Experimental Aging Research, 39: 536–564, 2013 Copyright # Taylor & Francis Group, LLC ISSN: 0361-073X print=1096-4657 online DOI: 10.1080/0361073X.2013.839298
EXPLICIT (SEMANTIC) MEMORY FOR MUSIC IN PATIENTS WITH MILD COGNITIVE IMPAIRMENT AND EARLY-STAGE ALZHEIMER’S DISEASE
Manuela Kerer Department of Psychology, University of Innsbruck, Innsbruck, Austria
Josef Marksteiner Department of Psychiatry, Medical University Innsbruck, Innsbruck, Austria and Department of Psychiatry and Psychotherapy A, Hospital Hall, Hall, Austria
Hartmann Hinterhuber Department of Psychiatry, Medical University Innsbruck, Innsbruck, Austria
Guerino Mazzola School of Music, University of Minnesota, Minneapolis, Minnesota, USA
Georg Kemmler Department of Psychiatry, Medical University Innsbruck, Innsbruck, Austria
Received 25 June 2012; accepted 15 December 2012. Address correspondence to Manuela Kerer, Department of Psychology, University of Innsbruck, Innrain 52 A, A-6020 Innsbruck, Austria. E-mail: [email protected]
Explicit Memory for Music in MCI and AD
537
Harald R. Bliem Department of Psychology, University of Innsbruck, Innsbruck, Austria
Elisabeth M. Weiss Department of Biological Psychology, Karl Franzens University Graz, Graz, Austria Background=Study Context: Explicit memory for music was investigated by using a new test with 24 existing and 3 newly composed pieces. Methods: Ten patients with mild cognitive impairment (MCI) and 10 patients with early stage of Alzheimer’s disease (AD) were compared with 23 healthy subjects, in terms of verbal memory of music by the identification of familiar music excerpts and the discrimination of distortion and original timbre of musical excerpts. Results: MCI and Alzheimer’s patients showed significantly poorer performances in tasks requiring verbal memory of musical excerpts than the healthy participants. For discrimination of musical excerpts, MCI and AD patients surprisingly performed significantly better than the healthy comparison subjects. Conclusion: Our results support the notion of a specialized memory system for music.
Music as an intervention is a safe and effective method for treating agitation and anxiety in moderately affected and severe dementia of the Alzheimer’s type (Sherratt, Thornton, & Hatton, 2004; Svansdottir & Snaedal, 2006). Preserved cognitive skills in the field of music may provide possibilities for interventions to improve communicational skills and other cognitive functions in patients affected with this disease (Baird & Samson, 2009). Moreover the notion of a specialized memory system for music—distinct from other domains such as verbal and visual memory—could emerge. This would suggest that memory for music engages brain regions that are not affected by Alzheimer’s disease (AD) pathology (Peretz & Coltheart, 2003). Therefore, proof of preserved memory for music in mild cognitive impairment (MCI) and early AD patients is of great clinical and scientific relevance. Dementia is characterized by progressive decline in cognitive functions such as memory, attention, and language, leading to impaired abilities to perform activities of daily living and also to neuropsychiatric symptoms or behavioral changes. The transitional state between
538
M. Kerer et al.
cognitive changes of normal aging and fully developed clinical features of dementia constitutes the diagnostic group of MCI. MCI patients typically have intact activities of daily living, but report about memory problems and show slight deficits in objective neuropsychological tests (test scores, 1.5 standard deviations below the average of standardized norms) that are not of sufficient severity to define dementia (Winblad et al., 2004; Morris et al., 2001; Petersen, 2004; Petersen et al., 1999, 2001; Tierney et al., 1996). However, it should be noted that the term MCI has been controversially discussed, because it covers diverse populations of patients who attend memory clinics and a range of pathological disorders (Dubois & Albert, 2007). Memory for Music Baird and Samson (2009) propose a concept of different types of musical memory as described in nonmusical domains that may be differentially impaired in AD. Long-term memory can be described as representative of two different forms: explicit and implicit memory. This is a distinction that has become fundamental since Tulving first proposed it in 1972. Explicit (declarative) memory is the conscious, intentional recollection of previous experiences, events, facts, and information. It is divided into episodic and semantic memory, which are both associated with different kinds of conscious awareness (Tulving, 2002). Related to these distinctions, episodic musical memory can be defined as the ability to retrieve the spatiotemporal, personal, and emotional contexts of the musical experience. On the other hand, semantic or conceptual musical memory is responsible for factual musical knowledge, associative or emotional concepts that are not linked to the retrieval of a specific personal experience or autobiographical event. Implicit (nondeclarative) memory is characterized by a lack of conscious awareness in the act of recollection, including priming, procedural memory, or motor skill learning, which are critical for playing a musical instrument (Baird & Samson, 2009). Samson and Peretz (2005) examined the relationship between musical preferences and prior exposure to music in patients with either left or right temporal lobe lesions and in one amnesic patient with bilateral lesions of the temporal lobe. Participants with left temporal lobe lesions preferred the melodies to which they were previously exposed to, thereby demonstrating an implicit exposure effect on musical preference, whereas participants with right temporal lobe lesions did not show this effect. These findings suggest that right temporal lobe structures play a critical role in the formation of melody
Explicit Memory for Music in MCI and AD
539
representations that support both priming and memory recognition, whereas left temporal lobe structures are more involved in the explicit retrieval of melodies. In the case of the amnesic patient, the exposure effect on musical preference was also absent; however, repeated exposure to melodies was found to enhance both musical preference and recognition. This remaining capacity of the patient’s memory observed through melody repetition suggests that extensive exposure may assist both implicit and explicit memory in the presence of global amnesia. Mazzola (2002) strongly supports a key function of music in opening memory contents, according to the hippocampal gate function as suggested by Winson (1985), by stimulating the hippocampal formation. Text and melody of a song seem to have separate representations in memory, making singing a dual task to perform, at least in the first steps of learning. Musical training has little impact on performance in this field, suggesting that vocal learning is a basic and widespread skill (Racette & Peretz, 2007). Neural Correlates Lesion and neuroimaging studies of musical memory demonstrate involvement of temporal and frontal lobe regions. Familiar music is associated with bitemporal activation (Platel, 2005) and bitemporal damage seems to cause music agnosia, or an inability to recognize familiar melodies (Peretz, 1996; Peretz & Gagnon, 1999). Eustache, Lechevalier, Viader, and Lambert (1990) observed a patient with left temporoparietal lesion after ischemic brain damage that demonstrated impaired recognition of familiar melodies, but showed intact discrimination. They hypothesized that identification and discrimination involve distinct mechanisms within the processing of auditory stimuli, and that they may be selectively disrupted in brain-damaged subjects. Hsieh, Hornberger, Piguet, and Hodges (2011) tested patients with semantic dementia and highlighted the role of the right temporal pole in the processing of known tunes and faces. The majority of neuroimaging studies have reported activation within the auditory association areas of the superior temporal gyrus (Satoh, Takeda, Nagata, Shimosegawa, & Kuzuhara, 2006; Watanabe, Yagishita, & Kikyo, 2008; Zatorre, Halpern, Perry, Meyer, & Evans, 1996; Halpern & Zatorre 1999). Additionally, frontal regions and middle frontal lobes were associated with musical imagery of familiar melodies (Zatorre et al., 1996; Halpern & Zatorre, 1999). Furthermore, functional imaging studies (Platel, Baron, Desgranges, Bernard, & Eustache, 2003; Satoh et al., 2006) and focal lesion studies
540
M. Kerer et al.
(Stewart, von Kriegstein, Warren, & Griffiths, 2006) suggest the involvement of brain areas beyond the anterior temporal lobe, implicating a distributed network of perisylvian areas in processes such as familiar melody recognition. Neuropathological and atrophic changes associated with early pathology in AD are relatively focal, predominately affecting the temporal lobes, especially the medial temporal lobe memory system (Dickerson & Sperling, 2009). These changes implicate the hallmark feature of impaired episodic and semantic memory function; AD patients indeed exhibit deficits on explicit tasks (Kensinger, Shearer, Locascio, Growdon, & Corkin, 2003; Laisney et al., 2011; Carlesimo & Oscar-Berman, 1992). Nevertheless neuroimaging data suggest that musical memory relies on parts of the brain less affected by AD. Weinstein et al. (2011) examined a semiprofessional musician with semantic dementia and came to the conclusion that long-term representations of words and objects in semantic memory may be dissociated from meaningful knowledge in other domains, such as music. Memory for Music in AD Knowledge of musical structures may remain intact and accessible, even when explicit judgements and overt recognition have been lost (Tillmann, Peretz, Bigand, & Gosselin, 2007). In a study of Quoniam et al. (2003), AD patients were able to develop a positive affective bias of judgement for previously heard melodies. Music in general is able to stimulate long and short-term memory in patients with Alzheimer’s disease and increases self-esteem and social interaction in elders. Numerous studies have demonstrated the functionality of music therapy in patients with neurological disorders or dementia of Alzheimer’s type (Za´rate & Dı´az, 2001; Svansdottir & Snaedal, 2006; Guetin et al., 2009). Furthermore, exposure to music has been reported to produce transient increases in cognitive performance and music enhances attention processes or effects on autobiographical memory that can be demonstrated in Alzheimer’s disease (Thompson, Moulin, Hayre, & Jones, 2005; Irish et al., 2006). Explicit and Implicit Musical Memory in AD Case Studies Until now, several case studies in AD patients have shown that some forms of musical memory are spared in spite of dementia. Table 1 summarizes the results of these studies.
Explicit Memory for Music in MCI and AD
541
Table 1. Summary of case studies exploring musical memory in AD patients Authors (Year)
Patients
Results in regard to musical memory
Beatty et al. (1994)
Amateur musician (male) MMSE 20=30: ‘‘moderate’’
Cowles et al. (2003)
Amateur musician (male) MMSE 14=30: ‘‘moderate’’
Crystal, Grober, & Masur (1989)
Musician (male) Amnestic disorder; changed to AD after 7 years; MMSE not reported Amateur musician (female) MMSE 8=30: ‘‘severe’’ Musician (female) MMSE declined from 22=30 to 5=30: ‘‘severe’’ Music teacher (female) Two alternative diagnoses proposed: AD or Heidenhain’s disease
Intact procedural memory (trombone, Dixieland band) Impaired naming of well-known pieces that the patient was playing Ability to learn and recall a novel violin composition Mildly impaired naming of Christmas song titles Intact procedural memory (piano) Impaired naming of composer= title of familiar pieces
Cuddy & Duffin (2005) Fornazzari et al. (2006) Polk & Kertesz (1993)
Vanstone, Cuddy, Duffin, & Alexander (2009)
Amateur musician (female) MMSE 17=30: ‘‘moderate’’
Intact recognition of familiar music Intact procedural memory (piano) Ability to learn and recall a novel piano composition Correct naming and singing of the last note of familiar melodies; correct naming from written notation Impaired procedural memory (piano) Correct distinction of familiar from unfamiliar tunes and lyrics of tunes Correct singing of tunes after heard its spoken lyrics
Dissociation between explicit (semantic) and implicit (procedural) musical memory forms is apparent, supporting Baird and Samson’s (2009) proposal for distinction of these types of musical memory. Group Studies Few studies have investigated the association between memory for music and dementia in larger population groups. Vanstone and Cuddy (2010) compared 12 patients with moderate or severe AD and 12 healthy, older adult controls in distinguishing familiar from novel tunes, in identifying distortions in melodies, and in singing familiar tunes. A significant impairment of the AD participants was shown. In contrast, comparing each individual case with the control group revealed that five participants from the AD group performed
542
M. Kerer et al.
within the range of the control group on most tasks. Four participants performed below the range of the control group, but their scores were above the level of chance. Halpern and O’Connor (2000) presented short, unfamiliar melodies to young and older adults and to AD patients. Young adults showed retention of the melodies, older adults showed little explicit memory but did show the mere exposure effect, whereas AD patients showed neither. No correlation between musical and verbal long-term memory was found in Alzheimer’s patients and in older healthy adults (Me´nard & Belleville, 2009). Bartlett, Halpern, and Dowling (1995) found that distinguishing different sources of global familiarity is a factor in tune recognition and suggested that this type of source monitoring is impaired in AD. Quoniam et al. (2003) examined recognition of unfamiliar melodies in 10 patients with mild AD (Mini-Mental State Examination [MMSE] score: 22–25). In comparison with age-matched healthy controls and depressed patients, AD patients showed significantly impaired recognition of unfamiliar melodies. Aims and Hypothesis of this Study The purpose of the current study was twofold. Firstly, we wanted to test explicit memory for music in different stages of early dementia in terms of identification of familiar music excerpts. For this purpose, subjects were instructed to name the title of the music piece, or if the subject failed, to associate freely where they knew the piece from, or for the easiest stage, to recognize the correct title out of four possible titles. Secondly, we wanted to analyze explicit memory of participants in terms of ability to discriminate by exploring their ability to remember familiar melodic lines. For this purpose, the participants judged whether pieces were correctly rendered and utilized their memory of the timbre (vocal vs. instrumental). We hypothesized lower outcomes in the title-naming task, in free-associating, and in choosing out of four titles for MCI and early-dementia participants in comparison with the controls. But concerning the discrimination of the distorted musical excerpts and the judging of the original instrumental or vocal presentation, we suggested a trial within the control group range for the clinical group. Our findings may contribute to solve the question to which extent various dimensions of musical recognition and explicit memory for music are spared in MCI and early dementia.
Explicit Memory for Music in MCI and AD
543
METHODS Subjects: Demographic Data and Clinical Characteristics Forty-three subjects older than 60 years, with intact auditory functions, normal or corrected-to-normal sight, were tested on an extensive neuropsychological battery. This included the MMSE examination (Folstein, Folstein, & McHugh, 1975), verbal memory tests (learning, free recall, and recognition subtests of the CERAD [Consortium to Establish a Registry for Alzheimer’s Disease] battery; Rosen 1984), figural memory tests (free recall, CERAD, NAI [Nu¨rnberger Alters-Inventar] figure test; Oswald & Fleischmann, 1997), object-naming tests (Boston Naming Test—short version, CERAD), categorical and lexical verbal fluency tests (animals=minute, words starting with s=minute), tests on planning (CLOX [An Exclusive Clock Drawing Task] Test Part 1; Sunderland et al., 1989), constructive abilities tests (copy geometrical shapes, CERAD, CLOX Test Part 2), assessment of divided attention and cognitive flexibility (Trail Making Test-B; Reitan & Wolfson, 1985). Furthermore, depression was evaluated with the Geriatric Depression Scale (GDS; Yesavage et al., 1982). Additional investigations included an informal interview, computed tomography (CT) or magnetic resonance imaging (MRI) of the brain and routine blood samples. Overall exclusion criteria for participation were history of stroke, head trauma, substance abuse, and major neurological (other than Dementia Alzheimer’s type or MCI), psychiatric, or metabolic disorders that may compromise cognition. Ten patients (9 females and 1 male) with early AD, diagnosed according to the criteria of DSM-IV-TR (Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision), NINCDS-ADRDA (National Institute of Neurological and Communicative Disorders and Stroke–Alzheimer’s Disease and Related Disorders Association), and the MMSE (20–24) were recruited from an outpatient clinic located at the Department of Psychiatry in Innsbruck, Austria. All patients with early AD were treated with cholinesterase inhibitors. Ten subjects (5 females, 5 males) were classified as having MCI without dementia (e.g., Petersen, 2004). They complained about subjective memory deficits, but had no evident functional impairment in daily-life activities. Also, they had mild impairment on one or two cognitive domains (scores in the neuropsychological testing were at or below 1.5 standard deviations of standardized norms). Twenty-three healthy subjects (16 females, 7 males) were selected from our healthy subject pool. Inclusion criterion for healthy elderly comparison subjects was a lack of cognitive impairment as obtained by the neuropsychological battery. None of the
M. Kerer et al.
544
Table 2. Demographic data and clinical characteristics (mean standard deviation) of the participants differentiated by diagnosis (controls, mild cognitive impairment [MCI] group, and early Alzheimer’s disease [AD] group)
Characteristic Age Education (years) MMSE Depression (GDS)
Controls (n ¼ 23; 16 F, 7 M)
MCI (n ¼ 10; 5 F, 5 M)
Early AD (n ¼ 10, 9 F, 1 M)
Chi-square
df
p valuea
71.83 7.44 10.09 2.23 29.57 0.66 8.7 6.2
78.7 6.72 12 4.27 26.4 0.84 9.7 4.5
79.4 5.89 8.7 1.16 21.8 1.4 10.8 5.75
8.153 5.199 36.337 1.681
2 2 2 2
EXPLICIT (SEMANTIC) MEMORY FOR MUSIC IN PATIENTS WITH MILD COGNITIVE IMPAIRMENT AND EARLY-STAGE ALZHEIMER’S DISEASE
Manuela Kerer Department of Psychology, University of Innsbruck, Innsbruck, Austria
Josef Marksteiner Department of Psychiatry, Medical University Innsbruck, Innsbruck, Austria and Department of Psychiatry and Psychotherapy A, Hospital Hall, Hall, Austria
Hartmann Hinterhuber Department of Psychiatry, Medical University Innsbruck, Innsbruck, Austria
Guerino Mazzola School of Music, University of Minnesota, Minneapolis, Minnesota, USA
Georg Kemmler Department of Psychiatry, Medical University Innsbruck, Innsbruck, Austria
Received 25 June 2012; accepted 15 December 2012. Address correspondence to Manuela Kerer, Department of Psychology, University of Innsbruck, Innrain 52 A, A-6020 Innsbruck, Austria. E-mail: [email protected]
Explicit Memory for Music in MCI and AD
537
Harald R. Bliem Department of Psychology, University of Innsbruck, Innsbruck, Austria
Elisabeth M. Weiss Department of Biological Psychology, Karl Franzens University Graz, Graz, Austria Background=Study Context: Explicit memory for music was investigated by using a new test with 24 existing and 3 newly composed pieces. Methods: Ten patients with mild cognitive impairment (MCI) and 10 patients with early stage of Alzheimer’s disease (AD) were compared with 23 healthy subjects, in terms of verbal memory of music by the identification of familiar music excerpts and the discrimination of distortion and original timbre of musical excerpts. Results: MCI and Alzheimer’s patients showed significantly poorer performances in tasks requiring verbal memory of musical excerpts than the healthy participants. For discrimination of musical excerpts, MCI and AD patients surprisingly performed significantly better than the healthy comparison subjects. Conclusion: Our results support the notion of a specialized memory system for music.
Music as an intervention is a safe and effective method for treating agitation and anxiety in moderately affected and severe dementia of the Alzheimer’s type (Sherratt, Thornton, & Hatton, 2004; Svansdottir & Snaedal, 2006). Preserved cognitive skills in the field of music may provide possibilities for interventions to improve communicational skills and other cognitive functions in patients affected with this disease (Baird & Samson, 2009). Moreover the notion of a specialized memory system for music—distinct from other domains such as verbal and visual memory—could emerge. This would suggest that memory for music engages brain regions that are not affected by Alzheimer’s disease (AD) pathology (Peretz & Coltheart, 2003). Therefore, proof of preserved memory for music in mild cognitive impairment (MCI) and early AD patients is of great clinical and scientific relevance. Dementia is characterized by progressive decline in cognitive functions such as memory, attention, and language, leading to impaired abilities to perform activities of daily living and also to neuropsychiatric symptoms or behavioral changes. The transitional state between
538
M. Kerer et al.
cognitive changes of normal aging and fully developed clinical features of dementia constitutes the diagnostic group of MCI. MCI patients typically have intact activities of daily living, but report about memory problems and show slight deficits in objective neuropsychological tests (test scores, 1.5 standard deviations below the average of standardized norms) that are not of sufficient severity to define dementia (Winblad et al., 2004; Morris et al., 2001; Petersen, 2004; Petersen et al., 1999, 2001; Tierney et al., 1996). However, it should be noted that the term MCI has been controversially discussed, because it covers diverse populations of patients who attend memory clinics and a range of pathological disorders (Dubois & Albert, 2007). Memory for Music Baird and Samson (2009) propose a concept of different types of musical memory as described in nonmusical domains that may be differentially impaired in AD. Long-term memory can be described as representative of two different forms: explicit and implicit memory. This is a distinction that has become fundamental since Tulving first proposed it in 1972. Explicit (declarative) memory is the conscious, intentional recollection of previous experiences, events, facts, and information. It is divided into episodic and semantic memory, which are both associated with different kinds of conscious awareness (Tulving, 2002). Related to these distinctions, episodic musical memory can be defined as the ability to retrieve the spatiotemporal, personal, and emotional contexts of the musical experience. On the other hand, semantic or conceptual musical memory is responsible for factual musical knowledge, associative or emotional concepts that are not linked to the retrieval of a specific personal experience or autobiographical event. Implicit (nondeclarative) memory is characterized by a lack of conscious awareness in the act of recollection, including priming, procedural memory, or motor skill learning, which are critical for playing a musical instrument (Baird & Samson, 2009). Samson and Peretz (2005) examined the relationship between musical preferences and prior exposure to music in patients with either left or right temporal lobe lesions and in one amnesic patient with bilateral lesions of the temporal lobe. Participants with left temporal lobe lesions preferred the melodies to which they were previously exposed to, thereby demonstrating an implicit exposure effect on musical preference, whereas participants with right temporal lobe lesions did not show this effect. These findings suggest that right temporal lobe structures play a critical role in the formation of melody
Explicit Memory for Music in MCI and AD
539
representations that support both priming and memory recognition, whereas left temporal lobe structures are more involved in the explicit retrieval of melodies. In the case of the amnesic patient, the exposure effect on musical preference was also absent; however, repeated exposure to melodies was found to enhance both musical preference and recognition. This remaining capacity of the patient’s memory observed through melody repetition suggests that extensive exposure may assist both implicit and explicit memory in the presence of global amnesia. Mazzola (2002) strongly supports a key function of music in opening memory contents, according to the hippocampal gate function as suggested by Winson (1985), by stimulating the hippocampal formation. Text and melody of a song seem to have separate representations in memory, making singing a dual task to perform, at least in the first steps of learning. Musical training has little impact on performance in this field, suggesting that vocal learning is a basic and widespread skill (Racette & Peretz, 2007). Neural Correlates Lesion and neuroimaging studies of musical memory demonstrate involvement of temporal and frontal lobe regions. Familiar music is associated with bitemporal activation (Platel, 2005) and bitemporal damage seems to cause music agnosia, or an inability to recognize familiar melodies (Peretz, 1996; Peretz & Gagnon, 1999). Eustache, Lechevalier, Viader, and Lambert (1990) observed a patient with left temporoparietal lesion after ischemic brain damage that demonstrated impaired recognition of familiar melodies, but showed intact discrimination. They hypothesized that identification and discrimination involve distinct mechanisms within the processing of auditory stimuli, and that they may be selectively disrupted in brain-damaged subjects. Hsieh, Hornberger, Piguet, and Hodges (2011) tested patients with semantic dementia and highlighted the role of the right temporal pole in the processing of known tunes and faces. The majority of neuroimaging studies have reported activation within the auditory association areas of the superior temporal gyrus (Satoh, Takeda, Nagata, Shimosegawa, & Kuzuhara, 2006; Watanabe, Yagishita, & Kikyo, 2008; Zatorre, Halpern, Perry, Meyer, & Evans, 1996; Halpern & Zatorre 1999). Additionally, frontal regions and middle frontal lobes were associated with musical imagery of familiar melodies (Zatorre et al., 1996; Halpern & Zatorre, 1999). Furthermore, functional imaging studies (Platel, Baron, Desgranges, Bernard, & Eustache, 2003; Satoh et al., 2006) and focal lesion studies
540
M. Kerer et al.
(Stewart, von Kriegstein, Warren, & Griffiths, 2006) suggest the involvement of brain areas beyond the anterior temporal lobe, implicating a distributed network of perisylvian areas in processes such as familiar melody recognition. Neuropathological and atrophic changes associated with early pathology in AD are relatively focal, predominately affecting the temporal lobes, especially the medial temporal lobe memory system (Dickerson & Sperling, 2009). These changes implicate the hallmark feature of impaired episodic and semantic memory function; AD patients indeed exhibit deficits on explicit tasks (Kensinger, Shearer, Locascio, Growdon, & Corkin, 2003; Laisney et al., 2011; Carlesimo & Oscar-Berman, 1992). Nevertheless neuroimaging data suggest that musical memory relies on parts of the brain less affected by AD. Weinstein et al. (2011) examined a semiprofessional musician with semantic dementia and came to the conclusion that long-term representations of words and objects in semantic memory may be dissociated from meaningful knowledge in other domains, such as music. Memory for Music in AD Knowledge of musical structures may remain intact and accessible, even when explicit judgements and overt recognition have been lost (Tillmann, Peretz, Bigand, & Gosselin, 2007). In a study of Quoniam et al. (2003), AD patients were able to develop a positive affective bias of judgement for previously heard melodies. Music in general is able to stimulate long and short-term memory in patients with Alzheimer’s disease and increases self-esteem and social interaction in elders. Numerous studies have demonstrated the functionality of music therapy in patients with neurological disorders or dementia of Alzheimer’s type (Za´rate & Dı´az, 2001; Svansdottir & Snaedal, 2006; Guetin et al., 2009). Furthermore, exposure to music has been reported to produce transient increases in cognitive performance and music enhances attention processes or effects on autobiographical memory that can be demonstrated in Alzheimer’s disease (Thompson, Moulin, Hayre, & Jones, 2005; Irish et al., 2006). Explicit and Implicit Musical Memory in AD Case Studies Until now, several case studies in AD patients have shown that some forms of musical memory are spared in spite of dementia. Table 1 summarizes the results of these studies.
Explicit Memory for Music in MCI and AD
541
Table 1. Summary of case studies exploring musical memory in AD patients Authors (Year)
Patients
Results in regard to musical memory
Beatty et al. (1994)
Amateur musician (male) MMSE 20=30: ‘‘moderate’’
Cowles et al. (2003)
Amateur musician (male) MMSE 14=30: ‘‘moderate’’
Crystal, Grober, & Masur (1989)
Musician (male) Amnestic disorder; changed to AD after 7 years; MMSE not reported Amateur musician (female) MMSE 8=30: ‘‘severe’’ Musician (female) MMSE declined from 22=30 to 5=30: ‘‘severe’’ Music teacher (female) Two alternative diagnoses proposed: AD or Heidenhain’s disease
Intact procedural memory (trombone, Dixieland band) Impaired naming of well-known pieces that the patient was playing Ability to learn and recall a novel violin composition Mildly impaired naming of Christmas song titles Intact procedural memory (piano) Impaired naming of composer= title of familiar pieces
Cuddy & Duffin (2005) Fornazzari et al. (2006) Polk & Kertesz (1993)
Vanstone, Cuddy, Duffin, & Alexander (2009)
Amateur musician (female) MMSE 17=30: ‘‘moderate’’
Intact recognition of familiar music Intact procedural memory (piano) Ability to learn and recall a novel piano composition Correct naming and singing of the last note of familiar melodies; correct naming from written notation Impaired procedural memory (piano) Correct distinction of familiar from unfamiliar tunes and lyrics of tunes Correct singing of tunes after heard its spoken lyrics
Dissociation between explicit (semantic) and implicit (procedural) musical memory forms is apparent, supporting Baird and Samson’s (2009) proposal for distinction of these types of musical memory. Group Studies Few studies have investigated the association between memory for music and dementia in larger population groups. Vanstone and Cuddy (2010) compared 12 patients with moderate or severe AD and 12 healthy, older adult controls in distinguishing familiar from novel tunes, in identifying distortions in melodies, and in singing familiar tunes. A significant impairment of the AD participants was shown. In contrast, comparing each individual case with the control group revealed that five participants from the AD group performed
542
M. Kerer et al.
within the range of the control group on most tasks. Four participants performed below the range of the control group, but their scores were above the level of chance. Halpern and O’Connor (2000) presented short, unfamiliar melodies to young and older adults and to AD patients. Young adults showed retention of the melodies, older adults showed little explicit memory but did show the mere exposure effect, whereas AD patients showed neither. No correlation between musical and verbal long-term memory was found in Alzheimer’s patients and in older healthy adults (Me´nard & Belleville, 2009). Bartlett, Halpern, and Dowling (1995) found that distinguishing different sources of global familiarity is a factor in tune recognition and suggested that this type of source monitoring is impaired in AD. Quoniam et al. (2003) examined recognition of unfamiliar melodies in 10 patients with mild AD (Mini-Mental State Examination [MMSE] score: 22–25). In comparison with age-matched healthy controls and depressed patients, AD patients showed significantly impaired recognition of unfamiliar melodies. Aims and Hypothesis of this Study The purpose of the current study was twofold. Firstly, we wanted to test explicit memory for music in different stages of early dementia in terms of identification of familiar music excerpts. For this purpose, subjects were instructed to name the title of the music piece, or if the subject failed, to associate freely where they knew the piece from, or for the easiest stage, to recognize the correct title out of four possible titles. Secondly, we wanted to analyze explicit memory of participants in terms of ability to discriminate by exploring their ability to remember familiar melodic lines. For this purpose, the participants judged whether pieces were correctly rendered and utilized their memory of the timbre (vocal vs. instrumental). We hypothesized lower outcomes in the title-naming task, in free-associating, and in choosing out of four titles for MCI and early-dementia participants in comparison with the controls. But concerning the discrimination of the distorted musical excerpts and the judging of the original instrumental or vocal presentation, we suggested a trial within the control group range for the clinical group. Our findings may contribute to solve the question to which extent various dimensions of musical recognition and explicit memory for music are spared in MCI and early dementia.
Explicit Memory for Music in MCI and AD
543
METHODS Subjects: Demographic Data and Clinical Characteristics Forty-three subjects older than 60 years, with intact auditory functions, normal or corrected-to-normal sight, were tested on an extensive neuropsychological battery. This included the MMSE examination (Folstein, Folstein, & McHugh, 1975), verbal memory tests (learning, free recall, and recognition subtests of the CERAD [Consortium to Establish a Registry for Alzheimer’s Disease] battery; Rosen 1984), figural memory tests (free recall, CERAD, NAI [Nu¨rnberger Alters-Inventar] figure test; Oswald & Fleischmann, 1997), object-naming tests (Boston Naming Test—short version, CERAD), categorical and lexical verbal fluency tests (animals=minute, words starting with s=minute), tests on planning (CLOX [An Exclusive Clock Drawing Task] Test Part 1; Sunderland et al., 1989), constructive abilities tests (copy geometrical shapes, CERAD, CLOX Test Part 2), assessment of divided attention and cognitive flexibility (Trail Making Test-B; Reitan & Wolfson, 1985). Furthermore, depression was evaluated with the Geriatric Depression Scale (GDS; Yesavage et al., 1982). Additional investigations included an informal interview, computed tomography (CT) or magnetic resonance imaging (MRI) of the brain and routine blood samples. Overall exclusion criteria for participation were history of stroke, head trauma, substance abuse, and major neurological (other than Dementia Alzheimer’s type or MCI), psychiatric, or metabolic disorders that may compromise cognition. Ten patients (9 females and 1 male) with early AD, diagnosed according to the criteria of DSM-IV-TR (Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision), NINCDS-ADRDA (National Institute of Neurological and Communicative Disorders and Stroke–Alzheimer’s Disease and Related Disorders Association), and the MMSE (20–24) were recruited from an outpatient clinic located at the Department of Psychiatry in Innsbruck, Austria. All patients with early AD were treated with cholinesterase inhibitors. Ten subjects (5 females, 5 males) were classified as having MCI without dementia (e.g., Petersen, 2004). They complained about subjective memory deficits, but had no evident functional impairment in daily-life activities. Also, they had mild impairment on one or two cognitive domains (scores in the neuropsychological testing were at or below 1.5 standard deviations of standardized norms). Twenty-three healthy subjects (16 females, 7 males) were selected from our healthy subject pool. Inclusion criterion for healthy elderly comparison subjects was a lack of cognitive impairment as obtained by the neuropsychological battery. None of the
M. Kerer et al.
544
Table 2. Demographic data and clinical characteristics (mean standard deviation) of the participants differentiated by diagnosis (controls, mild cognitive impairment [MCI] group, and early Alzheimer’s disease [AD] group)
Characteristic Age Education (years) MMSE Depression (GDS)
Controls (n ¼ 23; 16 F, 7 M)
MCI (n ¼ 10; 5 F, 5 M)
Early AD (n ¼ 10, 9 F, 1 M)
Chi-square
df
p valuea
71.83 7.44 10.09 2.23 29.57 0.66 8.7 6.2
78.7 6.72 12 4.27 26.4 0.84 9.7 4.5
79.4 5.89 8.7 1.16 21.8 1.4 10.8 5.75
8.153 5.199 36.337 1.681
2 2 2 2
