[en] BACKGROUND: Encoding of new information is considered to be impossible in people with Alzheimer's disease (PWAD) at a moderate to severe stage. However, a few case studies reported new learning under special circumstances, especially with music.
OBJECTIVE: This article aims at clarifying PWAD's learning capacities toward unknown material under more ecological settings, which is repeated exposure without encoding instruction.
METHODS: Twenty-three PWAD (Age: m = 84.6(5.2), 5≤MMSE≤19) underwent presentations of unknown artistic pieces (targets) through 8 daily individual sessions. These sessions were followed by a test session, during which their knowledge of the targets was assessed through a verbal and behavioral scale (the sense of familiarity scale) against a series of unknown items (distractors).
RESULTS: Through this design, we were able to objectify encoding of three types of targets (verses, paintings, and music) against distractors the day after exposure sessions, and 2 months after the last presentation (study 1). Music and paintings were eventually well-encoded by most participants, whereas poems encoding was poorer. When compared to distractors, target items were significantly better recognized. We then compared the recognition of target paintings against two types of painting distractors, either perceptually or semantically related (study 2). The targets were better recognized than all three painting distractors, even when they were very close to the targets.
CONCLUSION: Despite massive anterograde amnesia, our results clearly showed that recognition-based learning without conscious memory of the encoding context is preserved in PWAD at a severe stage, revealed through an increasing sense of familiarity following repeated exposure. These findings could open new perspective both for researchers and clinicians and improve the way we understand and care for PWAD living in healthcare facilities.
Disciplines :
Neurosciences & behavior
Author, co-author :
Coppalle, Renaud ; Université de Liège - ULiège > GIGA > GIGA CRC In vivo Imaging - Aging & Memory ; Normandie Univ, UNICAEN, PSL Université Paris, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France
Mauger, Caroline; Normandie Univ, UNICAEN, PSL Université Paris, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France
Quernet, Sophie; Les Pervenches, Groupe Hom'Ageinstitution>, Biéville-Beuville, France
Dewald, Axel; Les Pervenches, Groupe Hom'Ageinstitution>, Biéville-Beuville, France
Letortu, Odile; Les Pervenches, Groupe Hom'Ageinstitution>, Biéville-Beuville, France
Desgranges, Béatrice; Normandie Univ, UNICAEN, PSL Université Paris, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France
Groussard, Mathilde; Normandie Univ, UNICAEN, PSL Université Paris, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France
Platel, Hervé; Normandie Univ, UNICAEN, PSL Université Paris, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France
Language :
English
Title :
New Long-Term Encoding in Severely Amnesic Alzheimer's Disease Patients Revealed Through Repeated Exposure to Artistic Items.
New paradigms relying on sense of familiarity preservation may thus be important for both diagnosis and care, as they could provide a more accurate view of what PWAD until an advanced stage can still do, and within which modalities. By having this kind of information, care facilities could be designed to encourage the emergence of sense of familiarity for example, and therefore allow a faster and smoother integration in specialized care units for PWAD. More precisely, finding ways to increase SoF faster may help alleviate the burden of both residents and caregivers while confronted with a new entry into such care facilities. Hence, some familiarization to settings, places and people could be performed in order to prepare PWAD for entering into a care facility, making it a more “familiar” place, and diminishing anxiety and associated behavioral troubles. Possible applications also involve preparing PWAD for excursions. An application towards caregivers would be the possibility of using familiarity-based learning as a lever to modify caregivers’ and families’ conception of PWAD, especially regarding the This work was supported by a FEDER (Fonds Européen de Développement Régional) grant of Nor-mandie(n◦2889/33527). The authors would like to thank the “Hom’Age” Retirement Houses group for opening their doors to our research team. Many thanks to Rocio Gonzales, Alice Breton, Sauvane Carrière for data gathering and helping creating the protocols. Finally, the authors would like to acknowledge Mathilde Thomas for extensive research on bibliography about learning in AD, Marty Fiati and Melanie Ambler for Proof reading, and Sebastien Polvent and Mickaël Laisney for their help on the statistical analyses.
Weintraub S, Wicklund AH, Salmon DP (2012) The neuropsychological profile of Alzheimer disease. Cold Spring Harb Perspect Med 2, a006171.
Dubois B, Feldman HH, Jacova C, Hampel H, Molinuevo JL, BlennowK, Dekosky ST, Gauthier S, Selkoe D, Bateman R, Cappa S, Crutch S, Engelborghs S, Frisoni GB, Fox NC, Galasko D, Habert MO, Jicha GA, Nordberg A, Pasquier F, Rabinovici G, Robert P, Rowe C, Salloway S, Sarazin M, Epelbaum S, de Souza LC, Vellas B, Visser PJ, Schneider L, Stern Y, Scheltens P, Cummings JL (2014) Advancing research diagnostic criteria for Alzheimer's disease: The IWG-2 criteria. Lancet Neurol 13, 614-629.
Grober E, Buschke H, Crystal H, Bang S, Dresner R (1988) Screening for dementia by memory testing. Neurology 38, 900-903.
Nestor PJ, Fryer TD, Hodges JR (2006) Declarative memory impairments in Alzheimer's disease and semantic dementia. Neuroimage 30, 1010-1020.
Schacter DL (1987) Implicit memory: History and current status. J Exp Psychol Learn Mem Cogn 13, 501-518.
Zajonc RB (1980) Feeling and thinking: Preferences need no inferences. Am Psychol 35, 151-175.
Willems S, Adam S, Van der LindenM(2002) Normal mere exposure effect with impaired recognition in Alzheimer's disease. Cortex 38, 77-86.
Deason RG, Strong JV, Tat MJ, Simmons-Stern NR, Budson AE (2019) Explicit and implicit memory for music in healthy older adults and patients with mild Alzheimer's disease. J Clin Exp Neuropsychol 41, 158-169.
Kessels RPC, Remmerswaal M, Wilson BA (2011) Assessment of nondeclarative learning in severe Alzheimer dementia. Alzheimer Dis Assoc Disord 25, 179-183.
Willems S, Salmon E, Van der Linden M (2008) Implicit/explicit memory dissociation in Alzheimer's disease: The consequence of inappropriate processing Neuropsychology 22, 710-717.
HenkeK(2010)Amodel for memory systems based on processing modes rather than consciousness. Nat Rev Neurosci 11, 523-532.
Tulving E, Hayman CAG, Macdonald CA (1991) Longlasting perceptual priming and semantic learning in amnesia: A case experiment. J Exp Psychol Learn Mem Cogn 17, 595-617.
Baird A, Umbach H, Thompson WF (2017) A nonmusician with severe Alzheimer's dementia learns a new song. Neurocase 23, 36-40.
Sharon T, Moscovitch M, Gilboa A (2011) Rapid neocortical acquisition of long-term arbitrary associations independent of the hippocampus. Proc Natl Acad Sci U S A 108, 1146-1151.
Norberg A, Melin E, Asplund K (1986) Reactions to music, touch and object presentation in the final stage of dementia. An exploratory study. Int J Nurs Stud 23, 315-323.
Gagnon L, Peretz I, Fulop T (2009) Musical structural determinants of emotional judgments in dementia of the Alzheimer type. Neuropsychology 23, 90-97.
Ueda T, Suzukamo Y, Sato M, Izumi S-I (2013) Effects of music therapy on behavioral and psychological symptoms of dementia:Asystematic reviewand meta-analysis. Ageing Res Rev 12, 628-641.
Sixsmith A, Gibson G (2007) Music and the wellbeing of people with dementia. Ageing Soc 27, 127-145.
Groussard M, Mauger C, Platel H (2013) Lamemoire musicale a long terme au cours de l'evolution de la maladie d'Alzheimer. Geriatr Psychol Neuropsychiatr Vieil 11, 99-109.
Groussard M, Chan TG, Coppalle R, PlatelH(2019) Preservation of musical memory throughout the progression of Alzheimer's disease Toward a reconciliation of theoretical, clinical, and neuroimaging evidence. J Alzheimers Dis 68, 857-883.
Fraile E, Bernon D, Rouch I, Pongan E, Tillmann B, Leveque Y (2019) The effect of learning an individualized song on autobiographical memory recall in individuals with Alzheimer's disease:Apilot study. J Clin Exp Neuropsychol 41, 760-768.
Samson S, Dellacherie D, Platel H (2009) Emotional power of music in patients with memory disorders: Clinical implications of cognitive neuroscience. Ann N Y Acad Sci 1169, 245-255.
Platel H, Groussard M (2014) La musique et la peinture comme revelateurs de capacites d'apprentissages preservees chez des patients Alzheimer a un stade modere a severe. In Neuropsychologie et Art pp. 396.
Perneczky R,Wagenpfeil S, Komossa K, Grimmer T, Diehl J, Kurz A (2006) Mapping scores onto stages: MiniMental State Examination and Clinical Dementia Rating. Am J Geriatr Psychiatry 14, 139-144.
McKhannGM(2011) Changing concepts of Alzheimer disease. JAMA 305, 2458-2459.
Reisberg B, Jamil IA, Khan S, Monteiro I, Torossian C, Ferris S, Sabbagh M, Gauthier S, Auer S, Shulman MB, Kluger A, Franssen E,Wegiel J (2010) Staging dementia. In Principles and Practice of Geriatric Psychiatry 3rd edition, Abou-SalehMT, Katona C,Kumar A, eds.Wiley,NewYork, pp. 162-169.
Coppalle R, Mauger C, Hommet M, Segobin S, Letortu O, De la Sayette V, Quillard A, Eustache F, Desgranges B, Platel H, Groussard M (2019) Recognition-based memory through familiarity assessment in severe Alzheimer's disease. Brain Cogn 137, 103639.
O'ConnorMK,AllyBA(2010) Using stimulus form change to understand memorial familiarity for pictures and words in patients with mild cognitive impairment and Alzheimer's disease. Neuropsychologia 48, 2068-2074.
Fritz CO, Morris PE, Richler JJ (2012) Effect size estimates: Current use, calculations, and interpretation. J Exp Psychol Gen 141, 2-18.
Folstein MF, Folstein SE, McHugh PR (1975) "Minimental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12, 189-198.
Signoret JL, Allard M, Benoit N, Bolgert F, Bonvarlet M, Eustache F (1999) B.E.C. 96: Evaluation des troubles de memoire et des desordres cognitifs associes IPSEN, Paris.
De Partz MP, BilocqV, DeWildeV(2001) Lexis: Tests pour le diagnostic des troubles lexicaux chez le patient aphasique Solal, Marseille.
Platel H, Groussard M (2010) La memoire semantique musicale: Apport des donnees de la neuropsychologie clinique et de la neuro-imagerie fonctionnelle. Rev Neuropsychol 2, 61-69.
Peck KJ, Girard TA, Russo FA, Fiocco AJ (2016) Music and memory in Alzheimer's disease and the potential underlying mechanisms. J Alzheimers Dis 51, 949-959.
Delgado C,MunozNeira C, Soto A, Martinez M, Henriquez F, Flores P, SlachevskyA(2016) Comparison of the psychometric properties of the "word" and "picture" versions of the Free and Cued Selective Reminding Test in a Spanishspeaking cohort of patients with mild Alzheimer's disease and cognitively healthy controls. Arch Clin Neuropsychol 13, 165-175.
Slattery CF, Agustus JL, Paterson RW, McCallion O, Foulkes AJM, Macpherson K, Carton AM, Harding E, Golden HL, Jaisin K, Mummery CJ, Schott JM,Warren JD (2019) The functional neuroanatomy of musical memory in Alzheimer's disease. Cortex 115, 357-370.
Ally BA, Gold CA, Budson AE (2009) An evaluation of recollection and familiarity in Alzheimer's disease and mild cognitive impairment using receiver operating characteristics. Brain Cogn 69, 504-513.
Kohler S, Moscovitch M,Winocur G, McIntosh AR (2000) Episodic encoding and recognition of pictures and words: Role of the human medial temporal lobes. Acta Psychol (Amst) 105, 159-179.
Deloche G, HannequinD(1997) Test de denomination orale d'images: DO80 Centre de Psychologie appliquee, Paris.
Barbeau E, Didic M, Tramoni E, Felician O, Joubert S, Sontheimer A, Ceccaldi M, Poncet M (2004) Evaluation of visual recognition memory in MCI patients. Neurology 62, 1317-1322.
Westerberg CE, Paller KA, Weintraub S, Mesulam MM, Mayes AR, Holdstock JS, Reber PJ (2006) When memory does not fail: Familiarity-based recognition in mild cognitive impairment and Alzheimer's disease. Neuropsychology 20, 193-205.
Ellis M, Astell A (2017) Communicating with people living with dementia who are nonverbal: The creation of Adaptive Interaction. PLoS One 12, 2-3.
Halpern AR, O'Connor MG (2000) Implicit memory for music in Alzheimer's disease. Neuropsychology 14, 391-397.
Son GR, Therrien B, Whall A (2002) Implicit memory and familiarity among elders with dementia. J Nurs Scholarsh 34, 263-267.
Barbeau E (2011) Les modeles de la memoire: Approche anatomo-fonctionnelle et representationnelle hierarchique. Rev Neuropsychol 3, 104-111.
Yonelinas AP (2002) The nature of recollection and familiarity: A review of 30 years of research. J Mem Lang 46, 441-517.
Eichenbaum H, Yonelinas AP, Ranganath C (2007) The medial temporal lobe and recognition memory. Annu Rev Neurosci 30, 123-152.
Tulving E (1985) How many memory systems are there Am Psychol 40, 385-398.
Holdstock J (2002) Differential involvement of the hippocampus and temporal lobe cortices in rapid and slow learning of new semantic information. Neuropsychologia 40, 748-768.
Guillery B, Desgranges B, Katis S, De La Sayette V, Viader F, Eustache F (2001) Semantic acquisition without memories: Evidence from transient global amnesia. Neuroreport 12, 3865-3869.
Pitel AL, Beaunieux H, GuilleryGirard B,Witkowski T, de la Sayette V, Viader F, Desgranges B, Eustache F (2009) How do Korsakoff patients learn new concepts Neuropsychologia 47, 879-886.
Gold JJ, Squire LR (2005) Quantifying medial temporal lobe damage in memory-impaired patients. Hippocampus 15, 79-85.
Stark E. C, Bayley P, SquireLR(2002) Recognition memory for single items and for associations is similarly impaired following damage to the hippocampal region. Learn Mem 9, 238-242.
Kitchener EG, Hodges JR, McCarthy R (1998) Acquisition of post-morbid vocabulary and semantic facts in the absence of episodic memory. Brain 121, 1313-1327.
Eichenbaum H (2004) Hippocampus: Cognitive processes and neural representations that underlie declarative memory. Neuron 44, 109-120.
Anderson ND, Craik FIM (2006) The mnemonic mechanisms of errorless learning. Neuropsychologia 44, 2806-2813.
BaddeleyA,WilsonBA(1994)Whenimplicit learning fails: Amnesia and the problem of error elimination. Neuropsychologia 32, 53-68.
Komatsu SI, Mimura M, Kato M, Wakamatsu N, Kashima H (2000) Errorless and effortful processes involved in the learning of face-name associations by patients with alcoholic Korsakoff's syndrome. Neuropsychol Rehabil 10, 113-132.
Ehri LC, McCormick S (1998) Phases of word learning: Implications for instruction with delayed and disabled readers. Read Writ Q 14, 135-163.
LaBerge D, Samuels SJ (1974) Toward a theory of automatic information processing in reading. Cogn Psychol 6, 293-323.
Oliveira A, Pereira FC, Cardoso A (2001) Automatic reading and learning from text. In Proceedings of the International Symposium on Artificial Intelligence (ISAI'2001) pp. 1-12.