History of mild traumatic brain injury is associated with deficits in relational memory, reduced hippocampal volume, and less neural activity later in life

Frontiers in Aging Neuroscience

Volumn 5, Issue AUG, 2013, Pages

  Monti, Jim M ^a   Voss, Michelle W ^b   Pence, Ari ^a   McAuley, Edward ^a   Kramer, Arthur F ^a   Cohen, Neal J ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Iowa   (United States)

Author keywords

Aging; FMRI; Hippocampus; mTBI; Relational memory

Indexed keywords

ADULT; AGE; AGE DISTRIBUTION; AMNESIA; ARTICLE; BOLD SIGNAL; BRAIN CORTEX; BRAIN REGION; BRAIN SIZE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; EDUCATIONAL STATUS; ELECTROENCEPHALOGRAM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENDER; HIPPOCAMPUS; HUMAN; INFERIOR FRONTAL GYRUS; MALE; MIDDLE AGED; MIDDLE FRONTAL GYRUS; NUCLEAR MAGNETIC RESONANCE SCANNER; PARACINGULATE GYRUS; PARIETAL LOBE; POSTERIOR CINGULATE; PRECUNEUS; PREFRONTAL CORTEX; PUTAMEN; QUESTIONNAIRE; SUPERIOR FRONTAL GYRUS; SUPERIOR PARIETAL LOBULE; THALAMUS; TRAUMATIC BRAIN INJURY; YOUNG ADULT;

EID: 84897476443     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2013.00041     Document Type: Article

References (67)

1. American Congress of Rehabilitation Medicine. (1993). Definition of mild traumatic brain injury. J. Head Trauma Rehabil. 8, 86-87.
2. Andrews-Hanna, J. R., Snyder, A. Z., Vincent, J. L., Lustig, C., Head, D., Raichle, M. E., et al. (2007). Disruption of large-scale brain systems in advanced aging. Neuron 56, 924-935. doi: 10.1016/j.neuron.2007.10.038
3. Ariza, M., Serra-Grabulosa, J. M., Junqué, C., Ramírez, B., Mataró, M., Poca, A., et al. (2006). Hippocampal head atrophy after traumatic brain injury. Neuropsychologia 44, 1956-1961. doi: 10.1016/j.neuropsychologia.2005.11.007
4. Beauchamp, M. H., Ditchfield, M., Maller, J. J., Catroppa, C., Godfrey, C., Rosenfeld, J. V., et al. (2011). Hippocampus, amygdala and global brain changes 10 years after childhood traumatic brain injury. Int. J. Dev. Neurosci. 29, 137-143. doi: 10.1016/j.ijdevneu.2010.12.003
5. Beckmann, C. F., Jenkinson, M., and Smith, S. M. (2003). General multilevel linear modeling for group analysis in FMRI. Neuroimage 20, 1052-1063. doi: 10.1016/S1053-8119(03)00435-X
6. Bennett, D. A., Wilson, R. S., Boyle, P. A., Buchman, A. S., and Schneider, J. A. (2012). Relation of neuropathology to cognition in persons without cognitive impairment. Ann. Neurol. 72, 599-609. doi: 10.1002/ana.23654
7. Bigler, E. D., Anderson, C. V., and Blatter, D. D. (2002). Temporal lobe morphology in normal aging and traumatic brain injury. AJNR Am. J. Neuroradiol. 23, 255-266.
8. Blumbergs, P. C., Scott, G., Manavis, J., Wainwright, H., Simpson, D. A., and McLean, A. J. (1995). Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury. J. Neurotrauma 12, 565-572. doi: 10.1089/neu.1995.12.565
9. Bohbot, V. D., Kalina, M., Stepankova, K., Spackova, N., Petrides, M., and Nadel, L. (1998). Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia 36, 1217-1238. doi: 10.1016/S0028-3932(97)00161-9
10. Buckner, R. L., Head, D., Parker, J., Fotenos, A. F., Marcus, D., Morris, J. C., et al. (2004). A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual of total intracranial volume. Neuroimage 23, 724-738. doi: 10.1016/j.neuroimage.2004.06.018
11. Cabeza, R., Ciaramelli, E., Olson, I. R., and Moscovitch, M. (2008). The parietal cortex and episodic memory: an attentional account. Nat. Rev. Neurosci. 9, 613-625. doi: 10.1038/nrn2459
12. Centers for Disease Control, and Prevention, National Center for Injury Prevention, and Control. (2003). Report to Congress on Mild Traumatic Brain Injury in the United States: Steps to Prevent a Serious Public Health Problem. Atlanta, GA: Centers for Disease Control Prevention.
13. Cohen, N. J., and Eichenbaum, H. (1993). Memory, Amnesia and the Hippocampal System. Cambridge, UK: MIT Press.
14. Cohen, N. J., Ryan, J., Hunt, C., Romine, L., Wszalek, T., and Nash, C. (1999). Hippocampal system and declarative (relational) memory: summarizing the data from functional neuroimaging studies. Hippocampus 9, 83-98.
15. Corkin, S., Rosen, T. J., Sullivan, E. V., and Clegg, R. A. (1989). Penetrating head injury in young adulthood exacerbates cognitive decline in later years. J. Neurosci. 9, 3876-3883.
16. Damoiseaux, J. S., Beckmann, C. F., Arigita, E. J., Barkhof, F., Scheltens, P., Stam, C. J., et al. (2008). Reduced resting-state brain activity in the "default network" in normal aging. Cereb. Cortex 18, 1856-1864. doi: 10.1093/cercor/bhm207
17. De Beaumont, L., Theoret, H., Mongeon, D., Messier, J., Leclerc, S., Tremblay, S., et al. (2009). Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain 132(Pt 3), 695-708. doi: 10.1093/brain/awn347
18. Dobbins, I. G., Foley, H., Schacter, D. L., and Wagner, A. D. (2002). Executive control during episodic retrieval: multiple prefrontal processes subserve source memory. Neuron 35, 989-996. doi: 10.1016/S0896-6273(02)00858-9
19. Eichenbaum, H., and Cohen, N. J. (2001). From conditioning to Conscious Recollection: Multiple Memory Systems in the Brain. New York, NY: Oxford University Press.
20. Ekdahl, C. T., Claasen, J. H., Bonde, S., Kokaia, Z., and Lindvall, O. (2003). Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. U.S.A. 100, 13632-13637. doi: 10.1073/pnas.2234031100
21. Erickson, K. I., Prakash, R. S., Voss, M. W., Chaddock, L., Hu, L., Morris, K. S., et al. (2009). Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus 19, 1030-1039. doi: 10.1002/hipo.20547
22. Faul, M., Xu, L., Wald, M., and Coronado, V. (2010). Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations and Deaths, 2002-2006. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control.
23. Fischl, B., Salat, D. H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., et al. (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341-355. doi: 10.1016/S0896-6273(02)00569-X
24. Fjell, A. M., Westlye, L. T., Grydeland, H., Amilen, I., Espeseth, T., Reinvang, I., et al. (2013). Critical ages in the life course of the adult brain: nonlinear subcortical aging. Neurobiol. Aging 34, 2239-2247. doi: 10.1016/j.neurobiolaging.2013.04.006
25. Foster, T. C. (2007). Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell 6, 319-325. doi: 10.1111/j.1474-9726.2007.00283.x
26. Fotuhi, M., Hachinski, V., and Whitehouse, P. J. (2009). Changing perspectives regarding late-life dementia. Nat. Rev. Neurol. 5, 649-658. doi: 10.1038/nrneurol.2009.175
27. Gatson, J. W., Liu, M. M., Abdelfattah, K., Wigginton, J. G., Smith, S., Wolf, S., et al. (2013). Resveratrol decreases inflammation in the brain of mice with mild traumatic brain injury. J. Trauma Acute Care Surg. 74, 470-475. doi: 10.1097/TA.0b013e31827e1f51
28. Giza, C. C., and Hovda, D. A. (2001). The neurometabolic cascade of concussion. J. Athl. Train. 36, 228-235.
29. Guillozet, A. L., Weintraub, S., Mash, D. C., and Mesulam, M. M. (2003). Neurofibrillary tangles, amyloid, and memory in aging and mild cognitive impairment. Arch. Neurol. 60, 729-736. doi: 10.1001/archneur.60.5.729
30. Hannula, D. E., Ryan, J. D., Tranel, D., and Cohen, N. J. (2007). Rapid onset relational memory effects are evident in eye movement behavior, but not in hippocampal amnesia. J. Cogn. Neurosci. 19, 1690-1705. doi: 10.1162/jocn.2007.19.10.1690
31. Hannula, D. E., Tranel, D., and Cohen, N. J. (2006). The long and short of it: relational memory impairments in amnesia, even at short lags. J. Neurosci. 26, 8352-8359. doi: 10.1523/JNEUROSCI.5222-05.2006
32. Head, D., Rodrigue, K. M., Kennedy, K. M., and Raz, N. (2008). Neuroanatomical and cognitive mediators of age-related differences in episodic memory. Neuropsychology 22, 491-507. doi: 10.1037/0894-4105.22.4.491
33. Hirni, D. I., Kivisaari, S. L., Monsch, A. U., and Taylor, K. I. (2013). Distinct neuroanatomical bases of episodic and semantic memory performance in Alzheimer's disease. Neuropsychologia 51, 930-937. doi: 10.1016/j.neuropsychologia.2013.01.013
34. Hopkins, R. O., Tate, D. F., and Bigler, E. D. (2005). Anoxic versus traumatic brain injury: amount of tissue loss, not etiology, alters cognitive and emotional function. Neuropsychology 19, 233-242. doi: 10.1037/0894-4105.19.2.233
35. Jagust, W. (2013). Vulnerable neural systems and the borderland of brain aging and neurodegeneration. Neuron 77, 219-234. doi: 10.1016/j.neuron.2013.01.002
36. Johnson, V. E., Stewart, W., and Smith, D. H. (2010). Traumatic brain injury and amyloid-beta pathology: a link to alzheimer's disease. Nat. Rev. Neurosci. 11, 361-370.
37. Johnson, V. E., Stewart, W., and Smith, D. H. (2012). Widespread tau and amyloid-beta pathology many years after a single traumatic brain injury in humans. Brain Pathol. 22, 142-149. doi: 10.1111/j.1750-3639.2011.00513.x
38. Kennedy, K. M., Rodrigue, K. M., Devous Sr., M. D., Hebrank, A. C., Bischof, G. N., and Park, D. C. (2012). Effects of beta-amyloid accumulation on neural function during encoding across the adult lifespan. Neuroimage 62, 1-8. doi: 10.1016/j.neuroimage.2012.03.077
39. Kobayashi, Y., and Amaral, D. G. (2003). Macaque monkey retrosplenial cortex: II. cortical afferents. J. Comp. Neurol. 466, 48-79. doi: 10.1002/cne.10883
40. Konkel, A., Warren, D. E., Duff, M. C., Tranel, D. N., and Cohen, N. J. (2008). Hippocampal amnesia impairs all manner of relational memory. Front. Hum. Neurosci. 2:15. doi: 10.3389/neuro.09.015.2008
41. Martland, H. S. (1928). Punch drunk. JAMA 91, 1103-1107. doi: 10.1001/jama.1928.02700150029009
42. McAllister, T. W. (2011). Neurobiological consequences of traumatic brain injury. Dialogues Clin. Neurosci. 13, 287-300.
43. McKee, A., Stein, T. D., Nowinski, C. J., Stern, R. A., Daneshvar, D. H., Alvarez, V. E., et al. (2013). The spectrum of disease in chronic traumatic encephalopathy. Brain 136, 43-64.
44. Mesulam, M. M. (2000). "Aging, Alzheimer's disease, and dementia," in Principles of Behavioral and Cognitive Neurology, 2nd Edn., ed M. M. Mesulam (New York, NY: Oxford University Press), 439-507.
45. Moretti, L., Cristofori, I., Weaver, S. M., Chau, A., Portelli, J. N., and Grafman, J. (2012). Cognitive decline in older adults with a history of traumatic brain injury. Lancet Neurol. 11, 1103-1112. doi: 10.1016/S1474-4422(12)70226-0
46. Morey, R. A., Petty, C. M., Xu, Y., Hayes, J. P., Wagner, H. R., Lewis, D. V., et al. (2009). A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes. Neuroimage 45, 855-866. doi: 10.1016/j.neuroimage.2008.12.033
47. Noble, K. G., Grieve, S. M., Korgaonkar, M. S., Engelhardt, L. E., Griffith, E. Y., Williams, L. M., et al. (2012). Hippocampal volume varies with educational attainment across the life-span. Front. Hum. Neurosci. 6:307. doi: 10.3389/fnhum.2012.00307
48. Plassman, B. L., Havlik, R. J., Steffens, D. C., Helms, M. J., Newman, T. N., Drosdick, D., et al. (2000). Documented head injury in early adulthood and risk of alzheimer's disease and other dementias. Neurology 55, 1158-1166. doi: 10.1212/WNL.55.8.1158
49. Price, J. L., McKeel Jr., D. W., Buckles, V. D., Roe, C. M., Xiong, C., Grundman, M., et al. (2009). Neuropathology of nondemented aging: presumptive evidence for preclinical Alzheimer disease. Neurobiol. Aging 30, 1026-1036. doi: 10.1016/j.neurobiolaging.2009.04.002
50. Raz, N., Ghisletta, P., Rodrigue, K. M., Kennedy, K. M., and Lindenberger, U. (2010). Trajectories of brain aging in middle-aged and older adults: regional and individual differences. Neuroimage 51, 501-511. doi: 10.1016/j.neuroimage.2010.03.020
51. Raz, N., Lindenberger, U., Rodrigue, K. M., Kennedy, K. M., Head, D., Williamson, A., et al. (2005). Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex 15, 1676-1689. doi: 10.1093/cercor/bhi044
52. Rentz, D. M., Amariglio, R. E., Becker, J. A., Frey, M., Olson, L. E., Frishe, K., et al. (2011). Face-name associative memory performance is related to amyloid burden in normal elderly. Neuropsychologia 49, 2776-2783. doi: 10.1016/j.neuropsychologia.2011.06.006
53. Rockland, K. S., and Van Hoesen, G. W. (1999). Some temporal and parietal cortical connections converge in CA1 of the primate hippocampus. Cereb. Cortex 9, 232-237. doi: 10.1093/cercor/9.3.232
54. Ryan, J. D., Althoff, R. R., Whitlow, S., and Cohen, N. J. (2000). Amnesia is a deficit in relational memory. Psychol. Sci. 11, 454-461. doi: 10.1111/1467-9280.00288
55. Serrano, F., and Klann, E. (2004). Reactive oxygen species and synaptic plasticity in the aging hippocampus. Ageing Res. Rev. 3, 431-443. doi: 10.1016/j.arr.2004.05.002
56. Simons, J. S., and Spiers, H. J. (2003). Prefrontal and medial temporal lobe interactions in long-term memory. Nat. Rev. Neurosci. 4, 637-648. doi: 10.1038/nrn1178
57. Small, S. A., Schobel, S. A., Buxton, R. B., Witter, M. P., and Barnes, C. A. (2011). A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat. Rev. Neurosci. 12, 585-601. doi: 10.1038/nrn3085
58. Spalding, K. L., Bergmann, O., Alkass, K., Bernard, S., Salehpour, M., Huttner, H. B., et al. (2013). Dynamics of hippocampal neurogenesis in adult humans. Cell 153, 1219-1227. doi: 10.1016/j.cell.2013.05.002
59. Sperling, R. A., Laviolette, P. S., O'Keefe, K., O'Brien, J., Rentz, D. M., Pihlajamaki, M., et al. (2009). Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 63, 178-188. doi: 10.1016/j.neuron.2009.07.003
60. Staresina, B. P., and Davachi, L. (2009). Mind the gap: binding experiences across space and time in the human hippocampus. Neuron 63, 267-276. doi: 10.1016/j.neuron.2009.06.024
61. Sullivan, P., Petitti, D., and Barbaccia, J. (1987). Head trauma and age of onset of dementia of the alzheimer type. JAMA 257, 2289-2290. doi: 10.1001/jama.1987.03390170045014
62. Tashlykov, V., Katz, Y., Gazit, V., Zohar, O., Schreiber, S., and Pick, C. G. (2007). Apoptotic changes in the cortex and hippocampus following minimal brain trauma in mice. Brain Res. 1130, 197-205. doi: 10.1016/j.brainres.2006.10.032
63. Tremblay, S., De Beaumont, L., Henry, L. C., Boulanger, Y., Evans, A. C., Bourgouin, P., et al. (2013). Sports concussions and aging: a neuroimaging investigation. Cereb. Cortex 23, 1159-1166. doi: 10.1093/cercor/bhs102
64. Wagner, A. D., Shannon, B. J., Kahn, I., and Buckner, R. L. (2005). Parietal lobe contributions to episodic memory retrieval. Trends Cogn. Sci. 9, 445-453. doi: 10.1016/j.tics.2005.07.001
65. Walker, K. R., and Tesco, G. (2013). Molecular mechanisms of cognitive dysfunction in traumatic brain injury. Front. Aging Neurosci. 5:29. doi: 10.3389/fnagi.2013.00029
66. Watson, P. D., Voss, J. L., Warren, D. E., Tranel, D., and Cohen, N. J. (2013). Spatial reconstruction by patients with hippocampal damage is dominated by relational memory errors. Hippocampus 23, 570-580. doi: 10.1002/hipo.22115
67. Wu, A., Ying, Z., and Gomez-Pinilla, F. (2007). Omega-3 fatty acids supplementation restores mechanisms that maintain brain homeostasis in traumatic brain injury. J. Neurotrauma 24, 1587-1595. doi: 10.1089/neu.2007.0313