Hippocampal activation in patients with mild cognitive impairment is necessary for successful memory encoding
Tilo T Kircher, Susanne Weis, Katrin Freymann, Michael Erb, Frank Jessen, Wolfgang Grodd, Reinhard Heun, Dirk T Leube, Tilo T Kircher, Susanne Weis, Katrin Freymann, Michael Erb, Frank Jessen, Wolfgang Grodd, Reinhard Heun, Dirk T Leube
Abstract
Background: Episodic memory enables us to consciously recollect personally experienced past events. Memory performance is reduced in patients with mild cognitive impairment (MCI), an at-risk condition for Alzheimer's disease (AD).
Patients and methods: We used functional MRI (fMRI) to compare brain activity during memory encoding in 29 healthy elderly subjects (mean age 67.7 (SD 5.4) years) and 21 patients with MCI (mean age 69.7 (SD 7.0) years). Subjects remembered a list of words while fMRI data were acquired. Later, they had to recognise these words among a list of distractor words. The use of an event related paradigm made it possible to selectively analyse successfully encoded items in each individual. We compared activation for successfully encoded words between healthy elderly subjects and patients with MCI.
Results: The main intergroup difference was found in the left hippocampus and surrounding medial temporal lobe (MTL) regions for the patients with MCI compared with healthy subjects during successful encoding.
Conclusion: These results suggest that in patients with MCI, an increase in MTL activation is necessary for successful memory encoding. Hippocampal activation may help to link newly learned information to items already stored in memory. Increased activation in MTL regions in MCI may reflect a compensatory response to the beginning of AD pathology.
Conflict of interest statement
Competing interests: None.
Figures
References
- Dale A M, Buckner R L. Selective averaging of rapidly presented individual trials using fMRI. Hum Brain Mapp 19975329–340.
- Brewer J B, Zhao Z, Desmond J al Making memories: brain activity that predicts how well visual experience will be remembered. Science 19982811185–1187.
- Henson R. A mini‐review of fMRI studies of human medial temporal lobe activity associated with recognition memory. Q J Exp Psychol B 200558340–360.
- Heun R, Jessen F, Klose al Response‐related fMRI analysis during encoding and retrieval revealed differences in cerebral activation by retrieval success. Psychiatry Res 200099137–150.
- Heun R, Jessen F, Klose al Response‐related fMRI of veridical and false recognition of words. Eur Psychiatry 20041942–52.
- Leube D T, Erb M, Grodd al Successful episodic memory retrieval of newly learned faces activates a left fronto‐parietal network. Brain Res Cogn Brain Res 20031897–101.
- Otten L J, Henson R N, Rugg M. D. Depth of processing effects on neural correlates of memory encoding: relationship between findings from across‐ and within‐task comparisons, Brain 2001124399–412.
- Wagner A D, Schacter D L, Rotte al Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 19982811188–1191.
- Weis S, Klaver P, Reul al Neural correlates of successful declarative memory formation and retrieval: the anatomical overlap. Cortex 200440200–202.
- Weis S, Klaver P, Reul al Temporal and cerebellar brain regions that support both declarative memory formation and retrieval. Cereb Cortex 200414256–267.
- Fernandez G, Weyerts H, Schrader‐Bolsche al Successful verbal encoding into episodic memory engages the posterior hippocampus: a parametrically analyzed functional magnetic resonance imaging study. J Neurosci 1998181841–1847.
- Petersen R C, Smith G E, Waring S al Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 199956303–308.
- Petersen R C, Stevens J C, Ganguli al Practice parameter: early detection of dementia: mild cognitive impairment (an evidence‐based review). Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 2001561133–1142.
- Kato T, Knopman D, Liu H. Dissociation of regional activation in mild AD during visual encoding: a functional MRI study. Neurology 200157812–816.
- Machulda M M, Ward H A, Borowski al Comparison of memory fMRI response among normal, MCI, and Alzheimer's patients. Neurology 200361500–506.
- Small S A, Perera G M, DeLaPaz al Differential regional dysfunction of the hippocampal formation among elderly with memory decline and Alzheimer's disease. Ann Neurol 199945466–472.
- Sperling R A, Bates J F, Chua E al fMRI studies of associative encoding in young and elderly controls and mild Alzheimer's disease. J Neurol Neurosurg Psychiatry 20037444–50.
- Dickerson B C, Salat D H, Bates J al Medial temporal lobe function and structure in mild cognitive impairment. Ann Neurol 20045627–35.
- Bookheimer S Y, Strojwas M H, Cohen M al Patterns of brain activation in people at risk for Alzheimer's disease. N Engl J Med 2000343450–456.
- Dickerson B C, Salat D H, Greve D al Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology 200565404–411.
- Grady C L, Maisog J M, Horwitz al Age‐related changes in cortical blood flow activation during visual processing of faces and location. J Neurosci 1994141450–1462.
- Just M A, Carpenter P A, Keller T al Brain activation modulated by sentence comprehension. Science 1996274114–116.
- Raichle M E, Fiez J A, Videen T al Practice‐related changes in human brain functional anatomy during nonmotor learning. Cereb Cortex 199448–26.
- Oldfield R C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971997–113.
- Folstein M F, Folstein S E, McHugh P R. “Mini‐mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 197512189–198.
- Helmstaedter C, Lendt M, Lux S.Verbaler Lern‐ und Merkfähigkeitstest (VLMT). Hogrefe, Göttingen 2001
- Baschek I L, Bredenkamp J, Oehrle al Bestimmung der Bildhaftigkeit (I), Konkretheit (C) und der Bedeutungshaltigkeit (m') von 800 Substantiven (The determination of imagery (i), concreteness (c), and meaningfulness of 800 nouns). Z Exp Angew Psychol 197725353–396.
- Heun R, Freymann K, Erb al Mild cognitive impairment (MCI) and actual retrieval performance affect cerebral activation in the elderly. Neurobiol Aging 200728404–413.
- Slotnick S D, Moo L R, Segal J al Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Brain Res Cogn Brain Res 20031775–82.
- Talairach J, Tournoux ‐planar stereotaxic atlas of the human brain. Stuttgart: Thieme, 1988
- Mandzia J L, Black S E, McAndrews M al fMRI differences in encoding and retrieval of pictures due to encoding strategy in the elderly. Hum Brain Mapp 2004211–14.
- Backman L, Andersson J L, Nyberg al Brain regions associated with episodic retrieval in normal aging and Alzheimer's disease. Neurology 1999521861–1870.
- Grady C L, McIntosh A R, Beig al Evidence from functional neuroimaging of a compensatory prefrontal network in Alzheimer's disease. J Neurosci 200323986–993.
- Woodard J L, Grafton S T, Votaw J al Compensatory recruitment of neural resources during overt rehearsal of word lists in Alzheimer's disease. Neuropsychology 199812491–504.
- Stern E A, Bacskai B J, Hickey G al Cortical synaptic integration in vivo is disrupted by amyloid‐beta plaques. J Neurosci 2004244535–4540.
- Awh E, Jonides J, Smith E al Dissociation of storage and rehearsal in verbal working memory: evidence from PET. Psychol Sci 1996725–31.
- Jonides J, Schumacher E H, Smith E al The role of parietal cortex in verbal working memory. J Neurosci 1998185026–5034.
- DeKosky S T, Marek K. Looking backward to move forward: early detection of neurodegenerative disorders. Science 2003302830–834.
- Kircher T T, Erb M, Grodd al Cortical activation during cholinesterase‐inhibitor treatment in Alzheimer disease: preliminary findings from a pharmaco‐fMRI study. Am J Geriatr Psychiatry 2005131006–1013.
Source: PubMed