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Lost or unavailable? Exploring mechanisms that affect retrograde memory in mild cognitive impairment and Alzheimer's disease patients

Abstract

Retrograde amnesia has been largely documented in patients with amnestic mild cognitive impairment (a-MCI) and Alzheimer’s disease (AD). However, it is still not clear whether ineffectiveness in recalling past acquired information reflects loss of individual memory traces or failure to access specific stored traces. We aimed to disentangle the differential contribution of storage and retrieval processes to the pattern of retrograde amnesia in these patients. This issue was investigated in 18 a-MCI and 19 AD patients who were compared to 20 healthy controls. A novel questionnaire about public events was used; it consisted of two procedures (i.e., a free recall test and a true/false recognition test). Crucial differences emerged in the way the two groups of patients performed the experimental tasks. In fact, although both a-MCI and AD patients showed a similar pattern of impairment on the free recall test, a-MCI patients were able to normalise their performance on the recognition test, thus overcoming their deficits at the time of recall. Conversely, AD patients showed both reduced free recall ability and diminished sensitivity to benefit from recognition in recalling public events. Our findings suggest that the memory processes underlying RA were different for a-MCI and AD. Deficits in remote memory are prevalently explained by impaired retrieval abilities in a-MCI and by impaired storage in AD. This distinction between retrograde amnesia due to defective trace utilisation in a-MCI and trace storage in AD is consistent with the temporal unfolding of declining anterograde memory over the course of disease progression to AD.

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References

  1. 1.

    Dubois B, Feldman H, Jacova C, DeKosky S, Barberger-Gateau P, Cummings J, Delacourte A, Galasko D, Gauthier S, Jicha G, Meguro K, O'Brien J, Pasquier F, Robert P, Rossor M, Salloway S, Stern Y, Visser P, Scheltens P (2007) Research criteria for the diagnosis of Alzheimer's disease: revising the NINCDS–ADRDA criteria. Lancet Neurol 6:734–746. https://doi.org/10.1016/s1474-4422(07)70178-3

  2. 2.

    Albert M, DeKosky S, Dickson D, Dubois B, Feldman H, Fox N, Gamst A, Holtzman D, Jagust W, Petersen R, Snyder P, Carrillo M, Thies B, Phelps C (2011) 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 Dement 7:270–279. https://doi.org/10.1016/j.jalz.2011.03.008

  3. 3.

    Tierney M, Black S, Szalai J, Snow W, Fisher R, Nadon G, Chui H (2001) Recognition memory and verbal fluency differentiate probable Alzheimer disease from subcortical ischemic vascular dementia. Arch Neurol 58:1654. https://doi.org/10.1001/archneur.58.10.1654

  4. 4.

    Glosser G, Gallo J, Clark C, Grossman M (2002) Memory encoding and retrieval in frontotemporal dementia and Alzheimer's disease. Neuropsychology 16:190–196. https://doi.org/10.1037/0894-4105.16.2.190

  5. 5.

    Fine E, Delis D, Wetter S, Jacobson M, Hamilton J, Peavy G, Goldstein J, McDonald C, Corey-Bloom J, Bondi M, Salmon D (2008) Identifying the “source” of recognition memory deficits in patients with Huntington's disease or Alzheimer's disease: evidence from the CVLT-II. J Clin Exp Neuropsychol 30:463–470. https://doi.org/10.1080/13803390701531912

  6. 6.

    Carlesimo G, Perri R, Caltagirone C (2010) Category cued recall following controlled encoding as a neuropsychological tool in the diagnosis of Alzheimer’s disease: a review of the evidence. Neuropsychol Rev 21:54–65. https://doi.org/10.1007/s11065-010-9153-7

  7. 7.

    Ricci M, Graef S, Blundo C, Miller L (2012) Using the rey auditory verbal learning test (RAVLT) to differentiate Alzheimer's dementia and behavioural variant fronto-temporal dementia. Clin Neuropsychol 26:926–941. https://doi.org/10.1080/13854046.2012.704073

  8. 8.

    Perri R, Fadda L, Caltagirone C, Carlesimo G (2013) Word list and story recall elicit different patterns of memory deficit in patients with Alzheimer's disease, frontotemporal dementia, subcortical ischemic vascular disease, and lewy body dementia. J Alzheimer's Dis 37:99–107. https://doi.org/10.3233/JAD-130347

  9. 9.

    Lemos R, Duro D, Simoes M, Santana I (2014) The free and cued selective reminding test distinguishes frontotemporal dementia from Alzheimer's disease. Arch Clin Neuropsychol 29:670–679. https://doi.org/10.1093/arclin/acu031

  10. 10.

    Teichmann M, Epelbaum S, Samri D, Levy Nogueira M, Michon A, Hampel H, Lamari F, Dubois B (2017) Free and cued selective reminding test – accuracy for the differential diagnosis of Alzheimer's and neurodegenerative diseases: a large-scale biomarker-characterized monocenter cohort study (ClinAD). Alzheimer's Dement 13:913–923. https://doi.org/10.1016/j.jalz.2016.12.014

  11. 11.

    Braak H, Braak E (1995) Staging of alzheimer's disease-related neurofibrillary changes. Neurobiol Aging 16:271–278. https://doi.org/10.1016/0197-4580(95)00021-6

  12. 12.

    Du AT, Schuff N, Amend D, Laakso MP, Hsu YY, Jagust WJ, Yaffe K, Kramer JH, Reed B, Norman D, Chui HC, Chui HC (2001) Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer's disease. J Neurol Neurosurg Psychiatry 71:441–447. https://doi.org/10.1136/jnnp.71.4.441

  13. 13.

    Devanand D, Pradhaban G, Liu X, Khandji A, De Santi S, Segal S, Rusinek H, Pelton G, Honig L, Mayeux R, Stern Y, Tabert M, de Leon M (2007) Hippocampal and entorhinal atrophy in mild cognitive impairment: prediction of Alzheimer disease. Neurology 68:828–836. https://doi.org/10.1212/01.wnl.0000256697.20968.d7

  14. 14.

    Squire L, Stark C, Clark R (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306. https://doi.org/10.1146/annurev.neuro.27.070203.144130

  15. 15.

    Sarazin M, Berr C, De Rotrou J, Fabrigoule C, Pasquier F, Legrain S, Michel B, Puel M, Volteau M, Touchon J, Verny M, Dubois B (2007) Amnestic syndrome of the medial temporal type identifies prodromal AD: a longitudinal study. Neurology 69:1859–1867. https://doi.org/10.1212/01.wnl.0000279336.36610.f7

  16. 16.

    De Simone M, Perri R, Fadda L, De Tollis M, Turchetta C, Caltagirone C, Carlesimo G (2017) Different deficit patterns on word lists and short stories predict conversion to Alzheimer’s disease in patients with amnestic mild cognitive impairment. J Neurol 264:2258–2267. https://doi.org/10.1007/s00415-017-8623-8

  17. 17.

    De Simone M, Perri R, Fadda L, Caltagirone C, Carlesimo G (2019) Predicting progression to Alzheimer’s disease in subjects with amnestic mild cognitive impairment using performance on recall and recognition tests. J Neurol 266:102–111. https://doi.org/10.1007/s00415-018-9108-0

  18. 18.

    Lemos R, Marôco J, Simões M, Santiago B, Tomás J, Santana I (2015) The free and cued selective reminding test for predicting progression to Alzheimer's disease in patients with mild cognitive impairment: a prospective longitudinal study. J Neuropsychol 11:40–55. https://doi.org/10.1111/jnp.12075

  19. 19.

    Russo M, Campos J, Vázquez S, Sevlever G, Allegri R (2017) Adding Recognition discriminability index to the delayed recall is useful to predict conversion from mild cognitive impairment to Alzheimer's disease in the alzheimer's disease neuroimaging initiative. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2017.00046

  20. 20.

    Grande G, Vanacore N, Vetrano D, Cova I, Rizzuto D, Mayer F, Maggiore L, Ghiretti R, Cucumo V, Mariani C, Cappa S, Pomati S (2018) Free and cued selective reminding test predicts progression to Alzheimer’s disease in people with mild cognitive impairment. Neurol Sci 39:1867–1875. https://doi.org/10.1007/s10072-018-3507-y

  21. 21.

    Apostolova L, Dutton R, Dinov I, Hayashi K, Toga A, Cummings J, Thompson P (2006) Conversion of mild cognitive impairment to Alzheimer disease predicted by hippocampal atrophy maps. Arch Neurol 63:693. https://doi.org/10.1001/archneur.63.5.693

  22. 22.

    Ferreira L, Diniz B, Forlenza O, Busatto G, Zanetti M (2011) Neurostructural predictors of Alzheimer's disease: a meta-analysis of VBM studies. Neurobiol Aging 32:1733–1741. https://doi.org/10.1016/j.neurobiolaging.2009.11.008

  23. 23.

    Yang J, Pan P, Song W, Huang R, Li J, Chen K, Gong Q, Zhong J, Shi H, Shang H (2012) Voxelwise meta-analysis of gray matter anomalies in Alzheimer's disease and mild cognitive impairment using anatomic likelihood estimation. J Neurol Sci 316:21–29. https://doi.org/10.1016/j.jns.2012.02.010

  24. 24.

    Scarpazza C, De Simone M (2016) Voxel-based morphometry: current perspective. Neurosci Neuroecon 5:19–35. https://doi.org/10.2147/nan.s66439

  25. 25.

    Perri R, Carlesimo G, Serra L, Caltagirone C (2009) When the amnestic mild cognitive impairment disappears. Cognit Behav Neurol 22:109–116. https://doi.org/10.1097/wnn.0b013e3181a7225c

  26. 26.

    Grober E, Veroff A, Lipton R (2018) Temporal unfolding of declining episodic memory on the free and cued selective reminding test in the predementia phase of Alzheimer's disease: implications for clinical trials. Alzheimer's Dement 10:161–171. https://doi.org/10.1016/j.dadm.2017.12.004

  27. 27.

    Greene J, Hodges J, Baddeley A (1995) Autobiographical memory and executive function in early dementia of Alzheimer type. Neuropsychologia 33:1647–1670. https://doi.org/10.1016/0028-3932(95)00046-1

  28. 28.

    Hou C, Miller B, Kramer J (2005) Patterns of autobiographical memory loss in dementia. Int J Geriatr Psychiatry 20:809–815. https://doi.org/10.1002/gps.1361

  29. 29.

    Ivanoiu A, Cooper J, Shanks M, Venneri A (2006) Patterns of impairment in autobiographical memory in the degenerative dementias constrain models of memory. Neuropsychologia 44:1936–1955. https://doi.org/10.1016/j.neuropsychologia.2006.01.030

  30. 30.

    Leyhe T, Müller S, Milian M, Eschweiler G, Saur R (2009) Impairment of episodic and semantic autobiographical memory in patients with mild cognitive impairment and early Alzheimer's disease. Neuropsychologia 47:2464–2469. https://doi.org/10.1016/j.neuropsychologia.2009.04.018

  31. 31.

    El Haj M, Postal V, Le Gall D, Allain P (2011) Directed forgetting of autobiographical memory in mild Alzheimer's disease. Memory 19:993–1003. https://doi.org/10.1080/09658211.2011.626428

  32. 32.

    El Haj M, Antoine P, Nandrino J, Kapogiannis D (2015) Autobiographical memory decline in Alzheimer’s disease, a theoretical and clinical overview. Ageing Res Rev 23:183–192. https://doi.org/10.1016/j.arr.2015.07.001

  33. 33.

    De Simone M, Fadda L, Perri R, Aloisi M, Caltagirone C, Carlesimo G (2016) Does retrieval frequency account for the pattern of autobiographical memory loss in early Alzheimer's disease patients? Neuropsychologia 80:194–200. https://doi.org/10.1016/j.neuropsychologia.2015.11.024

  34. 34.

    Serra L, Bozzali M, Fadda L, De Simone M, Bruschini M, Perri R, Caltagirone C, Carlesimo G (2018) The role of hippocampus in the retrieval of autobiographical memories in patients with amnestic mild cognitive impairment due to Alzheimer's disease. J Neuropsychol. https://doi.org/10.1111/jnp.12174

  35. 35.

    Kirk M, Berntsen D (2018) A short cut to the past: cueing via concrete objects improves autobiographical memory retrieval in Alzheimer's disease patients. Neuropsychologia 110:113–122. https://doi.org/10.1016/j.neuropsychologia.2017.06.034

  36. 36.

    Kirk M, Berntsen D (2018) The life span distribution of autobiographical memory in Alzheimer’s disease. Neuropsychology 32:906–919. https://doi.org/10.1037/neu0000486

  37. 37.

    Dorrego M, Sabe L, García Cuerva A, Kuzis G, Tiberti C, Boller F, Starkstein S (1999) Remote memory in Alzheimer's disease. J Neuropsychiatry Clin Neurosci 11:490–497. https://doi.org/10.1176/jnp.11.4.490

  38. 38.

    Starkstein S, Boller F, Garau L (2005) A two-year follow-up study of remote memory in Alzheimer's disease. J Neuropsychiatry Clin Neurosci 17:336–341. https://doi.org/10.1176/jnp.17.3.336

  39. 39.

    Bizzozero I, Lucchelli F, Saetti M, Spinnler H (2008) Mild cognitive impairment does entail retrograde amnesia for public events. J Clin Exp Neuropsychol 31:48–56. https://doi.org/10.1080/13803390801978864

  40. 40.

    Leyhe T, Müller S, Eschweiler G, Saur R (2010) Deterioration of the memory for historic events in patients with mild cognitive impairment and early Alzheimer's disease. Neuropsychologia 48:4093–4101. https://doi.org/10.1016/j.neuropsychologia.2010.10.011

  41. 41.

    Smith C (2014) Retrograde memory for public events in mild cognitive impairment and its relationship to anterograde memory and neuroanatomy. Neuropsychology 28:959–972. https://doi.org/10.1037/neu0000117

  42. 42.

    De Simone M, Fadda L, Perri R, De Tollis M, Aloisi M, Caltagirone C, Carlesimo G (2017) Retrograde amnesia for episodic and semantic memories in amnestic mild cognitive impairment. J Alzheimer's Dis 59:241–250. https://doi.org/10.3233/JAD-170317

  43. 43.

    Greene J, Hodges J (1996) The fractionation of remote memory: evidence from a longitudinal study of dementia of Alzheimer type. Brain 119:129–142. https://doi.org/10.1093/brain/119.1.129

  44. 44.

    Greene J, Hodges J (1996) Identification of famous faces and famous names in early Alzheimer's disease: relationship to anterograde episodic and general semantic memory. Brain 119:111–128. https://doi.org/10.1093/brain/119.1.111

  45. 45.

    Thompson S, Graham K, Patterson K, Sahakian B, Hodges J (2002) Is knowledge of famous people disproportionately impaired with patients with early and questionable Alzheimer's disease? Neuropsychology 16:344–358. https://doi.org/10.1037/0894-4105.16.3.344

  46. 46.

    Seidenberg M, Guidotti L, Nielson K, Woodard J, Durgerian S, Zhang Q, Gander A, Antuono P, Rao S (2009) Semantic knowledge for famous names in mild cognitive impairment. J Int Neuropsychol Soc 15:9–18. https://doi.org/10.1017/s1355617708090103

  47. 47.

    Clague F, Graham K, Thompson S, Hodges J (2011) Is knowledge of famous people compromised in mild cognitive impairment? Cognit Behav Neurol 24:134–144. https://doi.org/10.1097/wnn.0b013e318234315a

  48. 48.

    Hodges J, Salmon D, Butters N (1993) Recognition and naming of famous faces in Alzheimer's disease: a cognitive analysis. Neuropsychologia 31:775–788. https://doi.org/10.1016/0028-3932(93)90128-m

  49. 49.

    Dall'Ora P, Della Sala S, Spinnler H (1989) Autobiographical memory its impairment in amnesic syndromes. Cortex 25:197–217. https://doi.org/10.1016/s0010-9452(89)80037-1

  50. 50.

    Kopelman MD (1991) Frontal dysfunction and memory deficits in the alcoholic Korsakoff syndrome and Alzheimer-type dementia. Brain 114:117–137. https://doi.org/10.1093/oxfordjournals.brain.a101852

  51. 51.

    Sala S, Laiacona M, Spinnler H, Trivelli C (1992) Is autobiographical impairment due to a deficit of recollection? an overview of studies on alzheimer dements, frontal and global amnesic patients. Theor Perspect Autobiogr Mem. https://doi.org/10.1007/978-94-015-7967-4_26

  52. 52.

    Sagar H, Cohen N, Sullivan E, Corkin S, Growdon J (1988) Remote memory function in Alzheimer's disease and Parkinson's disease. Brain 111:185–206. https://doi.org/10.1093/brain/111.1.185

  53. 53.

    Leplow B, Dierks C, Herrmann P, Pieper N, Annecke R, Ulm G (1997) Remote memory in Parkinson's disease and senile dementia. Neuropsychologia 35:547–557. https://doi.org/10.1016/s0028-3932(96)00116-9

  54. 54.

    Thomas-Antérion C, Jacquin K, Laurent B (2000) Differential mechanisms of impairment of remote memory in Alzheimer’s and frontotemporal dementia. Dement Geriatr Cogn Disord 11:100–106. https://doi.org/10.1159/000017221

  55. 55.

    Lucchelli F, Saetti M, Spinnler H (2018) Degenerative amnesia for past public events: an attempt to measure storage and retrieval. J Alzheimer's Dis 66:1083–1094. https://doi.org/10.3233/JAD-180436

  56. 56.

    Squire L (1987) Memory and brain. Oxford University Press, New York

  57. 57.

    Petersen R, Caracciolo B, Brayne C, Gauthier S, Jelic V, Fratiglioni L (2014) Mild cognitive impairment: a concept in evolution. J Intern Med 275:214–228. https://doi.org/10.1111/joim.12190

  58. 58.

    McKhann G, Knopman D, Chertkow H, Hyman B, Jack C, Kawas C, Klunk W, Koroshetz W, Manly J, Mayeux R, Mohs R, Morris J, Rossor M, Scheltens P, Carrillo M, Thies B, Weintraub S, Phelps C (2011) 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 Dement 7:263–269. https://doi.org/10.1016/j.jalz.2011.03.005

  59. 59.

    Carlesimo G, Caltagirone C, Gainotti G, Fadda L, Gallassi R, Lorusso S, Marfia G, Marra C, Nocentini U, Parnetti L (1996) The mental deterioration battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. Eur Neurol 36:378–384. https://doi.org/10.1159/000117297

  60. 60.

    Carlesimo GA, Buccione I, Fadda L, Graceffa A, Mauri M, Lorusso S, Bevilacqua G, Caltagirone C (2002) Standardizzazione di due test di memoria per uso clinico: Breve Racconto e Figura di Rey. Nuova Rivista di Neurologia 12:1–13

  61. 61.

    Monaco M, Costa A, Caltagirone C, Carlesimo G (2012) Forward and backward span for verbal and visuo-spatial data: standardization and normative data from an Italian adult population. Neurol Sci 34:749–754. https://doi.org/10.1007/s10072-012-1130-x

  62. 62.

    Giovagnoli AR, Del Pesce M, Mascheroni S, Simoncelli M, Laiacona M, Capitani E (1996) Trail making test: normative values from 287 normal adult controls. Ital J Neurol Sci 17:305–309

  63. 63.

    Nocentini U, Di Vincenzo S, Panella M, Pasqualetti P, Caltagirone C (2002) La valutazione delle funzioni esecutive nella pratica neuropsicologica: dal modified card sorting test al modified card sorting test-roma version. Dati di standardizzazione. Nuova Rivista di Neurologia 12:14–24

  64. 64.

    Miceli G, Laudanna A, Burani C, Capasso R (1994) Batteria per l’Analisi dei Deficit Afasici BADA: Università Cattolica del Sacro Cuore. Istituto di Psicologia, Servizio di Neuropsicologia, Consiglio Nazionale delle Ricerche

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Acknowledgements

This work has been supported by Ricerca Corrente grants (Italian Ministry of Health) from the IRCC Santa Lucia Foundation—Linea di ricerca: Neurologia Clinica e Comportamentale.

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Correspondence to Maria Stefania De Simone.

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This study was approved by the ethics committee of the Santa Lucia Foundation in accordance with the Declaration of Helsinki and its later amendments. All participants gave their written informed consent prior to their inclusion in the study.

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De Simone, M.S., De Tollis, M., Fadda, L. et al. Lost or unavailable? Exploring mechanisms that affect retrograde memory in mild cognitive impairment and Alzheimer's disease patients. J Neurol 267, 113–124 (2020) doi:10.1007/s00415-019-09559-8

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Keywords

  • Retrograde amnesia
  • Mild cognitive impairment
  • Alzheimer disease
  • Memory impairment
  • Public events