Verbal learning in Alzheimer’s disease and mild cognitive impairment:fine-grained acquisition and short-delay consolidation performance and neural correlates
[en] The aim of this study was to examine correlations between acquisition and short-delay consolidation and brain metabolism at rest measured by fluorodeoxyglucose positron emission tomography (FDG-PET) in 44 Alzheimer’s disease (AD) patients, 16 patients with mild cognitive impairment (MCI) who progressed to dementia (MCI-AD), 15 MCI patients who remained stable (MCI-S, 4–8 years of follow-up), and 20 healthy older participants. Acquisition and short-delay consolidation were calculated respectively as mean gained (MG) and lost (ML) access to items of the California Verbal Learning Task. MG performance suggests that acquisition is impaired in AD patients even at predementia stage (MCI-AD). ML performance suggests that short-delay consolidation is deficient only in confirmed AD patients. Variations in acquisition performance in control participants are related to metabolic activity in the anterior parietal cortex, an area
supporting task-positive attentional processes. In contrast, the acquisition deficit is related to decreased activity in the lateral temporal cortex, an area supporting semantic processes, in patients at an early stage of AD and is related to metabolic activity in the hippocampus, an area supporting associative processes, in confirmed AD patients.
Research center :
GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Disciplines :
Neurosciences & behavior
Author, co-author :
Genon, Sarah ; Université de Liège - ULiège > Département des sciences cliniques > Neuroimagerie des troubles de la mémoire et révalid. cogn.
Collette, Fabienne ; Université de Liège - ULiège > Département de Psychologie : cognition et comportement > Neuropsychologie
Moulin, Chris; University of Leeds, UK
LEKEU, Françoise ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie Sart Tilman
Bahri, Mohamed Ali ; Université de Liège - ULiège > Centre de recherches du cyclotron
Salmon, Eric ; Université de Liège - ULiège > Département des sciences cliniques > Neuroimagerie des troubles de la mémoire et révalid. cogn.
Bastin, Christine ; Université de Liège - ULiège > Centre de recherches du cyclotron
Language :
English
Title :
Verbal learning in Alzheimer’s disease and mild cognitive impairment:fine-grained acquisition and short-delay consolidation performance and neural correlates
Addis D.R., McAndrews M.P. Prefrontal and hippocampal contributions to the generation and binding of semantic associations during successful encoding. NeuroImage 2006, 33:1194-1206.
Diagnostic and Statistical Manual of Mental Disorders 1994, APA, American Psychiatric Association, Washington, DC. (4th ed.).
Bastin, C., Feyers, D., Jedidi, H., Bahri, M.A., Degueldre, C., Lemaire, C., Collette, F., Salmon, E., in press. Episodic autobiographical memory in amnestic mild cognitive impairment: what are the neural correlates? Hum. Brain Mapp.
Burianova H., McIntosh A.R., Grady C.L. A common functional brain network for autobiographical, episodic, and semantic memory retrieval. NeuroImage 2010, 49:865-874.
Cahn D.A., Sullivan E.V., Shear P.K., Heit G., Lim K.O., Marsh L., Lane B., Wasserstein P., Silverberg G.D. Neuropsychological and motor functioning after unilateral anatomically guided posterior ventral pallidotomy. Preoperative performance and three-month follow-up. Neuropsychiatry Neuropsychol. Behav. Neurol 1998, 11:136-145.
Chang Y.L., Bondi M.W., Fennema-Notestine C., McEvoy L.K., Hagler D.J., Jacobson M.W., Dale A.M. Brain substrates of learning and retention in mild cognitive impairment diagnosis and progression to Alzheimer's disease. Neuropsychologia 2010, 48:1237-1247. Alzheimer's Disease Neuroimaging Initiative.
Clément F., Belleville S., Mellah S. Functional neuroanatomy of the encoding and retrieval processes of verbal memory in MCI. Cortex 2010, 46:1005-1015.
Cohen N.J., Ryan J., Hunt C., Romine L., Wszalek T., Nash C. Hippocampal system and declarative (relational) memory: summarizing the data from functional neuroimaging studies. Hippocampus 1999, 9:83-98. 10.1002/(SICI)1098-1063(1999)9:1.
Conway M.A. Episodic memories. Neurospychologia 2009, 47:2305-2313.
Crowe S.F., O'Sullivan J.D., Peppard R.F., McNeill P.M., Bardenhagen F., Bowden S. Left posteroventral pallidotomy results in a deficit in verbal memory. Behav. Neurol 1998, 11:79-84.
Delis D.C., Kramer J.H., Kaplan E., Ober B. The California Verbal Learning Test-Second Edition 2000, Psychological Corporation, New-York.
Delis D.C., Massman P.J., Butters N., Salmon D.P. Profiles of demented and amnesic patients on the California Verbal Learning Test: implications for the assessment of memory disorders. Psychol. Assess 1991, 3:19-26.
Demakis G.J., Mercury M.G., Sweet J.J., Rezak M., Eller T., Vergenz S. Qualitative analysis of verbal fluency before and after unilateral pallidotomy. Clin. Neuropsychol 2003, 17:322-330.
Deweer B., Lehéricy S., Pillon B., Baulac M., Chiras J., Marsault C., Agid Y., Dubois B. Memory disorders in probable Alzheimer's disease: the role of hippocampal atrophy as shown with MRI. J. Neurol. Neurosurg. Psychiatry 1995, 58:590-597.
Dunlosky J., Salthouse T.A. A decomposition of age-related differences in multitrial free recall. Aging Neuropsychol. Cogn 1996, 3:2-14.
Farrar A.M., Font L., Pereira M., Mingote S., Bunce J.G., Chrobak J.J., Salamone J.D. Forebrain circuitry involved in effort-related choice: injections of the GABAA agonist muscimol into ventral pallidum alter response allocation in food-seeking behavior. Neuroscience 2008, 152:321-330.
Fox L.S., Olin J.T., Erblich J., Ippen C.G., Schneider L.S. Severity of cognitive impairment in Alzheimer's disease affects list learning using the California Verbal Learning Test (CVLT). Int. J. Geriatr. Psychiatry 1998, 13:544-549. 10.1002/(SICI)1099-1166(199808)13:8.
Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The Human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9673-9678.
Gelb D.J., Oliver E., Gilman S. Diagnostic criteria for Parkinson disease. Arch. Neurol 1999, 56:33-39.
Giovanello K.S., Schnyer D.M., Verfaellie M. A critical role for the anterior hippocampus in relational memory: evidence from an fMRI study comparing associative and item recognition. Hippocampus 2004, 14:5-8.
Greenaway M.C., Lacritz L.H., Binegar D., Weiner M.F., Lipton A., Munro Cullum C. Patterns of verbal memory performance in mild cognitive impairment, Alzheimer's disease, and normal aging. Cogn. Behav. Neurol 2006, 19:79-84.
Grober E., Kawas C. Learning and retention in preclinical and early Alzheimer's disease. Psychol. Aging 1997, 12:183-188.
Hachinski V.C., Iliff L.D., Zihka E., Du Boulay G.H., McAllister V.L., Marshall J., Russell R.W., Symon L. Cerebral blood flow in dementia. Arch. Neurol 1975, 32:632-637.
Junqué C., Alegret M., Nobbe F.A., Valldeoriola F., Pueyo R., Vendrell P., Tolosal E., Rumià J., Mercader J.M. Cognitive and behavioral changes after unilateral posteroventral pallidotomy: relationship with lesional data from MRI. Mov. Disord 1999, 14:780-789. 10.1002/1531-8257(199909)14:5.
Kramer J.H., Schuff N., Reed B.R., Mungas D., Du A.T., Rosen H.J., Jagust W.J., Miller B.L., Weiner M.W., Chui H.C. Hippocampal volume and retention in Alzheimer's disease. J. Int. Neuropsychol. Soc 2004, 10:639-643.
Kretschmer B.D. Functional aspects of the ventral pallidum. Amino Acids 2000, 19:201-210.
Laakso M.P., Soininen H., Partanen K., Helkala E.-L., Hartikainen P., Vainio P., Hallikainen M., Hänninen T., Riekkinen P.J. Volumes of hippocampus, amygdale and frontal lobes in MRI-based diagnosis of early Alzheimer's disease: correlation with memory functions. J. Neural Transm 1995, 9:73-86.
Libon D.J., Bogdanoff B., Cloud B.S., Skalina S., Giovannetti T., Gitlin H.L., Bonavita J. Declarative and procedural learning, quantitative measures of the hippocampus, and subcortical white alterations in Alzheimer's disease and ischaemic vascular dementia. J. Clin. Exp. Neuropsychol 1998, 20:30-41.
McClelland J.L., McNaughton B.L., O'Reilly R.C. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev 1995, 102:419-457.
McKeith I.G., Galasko D., Kosaka K., Perry E.K., Dickson D.W., Hansen L.A., Salmon D.P., Lowe J., Mirra S.S., Byrne E.J., Lennox G., Quinn N.P., Edwardson J.A., Ince P.G., Bergeron C., Burns A., Miller B.L., Lovestone S., Collerton D., Jansen E.N., Ballard C., de Vos R.A., Wilcock G.K., Jellinger K.A., Perry R.H. Consensus guidelines for the clinical and pathological diagnosis of dementia with Lewy bodies (DLB): report of the consortium on DBL international workshop. Neurology 1996, 47:1113-1124.
McKhann G., Drachman D., Folstein M., Katzman R., Price D., Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology 1984, 34:939-944.
Menon V., Boyett-Anderson J.M., Schatzberg A.F., Reiss A.L. Relating semantic and episodic memory systems. Cogn. Brain Res 2002, 13:261-265. 10.1016/S0926-6410(01)00120-3.
Meulenbroek O., Rijpkema M., Kessels R.P., Rikkert M.G., Fernández G. Autobiographical memory retrieval in patients with Alzheimer's disease. NeuroImage 2010, 53:331-340.
Miller R.R., Matzel L.D. Retrieval failure versus memory loss in experimental amnesia: definitions and processes. Learn. Mem 2006, 12:491-497.
Moscovitch M., Rosenbaum R.S., Gilboa A., Addis D.R., Westmacott C.G., McAndrews M.P., Levine B., Black S., Winocur G., Nadel L. Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J. Anat 2005, 207:35-66.
Moulin C.J., James N., Freeman J.E., Jones R.W. Deficient acquisition and consolidation: intertrial free recall performance in Alzheimer's disease and mild cognitive impairment. J. Clin. Exp. Neuropsychol 2004, 26:1-10.
Neary D., Snowden J.S., Gustafson L., Passant U., Stuss D., Black S., Freedman M., Kertesz A., Robert P.H., Albert M., Boone K., Miller B.L., Cummings J., Benson D.F. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 1998, 51:1546-1554.
Nyberg L., Forkstam C., Petersson K.M., Cabeza R., Ingvar M. Brain imaging of human memory systems: between-systems similarities and within-system differences. Cogn. Brain Res 2002, 13:281-292. 10.1016/S0926-6410(02)00052-6.
Petersen R.C., Doody R., Kurz A., Mohs R.C., Morris J.C., Rabins P.V., Ritchie K., Rossor M., Thal L., Winblad B. Current concepts in mild cognitive impairment. Arch. Neurol 2001, 58:1985-1992.
Petersen R.C., Jack C.R., Xu Y.-C., Waring S.C., O'Brien P.C., Smith G.E., Ivnik R.J., Tangalos E.G., Boeve B.F., Kokmen E. Memory and MRI-based hippocampal volumes in aging and AD. Neurology 2000, 54:581-587.
Petersen R.C., Smith G.E., Ivnik R.J., Kokmen E., Tangalos E.G. Memory function in very early Alzheimer's disease. Neurology 1994, 44:867-872.
Petersen R.C., Smith G.E., Stephen C.W., Robert J.I., Kokmen E., Tangelos E.G. Aging, memory, and mild cognitive impairment. Int. Psychogeriatr 1997, 9:65-69.
Petersen R.C., Smith G.E., Waring S.C., Ivnik R.J., Tangalos E.G., Kokmen E. Mild cognitive impairment: clinical characterization and outcome. Arch. Neurol 1999, 56:303-308.
Rabin L.A., Barr W.B., Burton L.A. Assessment practices of clinical neuropsychologists in the United States and Canada: a survey of INS, NAN, and APA Division 40 members. Arch. Clin. Neuropsychol 2005, 20:33-95.
Rey A. L'examen Clinique en psychologie 1964, Presses Universitaire de France, Paris.
Riordan H.J., Flashman L.A., Roberts D.W. Neurocognitive and psychosocial correlates of ventroposterolateral pallidotomy surgery in Parkinson's disease. Neurosurg. Focus 1997, 2:1-9.
Sara S.J., Hars B. In memory of consolidation. Learn. Mem 2006, 13:515-521.
Schmand B., de Bie R.M.A., Koning-Haanstra M., de Smet J.S., Speelman J.D., van Zomeren A.H. Unilateral pallidotomy in PD: a controlled study of cognitive and behavioral effects. Neurology 2000, 54:1058-1064.
Smith K.S., Tindell A.J., Aldridge J.W., Berridge K.C. Ventral pallidum in reward and motivation. Behav. Brain Res 2009, 23:155-167.
Spaniol J., Davidson P.S.R., Kim A.S.N., Han H., Moscovitch M., Grady C.L. Event-related fMRI studies of episodic encoding and retrieval: meta-analysis using activation likelihood estimation. Neuropsychologia 2009, 47:1765-1779.
Sperling R. Functional MRI studies of associative encoding in normal aging, mild cognitive impairment, and Alzheimer's disease. Ann. N. Y. Acad. Sci 2007, 1097:146-155.
Sperling R.A., Bates J.F., Chua E.F., Cocchiarella D.M., Rentz D.M., Rosen B.R., Schacter D.L., Albert M.S. fMRI studies of associative encoding in young and elderly controls and mild Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 2003, 74:44-50.
Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev 1992, 99:195-231.
Staresina B.P., Davachi L. Selective and shared contributions of the hippocampus and perirhinal cortex to episodic item and associative encoding. J. Cogn. Neurosci 2008, 20:1478-1489.
Swainson R., Hodges J.R., Galton C.J., Semple J., Michael A., Dunn B.D., Iddon J.L., Robbins T.W., Sahakian B.J. Early detection and differential diagnosis of Alzheimer's disease and depression with neuropsychological tasks. Dement. Geriatr. Cogn. Disord 2001, 12:265-280.
Trépanier L.L., Saint-Cyr J.A., Lozano A.M., Lang A.E. Neuropsychological consequences of posteroventral pallidotomy for the treatment of Parkinson's disease. Neurology 1998, 51:207-215.
Tulving E., Colotla V.A. Free recall of trilingual lists. Cogn. Psychol 1970, 1:86-98. 10.1016/0010-0285(70)90006-X.
Watkins M.J. Concept and measurement of primary memory. Psychol. Bull 1974, 81:695-711.
Welsh K., Butters N., Hughes J., Mohs R., Heyman A. Detection of abnormal memory decline in mild cases of Alzheimer's disease using CERAD neuropsychological measures. Arch. Neurol 1991, 48:278-281.
Woodard J.L., Dunlosky J.A., Salthouse T.A. Task decomposition analysis of intertrial free recall performance on the rey auditory verbal learning test in normal aging and Alzheimer's disease. J. Clin. Exp. Neuropsychol 1999, 21:666-676.
