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Piano playing in Alzheimer's disease: Longitudinalstudy of a single caseWilliam W. Beatty a , Clara L. Rogers a , Rubin L. Rogers a , Shelley English b , JulieA. Testa a b , Diana M. Orbelo b , Don A. Wilson c & Elliott D. Ross ba Department of Psychiatry and Behavioral Sciences , University of Oklahoma HealthSciences Center , PO Box 26901, Oklahoma City, OK, 73190b Oklahoma City Veterans Affairs Medical Center , Center for Alzheimer's andNeurodegenerative Diseases ,c Department of Radiological Sciences Oklahoma , Oklahoma City, USAPublished online: 17 Jan 2008.

To cite this article: William W. Beatty , Clara L. Rogers , Rubin L. Rogers , Shelley English , Julie A. Testa , Diana M.Orbelo , Don A. Wilson & Elliott D. Ross (1999) Piano playing in Alzheimer's disease: Longitudinal study of a singlecase, Neurocase: The Neural Basis of Cognition, 5:5, 459-469, DOI: 10.1080/13554799908402740

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Neurocose ( 1999) Vol. 5. pp. 459469 0 Oxford Univrrsity Press 1999

Piano Playing in Alzheimer’s Disease: Longitudinal Study of a Single Case

William W. Beattyl, Clara L. Rogers’, Rubin L. Rogers‘, Shelley English2, Julie A. Testa112, Diana M. Orbelo2, Don A. Wilson3 and Elliott D. Ross2

’Department of Psychiatry and Behavioral Sciences, University of Oklahoma Health Sciences Center, PO Box 26901, Oklahoma City, OK 731 90, *Oklahoma City Veterans Affairs Medical Center, Center for Alzheimer’s and Neurodegenerative Diseases, 3Department of Radiological Sciences, Oklahoma City, Oklahoma, USA

Abstract

Preserved musical performance by patients with Alzheimer’s disease (AD) has been attributed to an intact system for implicit musical cognition which may be localized in the right hemisphere. To examine this idea more thoroughly, we studied patient ML, a woman with AD who learned to play the piano as a child. Over three yearly evaluations, ML exhibited progressive deterioration in the following domains: language, visuospatial functions, attention, sequencing, picture priming, recognition of familiar songs, and discrimination of rhythm, meter, transposition, and major from minor keys, but pursuit rotor learning remained intact. By the third year of testing, ML also exhibited severe limb apraxia, but showed only subtle losses in the quality of her piano playing of familiar songs. She also showed immediate and accurate transfer of her playing skill from the piano to the xylophone. Preserved musical performance in AD seems to depend on circuits involving the basal ganglia, cerebellum and motor areas of the thalamus and cerebral cortex that remain relatively intact until the late stages of the disemse, but there is no evidence that the right hemisphere plays a special role in this phenomenon.

Introduction

Several recent reports (Beatty ef a/., 1988, 1994; Crystal et al., 1989; Polk and Kertesz, 1993) describe patients who met modem diagnostic criteria for possible or probable Alzheimer’s disease (AD) (McKhann et d., 1984) and continued to play musical instruments skillfully. For one of these patients, the diagnosis of AD was subsequently con- firmed by brain autopsy (Beatty ef a/., 1997).

Theoretical accounts of the phenomenon of preserved musical skill in AD have often assigned a major role to remote implicit memory. For example, Crystal ef nl. ( 1989), who demonstrated that their patient (a pianist) performed normally on a mirror-reading task, invoked this explanation, which is plausible because group studies of patients with AD indicate normal acquisition of simple motor skills (Dick, 1992; Eslinger and Damasio, 1986).

Polk and Kertesz (1993) studied two accomplished musi- cians with progressive dementia (possibly AD). The first patient, a guitarist, showed substantially greater atrophy of the left cortex than of the right. He continued to play the guitar skillfully and performed well on most other tests of music production, although he could not reproduce rhythms or write or copy music. The second patient, a pianist, suffered

primarily posterior cortical atrophy which was greater on the right side. She was not aphasic and could reproduce rhythms, but she was unable to play the piano competently. Noting that studies of patients who suffered unilateral strokes, surgical resection or unilateral intracarotid injections of anesthetics support the idea that language and artistic endeavors are subserved by largely separate circuits in the left and right hemispheres (Alajounine, 1948; Milner, 1962; Smith, 1966; Gordon and Bogen, 1974; Basso and Capitani, 1985), Polk and Kertesz ( 1993) suggested that relative sparing of right hemisphere function might be important for preserved musical ability in dementia. They also argued that their two case studies described above supported the existence of two parallel cognitive systems: ‘a left hemisphere system concerned with language, temporal sequence, and analytic musical processing and a right hemisphere system concerned with implicit musical cognition’.

The idea that preserved musical performance in AD depends upon the operation of an intact remote implicit memory system has considerable intuitive appeal because all of the patients learned to play musical instruments early in life and continued to practice their skills throughout adulthood.

Corresporiclrnce fo: William W. Beatty. Department of Psychiatry and Behavioral Sciences, University of Oklahoma Health Sciences Center. PO Box 26901 Oklahoma City. OK 73190. USA. Tel: (405) 271-2474: Fax: (405) 271-6236; e-tnail: william-beatty@ouhsc.edu

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460 W. W. Beatty er al.

Furthermore, three of. the patients who retained abilities at musical performance were impaired on tests that required them to identify songs or compositions that were played for them (Beatty er a/., 1988, 1994; Crystal et al., 1989). Yet each of these patients was able to play to command compositions whose titles they could neither recall nor recognize. These observations seem to fit the distinction (Cohen and Squire, 1980) between ‘knowing how’ and ’knowing that’ which characterizes implicit (procedural) and explicit (declarative) memory systems, respectively.

Other data, however, appear to pose difficulties for the remote implicit memory account of preserved musical per- tormance in AD. Patient GW, a pianist, was clinically apraxic and could not dress herself. She was unable to learn the Pursuit Rotor test of motor skill, even at the slowest turntable speed, but she showed immediate transfer when asked to play a simple tune on the piano and then on the xylophone, an instrument on which she had no formal training and had not seen for at least 1 1 years immediately before testing (Beatty ot a/, , 1988). Patient T, whose pre- and post-morbid trombone playing skill could not be discriminated except by professional musicians, did learn the Pursuit Rotor task, but he could not tie his shoes or his necktie, and another member of his Dixieland jazz band had to assemble his trombone before he could perform (Beatty er al., 1994, 1997).

The idea that retained musical performance in AD depends upon relative preservation of right hemisphere systems has also encountered difficulty. Beatty and Greiner ( 1998) studied 3 I dementia patients; 22 met criteria for possible or probable AD (McKhann er d. , 1984) and nine were considered to have vascular or mixed dementias (Roman et al., 1993). Based on reports from relatives and care-givers, as well as blind ratings of tape recordings of actual performances, 12 were considered musically skilled, seven were considered formerly musically skilled, and 12 were never musically skilled. The three groups were comparable in age, education and overall severity of dementia as assessed by the Mini- Mental State Exam (MMSE; Folstein er al., 1975). They also showed equally severe impairments on the Boston Naming Test (BNT; Kaplan er d., 1983), a measure of left hemisphere functioning, and the WISC-R Block Design Test (Wechsler, 1974). a measure of right hemisphere functioning.

Although the findings of Beatty and Greiner (1998) provide no evidence for relative sparing of right hemisphere functions in dementia patients who retain skill at musical performance, the data should be interpreted cautiously because of method- ological limitations that beset any cross-sectional study on this subject. These include low statistical power, the necessity of grouping patients with different performance skills (i.e. keyboard players, guitarists, horn players, solo singers, etc.), and the absence of pre-morbid recordings to determine whether the currently and formerly skilled musicians were of comparable skill before the onset of their dementias.

Longitudinal studies of individual patients with retained musical skills could circumvent some of the difficulties inherent in group studies by permitting comparison of neuro-

psychological (NP) test performance, brain structure, and musical knowledge and performance as they change over time with the progression of the patients’ demrntias. In the present paper, we describe a pianist with probable AD who was studied longitudinally as her MMSE scores declined from 13 to 5 over three annual evaluations. The NP battery included measures of implicit memory, left and right hemi- sphere function, attention, sequencing and semantic memory. These tests permitted evaluation of the hypothesis of Crystal et a/ . ( 1989) and Polk and Kertesz ( 1993).

Other tests, derived from the literature on music education, were designed to measure components of piano-playing ski I I . Musical knowledge and playing skill were evaluated u\ing techniques we developed and used in previous studies (Beatty et d., 1988; Beatty and Greiner, 1998). Finally, during the third year of the study, we attempted to teach her a song that was published after the onset of her dementia arid examined the transfer of her playing skill from the piano to the xylophone.

Case description ML is a right-handed Caucasian woman with 10 years o f education. She was 79 years old at the initial (Year I ) assessment. ML was born and raised in upstate New York. Following completion of schooling, she worked intermittently as a cook and a waitress, although her principal occupation was homemaker. ML has no formal training i n music; as a child, she learned to play the piano and the organ in church choir. Although her daughter believes that she may have been able to sight-read music a little, her principal way of learning to play new compositions was always by ear. Despite the family’s limited economic means, her daughter reports that ML always had an organ in the home.

ML suffered a serious bout of tuberculosis during the early 1940s, but recovered without persisting complications. She has suffered from hypertension (controlled by medica- tion) for about 20 years. Otherwise, her medical history is unremarkable.

Following the death of her husband when ML was 70. shc moved in with a daughter who lived in upstate New York. After about 2 years, that daughter’s failing health prevented her from caring for ML and at age 72 ML moved to Oklahoma to live with another daughter, where she still resides. For the next 3 years, ML experienced moderate memory problems which were attributed to aging by her physician. At age 75. her cognitive abilities began to decline and i1 diagnosis of dementia was considered, but NP evaluation was not performed. NP evaluation in Year I (age 79) established the existence of dementia unambiguously. Repeated testing (Year 2) demonstrated deterioration of cognitive function. An MR scan of the head revealed cortical and hippocampal atrophy and enlarged lateral ventricles without evidence of tumors, other intracerebral masses, infarcts or lacunes. Considering these results, as well as her medical history, the diagnosis of probable AD was made according to the criteria of’ McKhann

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Musical skill in Alzheimer's disease 461

et al. (1984). Results of NP testing and a second MR scan performed 1 year later, which revealed continued cognitive decline and hippocampal and cortical atrophy, support the diagnosis of probable AD.

Ten healthy elderly subjects who averaged 76.0 years of age (range 69-87) and 11.1 years of education (range 8-14) served as controls for the NP tests. Each control was tested once. Control subjects and ML's caregiver provided written informed consent after a thorough explanation of the proced- ures, which were approved by the local Institutional Review Board.

Procedure

ML was studied in three evaluations separated by approxi- mately 1 year. At each evaluation, the following data were collected.

1. Global Dementia Severity was measured with the MMSE (Folstein et d., 1975).

2. Language was measured with: (a) a 30-item version of the BNT (Kaplan et al., 1983), (b) a modified version of the Token Test (Lezak, 1995) consisting of 20 one- stage and 20 two-stage commands, and (c) a letter fluency test (FAS) and a category fluency test (animals, fruits, vegetables). For each component of the fluency tests, 60 s were allowed for the production of words that begin with the designated letter or were exemplars of the target category. At Year 3 only, the Western Aphasia Battery (Kertesz, 1982) was administered.

3. Visuospatial function was measured using the Block Design test from the WISC-R (Wechsler, 1974). The WISC-R version was used instead of the WAIS-R to reduce floor effects. In addition, the task of copying the intersecting pentagons from the MMSE was scored in the conventional way (0 = wrong, 1 = right) and with a more refined seven-point scale (0-6) adapted from Fisher et al. (1997). At Year 3 only, the Line Orientation and Facial Recognition Tests (Benton et al., 1983) were administered.

4. Attention was measured with: (a) Forward Digit Span from the WAIS-R (Wechsler, 1981), (b) Forward Visual Memory Span from the WMS-R (Wechsler, 1987) and (c) the letter and symbol cancellation tasks devised by Mesulam (1985). With the target letter or symbol in view, subjects attempted to cancel as many targets as possible as quickly as they could. Trials were terminated when subjects indicated they could not cancel any more targets. For both tests, the targets and distractors were randomly arrayed about a 21.6X27.9 cm sheet of paper.

5. Sequencing was studied using Part A of the Trailmaking Test (Reitan, 1958) and with a test of sequencing involving everyday activities (brushing your teeth, ordering a meal at a restaurant, changing a lightbulb, doing the laundry). For each problem, subjects were shown cards on which one component of the set of actions required to achieve the goal was printed (e.g. get

toothbrush, get toothpaste). Subjects were asked to order the set of cards to describe the sequence in which the actions would be performed to accomplish the objective.

6. Implicit memory was measured in three ways. Remote implicit memory was assessed with a systematic test of praxis modified from a test developed by Rapczak et (11.

(1989). The dependent variable was the number of actions performed correctly to command (i.e. pantomime). Two measures of anterograde implicit memory included the following. (a) Performance on 10 learning trials on the Pursuit Rotor test. With the turntable speed set at 30 r.p.m., subjects attempted to maintain contact of the stylus on a circular spot (1.8 cm in diameter) located near the edge of the turntable. Trials were 20 s long with an intertrial interval of 20 s. (b) The Gollin Figures Test (Gollin, 1960). The version used was identical to that used by Beatty et ul. (1998), including the length of the delay between Trials 1 and 2. After three practice tests, subjects attempted to name each of 20 degraded line drawings of common objects. On Trial 1, drawings were presented for 3 s in four blocks, beginning with the most degraded drawing of each object. Then, complete drawings of the objects were presented and subjects attempted to name these. After a 10 min delay filled with other tests, the procedure was repeated (i.e. Trial 2).

Musical knowledge and components of playing skill

I . The Christmas Tunes Test (Beatty et d., 1988) provides a measure of explicit knowledge of music. Subjects were played tape recordings of vocal versions of 20 well- known Christmas tunes and asked to name each tune. For items not correctly recalled, subjects were shown an index card on which the correct title and three plausible distractors were printed. They were asked to select the correct title from the four alternatives. Previous findings (Beatty et al., 1988) showed that nearly all normal controls, regardless of whether they had musical skill, recalled at least 18 titles correctly.

2. The Seashore Rhythm Test (Lezak, 1995) requires sub- jects to state whether each of two sound patterns have the same or different rhythms. Because the standard version of the test is much too difficult for dementia patients to perform, a modified version in which the interval between test pairs was lengthened was used (Beatty et al., 1988). On Year 3 only, the tester tapped out rhythms on a table and ML attempted to imitate them.

To test identification of notes on both clefs and octaves, notes were played on the piano. Subjects were asked to name the note and then play the note that was one octave higher or lower. To test ability to identify major and minor keys, tape recordings of various scales, chords and short passages of music were played, and subjects were asked to indicate whether the recorded segment was in a major or minor key. To test the ability to recognize transposition, subjects were played a series of two short melodies. In some of the pairs,

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363 W. W. Beatty ot al.

the two melodies were identical, while in others the second melody was transposed to a different key. For each pair of melodies, subjects indicated whether the melodies were the same or different. Meter perception was tested by playing a tape recording of excerpts of five waltzes and five marches. For each selection, subjects indicated whether the excerpt was a waltz or a march. Finger dexterity was tested by asking subjects to touch each finger in order forwards and backwards as rapidly as possible, and to imitate different finger move- ments made by the tester. Six healthy elderly pianists attained maximum scores on each of the above tests.

Piano-playing skill

To assess M L s ability to play the piano, videotape recordings were made while she played at the adult day care center she attends. She played tunes from her repertoire from memory. Examples included ‘Amazing Grace’, a church song, ‘Silent Night’. a Christmas song, and ‘Oh Susanna’, an American folk song. These recordings were played to two panels of raters who were blind to the year in which the recording was made. One panel ( N = 8) comprised professional music teachers from the Oklahoma City area; the other panel ( N = 7 ) comprised amateur musicians.

For each year, raters evaluated the quality of ML‘s playing on five-point Likert-type scales ( 1 = poor, 5 = excellent) tor accuracy, articulation, interpretation/style, rhythm, tempo, tone. quality and posture, attributes of skilled performance identified in the music education literature (Lehman, 1968; Colwell, 1970; Wing, 1971). Written definitions of these attributes were provided to the raters before and during the ratings. Subjects were also asked to rate the overall quality of M L s playing for each of the 3 years and to rank the quality of her playing skill from I = best to 3 = worst xross the three yearly sessions.

In a previous published study (Beatty and Greiner, 1998) of different elderly musicians, the inter-rater reliability for two skilled musicians who were blinded to the group status of the elderly musicians was moderately high ( r = 0.74). In a subsequent unpublished study, two different skilled musicians who were blinded to the group status of the elderly musicians achieved comparable inter-rater reliabilities ( r = 0.78).

Learning a new song

To ensure that ML could not have known the ‘new’ song pre-morbidly, we selected a song that was published in 1993, about I year after the estimated onset of her dementia. The song, ‘Jesus Will Still Be There’, was chosen because it is a gospel song, the type of music ML preferred, according to her daughter, who confirmed that ML had never heard the song before our study.

We employed several strategies in our attempt to teach ML. Initially, a skilled pianist (CLR or RLR) played alongside ML, encouraging her to imitate. On these initial training \essions, a tape recording of the song (instrumental version

on the piano) was played. The teachers first demonstrated the notes and added the chords. Training spanned approxi- mately 30 h over about 2 months. In addition, ;I copy of the tape was provided to ML‘s daughter, so that ML might listen to the song as often as possible.

We hoped to capitalize on the fact that ML played by ear. In our earlier attempt to teach a new song to patient GW (Beatty et ul., 1988), we discovered that although she could still sight-read, the shift in attention required at the end of the line completely disrupted GW’s performance.

Results

Table 1 summarizes the NP findings for the 3 years of testing for ML and for elderly controls. Here it can be seen that ML‘s performance on most of the language tesrs paralleled the decline in her overall cognitive status as indexed by the MMSE. The similarity in pattern of decline to that seen tor the MMSE was particularly clear for the BNT and FAS tests: performance on the category fluency test appeared to reach nadir by Year 2, whereas performance on the Token Test declined precipitously from Year 2 to Year 3. Performance on the Western Aphasia Battery, given on Year 3. was severely impaired (Aphasia Quotient = 60.5).

Performance on the various measures of visuospatial cogni- tion also declined in parallel to changes on the MMSE. Because Polk and Kertesz ( 1993) suggested that preserved musical playing skill in AD is associated with relative sparing of right hemisphere functions, it is important to compare ML‘s performances on the BNT and Block Design tests. Typically, this has been accomplished by expressing patients‘ performances on these tests as Z scores relative to perfornm- ance by age- and education-matched normal controls (Delis et ul., 1992). Because the variability in the Performance of the normal elderly on Block Design is much greater than on the BNT, Z scores for patients will usually be rnuch lower (i.e. more negative) on the BNT than on Block Design, which could lead to the illusion of right hemisphere sparing. To correct this problem, we created a measure, Per cent Deterioration, which adjusts the differential variability in the performance of the normal elderly on the BNT and Block Design tests. Using data from a population of approximately I00 healthy elderly controls obtained from the University of California at San Diego Alzheimer Disease Research Center as the reference, ML‘s performances on the BNT and Block Design tests were expressed as Z scores relative to the performance of controls of comparable age and education. Then, the maximum possible deterioration in Z score units given a raw test score of zero was calculated for the subgroup of controls of similar age and education to ML. Finally, M L s Z score for a particular test was divided by the Z score associated with a raw score of zero and the resulting ratio was converted to Percent Deterioration. Direct comparison of the percent deterioration by M L on the BNT versus the Block Design test reveals that deterioration on Block Design was substantially worse than on the BNT for al l 3 years.

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464 W. W. Beatty et al.

Table 2. Performance by ML on tests of music knowledge and components of playing skill

Year I Year 2 Year 3

Christmas Tunes Recall/?O Recognitiod20

Seoshore Rhythm/30 Identify Notes/X Identity OctavedB Ma,jor/M i nor

Scales/S Chords/S Paasages/-l

Meter PerceptiodlO l'ransposition/J Finger Dexterity/S

9 17 22

X X

S 5 4

10 4 5

3 20 22 n n 5 5 4

10 4 5

2 6

15 8 n 3 4 3 2 2 5

Table 3. Mean ratings 0 1 ML's playing skill

Year I Year 2 Year 3 F(2.28) for years

Overall performance Ratings Ranks

Attributes of skill Accuracy Articulation Interpretatiodstyle R h y t h in Tern po Tone quality Posture

3.60 3.28 3.13 1.40 2.33 2.27

3.21 3.07 2.93 3.46 3.46 3.08 3 . m 3.73 3 .20 3.40 2.93 3 .13 3.53 3.27 3.27 3 .50 3.40 3.30 3.87 3.80 3.53

< I 5.2 I *

< I 1.91 5.09* I .95 1.16

< 1 I .8n

Musical knowledge and components of playing skill

On the Christmas Tunes test (Table 2), ML performed poorly on recall for Years 1-3, but on Years 1 and 2 her performance improved substantially with recognition testing. By Year 3, even recognition of familiar Christmas tunes was grossly impaired.

On the Seashore Rhythm test, ML's performance for Years I and 2 was impaired but clearly above chance (i.e. raw score of IS). By Year 3, her performance was at chance. At Year 3, she was unable to copy rhythms tapped out on a table by the tester.

On each of the annual tests, ML attained maximum scores on tests of identifying notes and octaves, and finger dexterity. On Years 1 and 2, she also attained maximum scores on tests of meter perception, transposition, and identifying major and minor keys. By Year 3, her performance had clearly deteriorated on these measures.

Piano-playing skill

Table 3 summarizes the evaluations of ML's skill at playing the piano over the 3 years of the study. Preliminary analyses indicated no significant differences in the ratings by profes-

sional music teachers and amateur musicians, so the data from these two groups were pooled to increase statistical power.

In terms of overall rated quality, ML's performance showed a slight decline over time, which was not significant. However. when judges were asked to rank the quality of the perforrn- ances across years, 11 ranked ML's Year 1 performance best compared to two judges who favored Year 2 and two who considered the Year 3 performance of highest quality. Statistical analysis confirmed this pattern by showing that the average rankings for Year I were significantly better (i.e. lower numerical score) than those for Years 2 and 3 [ t ( 13) > 3.71, P < 0.0011.

Ratings of the attributes of playing skill exhibited a similar pattern to those of overall performance quality. On all attribute measures, ratings were higher (i.e. better) for Year I , but the main effect of year reached statistical significance only for the Interpretation/Style measure. Subsequent analysis showed that ratings on this measure were significantly lower for Year 3 compared to Years 1 and 2 [ t (14) > 2.34, P -: O.OSl, but there was no difference in the ratings for Years 1 and 2 .

These observations generally concur with those of M L s daughter. She reported that ML had exhibited a steady decline in the initiation of keyboard playing during the 9 years she had resided in the daughter's home, but no loss in the repertoire of songs that she actually played.

Cross-instrumental transfer of playing skill

At Year 3, ML's ability to transfer her playing skill from the piano to the xylophone was tested. First, the tester played 'Twinkle Twinkle Little Star' on the piano and MI, accurately played the song on the piano. Then, the tester performed ;L

single demonstration of how to play 'Twinkle Twinkle Little Star' on the xylophone (a child's toy xylophone was used). The tester then asked ML to play 'Twinkle Twinkle Little Star' on the xylophone, which she did immediately and accurately.

Learning a new song

Although ML was usually well motivated to attempt to play the unfamiliar song, her success was limited. On one occasion, she was able to play the entire song (4.5 min) accurately while listening to the tape recording; on two or three other occasions she played the introduction (approximately 1.5 min) accurately while listening to the tape recording. She was also able to play short segments (10-15 s) alone and from memory with cueing (approximately two notes) on several occasions. Inevitably, her performance broke down, usually because she began to play other gospel songs from her repertoire.

Although our attempt to teach ML to play a new song ultimately failed, it was more successful than our earlier effort with patient GW in the sense that ML remained highly motivated throughout the training and did play some passages correctly from memory. Matching the to-be-learnzd song to

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the patient's musical tastes and the fact that ML played by ear may account for the differential outcome.

Musical skill in Alzheimer's disease 465

1997 1998

MR findings

Figure 1 shows coronal MR sections of ML's brain at various levels from the basal ganglia to the cerebellum. For both Years 2 and 3 (MMSE = 9 and 5 , respectively), the ventricles and cortical sulci are enlarged bilaterally, and the basal ganglia, medial temporal lobe and cortical gyri are atrophied. On both the Year 2 and Year 3 scans, the atrophy seems somewhat greater on the left side of the brain. Differences in the severity of atrophy between the Year 2 and Year 3 scans are difficult to judge because the sections are not cut at exactly the same level. Although it is not clear in the figure, there was also mild bilateral atrophy of the cerebellar hemispheres.

Discussion

Over the course of the study, patient ML exhibited marked decline in a broad range of cognitive functions, including general abilities (expressive and receptive language, visuo- spatial construction, attention and sequencing), as well as capacities more closely linked to music (knowledge of Christmas tunes, identification of major and minor pieces, meter perception, transposition). Her performance also deteriorated on two of the three measures of implicit memory (praxis, picture priming). Despite these progressive losses, ML's ability to play the piano was only slightly affected.

In general, ML's retained ability to play the piano despite global dementia is consistent with other case reports in the literature (Beatty er id., 1988; Crystal rt al., 1989). What is distinctive about ML is the severity of her dementia and the fact that her piano-playing skill remained essentially intact, while her cognitive abilities including those related to music, declined progressively. Other studies of musicians with dementia have not reported longitudinal measures of cogni- tion and playing skill in a way that permitted a correlational analysis over time.

Fig. 1. Selected coronal sections from the 1997 (Year 2) and 1998 (Year 3) MR scans of patient ML's brain. The images are TI weighted (SETR775. TE18). The left side of the brain is shown on the right side of each section. (a) Note the bilateral enlargement of the lateral ventricles and the atrophy of the basal ganglia (arrows). The Sylvian Fissure (SF) is enlarged bilaterally and the cortical gyri are atrophied. (b) Note the bilateral atrophy of the hippocampi and adjacent structures of the hippocampal formation. The SF is enlarged bilaterally and the supramarginal gyrus (above the SF) and the superior temporal gyms (below the SF) are atrophied. The same pattern of gyral atrophy is evident in sections (c) and (d). (e) Note the atrophy of the angular gyrus (AG).

Neuropsychological issues

Polk and K e m z (1993) proposed the existence of a right hemisphere system concerned with implicit musical cognition

could support preserved musical ability in those dementia patients who exhibit this talent. Although the extent of lateral ventricular enlargement appeared greater on the left side of M L ' ~ brain, the MR scanS disclosed bihemispheric atrophy. NP testing documented global impairment at Year 1 which steadily worsened over the course of the study. Comparison of her performance on the BNT and Block Design test, a technique that has been used to classify AD patients with relatively greater left or right hemisphere dysfunction (Delis et al., 1992), revealed, if anything, greater impairment of right hemisphere function. However, it should

be emphasized that the NP tests demonstrated severe and generalized cognitive deficits.

Although ML performed normally on Trial 1 for each year on the Collin (fragmented) Figures task, her poor performances on the Line Orientation and Facial Recognition

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466 W. W. Beatty et a/.

tests are consistent with her severe impairment on the Block Design test; overall, these data suggest a pervasive pattern of right hemisphere dysfunction.

The persistence of ML's playing skill in the absence of evidence of right hemisphere sparing is consistent with our other studies (Beatty and Greiner, 1998) which revealed comparable deficits in left and right hemisphere functions among dementia patients who retained musical skill. One patient (Patient T; Beatty et al., 1994), whose trombone playing about 1 year after diagnosis with AD could not be distinguished from his pre-morbid level of skill, had greater atrophy of the right hemisphere than of the left (Graber et al., 1998). Taken together, these observations provide no support for the idea that preserved musical playing skill in AD is associated with relative sparing of the right (or left) hemi- sphere. I t should be noted, however, that neither the present nor earlier studies (Beatty and Greiner, 1998) included measures specific to right anterior cortical function.

Both Crystal et ul. (1989) and Polk and Kertesz (1993) attributed the retained playing ability of their patients to the operation of unspecified implicit memory systems. The general observation that ML's playing skill did not decline noticeably while her explicit musical knowledge (e.g. identi- fication of Christmas tunes) deteriorated progressively could be taken as support for the implicit memory explanation. Also consistent with the implicit memory explanation, ML showed normal learning on the Pursuit Rotor task. Most (Beatty et ul.. 1994; Beatty and Greiner, 1998), but not all (Beatty et d . , 1988), dementia patients who retained musical playing skill have performed normally on this test.

However, there are several difficulties with the simple implicit memory account. First, ML's performance on the test of praxis, which can be considered a measure of remote implicit memory, was severely impaired at Year 2 and worsened on Year 3. Her deficits in producing skilled move- ments to command (pantomime) might be attributed to her steadily worsening aphasia, but on the Year 3 tests she also failed to imitate movements involving the hands. Moreover, she pantomimed four of the five buccofacial movements correctly on Year 3, suggesting that she could understand the instructions for the task. Relative vulnerability of limb as opposed to buccofacial movements has been described previously for patients with AD (Rapczak et af., 1989), so ML appears typical in this respect. Acknowledging the difficulty of distinguishing failures arising from aphasia from those related to a loss of motor memory in such a severely demented patient, the contrast between ML's retained piano- playing skill and her performance in pantomiming and copying other highly overlearned motor responses is striking. Two other skilled musicians we have studied also exhibited dyspraxis, although not as severely as ML (Beatty et af., 1988, 1994). Further, the dementia patient studied by Polk and Kertesz (1993), and the stroke patient studied by Basso and Capitani ( 1985), retained musical skill despite severe disturbances in praxis. Evidently, there is little relationship between the neural mechanisms that control piano playing

and those that govern the skilled hand movements tested in the praxis examination.

The results of the Collin Figures picture priming test present a second problem for the implicit memory account. On this test, ML's priming scores steadily declined from Year 1 to Year 2, paralleling her losses in other cognitive domains. By contrast, she attained normal scores in identifying the fragmented figures on Trial 1 of each of the annual tests. This suggests that her worsening priming scores are more closely related to a memory defect than to a naming deticit. Although there is controversy about whether AD patients show normal (Gabrieli et a/., 1994) or somewhat impaired (Beatty et al., 1998) priming on the Collin Figures task. ML's steady decline in priming from Year 1 to Year 3 makes it highly unlikely that this implicit memory system is related to her retained playing skill.

Much research indicates that responses controlled by implicit memory systems are relatively inflexible; alterations in testing conditions between acquisition and retention usually lead to large losses in performance (Gabrieli, 1998). However, when asked to play a simple tune on the xylophone. ML showed immediate and accurate transfer from the piano. I n an earlier study, Beatty et al. (1988) observed a similar effect for another pianist with AD. Because playing the xylophone and the piano require different motor responses, 1 he implica- tion is that preserved musical skill in dementia involves something more than retention of specific highly overlearned motor sequences of the fingers. It is still reasonable to propose that preserved musical skill in dementia represents the action of some sort of implicit memory system, but the system must program general motor tendencies rather than specific motor responses.

Adequately testing the concept of a remote implicit memory system remains challenging because of the dissociation between praxis and musical performance demonstrated by ML and other dementia patients as described above. Thc alternative of inferring the status of remote implicit memory from performance on measures of anterograde implicit memory is also unsatisfactory. The heterogeneity in perform- ance across implicit memory tasks shown by lvlL is also evident in group studies (Salmon et l i l . , 1992; Meiran and Jelicic, 1995).

Neuroanatomical correlates

Examination of the MR scans revealed bilateral atrophy of the hippocampus and cortical gyri typical of a patient with AD. The extent of the atrophy in these brain areas could account for ML's profound and general impairments on most NP measures, including limb apraxia, which presumably relates to atrophy of the left angular and supramarginal gyri (Heilman and Gonzalez-Rothi, 1985). Her retained ability to play the piano, however, is probably controlled by other circuits. The obvious possibility is systems involving the motor parts of the thalamus and cortex and the basal ganglia

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Musical skill in Alzheimer’s disease 467

and cerebellum. These brain regions remain relatively intact until the end stages of AD (Kemper, 1984).

Sergent et al. (1992) used positron emission tomography to study healthy pianists while they performed a variety of musical tasks. Listening to music resulted in increased blood flow in the primary and secondary auditory cortices (areas 41 and 22). Compared to listening, playing and listening to scales played with the right hand resulted in activation of the left primary motor cortex (area 4) and the right cerebellum areas corresponding to the representation of the right hand as well as the left premotor cortex (area 6).

Consistent with the above formulation are observations of Patient T, the highly skilled trombone player who survived 3.5 years after he was initially studied (Beatty et d., 1994). Six months prior to his death, his caregivers reported that he could still play tunes on his trombone, provided that someone assembled the instrument, placed it into his hands and brought it up to his lips. At autopsy, which revealed the typical neuropathology of AD (Beatty er a/., 1997), the cerebellum was normal and there was mild neuronal loss with scattered plaques and tangles in the basal ganglia, the motor nuclei of the thalamus and the motor cortex.

Although a search of the literature did not reveal any studies of musically skilled patients, disease of the basal ganglia and cerebellum is often associated with deficits in acquiring motor skills such as pursuit rotor, mirror tracing and the serial reaction time task (e.g. Sanes et al., 1990; Willingham et c i l . , 1996; Gabrieli et d., 1997). Mildly to moderately demented patients with AD usually learn norm- ally, provided they can perform the tasks (e.g. Dick, 1992; Willingham et al., 1997).

The fact that MR scans revealed mild to moderate atrophy in the basal ganglia and cerebellum of ML‘s brain may appear to challenge the model developed above. However, ML showed normal pursuit rotor learning on all 3 years of testing. Because patients with diseases such as Huntington’s disease and Tourette’s syndrome, which affect the basal ganglia, are profoundly impaired on this task (Heindel et al., 1989; Stebbins et al., 1995; Gabrieli et ul., 1997), the implication is that the atrophy of the basal ganglia in her brain was comparatively modest.

In summary, the circuits that interconnect the basal ganglia, cerebellum and motor areas of the thalamus and cortex, which remain relatively intact until the end stages of AD, seem to be capable of controlling the performance of pre- morbidly acquired songs and tunes by musically talented dementia patients. The nature of the motor programs is not rigid or automatic, but somewhat flexible, as evidenced by the rapid and accurate shift from playing the piano to playing the xylophone shown by severely demented patients ML and GW (Beatty et al., 1988).

By contrast, the circuits that support skillful playing of well-known songs seem inadequate to allow learning to play new musical compositions. This might represent an incapacity of this circuitry to support new motor learning of this complexity or simply reflect disturbances of other cognitive

capacities such as sustained attention. Which explanation is correct is not clear because the only attempts to teach musicians with AD to play a new song involved patients whose dementia were already severe. Future longitudinal studies of less severely demented musicians with AD which combined NP and functional neuroimaging techniques could clarify the uncertainties about the neuroanatomical bases of preserved musical skills in dementia.

Acknowledgements

Partially supported by a grant from the Presbyterian Health Foundation. We thank Angela Brown, Almuth Kunkel, Charlotte Hanisch, Felix Hanisch, Janet Romanashin, Jennifer Ladd, Cynthia Pullin, Cynthia Jarboe, Judith Reeves, Shalah Smothers, Sylvia Ryan and Steve Serrell, who along with Ms Orbelo, Ms Testa and Ms English, served as expert raters, and Karen Hames for typing the manuscript. Dr David Salmon provided norms for healthy elderly persons on the BNT and the WISC-R Block Design. Drs James Scott, Julene Johnson and Alex Troster provided helpful criticism of an earlier draft. Finally, we thank ML and her daughter for their cooperation.

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Piano playing in Alzheimer’s disease: longitudinal study of a single case

W. W. Beatty, C. L. Rogers, R. L. Rogers, S. English, J. A. Testa, D. M. Orbelo, D. A. Wilson and E. D. Ross Abstract Preserved musical performance by patients with Alzheimer’s disease (AD) has been attributed to an intact system for implicit musical cognition which may be localized in the right hemisphere. To examine this idea more thoroughly, we studied patient ML. a woman with A D who learned to play the piano as a child. Over three yearly evaluations, ML exhibited progressive derioration in the following domains: language. visuospatial function>. attention, sequencing, picture priming. recognition of familiar songs, and discrimination of rhythm, mer. transposition, and major from minor keys, but pursuit rotor learning remained intact. By the third year of testing, ML also exhibited severe limb apraxia, but showed only subtle losses in the quality of her piano playing of familiar hongs. She also showed immediate and accurate transfer of her playing skill from the piano to the xylophone. Preserved musical performance in AD seems to depend on circuits involving the basal ganglia. cerebellum and motor areas of the thalamus and cerebral cortex that remain relatively intact until the late stages of the disease. but there is no evidence that the right hemisphere plays a special role in this phenomenon.

Journal

Neurocase Reference Number:

Primary diagnosis of interest

Author’s designation of case

Key theoretical issue

Neurocase 1999; 5 : 4.59-69

0170

Alzheimer’s disease

ML

Implicit and right hemisphere theories of preserved musical skill in dementia

Key words: Alzheimer’s disease; preserved musical skill

Scan, EEG and related measures

Standardized assessment MRI scan of the head

MMSE, BNT. Token test, Verbal Fluency, WISC-R Block Design, LOT. Facial Recognition, Digit Span, Visual Memory Span, Letter and Symbol Cancellation, Trails A. Praxis, Seashore Rhythm test

Other assessment Sequencing everyday activities. Pursuit Rotor, Gollin Figures test. Christmas Tunes test, Discrimination of rhythm, meter, transposition. major-minor key, ratings of performance skill

Lesion location

Lesion type

Language

Diffuse atrophy

Not known

English

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