Journal of Clinical and Experimental Neuropsychology

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Music as a mnemonic strategy to mitigate verbal

episodic memory in Alzheimer’s disease: Does
musical valence matter?

Stéphie Ratovohery, Alexia Baudouin, Juliette Palisson, Didier Maillet, Olivier

Bailon, Catherine Belin & Pauline Narme

To cite this article: Stéphie Ratovohery, Alexia Baudouin, Juliette Palisson, Didier Maillet, Olivier
Bailon, Catherine Belin & Pauline Narme (2019): Music as a mnemonic strategy to mitigate verbal
episodic memory in Alzheimer’s disease: Does musical valence matter?, Journal of Clinical and
Experimental Neuropsychology, DOI: 10.1080/13803395.2019.1650897

To link to this article: https://doi.org/10.1080/13803395.2019.1650897

Published online: 09 Aug 2019.

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JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY
https://doi.org/10.1080/13803395.2019.1650897

Music as a mnemonic strategy to mitigate verbal episodic memory in

Alzheimer’s disease: Does musical valence matter?
Stéphie Ratovoherya, Alexia Baudouinb, Juliette Palissonc, Didier Mailletd, Olivier Bailon, Catherine Belina,d
and Pauline Narmeb
a
Equipe Neuropsychologie du Vieillissement (EA 4468), Université de Paris, Boulogne-Billancourt, France; bMC2Lab, Université de Paris,
Boulogne-Billancourt, France; cService de Neurologie, UF Mémoire et maladies neurodégénératives, CHU Avicenne, APHP, Bobigny, France;
d
Service de Neurologie, Hôpital Saint-Louis, APHP, Université Paris Diderot, Paris, France

ABSTRACT ARTICLE HISTORY

Introduction: Music is increasingly used to improve cognition in clinical settings. However, it Received 2 August 2018
remains unclear whether its use as a mnemonic strategy is effective in Alzheimer’s disease (AD). Accepted 26 July 2019
The present study aimed at determining whether a musical mnemonic might mitigate patients’ KEYWORDS
learning of new verbal information and at exploring the effect of factors such as retention delay Mnemonics; verbal learning;
and emotional valence of the musical excerpt used. recall; positivity bias; socio-
Method: 13 patients with AD and 26 healthy comparisons (HC) with a low musical expertise were emotional selectivity theory
included. They learned texts about everyday life themes that were either set to familiar instru-
mental music, which was positively- or negatively-valenced, or spoken only. Immediate and
delayed recalls (after 10 min and 24 hours) were measured.
Results: Main results showed that (i) HC demonstrated better verbal episodic memory perfor-
mance than participants with AD; (ii) participants with AD encoded texts paired with positively-
valenced music better than texts paired with negatively-valenced music; (iii) participants with AD
recalled sung texts better than spoken texts (after 10 min and 24 hours), regardless of musical
valence while HC displayed better recall for texts paired with positively-valenced music.
Conclusions: Musical mnemonics may help people with AD learn verbal information that relates
to their daily life, regardless the musical expertise of the patients. This result gives promising
clinical insights showing that music processing is robust to brain damage in AD. Possible
hypotheses explaining the effectiveness of musical mnemonics in AD regardless the musical
valence are discussed (e.g., different processing between musical and spoken conditions; disap-
pearance of the positivity bias and implications with respect to the underlying socio-emotional
selectivity theory).

Introduction previous studies showing its effectiveness to support

psychological well being by enhancing mood (e.g.,
Alzheimer’s disease (AD), the most common demen-
anxiety and depression; Guétin et al., 2009;
tia, is characterized by significant, progressive mem-
Särkämö et al., 2014; Satoh et al., 2015; Sung,
ory loss. Impairments of episodic memory are
Chang, & Lee, 2010) and alleviating behavioral
usually the inaugural symptom – at least in the
symptoms (Livingston et al., 2014; Narme et al.,
case of typical amnestic forms. Considering the
2014; Ray & Mittelman, 2017)
growing population of older adults with dementia
Previous studies also reported a general cognitive
(Alzheimer’s Disease International, 2013) and the
improvement or preservation after music-based inter-
unsatisfactory impact of pharmacological therapies
ventions (Särkämö et al., 2014), enhancement of ver-
in AD, non-pharmacological treatments have
bal fluency (Thompson, Moulin, Hayre, & Jones,
received increasing empirical support during the
2005), self-consciousness (Arroyo-Anlló, Díaz, & Gil,
past decade to face one of the greatest health chal-
2013; Baird & Thompson, 2018) and memory (auto-
lenges of this century. Among them, music-based
biographical: Särkämö et al., 2014; Irish et al., 2006; El
interventions (e.g., music listening, singing) seem to
Haj, Fasotti, & Allain, 2012; verbal memory: Pongan
be promising tools for addressing various needs of
et al., 2017). Previous studies also showed that (i) AD
persons with dementia. The beneficial impact of
patients with a severe episodic memory decline may
music in patients with AD has been reported in

CONTACT Pauline Narme paulinenarme@gmail.com Laboratoire Mémoire Cerveau et Cognition, EA 7536, Université de Paris, MC2Lab, F-92100
Boulogne-Billancourt, France
© 2019 Informa UK Limited, trading as Taylor & Francis Group
2 S. RATOVOHERY ET AL.

still be able to learn new songs (Crystal, Grober, &
Masur, 1989; Samson, Dellacherie, & Platel, 2009) or
to recall/recognize familiar songs (Cuddy & Duffin,
2005; Cuddy, Sikka, & Vanstone, 2015; Prickett &
Moore, 1991); and that (ii) music can be used as
a mnemonic device in a variety of clinical settings
(Thaut, McIntosh, & Hoemberg, 2015; Thaut,
Peterson, McIntosh, & Hoemberg, 2014). For persons
with AD, prior research indicates that information
presented musically at encoding is better recognized
or even recalled than information that is presented
verbally (Moussard, Bigand, Belleville, & Peretz, 2014;
Palisson et al., 2015; Simmons-Stern, Budson, & Ally,
2010). However, Simmons-Stern et al. (2012) found
that such benefit was found for gist, but not details, of
encoded information. Such discrepancies could be
explained by methodological differences such as the
kind of musical stimuli, the way information are pre-
sented during the encoding stage, the dependent vari-
able used to measure memory performance and the
delay retention between encoding and retrieval. Table
1 provides a summary of past research in this area.
At least four factors should be taken into account
and first, the familiarity of the music for the partici-
pants. Studies in healthy populations suggested that the
benefit of musical encoding only occurs if the music
used is highly familiar (Korenman & Peynircioğlu,
2004; Purnell-Webb & Speelman, 2008). Consistently,
Moussard, Bigand, Belleville, and Peretz (2012)
reported, in a case study of a mild AD patient, that
sung lyrics led to worse performance than spoken lyrics
in immediate recall unless the lyrics were learned on
a familiar melody. Although Moussard et al. (2014)
found, in their group study, that the sung condition
benefited the retention of lyrics in AD independently of
melodic familiarity, previous research in music therapy
indicated that familiarity might be a key aspect to
intervention with this population. For example,
Gibbons (1977) showed that patients with AD strongly
prefer music that was popular during their young adult
years, suggesting that this kind of music may promote
participation in music therapy activities. Furthermore,
the effectiveness of music intervention might be asso-
ciated with the level of preference – and thus familiar-
ity – of music for patients (e.g., Clark, Lipe, & Bilbrey,
1998; Gerdner, 2000). A second factor that might
explain discrepant results in the literature is the num-
ber of exposures during the encoding stage. When
participants were exposed only once during the encod-
ing stage, results showed a benefit for the recollection
of gist but not of details (Simmons-Stern et al., 2010,
2012). By contrast, when using a reinforced encoding
procedure during which AD participants were repeat-
edly exposed to the lyrics or when lyrics were learned
step by step, results showed a musical advantage on
recall performance (Moussard et al., 2014; Palisson
et al., 2015). A third factor refers to the retention
delay. It can be seen (Table 1) that the benefit is not
consistently observed in immediate recall but found
after a 5 or 10 min delay. However, at longer term,
Baird, Samson, Miller, and Chalmers (2017) found no
mnemonic effect of sung compared with spoken

Table 1. Previous group studies investigating the impact of musical encoding on verbal information learning and retention in AD
patients and healthy comparisons (HC).
Authors Population Methods Memory measures Main results
Simmons-Stern AD (n = 12) 40 stimuli (4 line excerpts each): 20 Recognition judgment Better recognition for the sung lyrics than
et al. (2010) HC (n = 12) presented with their corresponding (Old/New) the spoken lyrics in AD (but not in HC)
sung recording vs 20 with their
spoken recording
Songs were unfamiliar
Simmons-Stern AD (n = 12) Similar to Simmons-Stern et al.’s study General content questions General content information was better
et al. (2012) HC (n = 17) (2010) except that lyrics were related followed by specific remembered when studied in sung
to common activities of daily living content questions then lyrics but specific content was not
Songs were unfamiliar a recognition test influenced by encoding condition
Better recognition for the sung lyrics than
the spoken lyrics in both groups
Moussard et al. AD (n = 8) 6 texts (8 lines each) either presented Immediate free recall Sung conditions did not influence lyrics
(2014) HC (n = 7) spoken, sung with unfamiliar or with 10 min delayed free recall recall in immediate recall but increased
familiar melody delayed recall in both groups.
Palisson et al. AD (n = 12) 3 texts (8 lines each): one presented Immediate free recall Sung texts remembered better than
(2015) HC (n = 15) with a sung recording, one spoken 5 min delayed free recall spoken texts, both immediately and
and one spoken associated with non- after a 5 min retention delay in AD and
musical material. HC
Song was familiar
Baird et al. (2017) AD (n = 11; 2 stimuli (2 sentences each) either Learning score Musicians with AD showed a better
5 musicians) presented in a sung or spoken 30 min delayed free recall learning of sung information compared
HC (n = 22; version, for a maximum of 5 learning 24-hour delayed free with non-musicians with AD.
15 musicians) trials (or until correctly recalled) recall and recognition However, no mnemonic effect of sung
Song was familiar compared with spoken information was
found in AD or in HC.
 JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY
information. It has also to be underlined that in the
latter study, authors changed the lyrics of a well-know
song, which might be counterproductive.
Surprisingly, researchers have not systematically
controlled for or even reported on the emotional
valence of the music used in their studies. As pre-
viously mentioned considering music-based interven-
tions, studies often provide an insufficient description
of the musical stimuli used (Robb, Carpenter, & Burns,
2011). Yet, the fact that music elicits intense emotions
(Blood & Zatorre, 2001; Khalfa, Peretz, Blondin, &
Robert, 2002; Salimpoor et al., 2013) is classically pre-
sented as one of the main possible mechanisms under-
lying the impact of music on memory (Ferreri &
Rodriguez-Fornells, 2017; Janata, Tillman, &
Bharucha, 2002; Peck, Girard, Russo, & Fiocco, 2016).
Furthermore, it is well known that healthy populations
remember emotional contents better than neutral ones
(Kensinger & Corkin, 2003; Kensinger & Schacter,
2008; for a review see Kensinger, 2009). Previous stu-
dies have reported an emotional memory enhancement
in AD patients when retrieval tasks are used
(Kalenzaga, Piolino, & Clarys, 2015; Nieuwenhuis-
Mark, Schalk, & de Graff, 2009; Schultz, de Castro, &
Bertolucci, 2009). However, this effect has been less
consistently found in AD (Hamann, Monarch, &
Goldstein, 2000; Kensinger, Brierley, Medford,
Growdon, & Corkin, 2002; for a review, see Klein-
Koerkamp, Baciu, & Hot, 2012). The valence effect
should also be considered. It is well known that older
adults recall negative information less well than posi-
tive information, a phenomenon known as the positiv-
ity bias (Charles, Mather, & Carstensen, 2003; Mather,
2012; Reed, Chan, & Mikels, 2014). This suggests that
musical valence may influence the benefit observed
when participants learn sung lyrics compared to spo-
ken ones. Consistently with this hypothesis, we pre-
viously showed that, in healthy older adults, the benefit
of a musical mnemonic on verbal learning was
observed when the musical excerpt was positively-
valenced but not when negatively-valenced
(Ratovohery, Baudouin, Gachet, Palisson, & Narme,
2018). In AD, the positivity bias is not always found.
Although some previous studies observed a positivity
bias in memory in AD (Brueckner & Moritz, 2009;
Huijbers, Bergmann, Olde Rikkert, & Kessels, 2011;
Sava, Krolak-Salmon, Delphin-Combe, Cloarec, &
Chainay, 2017), others did not (Chainay et al., 2014;
Fleming, Kim, Doo, Maguire, & Potkin, 2003). To
explain these discrepancies, some authors proposed
that the presence of the positivity bias depends on the
quality of the encoding (e.g., depth of encoding; Sava
et al., 2015), the retention delay (Kalanzaga, Lamidey,
3
Ergis, Clarys, & Piolino, 2016) or the type of task used
(see Klein-Koerkamp et al., 2012).
The present study first aimed at determining
whether the use of music as a mnemonic strategy
would be effective in AD to improve recall of new
verbal information. To investigate this issue, we com-
pared encoding and retrieval of two texts presented in
a musical condition (i.e., sung lyrics) compared to
a spoken text, in AD patients and healthy compari-
sons. To check the retention delay effect, we assessed
immediate and delayed recall (after 10 min and 24 h).
Based on our first study, we assumed that sung texts
would be better recalled than spoken texts in AD
patients regardless of the retention delay (Palisson
et al., 2015). Our second aim was to determine
whether the musical memory enhancement observed
when patients learn sung lyrics in comparison with
spoken ones may be modulated by the valence char-
acteristics of the musical background used. We parti-
cularly inquired whether AD patients would benefit
from the musical mnemonic when the musical excerpt
was positively-valenced but not when negatively-
valenced, consistently with our previous findings in
healthy older adults (Ratovohery et al., 2018). This
pattern would argue in favor of a positivity bias pre-
servation in AD.
Methods
Population
A total of 39 participants (healthy older adults: n = 26;
patients: n = 13) were included. Patients attended the
Memory Clinic at the Neurology department of
Avicenne Hospital (Assistance Publique des Hôpitaux
de Paris) and met the clinical criteria for probable
Alzheimer’s disease (McKhann et al., 2011). The sever-
ity of the disease was assessed by the French version of
the Mini-Mental State Examination during the research
visit (MMSE; Folstein, Folstein, & McHugh, 1975;
Kalafat, Hugonot-Diener, & Poitrenaud, 2003).
Patients were at the mild to moderate stage of the
disease (MMSE range: 16–28). We excluded patients
with neurological (e.g., cerebrovascular history or sus-
picion of mixed dementia) or psychiatric comorbidity
(except for mild depression).
Healthy older comparisons (HCs) had no neurolo-
gical or psychiatric history. The MMSE was adminis-
tered to exclude participants with a global cognitive
functioning impairment according to the validated
French cutoffs (Kalafat et al., 2003). They were
matched in terms of age and education level to patient
characteristics.
4 S. RATOVOHERY ET AL.
Overall, participants were native French speakers
and did not have a high musical expertise (as checked
by a score below 17/28 with the Musical Experience
Questionnaire, Ehrlé, 1998). Participants’ abilities to
process musical excerpts were assessed by the first
subtest of the Montreal Battery of Evaluation of
Amusia (MBEA; Peretz, Champod, & Hyde, 2003).
The MBEA battery was designed according to the func-
tional architecture model for musical processing pro-
posed by Peretz and Coltheart (2003) in order to assess
melodic and rhythmic perception. The first subtest
chosen here assessed whether participants were able
to distinguish pitch changes in melodies. Although, to
our knowledge, the MBEA has not been validated with
persons with AD, this tool seems the best available
measure of musical processing and has been used pre-
viously with this population (Campanelli et al., 2016).
We also checked the presence of depressive symptoms
using the Geriatric Depression Scale (GDS; Yesavage
et al., 1983) in patients with AD and in HCs. Based on
clinical cutoffs, we only excluded AD patients who scored
above 20/30 (a score above 11/30 suggests mild depres-
sion and a score above 20 indicates moderate to severe
symptoms; Bourque, Blanchard, & Vézina, 1990). This
choice was made based on the well-established result of
high prevalence of depression in AD (Benoit et al., 2012;
Lyketsos et al., 1997) and it was crucial to ensure that
results regarding musical valence were not confounded
with depression. According to the Helsinki Declaration
(World Medical Association, 2013), all participants gave
their written informed consent.
Demographic characteristics are summarized in
Table 2.
The two groups did not differ in terms of age (t(37)
= −0.28; p = 0.78; Cohen’s d = 0.009), education level
(t(37) = −0.51; p = 0.61; Cohen’s d = 0.02), musical
expertise (t(37) = 1.42; p = 0.16; Cohen’s d = 0.05) or
musical perception abilities (MBEA: t(37) = 1.79;
p = 0.08; Cohen’s d = 0.06). Although not significant,
a difference between HCs and AD patients appears on
Table 2. Participants’ characteristics.
HCs AD patients
(n = 26) (n = 13) p ences on valence ratings (for a more detailed
Age (years) 77.1 ± 8.2 (61–92) 77.9 ± 8.1 (63–88) 0.78
Gender (male/female) 20/6 7/6 0.06
Education (years) 10.7 ± 3.6 (7–20) 11.4 ± 4.1 (8–20) 0.61
Musical Expertise (/27) 5.7 ± 3.2 (1–12) 4.3 ± 2.3 (1–8) 0.16
MBEA first subtest (/30) 26.0 ± 3.8 (17–30) 23.3 ± 5.7 (12–28) 0.08
MMSE (/30) 29.2 ± 1.1 (25–30) 22.4 ± 3.5 (16–28) 0.001
GDS (/30) 5.2 ± 2.8 (1–10) 8.5 ± 4.3 (3–14) 0.007
Data are expressed in mean ± standard deviation (the range is presented in
brackets). AD: Alzheimer’s disease; MBEA: Montreal Battery of Evaluation
of Amusia; MMSE: Mini-Mental State Examination; GDS: Geriatric
Depression Scale.
the latter measure and, as it can be seen in Table 2,
some AD patients scored below the conventional cutoffs
for amusia in healthy young populations (it was the case
for 3 patients). Sex distribution did not significantly
differ (À2(1, N=39) = 3.69; p = 0.06; Cramer’s
V = 0.31). However the groups differed significantly in
cognitive functioning and mood. As expected, patients
obtained lower MMSE scores than HCs (t(37) = 9.16;
p = 0.001; Cohen’s d = 0.26). Patients also presented
higher depressive scores than HCs (t(37) = −2.85;
p = 0.007; Cohen’s d = 0.09). More precisely, 5 patients
scored above 10/30 (meaning 38%).
Material
Musical stimuli
In the present study, emotional status was manipulated
using valence elicited by musical excerpts. The two musi-
cal excerpts were the same as those used in our previous
study in normal aging (Ratovohery et al., 2018).
Beethoven’s Ode to Joy was used to elicit a positive
valence and Chopin’s Funeral March to elicit a negative
valence. The latter was used in its original form (using the
Pavel Serebriakov’s recording, taken from the album
“Beethoven, Chopin, & Rachmaninoff”) and a piano ver-
sion of Ode to Joy was selected to be of a similar complex-
ity to each other (using the piano version by Michael
Silverman, taken from the album “Bach for the Brain:
Classical music to make you smarter”).
In a pilot testing, these excerpts were chosen
among 20 musical excerpts based on a familiarity,
valence and arousal assessments. Twenty-eight
young adults (age: 23.9 ± 3.1; education:
15.9 ± 1.5) and 23 older adults (age: 71.8 ± 7.8;
education: 13.8 ± 4.9) were asked to assess (i)
familiarity (using a 10-point semantic differential
scale from 1: unfamiliar to 10: very familiar); (ii)
valence (from 1: highly negative to 10: highly posi-
tive); (iii) arousal (from 1: highly calming to 10:
highly stimulating). Both musical excerpts were
assessed as highly familiar to all participants
(young and older adults) and with a moderate arou-
sal. In addition, they were well rated as eliciting the
expected emotional valence without group differ-
description see Ratovohery et al., 2018). The same
arrangements of both musical excerpts were used
for the pilot testing and during the procedure of
the present study.
Texts
The texts were the same as those used in our previous
study in normal aging (Ratovohery et al., 2018). Each
 JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY
text was composed of a whole sentence talking about
everyday like themes (e.g., listening to music, going for
a walk) and were written story-like. There all were
subdivisible into 8 parts (containing each between 4
and 7 words and with a congruent meaning) to facil-
itate the learning procedure. They were comparable in
terms of (i) number of words (gardening: 40; shopping
list: 44; activities: 45) and (ii) lexical frequency checked
using a French lexical database (New, Pallier, Ferrand,
& Matos, 2001). In a second pilot testing, 22 young
adults (age: 22.4 ± 2.7; education: 14.6 ± 2.4) were
asked to learn and recall the three texts that were all
encoded in a spoken condition, according to the pro-
cedure of the main experiment (see details throughout
the next section). They were also asked to assess
whether each text evokes a negative or positive emo-
tion (using a 10-point semantic differential scale from
1: negative to 10: positive). We obtained similar learn-
ing and memory performance as similar valence for the
three texts (for detailed pretest results, see Ratovohery
et al., 2018). These results suggest that the three texts
did not differ in terms of learning difficulty and emo-
tion they may evoke.
The texts were then associated with music to create
emotional stimuli. Each text was assigned to each
experimental condition: (i) the shopping list text was
sung on the Ode to Joy melody (positive music); (ii) the
text about gardening was sung on the Funeral March
melody (negative music); (iii) the text about activities
was spoken in a neutral tone to constitute the control
(neutral) condition. A female professional singer pre-
recorded the three stimuli (two sung conditions and
one spoken condition). The recorded stimuli were then
played to the participants through the loudspeaker of
the computer. The music accompanied each sung con-
dition and was presented in the same form used during
the pilot. Since the texts were constructed to map onto
the musical rhythm, the association between texts and
conditions was not counterbalanced.
Procedure
Participants were individually tested in a quiet room
and the whole testing session lasted around two hours.
They were asked to learn successively three texts, each
one assigned to an experimental condition (positive
musical, negative musical, or spoken – neutral – con-
dition). The order of presentation of the three condi-
tions was (i) counterbalanced across participants and
(ii) randomly assigned.
Texts were both auditorily and visually presented on
a computer screen using Microsoft Powerpoint®
(Calibri font, size 32). In each condition, we used
5
a chaining procedure to teach participants the text, as
follows: (i) the entire text was presented and partici-
pants were instructed to try to memorize it, (ii) the first
line was presented twice and participants were asked to
repeat it before the line disappeared and they had to
recall it (immediate recall); (ii) the second line was
presented in the same way; (iii) the first two lines
were presented together; (iv) the third line then the
first three lines, and so on until either complete learn-
ing of the text or a stop criterion (failed to recall at least
65% of the words). This learning procedure was
adapted from the one used in Racette and Peretz’
study (2007), similarly to the one used in our previous
studies (Ratovohery et al., 2018; see also Palisson et al.,
2015). We calculated an immediate recall score as
a percentage of words accurately recalled out of the
presented text. We also measured encoding abilities as
the number of lines (out of eight) that a participant
could learn.
After the learning phase, a 10-min retention phase
ensued. During this time, participants completed the
first subtest of the MBEA. Participants were then
asked to recall as many words as possible from the
text previously presented (10 min delayed free recall).
When participants were unable to recall some words,
we provided an auditory cue using the first line of the
text. Throughout the procedure, the scoring was not
dependent on recall order. One point was given for
each word accurately recalled in either free or cued
recall, even if the words were given in a wrong order.
Following the delayed recall procedure, participants
learned the second randomly assigned text using the
same chaining procedure. During the second 10 min
delay, participants performed the visuo-construction
subtest from the Mattis Dementia Rating Scale
(Mattis, 1976), the digit span and the letter-number
sequencing tasks from the Wechsler Adult
Intelligence Scale 3rd edition (WAIS-III; Wechsler,
2001). Following the same procedure, learning of
the third text was then carried out. During the last
10 min delay, the digit symbol-coding subtest (WAIS
III; Wechsler, 2001) and the French version of
Baddeley’s dual task (Godefroy et al., 2010) were
administered.
Finally, long-term memory was assessed after
a 24-hour retention delay. At the end of the testing
procedure, to avoid informing the participants in
advance of the final assessment, we pretended that
a questionnaire was missing and told participants
that they would be contacted by phone the
following day to complete the missing document.
Every phone call has been made no more than
2 hours shorter or longer than 24 hours. During
6 S. RATOVOHERY ET AL.

Figure 1. Experiment procedure. The order of presentation of the three texts (and conditions) was counterbalanced across
participants. During the 10min delay, participants completed several tasks (the first subtest of the MBEA during the first interval;
the visuo-construction subtest from the Mattis Dementia Rating Scale, the digit span and the letter-number sequencing tasks from
the WAIS-III during the second interval; the digit-symbol-coding subtest from the WAIS-III and the French version of Baddeley’s dual
task during the last interval). MMSE: Mini-Mental State Examination; GDS: Geriatric Depression Scale.

the phone call, they were asked to recall the texts
they had learned the day before (a free recall was
followed by a cued recall when needed).
The whole procedure is summarized in Figure 1.
Finally, we checked that statistical findings survived
nonparametric analyzes. Data are expressed in mean
and standard errors of the mean. Analyzes were con-
ducted using SPSS software® (SPSS Inc., Chicago, IL,
USA). The threshold of significance was set at p < 0.05.

Statistics
Analyzes of variance with repeated measures
(ANOVA) were performed on each dependent variable
(number of lines learned; immediate recall; free and
cued recall after 10 min and 24 hours), with Group as
between-group factor (HCs, Patients) and Condition
(positive, negative, neutral/spoken) as within-group
factor. Analyzes of covariance (ANCOVA) were con-
ducted with GDS scores as a covariate to check whether
the higher depression scores in patients explained
between-group differences. All ANCOVAs showed
that the GDS scores as a covariate did not approach
significance.
To study the potential benefit related to musical
conditions according to the valence and the reten-
tion delay, we computed a benefit index by subtract-
ing the percentage of words recalled in the spoken
condition from the percentage of words recalled in
each musical condition (positive and negative).
A positive index indicated that the musical condition
was associated with better recall than the spoken
condition. An ANOVA was then performed with
Group as between-group factor (HCs, Patients),
Valence and Delay (immediate, 10 min, 24 hours)
as within-subjects factor. In addition, correlation
analyzes were performed using a Spearman test to
check (i) for any evidence for an association between
melodic processing deficits in AD and musical ben-
efit, (ii) whether the higher depression scores in
patients were associated with the musical benefit
index.
Results
Number of lines learned
The ANOVA showed a significant effect of Group,
F(1, 37) = 67.15; p = 0.001; ηp2 = 0.64. Patients
encoded fewer lines (5.13 ± 0.25) than HCs
(7.60 ± 0.17). The main effect of Condition was
also significant, F(2, 74) = 14.37; p = 0.001; ηp2
= 0.28, due to a lower performance during the
encoding stage when texts were spoken
(5.79 ± 0.25) rather than sung (positive music:
6.77 ± 0.13; negative music: 6.54 ± 0.16; all
p = 0.001) while the two musical conditions did
not differ. The Group x Condition interaction was
not significant, F(2, 74) = 2.51; p = 0.09; ηp2 = 0.06.
Immediate recall
A main effect of Group was found, F(1, 37) = 62.46;
p = 0.001; ηp2 = 0.63, indicating that HCs recalled
a higher percentage of words (89.03 ± 1.46) than
patients (68.99 ± 2.07). The main effect of encoding
condition was significant, F(2, 74) = 13.48; p = 0.001;
ηp2 = 0.27. Immediate recall was higher in the positive
music condition (84.1 ± 1.6) than in the negative music
(77.63 ± 1.54; p = 0.001) and spoken (75.29 ± 1.72;
p = 0.001) conditions, while the latter two conditions
did not differ (p = 0.2). The Group x Condition inter-
action was not significant, F(2, 74) = 2.63; p = 0.08; ηp2
= 0.07; Figure 2(a).
 JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY
Figure 2. Episodic memory performance in healthy comparisons and AD patients according to the encoding condition: (a)
percentage of words accurately recalled during the immediate recall; (b) percentage of words accurately recalled after a 10-min
retention delay (cued recall); (c) percentage of words accurately recalled after a 24-hour retention delay (cued recall). Bars represent
the standard error of the mean.
10 min delayed recall
The first ANOVA conducted on free recall revealed a main
effect of Group, F(1, 37) = 61.56; p = 0.001; ηp2 = 0.79. The
percentage of words recalled after a 10 min retention delay
was higher in HCs (64.27 ± 3.74) than in patients
(13.42 ± 5.29). A main effect of Condition was also
found, F(2, 74) = 6.93; p = 0.002; ηp2 = 0.16, due to higher
performance in the two musical conditions (positive music:
45.98 ± 3.68; negative music: 43.22 ± 4.53) than in the
spoken one (27.33 ± 5.16; both p = 0.01), while the two
musical conditions did not differ (p = 0.56). The Group
x Condition interaction was not significant, F(2, 74) = 2.24;
p = 0.11; ηp2 = 0.06.
A high proportion of patients did not retrieve any words
during the free recall (positive music: 61%; negative music:
38%; spoken: 92%), while this proportion was lower in HCs
(positive and negative conditions: <1%; spoken: 27%).
Thus, a second ANOVA was conducted on the percentage
of words recalled after the first sentence of the text was
given as a cue (cued recall). It revealed a main effect of
Group, F(1, 37) = 69.49; p = 0.001; ηp2 = 0.65, due to a lower
performance in patients (22.43 ± 4.91) than in HCs
(72.51 ± 3.47). The main effect of Condition, F(2,
74) = 19.05; p = 0.001; ηp2 = 0.34, and the Group
x Condition interaction, F(2, 74) = 4.97; p = 0.009; ηp2
= 0.12, were significant. Univariate ANOVAs were con-
ducted to further investigate this interaction. The
Condition effect in HCs, F(2, 50) = 6.74; p = 0.003; ηp2
= 0.21, showed that the best recall performance was
7
observed in the positive musical condition, followed by
negative musical and spoken conditions (both p = 0.003),
while the latter two did not differ (p = 0.33; Figure 2(b)).
A different pattern was observed in patients, F(2,
24) = 24.94; p = 0.001; ηp2 = 0.68, for whom both musical
conditions led to better recall than the spoken one (both
p = 0.001) without any difference according to the musical
valence (p = 0.52).
24-hour delayed recall
Given that the percentage of words recalled after a 24-
hour retention delay was dramatically poor in patients
(3.44 ± 5.07; versus HCs: 41.62 ± 3.58), the ANOVA
was only conducted on cued recall. It revealed a Group
effect, F(1, 37) = 44.41; p = 0.001; ηp2 = 0.55, with
poorer recall in patients (9.91 ± 4.98) than in HCs
(50.58 ± 3.52). The main effect of Condition, F(2,
74) = 10.81; p = 0.001; ηp2 = 0.23, and the Group
x Condition interaction, F(2, 74) = 3.90; p = 0.02;
ηp2 = 0.09, were significant. Further univariate
ANOVAs showed a Condition effect in HCs, F(2,
50) = 11.79; p = 0.001; ηp2 = 0.32, due to better recall
after the positive musical encoding than in the other
two conditions (both p = 0.001), while negative musical
and spoken conditions did not differ (p = 0.44).
A different pattern was observed in patients, F(2,
24) = 8.18; p = 0.002; ηp2 = 0.41, since both musical
conditions led to a better recall than the spoken one
8 S. RATOVOHERY ET AL.
(both p = 0.005; Figure 2(c)), without any difference
according to the musical valence (p = 0.55).
Emotional benefit
The emotional benefit index was calculated by subtracting
the percentage of words recalled in the spoken condition
from the percentage of words recalled in each musical
condition (a positive index revealed that the musical con-
dition was associated with better recall than the spoken
condition). The ANOVA conducted on this index revealed
no significant effect of Group, F(1, 37) = 3.05; p = 0.09; ηp2
= 0.07 (HCs: 8.04 ± 2.43; AD patients: 15.39 ± 3.44). The
main effect of Valence was significant, F(1, 37) = 9.24;
p = 0.004; ηp2 = 0.20, due to a higher benefit when the
music used was positively-valenced (14.58 ± 2.11) than
when negatively-valenced (8.86 ± 2.48). Furthermore, the
Group x Valence interaction was significant, F(1,
37) = 6.54; p = 0.01; ηp2 = 0.15. On closer scrutiny, uni-
variate ANOVAs showed that this interaction was driven
by a valence effect in HCs, F(1, 25) = 20.34; p = 0.001; ηp2
= 0.45, with a higher benefit with positively-valenced music
(13.31 ± 2.79) than when negatively-valenced (2.78 ± 3.26),
whereas the benefit did not differ according to the musical
valence in AD patients, F(1, 12) = 0.13; p = 0.73; ηp2 = 0.01
(positive: 15.85 ± 2.03; negative: 14.94 ± 2.51). However,
there was also a significant effect of delay, F(2, 74) = 7.97;
p = 0.001; ηp2 = 0.18, but the triple interaction Group
Figure 3. Musical benefit index in healthy comparisons and AD patients according to the retention delay and the musical valence.
This index was computed by subtracting the percentage of words recalled in the spoken condition from the percentage of words
recalled in each musical condition. For delayed recall, the cued scores were considered. Bars represent the standard error of the
mean.
x Valence x Delay was significant, F(2, 74) = 5.77; p = 0.005,
ηp2 = 0.14 (Figure 3).
In HCs, the Valence x Delay interaction, F(2, 50) = 3.97;
p = 0.03; ηp2 = 0.14, is explained by a greater benefit of
positively-valenced over negatively-valenced music as the
retention delay increases, while in AD patients, the trend of
Valence x Delay interaction, F(2, 24) = 3.22; p = 0.06; ηp2
= 0.21, revealed a different pattern: immediate performance
was better with positively-valenced than with negatively-
valenced music, F(1, 12) = 5.47; p = 0.04; ηp2 = 0.31, while
no difference according to the valence was observed
after 10 min (F(1, 12) = 0.44; p = 0.52; ηp2 = 0.04) or
24 h (F(1, 12) = 0.381; p = 0.55; ηp2 = 0.03).
Correlation analyzes
Considering that three patients of our AD sample
obtained a MBEA score below the conventional cutoffs
for amusia, supplemental analyzes were performed to
ensure that patients who scored poorly on the melodic
processing subtest of the MBEA also benefited from the
musical encoding. Correlations between this MBEA
score and the emotional musical benefit index in AD
group were not significant after 10 min (positive con-
dition: ρ = 0.22; p = 0.46; negative condition: ρ = 0.14;
p = 0.65) or after 24 h (positive condition: ρ = −0.02;
p = 0.96; negative condition: ρ = 0.18; p = 0.55).
Individual analyzes suggest that those three patients
 JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY
also have poor global recall performance indicating
a more advanced disease. Accordingly to this assump-
tion, the correlation between the MBEA and MMSE
scores was significant in AD group (ρ = 0.56; p = 0.04).
Considering that five patients scored above the clin-
ical depression cut off scores, supplemental analyzes
were performed to check whether higher depression
scores might influence the pattern observed on the
musical benefit. Correlations between the GDS scores
and the emotional musical benefit index in AD group
were not significant during the encoding (positive con-
dition: ρ = −0.33; p = 0.27; negative condition:
ρ = −0.05; p = 0.87), after 10 min (positive condition:
ρ = 0.39; p = 0.19; negative condition: ρ = 0.35;
p = 0.24) or after 24 h (positive condition: ρ = −0.14;
p = 0.64; negative condition: ρ = 0.27; p = 0.38).
Discussion
There is a growing literature on music-based interven-
tions to address a variety of goals in clinical settings,
especially in the field of dementia (e.g., Baird &
Thompson, 2018; Raglio, Filippe, Bellandi, & Stramba-
Badiale, 2014; Robb et al., 2018; van der Steen et al.,
2018). Nevertheless, the benefits of these interventions
on cognition remain unclear. The present study aimed
at investigating whether music may be effective as
a mnemonic strategy to help the learning of new verbal
information. To investigate this issue, we compared
encoding then immediate and delayed retrieval (after
10 min and 24 h) of two texts presented in a musical
condition (i.e., sung lyrics) compared to a spoken text,
in AD patients and healthy comparisons. The two sung
lyrics conditions differed in the valence characteristics
of the musical background (positive versus negative) in
order to determine whether the musical mnemonic
in AD might depend on emotional valence.
First, patients’ overall performance in verbal episo-
dic memory was lower than that of healthy compari-
sons, whatever the score considered. As expected,
patients with mild to moderate AD showed encoding
and retrieval deficits in episodic memory, which is well
known as a core symptom in typical amnestic forms
of AD (e.g., Sarazin et al., 2007) and classically
explained by medial temporal lobe atrophy including
the hippocampus (Sarazin et al., 2010).
Furthermore, consistently with our hypothesis, sung
texts were better remembered than spoken texts by AD
patients, for encoding scores (number of lines learned
and immediate recall). This was also true for delayed
recalls (see Palisson et al., 2015; Moussard et al., 2014
for converging results), suggesting that the retention
delay is not the main factor to explain the divergent
9
results reported in the literature (Table 1). Conversely,
the retention delay might impact the results if it is too
long with respect to the disease severity (e.g., Baird
et al., 2017 who proposed a delayed recall after
30 min to AD patients with a mean MMSE score of
17.5 ± 4.3). By contrast with Simmons-Stern’s results
(Simmons-Stern et al., 2012), the present findings sug-
gest that music might enhance recollection processes
and not only familiarity (see also Palisson et al., 2015;
Moussard et al., 2014 for convergent results). The fact
that familiar songs were chosen and that a reinforced
encoding procedure was used with a multimodal cod-
ing of texts (both visually and auditorily displayed)
might have ensured a richer and deeper encoding
(Craik & Lockhart, 1972). Interestingly, this mnemonic
effect of music was observed in AD patients without
musical background, thus suggesting that this effect
could be generalizable whatever the musical back-
ground of patients and cannot be explained by the
sparing of an over-learned complex skill in
musicians AD. Thus, this result offers clinical insights
by showing that music mnemonics seems to be an area
of functioning that is relatively robust to brain damage
in AD and could potentially offer a simple low-cost
strategy to maintain memory recall of a limited amount
of information (e.g., daily activities) in persons with
mild to moderate AD.
The second aim of the present study was to examine
whether this musical benefit on memory may be modu-
lated by the valence characteristics of the musical back-
ground used. Results showed that valence matters in
HCs since the benefit of musical encoding was
observed when the excerpt was positively-valenced
but not when negatively-valenced (see also
Ratovohery et al., 2018). This results is consistent
with the positivity bias reported in normal aging
(Charles et al., 2003; Reed et al., 2014). In AD,
a different pattern was observed: while the positivity
effect existed at short-term (immediate recall), no dif-
ference according to the valence was observed after
10 min or 24 h, meaning that this effect disappeared
after a retention delay. When considering the preva-
lence of AD patients who did not recall any words, it
appears that it was more frequently the case in the
spoken condition followed by the positive condition,
while less frequent in the negative condition. This
result suggests that the free recall after 10min may
even be easier when the sung text was encoded asso-
ciated with a negatively-valenced excerpt. These results
are consistent with the findings of Sava et al. (2015),
who found no positivity bias in free recall of visual
stimuli in AD patients. Consistently with their study,
we used a rich deep encoding, suggesting that the
10 S. RATOVOHERY ET AL.
intentional process during encoding was not sufficient
in AD to elicit the positivity bias in free recall tasks
(Sava et al., 2015; Reed et al., 2014; see also Kalanzaga
et al., 2016 for converging results using words). Thus,
the present study extends these findings to the musical
domain for the first time in AD, suggesting overall that
the positivity bias vanishes in this disease.
From a more theoretical perspective, this second result
may provide arguments in favor of the Socio-emotional
Selectivity theory (SST; Carstensen, Isaacowitz, &
Charles, 1999). This theory posits that the positivity effect
results from top-down strategies to regulate emotions.
Accordingly, the decline in cognitive resources associated
with AD is believed to prevent from such top-down
strategies from occurring, thus leading to the disappear-
ance of the positivity bias in this disease (see Kalanzaga
et al., 2016 for a discussion). Consistently, Landré et al.
(2013) showed that the emotional enhancement of mem-
ory decreased and even disappeared in AD when medial
temporal atrophy increased (Landré et al., 2013).
However, other alternatives hypotheses might explain
why musical mnemonics seem effective in AD regardless
the valence of the excerpts used. First, music influence
emotion in a positive way no matter its valence charac-
teristics (Croom, 2015). For example, Cuddy and collea-
gues found that music-evoked autobiographical
memories are more positive in AD than in young adults,
regardless the valence of the musical cue (Cuddy, Sikka,
Silveira, Bai, & Vanstone, 2017). Thus, it is possible that
both musical conditions were associated with positive
emotions and/or memories in AD, explaining why both
conditions lead to better memory. In the same way,
listening to music during the encoding stage may be
associated with reward feelings that could also help recol-
lection (Ferreri & Rodriguez-Fornells, 2017). Second,
both musical conditions led to a better recall than the
spoken encoding condition because of the modality dif-
ference (sung versus spoken). In this case, the benefit
observed might be explained by a preserved music pro-
cessing in AD, by contrast with a language processing
deficit (Baird & Thompson, 2019; Golden et al., 2017).
Consequently, sung text processing may be easier during
the encoding phase, leading to better subsequent recall.
Arguing in favor of music as playing a facilitating role,
Ferreri and colleagues showed that the dorsolateral pre-
frontal cortex – classically involved during encoding –
was deactivated in older adults during a musical encoding
of words in comparison with a silent encoding (Ferreri,
Aucouturier, Muthalib, Bigand, & Bugaiska, 2013; Ferreri
et al., 2014). Finally, from a methodological point of view,
although chosen based on pilot testing for valence, arou-
sal and familiarity properties, we cannot totally rule out
the possibility that our musical excerpts may have
differed in other characteristics that musical valence (for
example in terms of complexity and tempo) that might
have influenced performance (e.g., Ferreri & Verga,
2016). Contrary to what the present findings show, if
one musical excerpt was less complex than the other
one, better performance to learn and recall the text asso-
ciated with the less complex melody would have been
observed regardless the group considered. Also, the
Chopin’s excerpt has a slower tempo than the
Beethoven’s one. Sung stimuli with a slower presentation
rate can facilitate the learner’s ability to memorize
(Kilgour, Jakobson, & Cuddy, 2000). Consistently with
this assumption, the better recall performance should
have been observed in the negatively-valenced rather
than in the positively-valenced encoding condition. Yet,
we observed the reverse pattern in HCs. Thus, it seems
unlikely that these other possible differences between the
two musical excerpts, which have not been assessed and
controlled, may explain the findings observed in both
HCs and AD patients.
Some other methodological limitations also need to
be addressed. Unfortunately, it was not possible to
counterbalance the association between one text and
the music condition (positive or negative) due to the
fact that the texts were written to be sung on the
positive or the negative melody, and thus fitted only
one experimental condition. However, a pretest we
reported in Ratovohery et al. (2018) confirmed that
learning of the three texts when all presented spoken
without music led to similar encoding and retrieval
performance in healthy participants. This suggests
that performance differences observed when texts are
sung during the encoding stage may be explained by
differences between musical excerpts and their asso-
ciated characteristics rather than by differences
between texts themselves. We also chose to use one
melody for each valence due to practical considera-
tions. Indeed, the inclusion of added melodies to test
each valence would have be associated with a very long
lasting procedure, which could have not been tolerable
to participants with AD. Finally, concerning our AD
participants, we found that 23% of our sample scored
below the conventional cutoffs scores for amusia. It is
possible that these patients had poorer comprehension
abilities. Alternatively, this suggests that a few AD
patients may present melodic processing deficits at
a moderate stage of the disease (Campanelli et al.,
2016). However, we found that the MBEA score was
not correlated to the emotional musical benefit
observed in AD suggesting that our results were not
better explained by the characteristics of patients
group. Higher depression scores in AD group did not
influence the pattern observed on the musical benefit,
 JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY
as indicated by correlations analyzes, meaning that the
absence of positivity effect in AD may not be related to
a mood congruency effect (Mayler, Gayle, Meehan, &
Haarman, 1990).
The present study provides additional arguments
supporting the interest of using music as a mnemonic
strategy to maintain verbal episodic memory in AD
(Moussard et al., 2014; Palisson et al., 2015). Our
study also provides arguments showing that the musi-
cal benefit can be observed after a 24-hour delay
despite severe memory disorders in AD patients and
in a sample of non-musicians, suggesting that music
mnemonics seems to be an area of functioning that is
relatively robust to brain damage in AD. To the best of
our knowledge, the present study if the first one in the
field of musical mnemonic to give a specific attention
to the effect of musical valence. Although our results
show a musical mnemonic effectiveness regardless of
the valence of the excerpts used, other musical features
(i.e., complexity, rhythm, harmonic structure) might
explain or at least contribute to this effectiveness.
Future studies are needed to better describe the non-
musical and musical features involved to help clinicians
(i.e., psychologists, music therapists) to select appro-
priate music to try to maintain memory in mild to
moderate AD.
Acknowledgments
The authors are grateful to the Psychology students Prudence
Perriet and Aude Gachet who assisted the first author in
carrying out the evaluations of the healthy comparisons and
patients, and Ullie Bin who recorded the audio lyrics (spoken
and sung versions). We also thank Elizabeth Rowley-Jolivet for
English language editing of the manuscript.
Disclosure statement
No potential conflict of interest was reported by the authors.
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