-related, environmental, and personality factors. Brain Injury, 9, 2126.Google Scholar
Kraus, M., Susmaras, T., Caughlin, B., Walker, C., Sweeney, J., & Little, D. (2007). White matter integrity and cognition in chronic traumatic brain injury: A diffusion tensor imaging study. Brain, 130, 25082519.Google Scholar
Kwok, F., Lee, T., Leung, C., & Poon, W. (2008). Changes of cognitive functioning following mild traumatic brain injury over a 3-month period. Brain Injury, 22, 740751.Google Scholar
Lange, R., Iverson, G., & Franzen, M. (2009). Neuropsychological functioning following complicated vs. Uncomplicated mild traumatic brain injury. Brain Injury, 23, 8391.Google Scholar
Larrabee, G. (1997). Neuropsychological outcome, post concussion symptoms, and forensic considerations in mild closed head trauma. Seminar in Clinical Neuropsychiatry, 2, 196206.Google ScholarPubMed
Lees-Haley, P., Fox, D., & Courtney, J. (2001). A comparison of complaints by mild brain injury claimants and other claimants describing subjective experiences immediately following their injury. Archives of Clinical Neuropsychology, 16, 689695.Google Scholar
Levin, H. (1992). Neurobehavioral recovery. Journal of Neurotrauma, 9, S359S373.Google ScholarPubMed
Levin, H., Mattis, S., Ruff, R., Eisenberg, H., Marshjall, L., Tabaddor, K., et al. (1987). Neurobehavioral outcome following minor head injury: A three center study. Journal of Neurosurgery, 66, 234243.CrossRefGoogle ScholarPubMed
Lo, C., Shifteh, K., Gold, T., Bello, J., & Lipton, M. (2009). Diffusion tensor imaging abnormalities in patients with mild traumatic brain injury and neurocognitive impairment. Journal of Computer Assisted Tomography, 33, 293297.Google Scholar
Logan, G. (1998). Toward an instance theory of automatization. Psychological Review, 95, 492527.Google Scholar
Luek, S. (1976). Spontaneous categorizers retain more than spontaneous alphabetizers. Memory & Cognition, 4, 476482.Google Scholar
Lundin, A., de Boussard, C., Edman, G., & Borg, J. (2006). Symptoms and disability until 3 months after mild TBI. Brain Injury, 20, 799806.Google Scholar
Macciocchi, S., Barth, J., Alves, W., Rimel, R., & Jane, J. (1996). Neuropsychological functioning and recovery after mild head injury in collegiate athletes. Neurosurgery, 36, 510514.Google Scholar
MacKenzie, J., Siddiqi, F., Babb, J., Bagley, L., Mannon, L., Sinson, G., et al. (2002). Brain atrophy in mild or moderate traumatic brain injury: A longitudinal quantitative analysis. AJNR American Journal of Neuroradiology, 23, 15091515.Google ScholarPubMed
Maddocks, D., & Saling, M. (1996). Neuropsychological deficits following concussion. Brain Injury, 10, 99103.CrossRefGoogle ScholarPubMed
McAllister, T., Flashman, L., McDonald, B., & Saykin, A. (2006). Mechanisms of working memory dysfunction after mild and moderate TBI: Evidence from functional MRI and neurogenetics. Journal of Neurotrauma, 23, 14501467.CrossRefGoogle ScholarPubMed
Medina, D., DeToledo-Morrell, L., Urresta, F., Gabrieli, J.D., Moseley, M., Fleischman, D., et al. (2006). White matter changes in mild cognitive impairment and ad: A diffusion tensor imaging study. Neurobiology of Aging, 27, 663672.CrossRefGoogle Scholar
Mooney, G., & Speed, J. (2001). The association between mild traumatic brain injury and psychiatric conditions. Brain Injury, 15, 865877.Google Scholar
Mooney, G., Speed, J., & Sheppard, S. (2005). Factors related to recovery after mild traumatic brain injury. Brain Injury, 19, 975987.Google Scholar
Niogi, S., Mukherjee, P., Ghajar, J., Johnson, C., Kolster, R., Sarkar, R., et al. (2008). Extent of microstructural white matter injury in post concussive syndrome correlates with impaired cognitive reaction time: A 3t diffusion tensor imaging study of mild traumatic brain injury. AJNR American Journal of Neuroradiology, 29, 967973.CrossRefGoogle Scholar
Orff, H., Ayalon, L., & Drummond, S. (2009). Traumatic brain injury and sleep disturbance: A review of current research. Journal of Head Trauma Rehabilitation, 24, 155165.Google Scholar
Pagulayan, K., Temkin, N., Machamer, J., & Dikmen, S. (2006). A longitudinal study of health-related quality of life after traumatic brain injury. Archives of Physical Medicine and Rehabilitation, 87, 611618.Google Scholar
Ponsford, J., Willmott, C., Rothwell, A., Cameron, P., Kelly, A., Nelms, R., et al. (2000). Factors influencing outcome following mild traumatic brain injury in adults. Journal of the International Neuropsychological Society, 6, 568579.Google Scholar
Poonawalla, A., & Zhou, X. (2004). Analytical error propagation in diffusion anisotropy calculations. Journal of Magnetic Resonance Imaging, 19, 489498.CrossRefGoogle ScholarPubMed
Rao, S., Mukundan, C., Jamuna, B., Das, B., Shastry, K., Hegde, T., et al. (1997). Patterns of association between symptoms and neuropsychological deficits in post traumatic syndrome. NIMHANS Journal, 15, 157167.Google Scholar
Reid-Arndt, S., Nehl, C., & Hinkebein, J. (2007). The frontal systems behaviour scale (FrSBe) as a predictor of community integration following a traumatic brain injury. Brain Injury, 21, 13611369.Google Scholar
Ribeiro, F., Guerreiro, M., & De Mendonça, A. (2007). Verbal learning and memory deficits in mild cognitive impairment. Journal of Clinical and Experimental Neuropsychology, 29, 187197.Google Scholar
Ropper, A., & Brown, R. (2005). Adams and Victor’s Principles of Neurology (8th ed.). New York: McGraw-Hill.Google Scholar
Rothweiler, B., Temkin, N., & Dikmen, S. (1998). Aging effect on psychosocial outcome in traumatic brain injury. Archives of Physical Medicine and Rehabilitation, 79, 881887.CrossRefGoogle ScholarPubMed
Rutgers, D., Toulgoat, F., Cazejust, J., Fillard, P., Lasjaunias, P., & Ducreux, D. (2008). White matter abnormalities in mild traumatic brain injury: A diffusion tensor imaging study. AJNR American Journal of Neuroradiology, 29, 514519.Google Scholar
Satz, P., Alfano, M., Light, R., Morgenstern, H., Zaucha, K., Asarnow, R., et al. (1999). Persistent post-concussive syndrome: A proposed methodology and literature review to determine the effects, if any, of mild head and other bodily injury. Journal of Clinical and Experimental Neuropsychology, 21, 620628.Google Scholar
Schmahmann, J.D., Smith, E.E., Eichler, F.S., & Filley, C.M. (2008). Cerebral white matter. Neuroanatomy, clinical neurology, and neurobehavioral correlates. Annals of the New York Academy of Sciences, 1142, 266309.Google Scholar
Sigurdardottir, S., Andelic, N., Roe, C., Jerstad, T., & Schanke, A. (2009). Post-concussion symptoms after traumatic brain injury at 3 and 12 months post-injury: A prospective study. Brain Injury, 23, 489497.CrossRefGoogle ScholarPubMed
Silver, C. (2000). Ecological validity of neuropsychological assessment in childhood traumatic brain injury. Journal of Head Trauma Rehabilitation, 15, 973988.Google Scholar
Silverberg, N., & Millis, S. (2009). Impairment versus deficiency in neuropsychological assessment: Implications for ecological validity. Journal of the International Neuropsychological Society, 15, 94102.Google Scholar
Smith-Seemiller, L., Fow, N., Kant, R., & Franzen, M. (2003). Presence of post-concussion syndrome symptoms in patients with chronic pain vs mild traumatic brain injury. Brain Injury, 17, 199206.Google Scholar
Sterr, A., Herron, K., Hayward, C., & Montaldi, D. (2006). Are mild head injuries as mild as we think? Neurobehavioral concomitants of chronic post-concussion syndrome. BMC Neurology, 6, 7.CrossRefGoogle ScholarPubMed
Suhr, J., & Gunstad, J. (2002). Postconcussive symptom report: The relative influence of head injury and depression. Journal of Clinical and Experimental Neuropsychology, 24, 981993.CrossRefGoogle ScholarPubMed
Tagliaferri, F., Compagnone, C., Korsic, M., Servadei, F., & Kraus, J. (2006). A systematic review of brain injury epidemiology in Europe. Acta Neurochirurgica, 148, 255268.Google Scholar
Teasdale, T., & Engberg, A. (1997). Duration of cognitive dysfunction after concussion, and cognitive dysfunction as a risk factor: A population study of young men. British Medical Journal, 315, 569572.Google Scholar
Vanderploeg, R., Belanger, H., & Curtiss, G. (2009). Mild traumatic brain injury and posttraumatic stress disorder and their associations with health symptoms. Archives of Physical Medicine and Rehabilitation, 90, 10841093.Google Scholar
Vanderploeg, R., Curtiss, G., & Belanger, H. (2005). Long-term neuropsychological outcomes following mild traumatic brain injury. Journal of the International Neuropsychological Society, 11, 228236.Google Scholar
Wakana, S., Jiang, H., Nagae-Poetscher, L., van Zijl, P., & Mori, S. (2004). Fiber tract-based atlas of human white matter anatomy. Radiology, 230, 7787.Google Scholar
Weber, J. (2007). Experimental models of repetitive brain injuries. Progress in Brain Research, 161, 253261.Google Scholar
Williams, C., Lees-Haley, P., & Brown, R. (1993). Human response to traumatic events: An integration of counterfactual thinking, hindsight bias, and attribution theory. Psychological Reports, 72, 483494.CrossRefGoogle ScholarPubMed
Willmott, C., Ponsford, J., Hocking, C., & Schönberger, M. (2009). Factors contributing to attentional impairments after traumatic brain injury. Neuropsychology, 23, 424432.Google Scholar
Wood, R. (2004). Understanding the ‘miserable minority’: A diathesis-stress paradigm for post-concussional syndrome. Brain Injury, 18, 11351153.CrossRefGoogle Scholar
Wood, R. (2009). The scientist-practitioner model: How do advances in clinical and cognitive neuroscience affect neuropsychology in the courtroom? Journal of Head Trauma Rehabilitation, 24, 8899.CrossRefGoogle ScholarPubMed
Wozniak, J., Krach, L., Ward, E., Mueller, B., Muetzel, R., Schnoebelen, S., et al. (2007). Neurocognitive and neuroimaging correlates of pediatric traumatic brain injury: A diffusion tensor imaging (DTI) study. Archives of Clinical Neuropsychology, 22, 555568.Google Scholar
Yeates, K., & Taylor, H. (2005). Neurobehavioural outcomes of mild head injury in children and adolescents. Pediatric Rehabilitation, 8, 516.Google Scholar