|
|
J Neurol Neurosurg Psychiatry. 2002 August; 73(2): 173–181. doi: 10.1136/jnnp.73.2.173. | PMCID: PMC1737985 |
Functional reorganisation of memory after traumatic brain injury: a study with H2150 positron emission tomography B Levine, R Cabeza, A McIntosh, S Black, C Grady, and D Stuss Rotman Research Institute, Baycrest Centre for Geriatric Care, Toronto, Canada. Email: levine/at/psych.utoronto.ca Objective: To study the effects of moderate to severe traumatic brain injury (TBI) on the functional neuroanatomy supporting memory retrieval. Methods: Subjects were six patients who had sustained a moderate to severe TBI about four years before scanning and had since made a good recovery. Eleven healthy young adults matched to the patients for age and education served as controls. An established H2150 positron emission tomography paradigm was used to elicit brain activations in response to memory retrieval. TBI patients' patterns of brain activation were compared statistically with those of control subjects. Both group and individual case data were analysed. Results: Both TBI patients and controls engaged frontal, temporal, and parietal regions known to be involved in memory retrieval, yet the TBI patients showed relative increases in frontal, anterior cingulate, and occipital activity. The hemispheric asymmetry characteristic of controls was attenuated in patients with TBI. Reduced activation was noted in the right dorsomedial thalamus. Although local aspects of this pattern were affected by the presence of focal lesions and performance differences, the overall pattern was reliable across patients and comparable to functional neuroimaging results reported for normal aging, Alzheimer's disease, and other patients with TBI. Conclusions: The TBI patients performed memory tasks using altered functional neuroanatomical networks. These changes are probably the result of diffuse axonal injury and may reflect either cortical disinhibition attributable to disconnection or compensation for inefficient mnemonic processes. The Full Text of this article is available as a PDF (302K). These references are in PubMed. This may not be the complete list of references from this article. - Kurtzke JF. The current neurologic burden of illness and injury in the United States. Neurology. 1982 Nov;32(11):1207–1214. [PubMed]
- Dikmen SS, Ross BL, Machamer JE, Temkin NR. One year psychosocial outcome in head injury. J Int Neuropsychol Soc. 1995 Jan;1(1):67–77. [PubMed]
- Gray BG, Ichise M, Chung DG, Kirsh JC, Franks W. Technetium-99m-HMPAO SPECT in the evaluation of patients with a remote history of traumatic brain injury: a comparison with x-ray computed tomography. J Nucl Med. 1992 Jan;33(1):52–58. [PubMed]
- Langfitt TW, Obrist WD, Alavi A, Grossman RI, Zimmerman R, Jaggi J, Uzzell B, Reivich M, Patton DR. Computerized tomography, magnetic resonance imaging, and positron emission tomography in the study of brain trauma. Preliminary observations. J Neurosurg. 1986 May;64(5):760–767. [PubMed]
- Goldenberg G, Oder W, Spatt J, Podreka I. Cerebral correlates of disturbed executive function and memory in survivors of severe closed head injury: a SPECT study. J Neurol Neurosurg Psychiatry. 1992 May;55(5):362–368. [PubMed]
- Ichise M, Chung DG, Wang P, Wortzman G, Gray BG, Franks W. 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. 1994 Feb;35(2):217–226. [PubMed]
- Fontaine A, Azouvi P, Remy P, Bussel B, Samson Y. Functional anatomy of neuropsychological deficits after severe traumatic brain injury. Neurology. 1999 Dec 10;53(9):1963–1968. [PubMed]
- Duara R, Barker WW, Chang J, Yoshii F, Loewenstein DA, Pascal S. Viability of neocortical function shown in behavioral activation state PET studies in Alzheimer disease. J Cereb Blood Flow Metab. 1992 Nov;12(6):927–934. [PubMed]
- Cabeza R, Grady CL, Nyberg L, McIntosh AR, Tulving E, Kapur S, Jennings JM, Houle S, Craik FI. Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study. J Neurosci. 1997 Jan 1;17(1):391–400. [PubMed]
- Grady CL, McIntosh AR, Horwitz B, Maisog JM, Ungerleider LG, Mentis MJ, Pietrini P, Schapiro MB, Haxby JV. Age-related reductions in human recognition memory due to impaired encoding. Science. 1995 Jul 14;269(5221):218–221. [PubMed]
- Bäckman L, Andersson JL, Nyberg L, Winblad B, Nordberg A, Almkvist O. Brain regions associated with episodic retrieval in normal aging and Alzheimer's disease. Neurology. 1999 Jun 10;52(9):1861–1870. [PubMed]
- Woodard JL, Grafton ST, Votaw JR, Green RC, Dobraski ME, Hoffman JM. Compensatory recruitment of neural resources during overt rehearsal of word lists in Alzheimer's disease. Neuropsychology. 1998 Oct;12(4):491–504. [PubMed]
- Weiller C, Isensee C, Rijntjes M, Huber W, Müller S, Bier D, Dutschka K, Woods RP, Noth J, Diener HC. Recovery from Wernicke's aphasia: a positron emission tomographic study. Ann Neurol. 1995 Jun;37(6):723–732. [PubMed]
- Engelien A, Silbersweig D, Stern E, Huber W, Döring W, Frith C, Frackowiak RS. The functional anatomy of recovery from auditory agnosia. A PET study of sound categorization in a neurological patient and normal controls. Brain. 1995 Dec;118(Pt 6):1395–1409. [PubMed]
- Buckner RL, Corbetta M, Schatz J, Raichle ME, Petersen SE. Preserved speech abilities and compensation following prefrontal damage. Proc Natl Acad Sci U S A. 1996 Feb 6;93(3):1249–1253. [PubMed]
- McAllister TW, Saykin AJ, Flashman LA, Sparling MB, Johnson SC, Guerin SJ, Mamourian AC, Weaver JB, Yanofsky N. Brain activation during working memory 1 month after mild traumatic brain injury: a functional MRI study. Neurology. 1999 Oct 12;53(6):1300–1308. [PubMed]
- Gross H, Kling A, Henry G, Herndon C, Lavretsky H. Local cerebral glucose metabolism in patients with long-term behavioral and cognitive deficits following mild traumatic brain injury. J Neuropsychiatry Clin Neurosci. 1996 Summer;8(3):324–334. [PubMed]
- Levine B, Black SE, Cabeza R, Sinden M, Mcintosh AR, Toth JP, Tulving E, Stuss DT. Episodic memory and the self in a case of isolated retrograde amnesia. Brain. 1998 Oct;121 (:1951–1973. [PubMed]
- Kirkby BS, Van Horn JD, Ostrem JL, Weinberger DR, Berman KF. Cognitive activation during PET: a case study of monozygotic twins discordant for closed head injury. Neuropsychologia. 1996 Jul;34(7):689–697. [PubMed]
- Ricker JH, Müller RA, Zafonte RD, Black KM, Millis SR, Chugani H. Verbal recall and recognition following traumatic brain injury: a [0-15]-water positron emission tomography study. J Clin Exp Neuropsychol. 2001 Apr;23(2):196–206. [PubMed]
- Christodoulou C, DeLuca J, Ricker JH, Madigan NK, Bly BM, Lange G, Kalnin AJ, Liu WC, Steffener J, Diamond BJ, Ni AC. Functional magnetic resonance imaging of working memory impairment after traumatic brain injury. J Neurol Neurosurg Psychiatry. 2001 Aug;71(2):161–168. [PubMed]
- Price CJ, Friston KJ. Scanning patients with tasks they can perform. Hum Brain Mapp. 1999;8(2-3):102–108. [PubMed]
- Ogawa T, Sekino H, Uzura M, Sakamoto T, Taguchi Y, Yamaguchi Y, Hayashi T, Yamanaka I, Oohama N, Imaki S. Comparative study of magnetic resonance and CT scan imaging in cases of severe head injury. Acta Neurochir Suppl (Wien). 1992;55:8–10. [PubMed]
- Levin HS, Amparo E, Eisenberg HM, Williams DH, High WM, Jr, McArdle CB, Weiner RL. Magnetic resonance imaging and computerized tomography in relation to the neurobehavioral sequelae of mild and moderate head injuries. J Neurosurg. 1987 May;66(5):706–713. [PubMed]
- Kapur S, Tulving E, Cabeza R, McIntosh AR, Houle S, Craik FI. The neural correlates of intentional learning of verbal materials: a PET study in humans. Brain Res Cogn Brain Res. 1996 Nov;4(4):243–249. [PubMed]
- Stuss DT, Binns MA, Carruth FG, Levine B, Brandys CE, Moulton RJ, Snow WG, Schwartz ML. The acute period of recovery from traumatic brain injury: posttraumatic amnesia or posttraumatic confusional state? J Neurosurg. 1999 Apr;90(4):635–643. [PubMed]
- Levine B, Dawson D, Boutet I, Schwartz ML, Stuss DT. Assessment of strategic self-regulation in traumatic brain injury: its relationship to injury severity and psychosocial outcome. Neuropsychology. 2000 Oct;14(4):491–500. [PubMed]
- Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet. 1974 Jul 13;2(7872):81–84. [PubMed]
- Levin HS, O'Donnell VM, Grossman RG. The Galveston Orientation and Amnesia Test. A practical scale to assess cognition after head injury. J Nerv Ment Dis. 1979 Nov;167(11):675–684. [PubMed]
- Baker SP, O'Neill B, Haddon W, Jr, Long WB. The injury severity score: a method for describing patients with multiple injuries and evaluating emergency care. J Trauma. 1974 Mar;14(3):187–196. [PubMed]
- Cabeza R, Nyberg L. Imaging cognition II: An empirical review of 275 PET and fMRI studies. J Cogn Neurosci. 2000 Jan;12(1):1–47. [PubMed]
- Ricker JH, Zafonte RD. Functional neuroimaging and quantitative electroencephalography in adult traumatic head injury: clinical applications and interpretive cautions. J Head Trauma Rehabil. 2000 Apr;15(2):859–868. [PubMed]
- Nyberg L. Mapping episodic memory. Behav Brain Res. 1998 Feb;90(2):107–114. [PubMed]
- Lepage M, Ghaffar O, Nyberg L, Tulving E. Prefrontal cortex and episodic memory retrieval mode. Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):506–511. [PubMed]
- Düzel E, Cabeza R, Picton TW, Yonelinas AP, Scheich H, Heinze HJ, Tulving E. Task-related and item-related brain processes of memory retrieval. Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1794–1799. [PubMed]
- Henson RN, Shallice T, Dolan RJ. Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. Brain. 1999 Jul;122(Pt 7):1367–1381. [PubMed]
- Tulving E, Kapur S, Craik FI, Moscovitch M, Houle S. Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2016–2020. [PubMed]
- Reuter-Lorenz PA, Jonides J, Smith EE, Hartley A, Miller A, Marshuetz C, Koeppe RA. Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J Cogn Neurosci. 2000 Jan;12(1):174–187. [PubMed]
- Dupont S, Van de Moortele PF, Samson S, Hasboun D, Poline JB, Adam C, Lehéricy S, Le Bihan D, Samson Y, Baulac M. Episodic memory in left temporal lobe epilepsy: a functional MRI study. Brain. 2000 Aug;123 (:1722–1732. [PubMed]
- Becker JT, Mintun MA, Aleva K, Wiseman MB, Nichols T, DeKosky ST. Compensatory reallocation of brain resources supporting verbal episodic memory in Alzheimer's disease. Neurology. 1996 Mar;46(3):692–700. [PubMed]
- Bookheimer SY, Strojwas MH, Cohen MS, Saunders AM, Pericak-Vance MA, Mazziotta JC, Small GW. Patterns of brain activation in people at risk for Alzheimer's disease. N Engl J Med. 2000 Aug 17;343(7):450–456. [PubMed]
- Nolde SF, Johnson MK, D'Esposito M. Left prefrontal activation during episodic remembering: an event-related fMRI study. Neuroreport. 1998 Oct 26;9(15):3509–3514. [PubMed]
- Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain. 1995 Feb;118 (:279–306. [PubMed]
- Barch DM, Braver TS, Nystrom LE, Forman SD, Noll DC, Cohen JD. Dissociating working memory from task difficulty in human prefrontal cortex. Neuropsychologia. 1997 Oct;35(10):1373–1380. [PubMed]
- Cummings JL. Frontal-subcortical circuits and human behavior. Arch Neurol. 1993 Aug;50(8):873–880. [PubMed]
- Stuss DT, Guberman A, Nelson R, Larochelle S. The neuropsychology of paramedian thalamic infarction. Brain Cogn. 1988 Dec;8(3):348–378. [PubMed]
- Terayama Y, Meyer JS, Kawamura J, Weathers S. Role of thalamus and white matter in cognitive outcome after head injury. J Cereb Blood Flow Metab. 1991 Sep;11(5):852–860. [PubMed]
- Ross DT, Graham DI, Adams JH. Selective loss of neurons from the thalamic reticular nucleus following severe human head injury. J Neurotrauma. 1993 Summer;10(2):151–165. [PubMed]
- STRICH SJ. Diffuse degeneration of the cerebral white matter in severe dementia following head injury. J Neurol Neurosurg Psychiatry. 1956 Aug;19(3):163–185. [PubMed]
- Adams JH, Graham DI, Murray LS, Scott G. Diffuse axonal injury due to nonmissile head injury in humans: an analysis of 45 cases. Ann Neurol. 1982 Dec;12(6):557–563. [PubMed]
- Povlishock JT. Traumatically induced axonal injury: pathogenesis and pathobiological implications. Brain Pathol. 1992 Jan;2(1):1–12. [PubMed]
- Povlishock JT. Pathobiology of traumatically induced axonal injury in animals and man. Ann Emerg Med. 1993 Jun;22(6):980–986. [PubMed]
- Christman CW, Salvant JB, Jr, Walker SA, Povlishock JT. Characterization of a prolonged regenerative attempt by diffusely injured axons following traumatic brain injury in adult cat: a light and electron microscopic immunocytochemical study. Acta Neuropathol (Berl). 1997 Oct;94(4):329–337. [PubMed]
- Povlishock JT, Erb DE, Astruc J. Axonal response to traumatic brain injury: reactive axonal change, deafferentation, and neuroplasticity. J Neurotrauma. 1992 Mar;9 Suppl 1:S189–S200. [PubMed]
- Levin HS, Goldstein FC. Organization of verbal memory after severe closed-head injury. J Clin Exp Neuropsychol. 1986 Dec;8(6):643–656. [PubMed]
- Labbé C, Froment JC, Kennedy A, Ashburner J, Cinotti L. Positron emission tomography metabolic data corrected for cortical atrophy using magnetic resonance imaging. Alzheimer Dis Assoc Disord. 1996 Fall;10(3):141–170. [PubMed]
- D'Esposito M, Zarahn E, Aguirre GK, Shin RK, Auerbach P, Detre JA. The effect of pacing of experimental stimuli on observed functional MRI activity. Neuroimage. 1997 Aug;6(2):113–121. [PubMed]
- Kapur S, Rose R, Liddle PF, Zipursky RB, Brown GM, Stuss D, Houle S, Tulving E. The role of the left prefrontal cortex in verbal processing: semantic processing or willed action? Neuroreport. 1994 Oct 27;5(16):2193–2196. [PubMed]
- Gallucci M, Bozzao A, Splendiani A, Masciocchi C, Passariello R. Wernicke encephalopathy: MR findings in five patients. AJNR Am J Neuroradiol. 1990 SepâOct;11(5):887–892. [PubMed]
- Ashikaga R, Araki Y, Ono Y, Itami N, Akamatsu M, Kinoshita K, Ishida O. FLAIR appearance of Wernicke encephalopathy. Radiat Med. 1997 Jul–Aug;15(4):251–253. [PubMed]
- Oka M, Terae S, Kobayashi R, Kudoh K, Chu BC, Kaneko K, Yoshida M, Kaneda M, Suzuki Y, Miyasaka K. Diffusion-weighted MR findings in a reversible case of acute Wernicke encephalopathy. Acta Neurol Scand. 2001 Sep;104(3):178–181. [PubMed]
|