Contextual novelty detection and novelty-related memory enhancement in amnestic Mild Cognitive Impairment

[en] <p>Introduction: Though novelty processing plays a critical role in memory function, little is known about how it influences learning in memory-impaired populations, such as amnestic Mild Cognitive Impairment (aMCI).Methods: 21 aMCI patients and 22 age- and education-matched healthy older participants performed two tasks— (i) an oddball paradigm where fractals that were often repeated (60% of the stimuli), less frequently repeated (20%), or novel (presented once each) were shown to assess novelty preference (longer viewing time for novel than familiar stimuli), and (ii) a Von Restorff paradigm assessing novelty-related effects on memory. Participants studied 22 lists of 10 words. Among these lists, 18 contained an isolated word different from the others by its distinctive aspect, here the font size (90-point, 120-point or 150-point against 60-point for non-isolated words). The remaining four were control lists without isolated words. After studying each list, participants freely recalled the maximum words possible.Results: For the oddball task, a group-by-stimulus type ANOVA on median viewing times revealed a significant effect of stimulus type, but not of group. Both groups spent more time on novel stimuli. For the Von Restorff task, both aMCI and healthy controls recalled the isolated words (presented in 120-point or 150-point, but not 90-point) better than others (excluding primacy and recency effects). Novelty-related memory benefit—gain factor—was computed as the difference between the recall scores for isolated and other words. A group-by-font size ANOVA on gain factors revealed no group effect, nor interaction, suggesting that aMCI patients benefited from novelty, alike controls.Conclusion: Novelty preference and the boosting effect of isolation-related novelty on subsequent recall seem preserved despite impaired episodic memory in aMCI patients. This is discussed in the light of contemporary divergent theories regarding the relationship between novelty and memory, as either being independent or parts of a continuum.</p>

Disciplines :

Neurosciences & behavior

Author, co-author :

Servais, Anaïs ; Université de Liège - ULiège > GIGA > GIGA CRC In vivo Imaging - Aging & Memory

Barbeau, Emmanuel J.; Brain and Cognition Research Center, CNRS UMR5549, Toulouse, France

Bastin, Christine ; Université de Liège - ULiège > GIGA > GIGA CRC In vivo Imaging - Aging & Memory

Language :

English

Title :

Contextual novelty detection and novelty-related memory enhancement in amnestic Mild Cognitive Impairment

Publication date :

2024

Journal title :

Cortex: A Journal Devoted to the Study of the Nervous System and Behavior

ISSN :

0010-9452

eISSN :

1973-8102

Volume :

172

Pages :

72-85

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

10.31234/osf.io/6az2g

Available on ORBi :

since 15 December 2023

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Bibliography

Albert, M.S., DeKosky, S.T., Dickson, D., Dubois, B., Feldman, H.H., Fox, N.C., Phelps, C.H., The diagnosis of mild cognitive impairment due to Alzheimer's disease: Recommendations from the National Institute on aging-Alzheimer's association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimer's & Dementia: the Journal of the Alzheimer's Association 7:3 (2011), 270–279, 10.1016/j.jalz.2011.03.008.
Atkinson, R.C., Shiffrin, R.M., Human memory: A proposed system and its control processes. Spence, K.W., Spence, J.T., (eds.) The psychology of learning and motivation: Advances in re- search and theory, Vol. 2, 1968, Academic Press, New York, 89–195.
Barbeau, E.J., Chauvel, P., Moulin, C.J., Regis, J., Liégeois-Chauvel, C., Hippocampus duality: Memory and novelty detection are subserved by distinct mechanisms. Hippocampus 27:4 (2017), 405–416, 10.1002/hipo.22699.
Bastin, C., Delhaye, E., Moulin, C., Barbeau, E.J., Novelty processing and memory impairment in Alzheimer's disease: A review. Neuroscience and Biobehavioral Reviews 100 (2019), 237–249, 10.1016/j.neubiorev.2019.02.021.
Belleville, S., Ménard, M.C., Lepage, E., Impact of novelty and type of material on recognition in healthy older adults and persons with mild cognitive impairment. Neuropsychologia 49:10 (2011), 2856–2865, 10.1016/j.neuropsychologia.2011.06.011.
Bird, C.M., Davies, R.A., Ward, J., Burgess, N., Effects of pre-experimental knowledge on recognition memory. Learning & Memory 18:1 (2011), 11–14, 10.1101/lm.1952111.
Braak, H., Thal, D.R., Ghebremedhin, E., Del Tredici, K., Stages of the pathologic process in Alzheimer disease: Age categories from 1 to 100 years. Journal of Neuropathology and Experimental Neurology 70:11 (2011), 960–969, 10.1097/NEN.0b013e318232a379.
Brown, M.W., Bashir, Z.I., Evidence concerning how neurons of the perirhinal cortex may affect familiarity discrimination. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences 357:1424 (2002), 1083–1095, 10.1098/rstb.2002.1097.
Chau, S.A., Herrmann, N., Eizenman, M., Chung, J., Lanctôt, K.L., Exploring visual selective attention towards novel stimuli in Alzheimer's disease patients. Dementia and Geriatric Cognitive Disorders Extra 5:3 (2015), 492–502 0.1159/000442383.
Chau, S.A., Herrmann, N., Sherman, C., Chung, J., Eizenman, M., Kiss, A., Lanctôt, K.L., Visual selective attention toward novel stimuli predicts cognitive decline in Alzheimer's disease patients. Journal of Alzheimer's disease 55:4 (2017), 1339–1349, 10.3233/JAD-160641.
Crutcher, M.D., Calhoun-Haney, R., Manzanares, C.M., Lah, J.J., Levey, A.I., Zola, S.M., Eye tracking during a visual paired comparison task as a predictor of early dementia. American Journal of Alzheimer's Disease and Other Dementias 24:3 (2009), 258–266, 10.1177/1533317509332093.
Cunha, C., Guerreiro, M., de Mendonca, A., Oliveira, P.E., Santana, I., Serial position effects in Alzheimer's disease, mild cognitive impairment, and normal aging: Predictive value for conversion to dementia. Journal of Clinical and Experimental Neuropsychology 34:8 (2012), 841–852, 10.1080/13803395.2012.689814.
Daffner, K.R., Chong, H., Riis, J., Rentz, D.M., Wolk, D.A., Budson, A.E., Holcomb, P.J., Cognitive status impacts age-related changes in attention to novel and target events in normal adults. Neuropsychology 21:3 (2007), 291–300, 10.1037/0894-4105.21.3.291.
Daffner, K.R., Rentz, D.M., Scinto, L.F., Faust, R., Budson, A.E., Holcomb, P.J., Pathophysiology underlying diminished attention to novel events in patients with early AD. Neurology 56:10 (2001), 1377–1383, 10.1212/wnl.56.10.1377.
Davelaar, E.J., A novelty-induced change in episodic (NICE) context account of primacy effects in free recall. Psychology (Savannah, Ga.) 4:9 (2013), 695–703, 10.4236/psych.2013.49099.
Faul, F., Erdfelder, E., Lang, A.-G., Buchner, A., G∗Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods 39 (2007), 175–191, 10.3758/BF03193146.
Ferrand, L., New, B., Brysbaert, M., Keuleers, E., Bonin, P., Méot, A., Augustinova, M., Pallier, C., The French Lexicon project: Lexical decision data for 38,840 French words and 38,840 pseudowords. Behavior Research Methods 42:2 (2010), 488–496, 10.3758/BRM.42.2.488.
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. Journal of Psychiatric Research 12:3 (1975), 189–198, 10.1016/0022-3956(75)90026-6.
Frank, D., Kafkas, A., Expectation-driven novelty effects in episodic memory. Neurobiology of Learning and Memory, 183, 2021, 107466, 10.1016/j.nlm.2021.107466.
GREFEX, Groupe de Réflexion sur l'Evaluation des Fonctions exécutives. L'évaluation des fonctions exécutives en pratique clinique. Revue de Neuropsychologie 11 (2001), 383–434.
Grober, E., Buschke, H., Genuine memory deficits in dementia. Developemental Neuropsychology 3 (1987), 13–36.
Howieson, D.B., Mattek, N., Seeyle, A.M., Dodge, H.H., Wasserman, D., Zitzelberger, T., Jeffrey, K., Serial position effects in mild cognitive impairment. Journal of Clinical and Experimental Neuropsychology 33:3 (2011), 292–299, 10.1080/13803395.2010.516742.
Hunt, R.R., The subtlety of distinctiveness: What von Restorff really did. Psychonomic Bulletin & Review 2:1 (1995), 105–112, 10.3758/bf03214414.
Jonin, P.Y., Duche, Q., Bannier, E., Corouge, I., Ferre, J.C., Belliard, S., Barbeau, E.J., Building memories on prior knowledge: Behavioral and fMRI evidence of impairment in early Alzheimer's disease. Neurobiology of Aging 110 (2022), 1–12, 10.1016/j.neurobiolaging.2021.10.013.
Kafkas, A., Montaldi, D., Two separate, but interacting, neural systems for familiarity and novelty detection: A dual-route mechanism. Hippocampus 24:5 (2014), 516–527, 10.1002/hipo.22241.
Kafkas, A., Montaldi, D., How do memory systems detect and respond to novelty?. Neuroscience Letters 680 (2018), 60–68, 10.1016/j.neulet.2018.01.053.
Kishiyama, M.M., Yonelinas, A.P., Lazzara, M.M., The von Restorff effect in amnesia: The contribution of the hippocampal system to novelty-related memory enhancements. Journal of Cognitive Neuroscience 16:1 (2004), 15–23, 10.1162/089892904322755511.
Klever, L., Islam, J., Võ, M.L.H., Billino, J., Effects of prior knowledge on memory for objects in real-world scenes: Schema violations benefit memory and metacognitive performance. Journal of Vision, 21(9), 2021, 1950, 10.1167/jov.21.9.1950 1950.
Kumaran, D., Maguire, E.A., Match mismatch processes underlie human hippocampal responses to associative novelty. The Journal of Neuroscience 27:32 (2007), 8517–8524, 10.1523/JNEUROSCI.1677-07.2007.
Lorents, A., Ruitenberg, M.F.L., Schomaker, J., Novelty-induced memory boosts in humans: The when and how. Heliyon, 9(3), 2023, e14410, 10.1016/j.heliyon.2023.e14410.
Mathôt, S., Schreij, D., Theeuwes, J., OpenSesame: An open-source, graphical experiment builder for the social sciences. Behavior Research Methods 44:2 (2012), 314–324, 10.3758/s13428-011-0168-7.
McKhann, G.M., Knopman, D.S., Chertkow, H., Hyman, B.T., Jack, C.R. Jr., Kawas, C.H., Klunk, W.E., Koroshetz, W.J., Manly, J.J., Mayeux, R., Mohs, R.C., Morris, J.C., Rossor, M.N., Scheltens, P., Carrillo, M.C., Thies, B., Weintraub, S., Phelps, C.H., The diagnosis of dementia due to Alzheimer's disease: Recommendations from the National Institute on aging-Alzheimer's association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimer's & dementia : the journal of the Alzheimer's Association 7:3 (2011), 263–269, 10.1016/j.jalz.2011.03.005.
Nie, J., Qiu, Q., Phillips, M., Sun, L., Yan, F., Lin, X., Li, X., Early diagnosis of mild cognitive impairment based on eye movement parameters in an aging Chinese population. Frontiers in Aging Neuroscience, 12, 2020, 221, 10.3389/fnagi.2020.00221.
Petersen, R.C., Negash, S., Mild cognitive impairment: An overview. CNS Spectrums 13:1 (2008), 45–53, 10.1017/s1092852900016151.
Petersen, R.C., Roberts, R.O., Knopman, D.S., Boeve, B.F., Geda, Y.E., Ivnik, R.J., Jack, C.R. Jr., Mild cognitive impairment: Ten years later. Archives of Neurology 66:12 (2009), 1447–1455, 10.1001/archneurol.2009.266.
Quent, J.A., Henson, R.N., Greve, A., A predictive account of how novelty influences declarative memory. Neurobiology of Learning and Memory, 179, 2021, 107382, 10.1016/j.nlm.2021.107382.
Quintana, D.S., Williams, D.R., Bayesian alternatives for common null-hypothesis significance tests in psychiatry: A non-technical guide using JASP. BMC Psychiatry, 18(1), 2018, 178, 10.1186/s12888-018-1761-4.
Reichardt, R., Polner, B., Simor, P., Novelty manipulations, memory performance, and predictive coding: The role of unexpectedness. Frontiers in Human Neuroscience, 14, 2020, 152, 10.3389/fnhum.2020.00152.
Reichardt, R., Polner, B., Simor, P., The graded novelty encoding task: Novelty gradually improves recognition of visual stimuli under incidental learning conditions. Behavior Research Methods 55 (2022), 1587–1600, 10.3758/s13428-022-01891-8.
Schomaker, J., Unexplored territory: Beneficial effects of novelty on memory. Neurobiology of Learning and Memory 161 (2019), 46–50, 10.1016/j.nlm.2019.03.005.
Schomaker, J., Meeter, M., Short- and long-lasting consequences of novelty, deviance and surprise on brain and cognition. Neuroscience and Biobehavioral Reviews 55 (2015), 268–279, 10.1016/j.neubiorev.2015.05.002.
Schomaker, J., van Bronkhorst, M.L., Meeter, M., Exploring a novel environment improves motivation and promotes recall of words. Frontiers in Psychology, 5, 2014, 918, 10.3389/fpsyg.2014.00918.
Schomaker, J., Wittmann, B.C., Effects of active exploration on novelty-related declarative memory enhancement. Neurobiology of Learning and Memory, 179, 2021, 107403, 10.1016/j.nlm.2021.107403.
St-Hilaire, A., Hudon, C., Vallet, G.T., Bherer, L., Lussier, M., Gagnon, J.F., Macoir, J., Normative data for phonemic and semantic verbal fluency test in the adult French–Quebec population and validation study in Alzheimer's dis- ease and depression. The Clinical Neuropsychologist 30:7 (2016), 1126–1150, 10.1080/13854046.2016.1195014.
Stroop, J.R., Studies of interference in serial verbal reactions. The Journal of Economic Perspectives: a Journal of the American Economic Association 18 (1935), 643–662.
Tulving, E., Kroll, N., Novelty assessment in the brain and long-term memory encoding. Psychonomic Bulletin & Review 2:3 (1995), 387–390, 10.3758/bf03210977.
Tulving, E., Rosenbaum, R.S., What do explanations of the distinctiveness effect need to explain?. Hunt, R.R., Worthen, J.B., (eds.) Distinctiveness and memory, 2006, Oxford University Press, New York, NY, 407–423.
Underwood, G., Perceptual distinctiveness and proactive interference in the primacy effect. The Quarterly Journal of Experimental Psychology: QJEP 27:2 (1975), 289–294, 10.1080/14640747508400487.
Vitali, P., Minati, L., Chiarenza, G., Brugnolo, A., Girtler, N., Nobili, F., De Leo, C., Rosati, P., Rodriguez, G., The Von Restorff effect in ageing and Alzheimer's disease. Neurological sciences : Official Journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology 27:3 (2006), 166–172, 10.1007/s10072-006-0662-3.
Võ, M.L.H., The meaning and structure of scenes. Vision Research 181 (2021), 10–20, 10.1016/j.visres.2020.11.003.
Von Restorff, H., Uber die Wirkung von Bereichsbildungen im Spurenfeld [The effects of field formation in the trace field]. Psychologische Forschung 18 (1933), 199–234.