Preservation of Musical Memory Throughout the Progression of Alzheimer's Disease? Toward a Reconciliation of Theoretical, Clinical, and Neuroimaging Evidence.
[en] Through this review of 25 clinical and experimental works on long-term musical memories in Alzheimer's disease (AD) patients, we attempt to clarify the conceptual understanding of musical memories, identify their evolution across the stages of the pathology, and propose possible explanations concerning the neural and cognitive mechanisms that underpin the preservation and impairment of certain musical memories. After clarifying the different kind of musical memories, we investigated their alterations throughout AD's progression from mild to severe stages. Both procedural and retrograde semantic memory seem relatively spared in AD, while episodic memory appears to be impaired early. Moreover, partial preservation of music encoding in AD can be revealed through paradigms that are especially designed for AD patients (relying on behavioral cues, using adapted settings, etc.). Although seldomly used, they would definitely help understanding the preserved capacities in every stage of AD. However, more research is needed to better understand this phenomenon and assess its specificity to music or other types of supports. These findings could lead to multiple applications in care settings and research designs, bringing more nuanced understanding of how long-term musical memory degrades throughout the course of AD, and should encourage us to prioritize patients' preserved cognitive abilities in current AD recreational and care programs.
Disciplines :
Neurosciences & behavior
Author, co-author :
Groussard, Mathilde; Normandie Univ, UNICAEN, PSL Research University, EPHE, INSERM, CHU de Caen, Cyceron, Caen, France
Chan, Tyler G; The Grossman Institute for Neuroscience, Quantitative Biology, and Human Behavior, The University of Chicago, Chicago, IL, USA
Coppalle, Renaud ; Université de Liège - ULiège > GIGA > GIGA CRC In vivo Imaging - Aging & Memory ; Normandie Univ, UNICAEN, PSL Research University, EPHE, INSERM, CHU de Caen, Cyceron, Caen, France
Platel, Hervé; Normandie Univ, UNICAEN, PSL Research University, EPHE, INSERM, CHU de Caen, Cyceron, Caen, France
Language :
English
Title :
Preservation of Musical Memory Throughout the Progression of Alzheimer's Disease? Toward a Reconciliation of Theoretical, Clinical, and Neuroimaging Evidence.
BeattyWW, Zavadil KD, Bailly RC, Rixen GJ (1988) Preserved musical skill in a severely demented patient. Int J Clin Neuropsychol 10, 158-164.
Crystal HA, Grober E, Masur D (1989) Preservation of musical memory in Alzheimer's disease. J Neurol Neurosurg Psychiatry 52, 1415-1416.
Neugroschl J, Wang S (2011) Alzheimer's disease: Diagnosis and treatment across the spectrum of disease severity. Mt Sinai J Med A J Transl Pers Med 78, 596-612.
Raglio A, Bellelli G, Traficante D, Gianotti M, Ubezio MC, Villani D, Trabucchi M (2008) Efficacy of music therapy in the treatment of behavioral and psychiatric symptoms of dementia. Alzheimer Dis Assoc Disord 22, 158-162.
Herholz SC, Herholz RS, Herholz K (2013) Nonpharmacological interventions and neuroplasticity in early stage Alzheimer's disease. Expert Rev Neurother 13, 1235-1245.
Tomaino CM (2013) Meeting the complex needs of individuals with dementia through music therapy. Music Med 5, 234-241.
Särkämö T, Tervaniemi M, Laitinen S, Numminen A, Kurki M, Johnson JK, Rantanen P (2014) Cognitive, emotional, and social benefits of regular musical activities in early dementia: Randomized controlled study. Gerontologist 54, 634-650.
Chu H, Yang C-Y, Lin Y, Ou K-L, Lee T-Y, O'Brien AP, Chou K-R (2014) The impact of group music therapy on depression and cognition in elderly persons with dementia: Arandomized controlled study. Biol Res Nurs 16, 209-217.
Samson S, Clément S, Narme P, Schiaratura L, Ehrlé N (2015) Efficacy of musical interventions in dementia: Methodological requirements of nonpharmacological trials. Ann N Y Acad Sci 1337, 249-255.
Crowe M, Andel R, Pedersen NL, Johansson B, Gatz M (2003) Does participation in leisure activities lead to reduced risk of Alzheimer's disease? A prospective study of Swedish twins. J Gerontol Ser B Psychol Sci Soc Sci 58, 249-255.
Sanders A, Verghese J (2007) Leisure activities and the risk of dementia in the elderly. Res Pract Alzheimers Dis 12, 54-58.
Balbag MA, Pedersen NL, GatzM(2014) Playing a musical instrument as a protective factor against dementia and cognitive impairment: A population-based twin study. Int J Alzheimers Dis 2014, 836748.
Tulving E (1972) Episodic and semantic memory. Organ Mem 1, 381-403
Tulving E (1985) How many memory systems are there? Am Psychol 40, 385-398.
Van Hedger SC, Heald SL, Nusbaum HC (2018) Longterm pitch memory for music recordings is related to auditory working memory precision. Q J Exp Psychol (Hove) 71, 879-891.
Peretz I, Gosselin N, Belin P, Zatorre RJ, Plailly J, Tillmann B (2009) Music lexical networks: The cortical organization of music recognition. Ann N Y Acad Sci 1169, 256-265.
Peretz I, ColtheartM(2003) Modularity of music processing. Nat Neurosci 6, 688-691.
PatelAD(2013) Sharing and nonsharing of brain resources for language and music. In Language, Music, and the Brain, Arbib M, ed. MIT PRess, Cambridge, MA, pp. 329-355.
Platel H, Groussard M (2010) La mémoire sémantique musicale: Apport des données de la neuropsychologie clinique et de la neuro-imagerie fonctionnelle. Rev Neuropsychol 2, 61-69.
Platel H, Baron JC, Desgranges B, Bernard F, Eustache F (2003) Semantic and episodic memory of music are subserved by distinct neural networks. Neuroimage 20, 244-256.
Bruce V, Young A (1986) Understanding face recognition. Br J Psychol 77 (Pt 3), 305-327.
Koelsch S, Siebel WA (2005) Towards a neural basis of music perception. Trends Cogn Sci 9, 578-584.
Spaniol J, Davidson PSR, Kim ASN, Han H, Moscovitch M, Grady CL (2009) Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation. Neuropsychologia 47, 1765-1779.
Winocur G, Moscovitch M (2011) Memory transformation and systems consolidation. J Int Neuropsychol Soc 17, 766-780.
Dudai Y, Karni A, Born J (2015) The consolidation and transformation of memory. Neuron 88, 20-32.
Foster NA, Valentine ER (2001) The effect of auditory stimulation on autobiographical recall in dementia. Exp Aging Res 27, 215-228.
ConwayMA(2001) Sensory-perceptual episodic memory and its context: Autobiographical memory. Philos Trans R Soc B Biol Sci 356, 1375-1384.
Hirst W, Manier D (2008) Towards a psychology of collective memory. Memory 16, 183-200.
Penfield W, Milner B (1958) Memory deficit produced by bilateral lesions in the hippocampal zone. Arch Neurol Psychiatry 79, 475-497.
Berthoz A (1993) Multisensory control of movement, Oxford University Press.
Graf P, Schacter DL (1985) Implicit and explicit memory for new associations in normal and amnesic subjects. J Exp Psychol Learn Mem Cogn 11, 501-518.
Nadel L, Hardt O (2011) Update on memory systems and processes. Neuropsychopharmacology 36, 251-273.
Henke K (2010) A model for memory systems based on processing modes rather than consciousness. Nat Rev Neurosci 11, 523-532.
Patel B, Perera M, Pendleton J, Richman A, Majumdar B (2014) Psychosocial interventions for dementia: From evidence to practice. Adv Psychiatr Treat 20, 340-349.
Beard RL (2012) Art therapies and dementia care: A systematic review. Dementia 11, 633-656.
Omar R, Hailstone JC, Warren JDJE, Crutch SJ, Warren JDJE (2010) The cognitive organization of music knowledge: A clinical analysis. Brain 133, 1200-1213.
Johnson JK, Chang CC, Brambati SM, Migliaccio R, Gorno-Tempini ML, Miller BL, Janata P (2011) Music recognition in frontotemporal lobar degeneration and Alzheimer disease. Cogn Behav Neurol 24, 74-84.
Hsieh S, Hornberger M, Piguet O, Hodges JR (2011) Neural basis of music knowledge: Evidence from the dementias. Brain 134, 2523-2534.
Cuddy LL, Duffin JM, Gill SS, Brown CL, And RS, Vanstone AD (2012) Memory for melodies and lyrics in Alzheimer's disease. Music Percept 29, 479-491.
Vanstone AD, Sikka R, Tangness L, Sham R, Garcia A, Cuddy LL (2012) Episodic and semantic memory for melodies in Alzheimer's disease. Music Percept 29, 501-507.
Kerer M, Marksteiner J, Hinterhuber H, Mazzola G, Kemmler G, Bliem HR,WeissEM(2013) Explicit (semantic) memory for music in patients with mild cognitive impairment and early-stage Alzheimer's disease. Exp Aging Res 39, 536-564.
Basaglia-Pappas S, Laterza M, Borg C, Richard-Mornas A, Favre E, Thomas-Antérion C (2013) Exploration of verbal and non-verbal semantic knowledge and autobiographical memories starting from popular songs in Alzheimer's disease. Int Psychogeriatrics 25, 785-795.
Halpern AR, O'Connor MG (2000) Implicit memory for music in Alzheimer's disease. Neuropsychology 14, 391-397.
Quoniam N, Ergis A-M, Fossati P, Peretz I, Samson S, Sarazin M, Allilaire J-F (2003) Implicit and explicit emotional memory for melodies in Alzheimer's disease and depression. Ann N Y Acad Sci 999, 381-4.
Moussard A, Bigand E, Clément S, Samson S (2008) Préservation des apprentissages implicites en musique dans le vieillissement normal et la maladie d'Alzheimer. Rev Neuropsychol 18, 127-152.
Ménard MC, Belleville S (2009) Musical and verbal memory in Alzheimer's disease: A study of long-term and short-term memory. Brain Cogn 71, 38-45.
Campanelli A, Rendace L, Parisi F, D'Antonio F, Imbriano L, de Lena C, TrebbastoniA(2016) Musical cognition in Alzheimer's disease: Application of the Montreal Battery of Evaluation of Amusia. Ann N Y Acad Sci 1375, 28-37.
Folstein MF, Folstein SE, McHugh PR (1975) "Minimental state".Apractical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12, 189-198.
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 (2011) Staging dementia. In Principles and Practice of Geriatric Psychiatry, ed 3, Abou-Saleh MT, Katona C, Kumar A, eds. John Wiley & Sons, Chichester, pp. 162-169.
Golden HL, Clark CN, Nicholas JM, Cohen MH, Slattery CF, Paterson RW, Foulkes AJM, Schott JM, Mummery CJ, Crutch SJ, Warren JD (2017) Music perception in dementia. J Alzheimers Dis 55, 933-949.
Veitch DP, Weiner MW, Aisen PS, Beckett LA, Cairns NJ, Green RC, Harvey D, Jack CR, Jagust W, Morris JC, Petersen RC, Saykin AJ, Shaw LM, Toga AW, Trojanowski JQ (2019) Understanding disease progression and improving Alzheimer's disease clinical trials: Recent highlights from the Alzheimer's Disease Neuroimaging Initiative. Alzheimers Dement 15, 106-152.
Zajonc RB (1980) Feeling and thinking: Preferences need no inferences. Am Psychol 35, 151-175.
Esiri MM, Pearson RCA, Powell TPS (1986) The cortex of the primary auditory area in Alzheimer's disease. Brain Res 366, 385-387.
Lewis DA, Campbell MJ, Terry RD, Morrison JH (1987) Laminar and regional distributions of neurofibrillary tangles and neuritic plaques in Alzheimer's disease: A quantitative study of visual and auditory cortices. J Neurosci 7, 1799-1808.
Geula C, Mesulam MM (1996) Systematic regional variations in the loss of cortical cholinergic fibers in Alzheimer's disease. Cereb Cortex 6, 165-177.
Weintraub S, Wicklund AH, Salmon DP (2012) The neuropsychological profile of Alzheimer disease. Cold Spring Harb Perspect Med 2, a006171-a006171.
Beatty WW, Winn P, Adams RL, Allen EW, Wilson DA, Prince JR, Olson KA, Dean K, Littleford D (1994) Preserved cognitive skills in dementia of the Alzheimer type. Arch Neurol 51, 1040-1046.
Bartlett JC, Halpern AR, Dowling WJ (1995) Recognition of familiar and unfamiliar melodies in normal aging and Alzheimer's disease. Mem Cognit 23, 531-546.
Vanstone AD, Cuddy LL, Duffin JM, Alexander E (2009) Exceptional preservation of memory for tunes and lyrics: Case studies of amusia, profound deafness, and Alzheimer's disease. Ann N Y Acad Sci 1169, 291-294.
Samson S, Baird A, Moussard A, Clément S (2012) Does pathological aging affect musical learning and memory? Music Percept 29, 493-500.
Polk M, Kertesz A (1993) Music and language in degenerative disease of the brain. Brain Cogn 22, 98-117.
Beatty WW, Rogers CL, Rogers RL, English S, Testa JA, Orbelo DM,Wilson DA, Ross ED (1999) Piano playing in Alzheimer's disease: Longitudinal study of a single case. Neurocase 5, 459-469.
Cuddy LL, Duffin J (2005) Music, memory, and Alzheimer's disease: Is music recognition spared in dementia, and how can it be assessed? Med Hypotheses 64, 229-235.
Baird A, Umbach H, Thompson WF (2017) A nonmusician with severe Alzheimer's dementia learns a new song. Neurocase 23, 36-40.
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.
Fornazzari L, Castle T, Nadkarni S, Ambrose M, Miranda D, Apanasiewicz N, Phillips F (2006) Preservation of episodic musical memory in a pianist with Alzheimer disease. Neurology 66, 610-611.
Cowles A, BeattyWW, Nixon SJ, Lutz LJ, Paulk J, Paulk K, Ross ED (2003) Musical skill in dementia: A violinist presumed to have Alzheimer's disease learns to play a new song. Neurocase 9, 493-503.
Zatorre RJ (2003) Neural specializations for tonal processing. In The Cognitive Neuroscience of Music, Peretz I, Zatorre RJ, eds. Oxford University Press, pp. 231-246.
Limb CJ (2006) Structural and functional neural correlates of music perception. Anat Rec A Discov Mol Cell Evol Biol 288, 435-446.
Koelsch S (2014) Brain correlates of music-evoked emotions. Nat Rev Neurosci 15, 170-180.
Janata P (2015) Neural basis of music perception. Handb Clin Neurol 129, 187-205.
Reybrouck M, Vuust P, Brattico E (2018) Brain connectivity networks and the aesthetic experience of music. Brain Sci 8, 107-121.
Schulze K, Koelsch S (2012)Working memory for speech and music. Ann N Y Acad Sci 1252, 229-236.
Saito Y, Ishii K, Sakuma N, Kawasaki K, Oda K, Mizusawa H (2012) Neural substrates for semantic memory of familiar songs: Is there an interface between lyrics and melodies? PLoS One 7, e46354.
Freitas C, Manzato E, Burini A, Taylor MJ, Lerch JP, Anagnostou E (2018) Neural correlates of familiarity in music listening: A systematic review and a neuroimaging meta-analysis. Front Neurosci 12, 686.
Schwindt GC, Black SE (2009) Functional imaging studies of episodic memory in Alzheimer's disease: A quantitative meta-analysis. Neuroimage 45, 181-190.
Assal G (1973) [Wernicke's aphasia without amusia in a pianist]. Rev Neurol (Paris) 129, 251-255.
Lechevalier B, Eustache F, Rossa Y (1985) Les troubles de la perception de la musique d'origine neurologique, Masson, Paris.
Signoret JL, van Eeckhout P, Poncet M, Castaigne P (1987) [Aphasia without amusia in a blind organist.Verbal alexiaagraphia without musical alexia-agraphia in braille]. Rev Neurol (Paris) 143, 172-181.
Peretz I (1996) Can we lose memory for music? A case of music agnosia in a nonmusician. J Cogn Neurosci 8, 481-496.
Ettlinger M, Margulis EH, Wong PCM (2011) Implicit memory in music and language. Front Psychol 2, 211.
Groussard M, Rauchs G, Landeau B,Viader F, Desgranges B, Eustache F, Platel H (2010) The neural substrates of musical memory revealed by fMRI and two semantic tasks. Neuroimage 53, 1301-1309.
Chételat G, Desgranges B, Landeau B,Mézenge F, Poline JB, De La Sayette V, Viader F, Eustache F, Baron JC (2008) Direct voxel-based comparison between grey matter hypometabolism and atrophy in Alzheimer's disease. Brain 131, 60-71.
Jacobsen JH, Stelzer J, Fritz TH, Chételat G, La Joie R, Turner R (2015) Why musical memory can be preserved in advanced Alzheimer's disease. Brain 138, 2438-2450.
Groussard M, Mauger C, Platel H (2013) Musical longterm memory throughout the progression of Alzheimer disease. Geriatr Psychol Neuropsychiatr Vieil 11, 99-109.
Groussard M, La Joie R, Rauchs G, Landeau B, Chételat G, Viader F, Desgranges B, Eustache F, Platel H (2010) When music and long-term memory interact: Effects of musical expertise on functional and structural plasticity in the hippocampus. PLoS One 5, e13225.
Groussard M, Viader F, Landeau B, Desgranges B, Eustache F, PlatelH(2014) The effects of musical practice on structural plasticity: The dynamics of grey matter changes. Brain Cogn 90, 174-180.
Prickett CA, Smoore R (1991) The use of music to aid memory of Alzheimer's patients. J Music Ther 28, 101-110.
Wallace WT (1994) Memory for music: Effect of melody on recall of text. J Exp Psychol LearnMemCogn 20, 1471-1485.
Simmons-Stern NR, Budson AE, AllyBA(2010) Music as a memory enhancer in patients with Alzheimer's disease. Neuropsychologia 48, 3164-3167.
Moussard A, Bigand E, Belleville S, Peretz I (2014) Learning sung lyrics aids retention in normal ageing and Alzheimer's disease. Neuropsychol Rehabil 24, 894-917.
Baird A, Samson S, Miller L, Chalmers K (2017) Does music training facilitate the mnemonic effect of song? An exploration of musicians and nonmusicians with and without Alzheimer's dementia. J Clin Exp Neuropsychol 39, 9-21.
Palisson J, Roussel-Baclet C, Maillet D, Belin C, Ankri J, Narme P (2015) Music enhances verbal episodic memory in Alzheimer's disease. J Clin Exp Neuropsychol 37, 503-517.
Gedek B (1977) [Mycoses. Pathogenicity and diagnosis of dermatophytes, yeasts and molds]. In Fortschritte der Medizin. Oxford University Press, pp. 815-822.
Hailstone JC, Omar R, Warren JD (2009) Relatively preserved knowledge of music in semantic dementia. J Neurol Neurosurg Psychiatry 80, 808-809.
Omar R, Henley SMD, Bartlett JW, Hailstone JC, Gordon E, Sauter DA, Frost C, Scott SK, Warren JD (2011) The structural neuroanatomy of music emotion recognition: Evidence from frontotemporal lobar degeneration. Neuroimage 56, 1814-1821.
Weinstein J,Koenig P, Gunawardena D, McMillan C, Bonner M, Grossman M (2011) Preserved musical semantic memory in semantic dementia. Arch Neurol 68, 248-250.
Warren JD (2011) Music and semantic dementia. Arch Neurol 68, 1089.
Geroldi C, Metitieri T, Binetti G, Zanetti O, Trabucchi M, Frisoni GB (2000) Pop music and frontotemporal dementia. Neurology 55, 1935-1936.
Downey LE, Blezat A, Nicholas J, Omar R, Golden HL, Mahoney CJ, Crutch SJ, Warren JD (2013) Mentalising music in frontotemporal dementia. Cortex 49, 1844-1855.
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.
Fauvel B, Groussard M, Eustache F, Desgranges B, Platel H (2013) Neural implementation of musical expertise and cognitive transfers: Could they be promising in the framework of normal cognitive aging? Front Hum Neurosci 7, 693.
Fauvel B, Groussard M, Mutlu J, Arenaza-Urquijo EM, Eustache F, Desgranges B, Platel H (2014) Musical practice and cognitive aging: Two cross-sectional studies point to phonemic fluency as a potential candidate for a usedependent adaptation. Front Aging Neurosci 6, 227.
Cantou P, Platel H, Desgranges B, Groussard M (2018) How motor, cognitive and musical expertise shapes the brain: Focus on fMRI and EEG resting-state functional connectivity. J Chem Neuroanat 89, 60-68.
Sauer PE, Fopma-Loy J, Kinney JM, Lokon E (2016) "It makes me feel like myself": Person-centered versus traditional visual arts activities for people with dementia. Dementia 15, 895-912.
