How mild traumatic brain injury may affect declarative memory performance in the post-acute stage

Journal of Neurotrauma

Volumn 27, Issue 9, 2010, Pages 1585-1595

  Stulemeijer, Maja ^a   Vos, Pieter E ^a   Van Der Werf, Sieberen ^a   Van Dijk, Gert ^b   Rijpkema, Mark ^c   Fernández, Guillén ^a,c  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b CANISIUS WILHELMINA HOSPITAL   (Netherlands)

^c RADBOUD UNIVERSITY   (Netherlands)

Author keywords

functional magnetic resonance imaging; memory; mild brain concussion; neuropsychological tests

Indexed keywords

ADULT; AMNESIA; ARTICLE; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; DECLARATIVE MEMORY; DISEASE SEVERITY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; MILD TRAUMATIC BRAIN INJURY; NEUROIMAGING; NEUROPSYCHOLOGICAL TEST; PREFRONTAL CORTEX; TASK PERFORMANCE; TEMPORAL LOBE; TRAUMATIC BRAIN INJURY;

ACUTE DISEASE; ADOLESCENT; ADULT; BRAIN INJURIES; FEMALE; HUMANS; MALE; MEMORY; MEMORY DISORDERS; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; TEMPORAL LOBE; YOUNG ADULT;

EID: 77957297788     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2010.1298     Document Type: Article

References (82)

1. Aaronson, N. K., Muller, M., Cohen, P. D., Essink-Bot, M. L., Fekkes, M., Sanderman, R., Sprangers, M. A., Velde, A. T., and Verrips, E. (1998). Translation, validation, and norming of the Dutch language version of the SF-36 Health Survey in community and chronic disease populations. J. Clin. Epidemiol. 51, 1055-1068.
2. Ahmed, S., Bierley, R., Sheikh, J. I., and Date, E. S. (2000). Posttraumatic amnesia after closed head injury: a review of the literature and some suggestions for further research. Brain Inj. 14, 765-780.
3. Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N. J., Habel, U., Schneider, F., and Zilles, K. (2005). Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat. Embryol. 210, 343-352.
4. Arciniegas, D. B. (2003). The cholinergic hypothesis of cognitive impairment caused by traumatic brain injury. Curr. Psychiatry Rep. 5, 391-399.
5. Arciniegas, D. B., Topkoff, J. L., Rojas, D. C., Sheeder, J., Teale, P., Young, D. A., Sandberg, E., Reite, M. L., and Adler, L. E. (2001). Reduced hippocampal volume in association with p50 nonsuppression following traumatic brain injury. J. Neuropsychiatry Clin. Neurosci. 13, 213-221.
6. Arfanakis, K., Haughton, V. M., Carew, J. D., Rogers, B. P., Dempsey, R. J., and Meyerand, M. E. (2002). Diffusion tensor MR imaging in diffuse axonal injury. Am. J. Neuroradiol. 23, 794-802.
7. Baker, S. P., Oneill, B., Haddon, W., and Long, W. B. (1974). Injury Severity Score-Method for describing patients with multiple injuries and evaluating emergency Care. J. Trauma 14, 187-196.
8. Bazarian, J. J., Zhong, J., Blyth, B., Zhu, T., Kavcic, V., and Peterson, D. (2007). Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: a pilot study. J. Neurotrauma 24, 1447-1459.
9. Beck, A. T., Guth, D., Steer, R. A., and Ball, R. (1997). Screening for major depression disorders in medical inpatients with the Beck Depression Inventory for Primary Care. Behav. Res. Ther. 35, 785-791.
10. Belanger, H. G., Vanderploeg, R. D., Curtiss, G., and Warden, D. L. (2007). Recent neuroimaging techniques in mild traumatic brain injury. J. Neuropsychiatry Clin. Neurosci. 19, 5-20. (Pubitemid 46294440)
11. Bergsneider, M., Hovda, D. A., McArthur, D. L., Etchepare, M., Huang, S. C., Sehati, N., Satz, P., Phelps, M. E., and Becker, D. P. (2001). Metabolic recovery following human traumatic brain injury based on FDG-PET: time course and relationship to neurological disability. J. Head Trauma Rehabil. 16, 135-148.
12. Bigler, E. D. (2007). Anterior and middle cranial fossa in traumatic brain injury: Relevant neuroanatomy and neuropathology in the study of neuropsychological outcome. Neuropsychology 21, 515-531.
13. Bohnen, N., Van Zutphen, W., Twijnstra, A., Wijnen, G., Bongers, J., and Jolles, J. (1994). Late outcome of mild head injury: results from a controlled postal survey. Brain Inj. 8, 701-708.
14. Callicott, J. H., Mattay, V. S., Bertolino, A., Finn, K., Coppola, R., Frank, J. A., Goldberg, T. E., and Weinberger, D. R. (1999). Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. Cerebral Cortex 9, 20-26.
15. Cantu, R. C. (2001). Posttraumatic retrograde and anterograde amnesia: Pathophysiology and implications in grading and safe return to play. J. Athl. Train. 36, 244-248.
16. Cassidy, J. D., Carroll, L. J., Peloso, P. M., Borg, J., Von Holst, H., Holm, L., Kraus, J., and Coronado, V. G. (2004). Incidence, risk factors and prevention of mild traumatic brain injury: results of the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. J. Rehabil. Med. 43, 28-60. (Pubitemid 38268223)
17. Chen, J. K., Johnston, K. M., Collie, A., McCrory, P., and Ptito, A. (2007). A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. J. Neurol. Neurosurg. Psychiatry 78, 1231-1238.
18. Chen, S. H., and Desmond, J. E. (2005). Temporal dynamics of cerebro-cerebellar network recruitment during a cognitive task. Neuropsychologia 43, 1227-1237.
19. Critchley, H. D., Corfield, D. R., Chandler, M. P., Mathias, C. J., and Dolan, R. J. (2000). Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans. J. Physiol. 523, 259-270.
20. Delis, D. C., Kramer, J. H., Kaplan, E., and Ober, B. A. (1987). California Verbal Learning Test. Harcourt Brace Jovanovich Inc.: New York.
21. Demakis, G. J. (2004). Frontal lobe damage and tests of executive processing: a meta-analysis of the category test, Stroop test, and trail-making test. J. Clin. Exp. Neuropsychol. 26, 441-450.
22. Easdon, C., Levine, B., O'Connor, C., Tisserand, D., and Hevenor, S. (2004). Neural activity associated with response inhibition following traumatic brain injury: an event-related fMRI investigation. Brain Cogn. 54, 136-138.
23. Egan, M. F., Kojima, M., Callicott, J. H., Goldberg, T. E., Kolachana, B. S., Bertolino, A., Zaitsev, E., Gold, B., Goldman, D., Dean, M., Lu, B., and Weinberger, D. R. (2003). The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112, 257-269.
24. Fernandez, G., and Tendolkar, I. (2001). Integrated brain activity in medial temporal and prefrontal areas predicts subsequent memory performance: human declarative memory formation at the system level. Brain Res. Bull. 55, 1-9.
25. Gevins, A., and Cutillo, B. Spatiotemporal dynamics of component processes in human working memory. (1993). Electroencephalogr. Clin. Neurophysiol. 87, 128-143.
26. Gowda, N. K., Agrawal, D., Bal, C., Chandrashekar, N., Tripati, M., Bandopadhyaya, G. P., Malhotra, A., and Mahapatra, A. K. (2006). Technetium Tc-99m ethyl cysteinate dimer brain single-photon emission CT in mild traumatic brain injury: a prospective study. Am. J. Neuroradiol. 27, 447-451.
27. Hillary, F. G., Genova, H. M., Chiaravalloti, N. D., Rypma, B., and DeLuca, J. (2006). Prefrontal modulation of working memory performance in brain injury and disease. Hum. Brain Mapp. 27, 837-847.
28. Hofman, P. A. M., Stapert, S. Z., Van Kroonenburgh, M. J. P. G., Jolles, J., De Kruijk, J., and Wilmink, J. T. (2001). MR imaging, single-photon emission CT, and neurocognitive performance after mild traumatic brain injury. Am. J. Neuroradiol. 22, 441-449.
29. Ichise, M., Chung, D. G., Wang, P., Wortzman, G., Gray, B., and Franks, W. (1994). Technetium-99M-Hmpao SPECT, CT, and MRI in the evaluation of patients with chronic traumatic brain injury-A correlation with neuropsychological performance. J. Nucl. Med. 35, 217-226.
30. Inglese, M., Makani, S., Johnson, G., Cohen, B. A., Silver, J. A., Gonen, O., and Grossman, R. I. (2005). Diffuse axonal injury in mild traumatic brain injury: a diffusion tensor imaging study. J. Neurosurg. 103, 298-303.
31. Iverson, G. L. (2005). Outcome from mild traumatic brain injury. Curr. Opin. Psychiatry 18, 301-317.
32. Jacobs, A., Put, E., Ingels, M., and Bossuyt, A. (1994). Prospective evaluation of technetium-99m-HMPAO SPECT in mild and moderate traumatic brain injury. J. Nucl. Med. 35, 942-947.
33. Jantzen, K. J., Anderson, B., Steinberg, F. L., and Kelso, J. A. S. (2004). A prospective functional MR imaging study of mild traumatic brain injury in college football players. Am. J. Neuroradiol. 25, 738-745.
34. Joy, S., Fein, D., and Kaplan, E. (2003). Decoding digit symbol: speed, memory, and visual scanning. Assessment 10, 56-65.
35. Kant, R., Smith-Seemiller, L., Isaac, G., and Duffy, J. (1997). Tc-HMPAO SPECT in persistent post-concussion syndrome after mild head injury: Comparison with MRI/CT. Brain Inj. 11, 115-124.
36. King, N. S., Crawford, S., Wenden, F. J., Moss, N. E., and Wade, D. T. (1995). The Rivermead Post Concussion Symptoms Questionnaire: a measure of symptoms commonly experienced after head injury and its reliability. J. Neurol. 242, 587-592.
37. Levin, H. S., Williams, D. H., Eisenberg, H. M., High Jr., W. H., and Guinto Jr., F. C. (1992). Serial MRI and neurobehavioural findings after mild to moderate closed head injury. J. Neurol. Neurosurg. Psychiatry 55, 255-262.
38. Lewine, J. D., Davis, J. T., Bigler, E. D., Thoma, R., Hill, D., Funke, M., Sloan, J. H., Hall, S., and Orrison, W. W. (2007). Objective documentation of traumatic brain injury subsequent to mild head trauma: multimodal brain imaging with MEG, SPECT, and MRI. J. Head Trauma Rehabil. 22, 141-155.
39. Lowenstein, D. H., Thomas, M. J., Smith, D. H., and McIntosh, T. K. (1992). Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J. Neuroscience 12, 4846-4853.
40. Lyeth, B. G., Jenkins, L. W., Hamm, R. J., Dixon, C. E., Phillips, L. L., Clifton, G. L., Young, H. F., and Hayes, R. L. (1990). Prolonged memory impairment in the absence of hippocampal cell death following traumatic brain injury in the rat. Brain Res. 526, 249-258.
41. Lorberboym, M., Lampl, Y., Gerzon, I., and Sadeh, M. (2002). Brain SPECT evaluation of amnestic ED patients after mild head trauma. Am. J. Emerg. Med. 20, 310-313.
42. Maldjian, J. A., Laurienti, P. J., Kraft, R. A., and Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19, 1233-1239.
43. Marshall, L. F., Eisenberg, H. M., Jane, J. A., Luerssen, T. G., Marmarou, A., and Foulkes, M. A. (1991). A new classification of head injury based on computerized tomography. J. Neurosurg. 75, s14-s20.
44. McAllister, T. W., Saykin, A. J., Flashman, L. A., Sparling, M. B., Johnson, S. C., Guerin, S. J., Mamourian, A. C., Weaver, J. B., and Yanofsky, N. (1999). Brain activation during working memory 1 month after mild traumatic brain injury: a functional MRI study. Neurology 53, 1300-1308.
45. McAllister, T. W., Sparling, M. B., Flashman, L. A., Guerin, S. J., Mamourian, A. C., and Saykin, A. J. (2001). Differential working memory load effects after mild traumatic brain injury. NeuroImage 14, 1004-1012.
46. McCullagh, S., Oucherlony, D., Protzner, A., Blair, N., and Feinstein, A. (2001). Prediction of neuropsychiatric outcome following mild trauma brain injury: an examination of the Glasgow Coma Scale. Brain Inj. 15, 489-497.
47. Meyer-Lindenberg, A., Poline, J. B., Kohn, P. D., Holt, J. L., Egan, M. F., Weinberger, D. R., and Berman, K. F. (2001). Evidence for abnormal cortical functional connectivity during working memory in schizophrenia. Am. J. Psychiatry 158, 1809-1817.
48. Meythaler, J. M., Peduzzi, J. D., Eleftheriou, E., and Novack, T. A. (2001). Current concepts: diffuse axonal injury-associated traumatic brain injury. Arch. Phys. Med. Rehabil. 82, 1461-1471.
49. Nakayama, N., Okumura, A., Shinoda, J., Yasokawa, Y. T., Miwa, K., Yoshimura, S. I., and Iwama, T. (2006). Evidence for white matter disruption in traumatic brain injury without macroscopic lesions. J. Neurol. Neurosurg. Psychiatry 77, 850-855.
50. Olson, I. R., Page, K., Moore, K. S., Chatterjee, A., and Verfaellie, M. (2006). Working memory for conjunctions relies on the medial temporal lobe. J. Neuroscience 26, 4596-4601. (Pubitemid 44315359)
51. Owen, A. M., McMillan, K. M., Laird, A. R., and Bullmore, E. (2005). N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum. Brain Mapp. 25, 46-59.
52. Piekema, C., Kessels, R. P., Mars, R. B., Petersson, K. M., and Fernandez, G. (2006). The right hippocampus participates in short-term memory maintenance of object-location associations. Neuroimage 33, 374-382.
53. Pochon, J. B., Levy, R., Fossati, P., Lehericy, S., Poline, J. B., Pillon, B., Le Bihan, D., and Dubois B. (2002). The neural system that bridges reward and cognition in humans: an fMRI study. Proc. Natl. Acad. Sci. 99, 5669-5674.
54. Price, C. J., and Friston, K. J. (1999). Scanning patients with tasks they can perform. Hum. Brain Mapp. 8, 102-108.
55. Rizzo, P. A., Pierelli, F., Pozzessere, G., Floris, R., and Morocutti, C. (1983). Subjective posttraumatic syndrome. A comparison of visual and brain stem auditory evoked responses. Neuropsychobiology 9, 78-82.
56. Russell, W. R., and Smith, A. (1961). Post-traumatic amnesia in closed head injury. Arch. Neurol. 5, 4-17.
57. Rutgers, D. R., Toulgoat, F., Cazejust, J., Fillard, P., Lasjaunias, P., and Ducreux, D. (2008). White matter abnormalities in mild traumatic brain injury: a diffusion tensor imaging study. Am. J. Neuroradiol. 29, 514-519.
58. Sadowski-Cron, C., Schneider, J., Senn, P., Radanov, B. P., Ballinari, P., and Zimmermann, H. (2006). Patients with mild traumatic brain injury: immediate and long-term outcome compared to intra-cranial injuries on CT scan. Brain Inj. 20, 1131-1137.
59. Salmond, C. H., Chatfield, D. A., Menon, D. K., Pickard, J. D., and Sahakian, B. J. (2005). Cognitive sequelae of head injury: Involvement of basal forebrain and associated structures. Brain 128, 189-200.
60. Schmahmann, J. D., and Pandya, D. N. (1997). The cerebrocerebellar system. Int. Rev. Neurobiol. 41, 31-60.
61. Schmand, B., Bakker, D., Saan, R., and Louman, J. (1991). [The Dutch Reading Test for Adults: a measure of premorbid intelligence level]. Tijdschr. Gerontol. Geriatr. 22, 15-19.
62. Schoenhuber, R., Bortolotti, P., Malavasi, P., Marzolini, S., Tonelli, L., and Merli, G. A. (1983). Brain stem auditory evoked potentials in early evaluation of cerebral concussion. J. Neurosurg. Sci. 27, 157-159.
63. Shaw, N. A. (2002). The neurophysiology of concussion. Prog. Neurobiol. 67, 281-344.
64. Slemmer, J. E., Matser, E. J., De Zeeuw, C. I., and Weber, J. T. (2002). Repeated mild injury causes cumulative damage to hippocampal cells. Brain 125, 2699-2709.
65. Smits, M., Dippel, D. W., Houston, G. C., Wielopolski, P. A., Koudstaal, P. J., Hunink, M. G., and Van der Lugt, A. (2009). Postconcussion syndrome after minor head injury: brain activation of working memory and attention. Hum. Brain Mapp. 30, 2789-2803.
66. Snaphaan, L., Rijpkema, M., van Uden, I., Fernández, G., and de Leeuw, F. E. (2009). Reduced medial temporal lobe functionality in stroke patients: a functional magnetic resonance imaging study. Brain 132, 1882-1888.
67. Soustiel, J. F., Hafner, H., Chistyakov, A. V., Barzilai, A., and Feinsod, M. (2005). Trigeminal and auditory evoked responses in minor head injuries and post-concussion syndrome. Brain Inj. 9, 805-813.
68. Spielberger, C. D. (1983). Manual for the State-Trait Anxiety Inventory. Consulting Psychologists Press: Palo Alto, CA.
69. Squire, L. R., and Zola-Morgan, S. (1991). The medial temporal lobe memory system. Science 253, 1380-1386.
70. Stroop, J. R. (1935). Studies of interference in serial verbal reactions. J. Exp. Psychol. 18, 643-662.
71. Stulemeijer, M., Vos, P. E., and Van der Werf, S. P. (2007). Cognitive complaints after mild traumatic brain injury: things are not always what they seem. J. Psychosomat. Res. 63, 637-645.
72. Sundin, E. C., and Horowitz, M. J. (2002). Impact of Event Scale: psychometric properties. Br. J. Psychiatry 180, 205-209.
73. Ulug, A. M., Moore, D. F., Bojko, A. S., and Zimmerman, R. D. (1999). Clinical use of diffusion-tensor imaging for diseases causing neuronal and axonal damage. Am. J. Neuroradiol. 20, 1044-1048.
74. Umile, E. M., Sandel, M. E., Alavi, A., Terry, C. M., and Plotkin, R. C. (2002). Dynamic imaging in mild traumatic brain injury: Support for the theory of medial temporal vulnerability. Arch. Phys. Med. Rehabil. 83, 1506-1513.
75. Van der Naalt, J., Van Zomeren, A. H., Sluiter, W. J., and Minderhoud, J. M. (1999). One year outcome in mild to moderate head injury: the predictive value of acute injury characteristics related to complaints and return to work. J. Neurol. Neurosurg. Psychiatry 66, 207-213.
76. Von Wowern, F. (1966). Posttraumatic amnesia and confusion as an index of severity in head injury. Acta. Neurol. Scand. 42, 373-378.
77. Vos, P. E., Battistin, L., Birbamer, G., Gerstenbrand, F., Potapov, A., Prevec, T., Stephan, Ch. A., Traubner, P., Twijnstra, A., Vecsei, L., and von Wild, K. (2002). EFNS guideline on mild traumatic brain injury: report of an EFNS task force. Eur. J. Neurol. 9, 207-219.
78. Watson, M. R., Fenton, G. W., McClelland, R. J., Lumsden, J., Headley, M., and Rutherford, W. H. (1995). The post-concussional state: neurophysiological aspects. Br. J. Psychiatry 167, 514-521.
79. Wechsler, D. (1997a). Wechsler Adult Intelligence Scale-Third Edition (WAIS-III). Psychological Corporation: San Antonio, TX.
80. Wechsler, D. (1997b). Wechsler Memory Scale-III-Third Edition. Psychological Corporation: San Antonio, TX.
81. Weis, S., Klaver, P., Reul, J., Elger, C. E., and Fernandez, G. (2004). Temporal and cerebellar brain regions that support both declarative memory formation and retrieval. Cereb. Cortex 14, 256-267.
82. Zakzanis, K. K. (2001). Statistics to tell the truth, the whole truth, and nothing but the truth: formulae, illustrative numerical examples, and heuristic interpretation of effect size analyses for neuropsychological researchers. Arch. Clin. Neuropsychol. 16, 653-667.