Episodic Encoding in Normal Aging

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Aging, Neuropsychology, and Cognition: A Journal on Normal and Dysfunctional Development Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/nanc20

Episodic Encoding in Normal Aging: Attentional Resources Hypothesis Extended to Musical Material a

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Sophie Blanchet , Sylvie Belleville & Isabelle Peretz

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Department of Psychology , University of Montreal , Montreal, Quebec, Canada Published online: 01 Feb 2007.

To cite this article: Sophie Blanchet , Sylvie Belleville & Isabelle Peretz (2006) Episodic Encoding in Normal Aging: Attentional Resources Hypothesis Extended to Musical Material, Aging, Neuropsychology, and Cognition: A Journal on Normal and Dysfunctional Development, 13:3-4, 490-502 To link to this article: http://dx.doi.org/10.1080/13825580500428492

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Aging, Neuropsychology, and Cognition, 13:490–502, 2006 Copyright © Taylor & Francis Group, LLC ISSN: 1382-5585/05 print; 1744-4128 online DOI: 10.1080/13825580500428492

Episodic Encoding in Normal Aging: Attentional Resources Hypothesis Extended to Musical Material

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1744-4128 1382-5585/05 NANC Aging, Neuropsychology, and Cognition Cognition, Vol. 00, No. 0, June 2006: pp. 1–36

EpisodicBlanchet Sophie Encoding et al. in Normal Aging

SOPHIE BLANCHET, SYLVIE BELLEVILLE AND ISABELLE PERETZ Department of Psychology, University of Montreal, Montreal, Quebec, Canada

ABSTRACT The goal of the present study was to examine age-related changes in musical episodic memory for novel tunes. This was conducted by manipulating the encoding condition in a recognition paradigm. After receiving memory instructions (intentional condition), older and younger participants obtained equivalent hits. In contrast, when intentional encoding was accompanied by a dancing judgment (dancing + intentional condition), the recognition performance of the older persons was severely impaired. Impaired recognition was also found when participants only judged the excerpts without being instructed to memorize them (dancing judgment condition). Although older participants demonstrated a preserved ability to perform the dancing judgment on its own, this ability was not optimal and likely precluded the initiation of more elaborate encoding strategies. These results suggest that asking older persons to divide their attention in the study phase reduces the quality of their musical encoding. Given this extension to musical material, we discuss the notion that the age-related attentional resource decline appears to be domain-general rather than specific to verbal material.

According to one major model of aging and memory, age-related memory decline results from a decrease in attentional resources (Craik, 1986, 1977; Craik & Byrd, 1982; Hasher & Zack, 1979). In this view, age-related memory decline occurs in tandem with a reduction in the attentional resources that are needed in the most demanding encoding and retrieval situations (Craik, 1986, 1977; Craik & Byrd, 1982). This model can be examined with the divided attention paradigm, according to which success depends on the availability of attentional resources, as well as the ability to distribute them

Address correspondence to: Sophie Blanchet, Centre Interdisciplinaire de Recherche en Réadaptation et Intégration Sociale, Institut de Réadaptation en Déficience Physique de Québec, 525 Boulevard Hamel, G1M 2S8 Québec (Qc), Canada. E-mail: [email protected]

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efficiently according to a goal (Anderson, 1998). Tasks that involve encoding words in divided attention conditions are significantly more difficult for older rather than younger persons, whereas divided attention in retrieval does not induce age-related memory differences (Park et al., 1989; Fernandès & Moscovitch, 2000) except when there are competing material representations (Fernandès & Moscovitch, 2000). Notably, some research has not found these effects with encoding (Nyberg et al., 1997) or retrieval (Nyberg et al., 1997; Fernandes & Moscovitch, 2003). Furthermore, the attentional resource hypothesis predicts that age-related differences should be attenuated with increasing external support, such as in recognition (Haaland et al., 1983; Muramoto, 1984; Janowsky et al., 1996) as compared to cued or free recall (Craik & McDowd, 1987; Davis et al., 2003). In spite of its potential generalizability, the attentional resource hypothesis has been investigated mainly with verbal material. The goal of the present study was to assess whether variations in attentional demands can account for the age-related decline in memory for musical material. There are a number of ecological reasons why musical material is appropriate for assessing memory in aging. First, as with language, music is universal and ubiquitous in human cultures. Music is enjoyed by a very large number of people. Notably, it continues to represent an important aspect of quality of life with age (Cohen et al., 2002), as older persons maintain their musical knowledge into the late years (Gilbert & Beal, 1982; Halpern et al., 1996). Second, with the exception of formal concerts, listening to music while performing other tasks is common and memory for musical excerpts is most often assessed in conditions of divided attention. Thus, it is important to investigate this phenomenon beyond its ecological context and examine the effect of divided attention on memory for music in experimental situations. Finally, the study of music memory in aging may reveal different principles along which the resource hypothesis operates. Indeed, the study of music allows for an assessment of the interaction between attentional resource involvement and material-specific memory processes. The use of nonverbal material, such as musical material, may reveal the extent to which the resource hypothesis operates differently as a function of different types of material. In addition, it has been found that older persons perform as well as young persons in familiar tune recognition (Bartlett et al., 1995), but are impaired in unfamiliar tune recognition (Bartlett et al., 1995; Gaudreau & Peretz, 1999; Halpern et al., 1995; Halpern & O’Connor, 2000). This may be due to the fact that memorizing unfamiliar tunes is more attentionally demanding, consistent with the age-related attentional resource decline (Craik, 1977, 1986; Craik & Byrd, 1982). The goal of the present study was to explore whether the resource hypothesis of memory and aging can account for musical memory. This was conducted by manipulating the level of attentional allocation in encoding

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conditions in a recognition paradigm. Attention was manipulated at encoding because during this stage, memory and the concurrent task compete primarily for general resources, whereas they compete primarily for representational systems during retrieval (Fernandès & Moscovitch, 2000). To prevent the involvement of verbal processes, the stimuli used were uniquely novel tunes. In addition, our participants consisted of nonmusicians only, as individuals with formal training in music are more likely to use a verbal code to encode music (Dowling & Harwood, 1986; Lynch et al., 1991). Thus, an attentional requirement in this unfamiliar musical task may be particularly detrimental to nonmusicians who cannot rely on verbal strategies to perform the task. Above all, high levels of expertise seem to reduce age effects on the majority of tasks (Meinz, 2000). Three encoding conditions were examined in the current study. In the intentional condition, participants were required to listen to and remember novel melodies. In this condition, participants devoted all of their resources to encoding the material. In the dancing judgment condition, participants were asked to judge the type of dance associated with each melody, without any other instruction. There was no mention of a subsequent memory test. This condition oriented processing toward the structural characteristics of the musical excerpts and away from the memory aspect of the task. We wanted to measure whether orienting participants toward structural, yet salient, aspects of the melodies would affect recognition performance. Because participants were not in a condition that promoted the initiation of encoding strategies, they were all expected to exhibit a decrease in memory performance as compared to individuals in the intentional condition. In the third condition, the dancing judgment was combined with intentional encoding instructions. In this situation participants had to divide their attention between encoding the melodies intentionally and evaluating their rhythm. This condition was expected to be most detrimental to older persons due to their decline in attentional resources. Thus, the design used here relies on different learning instructions to manipulate attentional encoding. This is different from what has been used in the past with verbal material to manipulate attentional resources. This adds a unique element to our study, but also offers the advantage of mapping onto other memory tasks that are currently used in neuropsychology.

METHOD Participants Ninety adults, 45 younger and 45 older individuals, participated in the study. All participants were healthy, community-dwelling individuals recruited through advertisements in golden age centers and in magazines for seniors. They were interviewed to rule out a history of any of the following:

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alcoholism or substance abuse, cerebro-vascular accident, and present or previous treatment for acute or chronic psychiatric illness. None of the participants had any formal musical education or played an instrument for longer than 1 year. All participants reported normal audition. Individuals participated voluntarily and gave their written consent to participate. All individuals were given financial compensation for their transportation expenses. Participants were randomly assigned to one of three experimental conditions. Thus, there were 15 young and 15 aged participants per condition. Demographic information on the participants in each experimental condition is presented in Table 1. In each condition, the educational level of the younger and older individuals was equivalent, with the exception of a slightly higher educational level in younger than in older persons in the double encoding condition [t (20,59) = 2.31, p = .05]. However, education was not correlated with any of the response indices computed from recognition scores in younger or older participants. In addition, the vocabulary test was administered to assess the general knowledge of the different groups. A twoway ANOVA was conducted with condition (incidental, intentional, and incidental + intentional) and age as factors (young, old). The main condition effect [F(2, 72) = 6.25, p = .003] was significant, as the Mill Hill score was higher in the dancing judgment condition (m = 24.8 ± 5.66) and in the intentional condition (m = 25.4 ± 4.67) than in the intentional and incidental conditions (m = 20.7 ± 6.09). The main age effect was also significant [F(1, 72) = 7.43, p = .008], reflecting better ability in old persons (m = 25.05 ± 4.65) than young persons (m = 22.05 ± 4.65). This effect reflects the increased knowledge abilities that are well-established in normal aging (Park et al., 1996).The interaction between the condition and age group was not significant. To examine whether there is a relation between general knowledge and the different response indices (judgement, hits, false alarms, and bias indices), we conducted a correlational analysis between the scores obtained on

TABLE 1. Demographic Characteristics (Means and Standard Error) for Each Group of Younger and Older Participants in the Three Experimental Conditions Intentional Encoding Young M Age Education (Years) Mill-Hill Gender

22 13.13

SE

M

Young SE

SE

Old M

Young SE

Old

SE

M

SE

2.5 71 3.31 22.33 3.15 71.73 4.4 22.2 1.35 11.87 3.99 13.27 1.58 12.67 2.25 13.2

3.44 1.89

73.4 10.4

5.17 3.6

28.53 2.6 6m–9w

M

Intentional + Judgment

M

22.7 4.41 4m–11 w

m: men, w: women.

Old

Dancing Judgment

23.45 4.89 25.8 6.13 19.91 4.2 8m–7w 4m–11w 5m–10w

21.5 7.66 6m–9w

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the Mill Hill and the different response indices for the different conditions and age groups. None of the correlations were significant, indicating that the level of knowledge was not related to the different response indices.

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Stimuli and Apparatus Twenty novel musical sequences were used. They were selected from musical sequences used in the meter subtest of the Montreal Battery of Evaluation of Amusia for the testing of brain-damaged patients (Ayotte et al., 2002; Liégeois-Chauvel et al., 1998; Peretz, 1990). The stimuli were musical phrases that were comprised of two parts, according to the rules of the Western tonal system. An example is provided in Figure 1. Half of these sequences are written in a duple double meter (corresponding to a march) and half in a triple meter (corresponding to a waltz). Each selection lasted an average of 11 s. For the test phase, only the second part of each sequence served as a stimulus (see Figure 1). The second parts were four bars long, lasted approximately 4 s, and contained 8 to 19 tones (mean = 10.7). We emphasize that the second parts, which were a copy of the first parts but with a finale, constituted a better “entity” than the first parts alone. In the study phase, listening to two similar parts of each melody was intended to optimize the context. In contrast, choosing only the second part in the test phase allowed for a reduction in the length of this phase. All of the stimuli were computer-generated on a microcomputer running a MIDI (Musical Instruments Digital Interface) sequencing program (Sequencer Plus Gold, Voyetra, USA) that controlled a sample playback digital synthesizer (Roland Sound Canvas SC 50, Roland, USA). The scores were entered manually so that each tone occupied its precise value in terms of pitch and duration, keeping intensity and velocity constant, and was delivered with a piano sound.

FIGURE 1. Example of a march and the response choice provided to subjects at encoding. The second half of the march that served as a stimulus in the yes-no recognition test is presented below.

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Procedure A recognition paradigm was employed in a between-subjects design. During the study phase, 10 musical targets were presented twice in a different random order. The targets were always comprised of two parts to allow participants to build a stable representation of its metric structure. The instructions differed across conditions. In the intentional encoding condition, participants were asked to listen carefully to the melodies to remember them for later recognition. In the dancing judgment condition, participants were asked to judge whether each song presented was a “waltz” or a “march.” They were encouraged to tap along with what they perceived to be the underlying beat of each sequence. Participants’ responses were given orally. There was no mention of a subsequent memory test. In the intentional encoding + judgment condition, participants were asked both to memorize the melodies and make a waltz/ march judgment. In the test phase, 20 stimuli (10 targets mixed with 10 distractor melodies having a similar structure) were presented. Participants had to state verbally whether they recognized the tune from the previous phase or whether it was novel. During the study and test phases, participants were given as much time as necessary; however, this rarely exceeded 4–5 s. Participants were tested individually and the testing session lasted approximately 30 min. Data Analyses Three recognition indices were used as dependent variables: hit, false alarm, and decision criterion. A hit (H) corresponded to the correct recognition of a target. A false alarm (FA) corresponded to false recognition of a distractor. The decision criterion (Br) were calculated according to the twohigh threshold model (Snodgrass & Corwin, 1988) by combining hits and false alarms. Br was calculated with the following equation: Br = FA/(1-Pr). Finally, accuracy in dancing judgments was rated as correct if the decision matched the metric structure of the musical phrase. For each response index, a 2 (young, old) × 3 (intentional, dancing judgment, intentional + dancing judgment) between-subject analysis of variance (ANOVA) was conducted. As participants made the dancing judgment in only two conditions, a 2 (young, old) × 2 (dancing judgment, intentional + dancing judgment) ANOVA was conducted on each response measure in the study phase. Significant interactions were examined using simple effects analyses. Statistical analyses were run on SPSS software (10.0, Chicago, SPSS Inc.). RESULTS Methodological Considerations As the participants did not have any musical education, it was important to ensure that they could correctly distinguish between a waltz and a

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march. To that end, the dancing judgment at each individual level was considered. None of the individuals performed at chance levels (Ø) in identifying the two rhythm melodies, suggesting that all individuals discriminated between the waltz and march. In addition, to ensure that participants discriminated between the targets and the distractors, we calculated the discrimination index. The discrimination index was calculated with the following function: Pr = H–FA. It was required to be above chance levels (0). The means of the discrimination index for each condition appear in Table 2. Furthermore, a descriptive analysis of the discrimination index indicated that each individual performed above chance levels. Recognition Different response indices (hits, false alarms, and decision criterion) are presented in Table 2. The number of correct answers in judgments in the study phases of the incidental condition and the incidental + intentional condition appear in Table 3. The ANOVA on hits yielded a significant interaction between age and condition [F (2, 84) = 6.73, p < .002]. Simple effects analyses indicate that older adults produced significantly fewer hits than younger participants in the dancing judgment condition [F (1, 84) = 4.83, p < .0001] and in the judgment + intentional encoding condition [F (1, 84) = 24.52, p < .0001], but not in the intentional encoding condition (F < 1). In addition, the condition

TABLE 2. Recognition Performance (Means and Standard Error) for Each Group of Younger and Older Participants in the Three Experimental Conditions Intentional Encoding Young M Hits 8.66 FA 1.13 Pr 7.53 Br −0.08

SE

Dancing Judgment

Old M

1.11 8.60 1.19 2.13 1.96 6.47 0.19 −0.25

Young SE

M

1.35 9.40 1.85 0.40 2.29 9.00 2.01 −0.26

Intentional + Judgment

Old

SE

M

0.91 7.53 0.83 2.20 1.46 5.33 0.34 −0.74

Young SE

M

1.73 9.00 1.97 1.27 2.38 7.73 1.01 −0.27

SE

Old M

1.00 6.60 1.28 3.13 1.91 3.47 0.36 −0.49

SE 1.45 2.23 2.59 3.00

TABLE 3. Number of Correct Dancing Judgments (Means and Standard Error) in the Study Phase for Each Group of Younger and Older Participants Dancing Judgment

Younger Older

Intentional + Judgment

M

SE

M

SE

7.33 7.70

2.85 2.16

8.30 6.13

2.87 2.79

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effect was significant in older persons [F (2, 85) = 15.02, p < .002], but not younger persons [F (2, 85) = 0.92, p < .4]. The ANOVA conducted on the FAs indicated a main effect of age [F (1, 84) = 20.40, p < .0001], with older persons producing more FAs than younger persons overall. Neither the main effect of condition [F (2, 84) = 2.33, p < .104], nor the age by condition interaction, reached significance (F < 1). To determine whether the response groups were influenced by the involvement of different strategies, we conducted an ANOVA on the decision criterion (Br). The analysis indicated that there were no age or condition effects (F < 1 for both), and no interaction [F (2, 84) = 1. 34, p < .24]. Finally, the ANOVA performed on correct judgments in the study phases indicated a significant age by condition interaction [F (1, 56) = 13.36, p < .001]. Older adults made fewer correct judgments than younger adults in the judgment + intentional encoding condition [F (1, 57) = 19.63, p < .0001], but not in the dancing alone condition (F < 1). DISCUSSION The main goal of the present study was to examine age-related changes in the involvement of attentional resources in musical episodic memory for novel tunes. This was conducted by manipulating the encoding conditions in a recognition paradigm. When receiving memory instructions, the hit rates were equivalent in older and younger participants. Thus, when older participants were informed that their memory would be tested later, they encoded novel tunes spontaneously in a way that was efficient for recognizing them. This finding differs from that of Bartlett et al. (1995), who reported a marginally lower hit rate in older than younger participants in novel tune recognition. This discrepancy in the results can be explained by methodological differences between the studies. Bartlett et al. (1995) presented the tunes for study only once, whereas we presented the tunes twice. It is possible that older persons’ encoding of novel tunes benefited from this second presentation. The present results also indicate that informing older adults that memory will be tested later is not sufficient for them to initiate efficient encoding under divided attention conditions. Indeed, when intentional encoding was accompanied by a rhythm judgment, the older persons obtained fewer hits than younger persons. In the dancing judgment + intentional condition, participants were required to divide their attention between encoding and the waltz/march judgment. Notably, older persons’ ability to make the waltz/ march judgment was reduced in that condition, but not when they had to perform the judgment alone. This pattern of findings supports the notion that a secondary task performed at the time of intentional encoding disadvantages older persons, as has been shown previously (Park et al., 1989; Salthouse et al., 1984; Anderson, 1999). Older persons did not succeed in effectively

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dividing their attention between the two tasks. They were unable to use the encoding strategies that they used successfully in the simple intentional encoding condition. Thus, this impairment may reflect an age-related decline in attentional resources in episodic encoding (Anderson, 1999; Anderson et al., 1998). One possible explanation for the impaired performance in the dancing judgment+ intentional condition is that that the older group in this condition had a lower vocabulary level than that of individuals in the intentional condition. However, we do not believe that this is the case because there were no correlations between the response indices of the dancing judgment + intentional condition and the Mill Hill score. Also, both young and old participants in the dancing judgment + intentional condition obtained lower Mill Hill scores than those in the intentional condition. Intentional encoding is not only sufficient, but also necessary, for optimal recognition in older persons. Indeed, when making only a dancing judgment during the study phase, older persons performed more poorly than young persons. Thus, older persons were disadvantaged when they were not aware that their recognition of the novel tunes would be tested later. However, the fact that older persons were successful on the dancing judgment in isolation indicated that they maintain their knowledge of musical structure even without formal training (Lynch & Steffens, 1994). Our data are consistent with those of Halpern and O’Connor (2000) and Gaudreau and Peretz (1999), who found impairments in the ability of older persons to recognize unfamiliar melodies following incidental encoding. These results are consistent with the notion that when incidental encoding is oriented toward structural information rather than semantic information, the effect of age on recognition is enhanced (White, as cited in Craik, 1977; Craik & Tulving, 1975; Zelinski et al., 1978). Deciding whether the tune was a march or a waltz, which is a structural judgment, does not likely add enough meaningful information to each stimulus to promote later recognition, as confirmed by the lack of a positive orientation effect in younger persons as well. In a condition in which individuals are informed of a future test of their memory, they are likely to engage in other, more elaborate, processing of the unfamiliar musical stimuli at encoding. Finally, older persons produced more false alarms than young persons in all conditions. This is similar to studies of face recognition, in which the hit rate is found to be largely age-invariant, whereas the false alarm rate shows a clear age-related increase (Bartlett & Fulton, 1991; Bartlett & Leslie, 1986; Bartlett et al., 1989; Bartlett et al., 1991; Daum et al., 1996; Ferris et al., 1980; Smith & Winograd, 1978). Similar results have been reported by Blanchet et al. (2000), using other types of nonverbal material such as random shapes. The greater false alarm rate in older rather than younger participants is likely not due to a liberal strategy adopted by older persons, since the criteria did not differ between older and younger persons.

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This result is consistent with that of Bartlett et al. (1995). However, Bartlett et al. (1995) did not find a larger false alarm rate in older rather than younger persons. Our data rule out the notion that a greater false alarm rate is related to encoding processes such as those postulated by Taconnat and Insingrini (1995). Indeed, the false alarm (FA) rate was not sensitive to the different encoding conditions, in contrast to hits that were modulated by encoding. Therefore, FA may reflect age-related difficulties in differentiating old from new items at retrieval in general. Rankin and Kausler (1979) also found that older persons produced more false alarms than young persons following either shallow or deep encoding. The age-related increase in FA in older adults may be due to the fact that older persons base their recognition judgments more on familiarity or resemblance than on recollection or on retrieval of contextual information as stipulated by Jacoby (1991) and Bartlett (1993), respectively. Older persons might use a less distinctive process or cues at retrieval as compared to young persons. This high FA production may be due to age-related changes in frontal executive functions (Bäckman, 1991; Daum et al., 1996). Success in episodic memory tasks depends on the availability of attentional resources, as well as executive processes (Baddeley, 1986, 1996; Shallice & Burgess, 1991). Older persons seem to concentrate all their attention in encoding to ensure that it is efficient. These attentional and executive processes may be even more highly involved when the material is novel. In this way, the memorization of unfamiliar tunes, which solicit structural analysis, cannot be facilitated by pre-existing knowledge of the specific tunes. In addition, even if older persons exhibited greater general semantic knowledge than young persons, as indicated by the greater Mill Hill score in the former than the latter, these superior abilities do not help older people to process novel material. However, music can elicit a range of emotions, including the pleasure experienced when listening to the tunes. It would be interesting to examine whether orientation associated with pleasure or emotional judgments may be more efficient in providing effective encoding in older and younger persons. In turn, such encoding may be effective in decreasing the age-related effects of incidental memory for novel melodies. In sum, under conditions in which older participants were able to use all of their attentional resources to perform intentional memory encoding, recognition of unfamiliar melodies was similar to that of younger participants. In contrast, there was an age-related decline in making an incidental encoding, such as a dancing judgment, even when participants were informed that they should memorize the tunes. Although older participants demonstrated a preserved ability to perform the dancing judgment on its own, it was ineffective in implementing efficient and elaborate encoding. This age-related effect apparently results from a more general attentional age-related change that impacts on older adults. Thus, memory for musical material in normal older adults is not optimal when they are performing a

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concurrent activity. It is unclear whether the reverse is true, that is, if listening to music disrupts complex activities of daily living. Since music and processing appear to compete for resources, this is a possibility. In experimental studies, some have found a disruptive effect of concurrent noise on speech comprehension (Schneider et al., 2000) but others have failed to find a disruptive effect of white noise or verbal speech on short-term memory (Rouleau & Belleville, 1996). However, considering the ubiquity of musical background in our everyday life, the hypothesis that listening to music impacts on the completion of daily activities in older persons should be investigated further in the future. ACKNOWLEDGMENTS This study was supported by a post-doctoral fellowship to S. Blanchet from the Foundation of the Institut Universitaire de Gériatrie de Montréal and Groupe de Recherche en Neuropsychologie Expérimentale et Cognition, and by a CIHR grant and a FRSQ Chercheur-Boursier fellowship to S. Belleville. We thank Bernard Bouchard for his help with the technical aspects of the project, Gaëtane Chapelle for assisting with data collection, Francine Giroux for statistical support, and Janet Boseovski for editing.

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