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Aging Clinical and Experimental Research

Improvement of autobiographic memory recovery by


means of sad music in Alzheimer's Disease type
dementia
Juan Jos Meiln Garca1,2, Rosario Iodice1, Juan Carro1,2, Jos Antonio Snchez1,2,
Francisco Palmero3 and Ana Mara Mateos2
1University

of Salamanca, Department of Psychology, Salamanca, 2Contract for research collaboration


between The Neurosciences Institute of Castile and Leon and The National Reference Centre of Alzheimer
Disease (CRE Alzheimer's Salamanca-IMSERSO; Government of Spain), 3University Jaume I, Department
of Basic Psychology, Castelln, Spain

ABSTRACT. Background and aims: Autobiographic


memory undergoes progressive deterioration during the
evolution of Alzheimers disease (AD). The aim of
this study was to analyze mechanisms which facilitate recovery of autobiographic memories. We used a
repeatedly employed mechanism, music, with the addition of an emotional factor. Methods: Autobiographic memory provoked by a variety of sounds (music which was happy, sad, lacking emotion, ambient
noise in a coffee bar and no sound) was analyzed in a
sample of 25 patients with AD. Results: Emotional
music, especially sad music for remote memories, was
found to be the most effective kind for recall of autobiographic experiences. Conclusions: The factor evoking the memory is not the music itself, but rather the
emotion associated with it, and is useful for semantic
rather than episodic memory.
(Aging Clin Exp Res 2012; 24: 227-232)

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as the disease develops (1). This loss has a devastating effect on both patients and their caregivers, who witness
how a persons self slowly disappears.
However, this deterioration does not follow a linear
process. Autobiographic memory presents a dissociation which affects performance, due to the relation between its episodic and semantic components (2). It is a
form of episodic memory and, as such, is affected by the
deterioration of episodic memory. AD patients remember
remote events from their youth better than the more
recent ones of adulthood (3) and have more difficulty than
elderly persons without dementia in acquiring new autobiographic information and remembering these facts (1).
Researchers have attempted to clarify some of these
mechanisms which underlie recovery processes of autobiographic memory in AD. The aim is to develop a rehabilitation model to stimulate and favor the recovery of
autobiographic information in patients with AD, in order
to maintain and stimulate their best preserved capabilities,
in an attempt to achieve the best possible functional situation and quality of life. In this vein, reminiscence or then
life review technique (4) is an effort to maintain remote
and autobiographic memory even in people in states of
dementia. Reminiscence activates personal memory by focusing recall on the personal aspects of events, stimulating identity and the emotional aspects of memory. Although the reminiscence technique has had positive effects
on quality of life, handling of depression, and satisfaction
and well-being of patients with AD (4, 5), little evidence
has been found that it improves cognitive processes in
general or autobiographic memory in particular. Other

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Editrice Kurtis

INTRODUCTION
Alzheimers disease (AD) is a progressive neurodegenerative disorder with clearly defined clinical characteristics. Cognitive deterioration in AD includes practically
all cognitive abilities, but the most evidently affected one,
from onset, is memory. Memory loss is progressive,
starting with some mild word loss which gradually becomes more severe, until patients cannot even remember
their own personal history. This same process takes
place in autobiographic memory. At the onset of the
disease it is relatively preserved, but gradually deteriorates

Key words: Alzheimer, autobiographic memory, music therapy.


Correspondence: Rosario Iodice, University of Salamanca Department of Psychology. Avda. de la Merced, 109-131, E-37005 Salamanca,
Spain.
E-mail: rosarioiodice@usal.es
Received April 13, 2011; accepted in revised form July 7, 2011.
First published ahead of print July 21, 2011 as DOI: 10.3275/7874

227 Aging Clin Exp Res, Vol. 24, No. 3

Autobiographic memory and music in AD

modalities of memory recovery techniques are intended to


evoke memories which would otherwise no longer be accessible to patients. Examples are the imagery mnemonic tasks (6), which help patients to access memories by
means of multisensory facilitating contexts.
A recent effort in this direction has been sound stimulation based on musical pieces played to elderly patients and ones with slight cognitive impairment, Vivaldi or Mozart effect and its influence on memory
performance (7). Participants are exposed to a music
condition, compared with a non-music condition. The majority of these studies concluded that music has a positive
effect on memory performance in the elderly (8, 9),
mainly in short-term memory performance (10) and free
recall (11). If music can optimize cognitive performance in
memory, it may have important practical implications for
successful aging, and act as a palliative against the impairment of dementia, maintaining the self of AD patients
as long as possible (12-14).
Some authors have found a similar effect when exposing persons with dementia to classical music and verifying changes in the performance of autobiographic
memory tasks (15-17). Foster and Valentine (16) assessed the recall of different life stages (remote, middle and
recent periods) in a group of individuals with moderate AD
impairment using various musical stimuli (familiar music,
new music, absence of sound, and ambient noise in a
cafeteria bar). Patients with AD recalled life events more
easily in a condition of musical stimulation than in conditions in which there was no music.
One result of these studies is that memory performance in patients with dementia is very sensitive to recall
cues evoked by the music used. This is something which
does not occur in healthy older individuals, who do not
need external recall cues (15). Levine et al. (2) found
that autobiographical recollection is mediated by a fronto-temporo-parietal distributed system, with the antero-medial prefrontal cortex positioned to integrate sensory information with self-specific information. Other authors
(e.g. Foster and Valentine) (16) believe that, rather than resorting to associative facilitation of recall cues, this finding
shows an increase in attentional processes and in the
arousal caused by music. They found that recall with
sound was better than in silence and that performance was
better with music than with cafeteria noise, suggesting the
importance of structured sound. They did not find any differences in the effect of different types of music (familiar
vs novel); a surprising result, since familiar music should
evoke more memories than other sounds.
Other studies have documented the value of using
music to induce sad or happy moods in participants during cognitive tasks and to improve memory performance.
Sherratt et al. (18) demonstrated that, potentially, music
can provide an ideal opportunity to maximize social interactions and improve individual well-being in people with

severe cognitive impairment. Thompson et al. (19, 20)


provided support for this hypothesis of arousal and
mood, according to which the beneficial effect of music is
mediated both by the state of arousal and by the mood of
participants in the study. Both these aspects promote cognitive processing (21). In the case of regulation of the
emotional component, Mammarella et al. (8) showed
that the Vivaldi effect causes an increase in short-term
memory performance (phonological working memory
and phonemic fluency) in elderly individuals without
pathology, because emotional factors are involved. The
music enhances the level of arousal. This increase in
arousal results in a greater level of attention and consequently attentional processes benefit and/or promote a
positive mood.
The idea that emotion plays an important role in the
memory processes of patients with dementia is not new
and has been confirmed in general studies (22-24). Irish
et al. (15) demonstrated that the beneficial effects of
background music on autobiographical recall may be explained in terms of anxiety reduction. Also of interest is
the study by Gagnon et al. (25), which shows how the
emotional components produced by musical stimuli induce
an episodic recall capability in patients with AD similar to
that of elderly persons without pathology. As regards
the relation between emotion and autobiographic memory, it has been found that accessibility to emotionally
charged personal memories is better preserved than accessibility to neutral events in the remote past.
In this research we confirm that music serves as an
emotional type of recall event, but that the type of emotion induced by music activates different types of memories. We use the study design of Foster and Valentine
(16), who found that musical auditory stimulation has a direct beneficial effect on the autobiographic memory of individuals with AD, as opposed to non-musical stimulation.
We stimulate patients with AD using musical pieces
which give rise to emotional involvement and should favor the recovery of information in autobiographic memory, in contrast to other types of music which lack an
emotional component.
However, the nature of the relationship emotion vs
memory is controversial. Mammarella et al. (8) state that
the positive effects of music cannot be generalized to all
types of music. Studies of the different effects of each type
of music on peoples emotions generally regard the classics (26). One line of research suggests that positive affect
leads to greater flexibility in cognitive processing or supports assimilation processes (27, 28). Individuals draw active inferences beyond the information given and impose their own internal structures. Positive affect acts as
a semantic memory enhancer, whereas a negative mood
supports accommodation: the internal structures are
changed as a function of stimulus affordances. Thus,
the negative affective state is traced to specific autobio-

Aging Clin Exp Res, Vol. 24, No. 3 228

J.J. Meiln Garca, R. Iodice, J. Carro et al.

graphic topics as definite painful events congruent with


mood (29). Matsumoto (30) found that deeply depressed
patients improved their mood by reliving their memories
through sad music. Abercrombie et al. (31) posited that facilitation of recall/memory congruent with affective state
only takes place in individuals reporting high rates of
negative affect associated with stress or in individuals
suffering from depression, but not in persons with high
rates of positive affect. Meiln et al. (32) found that the
mood congruence effect occurs in the processing of
words in the category of sadness, but not in those of the
category of joy. Thus, according to the state dependence theory, the effect of emotional state is amplified in
subjects with depression, who may show disproportionate
retrieval of unhappy memories, an effect which may also
take place in people with AD. Thus, in addition to the four
types of music used by Foster and Valentine (16), we used
music with a large emotional component classified as
sad, music with an emotional component classified as
happy, and new music.
The second hypothesis stressed in our study is that the
emotion of sadness is more favorable to autobiographic recall than happiness, a hypothesis which has been gathering strength in recent years (32). Thus, negative recall
seems to function as an adaptive process which helps in
processes of recognizing memories associated with this
emotional state, a phenomenon that does not occur
with positive memories (33).
METHOD
Participants
Participants (n=25; mean age 80.68; SD 5.79) are patients from a National Reference Center of Alzheimer Disease (Salamanca, Spain) diagnosed (NINCDS-ADRDA) as
probable AD and with Geriatric Depression Scale (GDS)
= 4 (slight AD) (34). The aim was to compare the influence of different kinds of music as opposed to absence of
sound, in each patient with AD. The AD patients were
over 60 years of age, with no history of drug or alcohol
abuse, and had no symptoms of depression (GDS<10).
They are patients in the Centers program of cognitive
stimulation, and therefore all of them maintain their system of communication, auditory abilities, ability to read
and the ability to follow instructions (MMSE score
mean=14.6; SD 8.31).
Material
The auditory stimulation program consisted of five
pieces of music. Of the original pieces in the study by Foster and Valentine (16), we added one piece of music
with a high emotional value to fit our second hypothesis.
We used a musical piece catalogued as happy (Summer
by Vivaldi; catalogued as familiar music in Foster and
Valentine), and one catalogued as sad (Versa est in
Luctum, a Renaissance motet by Alonso Lobo for funeral

229 Aging Clin Exp Res, Vol. 24, No. 3

masses). Both of these pieces had been used in a previous


study which confirmed their effectiveness as inducers of
the corresponding emotional state (32) based on changes
in participants scores on the Positive Affect Negative Affect Scale (PANAS, 35). The following categories were
then added: cafeteria sounds (a recording made in a coffee bar in the city center), new music (Kang Time by Eric C.W. Peel) lacking an emotional component, and the
absence of sound. The latter functioned as the control variable in the experiment. The musical pieces were presented
in a Snoezelen room or as controlled multisensory stimulation by means of loudspeakers set homogeneously at
between 60 and 70 db.
The autobiographic memory questionnaire employed
here was the same as that used by Foster and Valentine
(16). It consists of the 28 questions on autobiographic
memory developed for the Mini-Mental State Examination
(MMSE) (36). As with the original, the purpose of the
questionnaire was to assess autobiographic memory at different moments of life: remote (from approximately 0 to
20 years of age: e.g., What was your first job?), mid-remote (from approximately 20 to 50 years of age: e.g,
How many children have you had?) and recent (the recent past and the present: e.g., Where do you live
now?). We did not attempt to make the questionnaire
equal in its levels of difficulty among age ranges, because our study aim was not to compare the different remote memory stages. One point was assigned for each
correct answer, with the exception of the second question,
which was assigned 3 points for the individuals date of
birth (one point for the day, one for the month and one
for the year). The total possible score was thus 30 points.
Each item was given one point if answered completely
correctly; 0.5 points if there was uncertainty about the
memory or if any of its terms was inexact; and 0 if there
was no response or if the information was incorrect. In order to evaluate the correctness of the responses, participants family members completed verification questionnaires and returned them to the experimenter.
Procedure
All participants had been previously evaluated by a
team of neuropsychologists. Sessions took place with
participants sitting in comfortable chairs, so that they
would be physically at ease and to help them feel relaxed.
Participants listened to the five musical pieces, each
piece in a different session, spaced by at least one week.
The conditions are described as happy music (HM), sad
music (SM), no sound (NS), coffee shop sound (CS) and
new music (NM). The order of the sessions was randomized for any participants in order to control for the effect of improvement of recall with time and repetition.
Sessions were individual and lasted 30 minutes. In each
session, participants listened to the musical piece corresponding to that session for five minutes. In the silence

Autobiographic memory and music in AD

condition this time elapsed while the questions were being prepared. After auditory stimulation, participants
were given the autobiographical questionnaire in order to
evaluate differing areas of memory: remote (Rem: 12
points), mid-remote (MRem: 8 points) and recent (Rec: 10
points). Questions were asked orally and repeated up
to three times if needed. Responses were given in writing.
To avoid the confabulation effect, participants were given precise instructions with regard to their inability to answer the questions. If they did not remember, they were
asked to say only I dont remember, to which the experimenter would respond, Dont worry if you cant
answer all the questions at the present time. At the
end of the session, participants were thanked for participating. The dependent variable was participants performance on the autobiographic memory questionnaire.
In order to avoid noise due to the differences among the
scales of the various time periods, points were changed to
percentages for statistical analysis.
RESULTS
Participants mean recall was 19.85 points (SD=6.80).
To analyze their performance outcomes, we ran a multivariate 5x3 ANOVA taking as factors the auditory condition (HM, SM, NM, CS, NS) and the time range of autobiographic memory (remote, mid-remote and recent periods). The dependent variable was performance on the
sub-scales of the autobiographic memory questionnaire.
Scores were converted to percentage for greater comparability. Orthogonal planned comparisons were subsequently carried out among them (see performance data in Table 1).
No significant effect of interaction was found between
the variables of music type and time range (F8,192=0.721).
The auditory factor showed a significant effect
(F4,96=5.851, p<0.001) of differences among the five auditory conditions. Orthogonal planned contrasts revealed
that significant differences were found between quiet
(NS) and Sounds (SM+HM+NM+CS; F 1,24=6.659,
p=0.016); recall was significantly better in Sounds
(mean=0.67) than in Quiet (mean=0.63). Recall was
significantly better (F1,24=9.916, p=0.004) in the two
types of emotional music (HM+SM; mean=0.69) than in

the two types of non-emotional sound (CS+NM;


mean=0.65). Non-significant differences were found between CS and NM (F1,24=1.309).
The time range factor showed a significant effect
(F2,48=42.935, p<0.001) of differences among the three
conditions: mean recall scores were 0.684 for remote,
0.756 for mid-remote, and 0.423 for recent memories.
For remote memory, the auditory condition factor
showed a significant effect (F4,96=3.578, p=0.009) of differences among the pieces of music. Orthogonal planned
contrasts showed no significant differences between quiet (NS) and Sounds (SM+HM+NM+CS; F1,24=0.757); the
recall was significantly better (F1,24=8.088, p=0.009) in
the two types of emotional music (HM+SM; mean=0.71)
than in the two types of non-emotional sound (CS+NS;
mean=0.66); non-significant differences were found between CS and NM (F1,24=0.021). However, in remote
memory, recall was significantly better in SM than in
HM (p=0.045), NM (p=0.010), CS (p=0.012) and NS
(p=0.017).
As regards the mid-remote autobiographic memory
range, the type of music showed a significant effect
(F4,96=2.589, p=0.042) of differences among the pieces.
Orthogonal planned contrasts showed no significant differences between quiet and Sounds (F1,24=3.904), between the two types of emotional music and the two types
of non-emotional sound (F1,24=2.975); no significant
differences were found between CS and NM (F1,24=1.799)
nor between SM and HM (F1,24=1.146).
For recent autobiographic memory, the auditory condition did not show a significant effect (F4,96=1.606) of differences among the pieces of music. Recent autobiographic memory thus functions differently from mid-remote and remote memory.
DISCUSSION
The aim of this study was to show that retrieval of information in autobiographic memory is more effective
when induced by an emotional musical stimulus. In this
case, confirming the findings of Foster and Valentine
(16), significant differences were found in autobiographic
memory performance in AD patients depending on the
presence of sound or its absence. According to Foster and

Table 1 - Performance on the Autobiographic Memory Questionnaire.


Total

Music Type
Happy Music
Sad Music
New Music
Coffee Shop Sound
No Sound

Mean

SD

Remote
Mean (SD)

Mid-Remote
Mean (SD)

Recent
Mean (SD)

19.98
21.08
19.90
19.30
18.98

6.47
5.95
6.30
7.45
7.59

9.64 (2.76)
10.20 (2.84)
9.28 (2.73)
9.32 (3.27)
9.42 (3.23)

6.16 (2.07)
6.44 (1.42)
6.22 (1.74)
5.80 (2.29)
5.62 (2.46)

4.20 (2.54)
4.56 (3.06)
4.40 (2.79)
4.14 (2.80)
3.86 (3.11)

Aging Clin Exp Res, Vol. 24, No. 3 230

J.J. Meiln Garca, R. Iodice, J. Carro et al.

Valentine (16), the ability to remember autobiographic information better after a musical stimulus is the result of an
increase in attention levels (arousal) or in attention absorption (37). We can add that this facilitating effect takes
place not only for attentional reasons but also as a result of
the importance of the emotional aspect. Emotion-inducing
music (happy and sad) evokes autobiographic memories in
AD patients better than non-musical sounds. It is the
emotional involvement rather than the music itself which
enhances autobiographical information. The induction of
an emotional component accompanies and favors the
retrieval of memories. The importance of the emotional
context in the consolidation of memories or long-term potentiation (LTP) in memory is well known. LTP undergoes
gradual deterioration in the aging process and is especially
virulent in cortical-type dementias, owing to neurological
damage in the amygdala and hippocampal regions (38).
Patients with AD show deficits in the recall of emotional
events, due to deterioration in these structures.
Also thought-provoking is the comment by Foster
and Valentine (16), regarding the areas of memory which
are more sensitive to musical stimuli. The area defined as
remote is more affected when participants listen to the
music, but this is not the case with mid-remote and recent
memories. Thus it seems to be confirmed once again the
fact that these types of autobiographic memory work
differently. In our study, the superiority of the music effect
was evident in the recall of remote but not mid-remote and
recent memories. As mentioned in the Introduction (2), remote memory seems to behave like semantic memory, affected by emotional recall cues, whereas recent memory
is episodic. The cause of this may be that autobiographic memory also depends on the hippocampal complex
and the medial temporal lobes dealing with episodic
memory. These are the areas in which brain lesions begin
in most AD patients. However, time is also a variable in
autobiographic information. The most recent memories
are essentially episodic, whereas more distant and remote
memories which have been repeatedly evoked lose their
temporal and contextual specificity and take on characteristics of personal semantic knowledge. Thus, Kazui et
al. (39) showed that personal semantic memory has features of both episodic and semantic memory, that semantic memory is transformed from episodic memory,
and that defective personal semantic memory is related to
both semantic and episodic memory dysfunction in persons in advanced stages of AD. The memory of past incidents or events, famous events which took place in
the past, celebrities, places in their life history or historical events which took place in their lifetime (without being directly autobiographic) are affected during the course
of the disease. In both cases, episodic or semantic, this
seems to be the result of problems in the strategic process
of evocation (1).
In addition, as expected we found differences between

231 Aging Clin Exp Res, Vol. 24, No. 3

the emotional types of music which evoke autobiographic


recall. Emotional music, especially if sad, enhances semantic autobiographical information. We found that sad
music gives vise to clear-cut differences in performance in
the retrieval of remote memory compared with happy music, and that this is not the case with mid-remote or recent
memories. It is music classified as sadness-inducing that
produces significant differences in autobiographic memory performance, in contrast to evocation by happy music (39) and by other non-emotional sounds. Thus, AD patients favored semantic details not connected with a particular time or place (2). Dreisbach and Goschke (27)
explain that sad music acts as a definitive and specific cue
to memories, whereas happy music acts as a general
activator of attention, which is not so important in autobiographic memory. It may thus be surmised that sad music maintains a greater adaptation level associated with AD
which is not achieved by happy music, and does so despite the absence of the symptoms of depression which
are typical of some AD patients.
However, an alternative explanation to the lack of
differences between happy music and the rest of the
sounds used in this study is that we did not investigate the
degree of emotion to which the piece of music gave rise
in patients with mild AD (33). We did not test or verify
whether the music promoted emotional states in AD patients. Sad music may evoke greater emotion in AD patients, and this may be a quantitative rather than a qualitative difference. In this respect, findings from other
studies are contradictory. Allen and Brosgole (40) showed
that the recognition of happy, sad, and angry musical expressions was impaired in participants with dementia,
whereas Gagnon et al. (25) and Drapeau et al. (41)
found preserved recognition of sadness and happiness
from music in mild DAT. Nonetheless, differences between happy and sad emotions were not found in any of
these studies.
Our way of approaching with two types of memories
so that they remain intact over the evolution of the disease, should therefore be different. These results show the
fundamental importance of neurofunctional rehabilitation, in particular sound therapy, and point to the need to
continue to inquire into what are the important parameters in the rehabilitating effects of sound therapy: the structural complexity of the music, recall cues, type of emotion,
and so on. The Vivaldi/Mozart effect might be more effective if we started to refer to it as the Chopin effect.
ACKNOWLEDGEMENTS
The authors are deeply grateful to the anonymous referee for the
thoroughness of the corrections made.

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