Download musical structure facilitates verbal learning in multiple sclerosis

Musical Structure Facilitates
325
M USICAL S TRUCTURE FACILITATES V ERBAL L EARNING
IN M ULTIPLE S CLEROSIS
the exact nature of memory deficits in MS remains
unclear. More important from a clinical point of view,
as Rao has ardently noted for many years (Rao, 1995), is
the lack of treatments for memory dysfunction in MS
(Bennett, Dittmar, & Raubach, 1991).
M ICHAEL H. T HAUT
Colorado State University
DAVID A. P ETERSON
University of California, San Diego
Memory and Music
K IMBERLY M. S ENA & G ERALD C. M CINTOSH
Colorado State University
that the temporal patterns in music and rhythm can be a mediating stimulus to
enhance cognitive function. We investigated here whether
a musical template would influence verbal learning and
memory performance in patients with multiple sclerosis
(MS). The patients were randomly divided into two
groups, hearing either a spoken or musical (sung) presentation of Rey’s Auditory Verbal Learning Test (AVLT).
Patients in the music condition showed significantly better word order memory than patients in the spoken condition. The evidence suggests that music enhances word
order memory in patients with MS. We discuss the possible neurobiological underpinning of this result.
THERE IS GROWING EVIDENCE
Received July 10, 2007, accepted October 28, 2007.
Key words: music, memory, multiple sclerosis, verbal,
plasticity
Multiple Sclerosis and Memory
The past two decades have seen an increasing awareness
of cognitive deficits in multiple sclerosis (MS). Many
MS patients have cognitive deficits (Amato, Ponziani,
Siracusa, & Sorbi, 2001; Kujala, Portin, & Ruutiainen,
1996; Peyser, Edwards, Poser, & Filskov, 1980; Rao,
1990, 1995). Memory is one of the most prevalent types
of cognitive deficit in MS and some memory deficits
present in early phases of the disease (Landro, Sletvold,
& Celius, 2000). Despite new memory test development
(Camp, Thompson, & Langdon, 2001) and several
research studies aimed at isolating the memory problems in MS (Deluca, Barbieriberger, & Johnson, 1994;
Marie & Defer, 2001; Rao, Staubinfaubert, & Leo, 1989),
Music Perception
VOLUME
25,
ISSUE
4,
PP.
325–330,
ISSN
0730-7829, ELECTRONIC
Many clinical reports have emphasized the relative
‘survival’ of musical memories in neurologic memory
disorders (Baur, Uttner, Ilmberger, Fesl, & Mai, 2000;
Haslam & Cook, 2002), dementia and Alzheimer’s disease (Cuddy & Duffin, 2005; Foster & Valentine, 2001;
Son, Therrien, & Whall, 2002). Music processing may
recruit not only declarative but also more automatic,
procedural learning and memory systems that are
spared in amnesia.
Music training and musical accompaniment can also
enhance memory for nonmusical material (Ho, Cheung,
& Chan, 2003; Jakobson, Cuddy, & Kilgour, 2003;
Rainey & Larsen, 2002; Wallace, 1994). Previous evidence
has shown music memory provides access to verbal
knowledge in patients with memory disorders (Baur
et al., 2000; Foster & Valentine, 2001; Haslam & Cook,
2002). Music rehearsal has been shown to be more
effective than verbal rehearsal in learning nonmusical
materials with learning disabled and developmentally
disabled students (Claussen & Thaut, 1997; Gfeller,
1983; Wolfe & Hom, 1993). Structured music listening
has been shown to enhance a broad range of cognitive
functions in autistic children (Bettison, 1996). Maeller
(1996) demonstrated that music can improve memory
in MS patients, with a trend toward greater improvement associated with severity of the disease. Thus, there
is mounting evidence that music can enhance a variety
of cognitive functions in neurologically impaired individuals. But if music can assist learning and memory,
what might be the neurophysiologic basis for this effect?
Music and Brain Plasticity
There is a small but growing body of evidence that
music modulates brain activity associated with nonmusical functions of the nervous system. We have evidence
ISSN
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DOI:10.1525/MP.2008.25.4.325
326
Michael H. Thaut, David A. Peterson, Kimberly M. Sena, & Gerald C. Mcintosh
that rhythmic entrainment can be used for sensorimotor
rehabilitation: the temporal structure of music can be
harnessed to rehabilitate motor function in brain damaged patient populations (Hummelsheim, 1999). Can a
similar strategy be used to rehabilitate impaired verbal
memory function? If the brain implements verbal learning and memory differently for musical and nonmusical
contexts, perhaps impaired nonmusical verbal memory
could be ameliorated by unimpaired musical verbal
memory. Plasticity in the functional organization of
brain networks is important in recovering verbal learning and memory function after, for example, traumatic
brain injury (Ricker, Hillary, & DeLuca, 2001). Occipital
cortex of congenitally blind individuals plays a prominent role in superior verbal memory performance relative to sighted individuals (Amedi, Raz, Pianka, Malach,
& Zohary, 2003). Music can play a role in brain plasticity,
through both its pitch characteristics (Shahin, Bosnyak,
Trainor, & Roberts, 2003) and temporal structure
(Merzenich, Schreiner, Jenkins, & Wang, 1993; Pantev,
Wollbrink, Roberts, Engelien, & Lutkenhoner, 1999).
Present Study
Learning and remembering spoken verbal information
is a common and important day-to-day function. Deficits
in verbal learning and memory can severely degrade a
patient’s quality of life. In this study we investigated
whether a musical template for verbal learning improves
verbal learning and memory. Given the practical significance of the sequence of verbal information, we specifically investigated whether music would improve learning
and memory for ordered word lists in patients with
multiple sclerosis. Music is naturally associated with
ordered word list recall in the form of lyrics, so perhaps
it could selectively enhance ordered word recall even in the
absence of rhyme and syntactic and semantic structure.
M = 53.8 (SD = 11.2), years of music training were M =
5.4 (SD = 6.3) and M = 10.2 (SD = 16.5), years of education were M = 15.3 (SD = 2.0) and M = 16.4 (SD =
3.5), and Expanded Disability Status Scale (EDSS) ratings were M = 4.6 (SD = 1.2) and M = 4.3 (SD = 1.1).
The two groups did not significantly differ in terms of
age, education, music training, or EDSS rating. The two
groups performed similarly on the Selective Reminding
Test and Logical Memory I subtest. Each group
included 9 females and 1 male.
Task and Stimuli
Unlike the more typical in person administration of the
Auditory Verbal Learning Test (AVLT, Lezak, 1995), we
used prerecorded sound files and remotely recorded
voice responses with the participants isolated in a
soundproofed booth. This served to maximize consistency of the test procedures. A single standard list of 15
words was repeated in ten trials, and the participant was
asked to free recall as many words as possible after each
list presentation (see Figure 1). The 15 words in the list
were semantically unrelated. The words were presented
at a rate of approximately one per second and the presentation order was the same on every trial. On each
trial, participants were instructed to listen carefully as
they would subsequently be asked to recall as many
words as possible. Recall of the list was tested without
further presentation of the original list after participants heard and free recalled a distractor list, and again
after a 20-minute nonverbal distractor task. Participants were not given feedback on any trials.
Participants were randomly assigned to either a
sung or spoken presentation of the AVLT. In the music
condition participants were asked to sing back as many
words as they recalled. This ensured modality congruence
Method
Participants
Participants were 20 right-handed volunteers with
relapsing-remitting MS, with normal hearing and no
history of other neurological or psychiatric conditions.
All participants volunteered and provided written,
informed consent approved by the institutional review
board. Participants were randomly assigned to one of
two conditions: with and without a musical template
providing temporal structure, hereafter referred to as
the “structured” and “unstructured” conditions. Respectively, the groups’ ages were M = 51.7 (SD = 9.3) and
FIGURE 1. Rey’s Auditory Verbal Learning Test (AVLT). There are ten
presentations of the same word list and one presentation of a new distractor word list. On each trial, participants heard the full list of 15 words
before being prompted to recall. Participants were asked to free recall
the words again (without additional presentation) in two memory tests,
m1 = immediate recall after the distractor list and m2 = recall after a 20
minute delay and distractor task.
Musical Structure Facilitates
between the learning stimulus and recall. In both conditions they were additionally instructed to recall items in
the order they were presented on the word list.
The sung and spoken conditions used identical word
lists of equal overall duration presented free field at 80
dB SPL. The sound files were recorded using the same
female vocalist for both conditions. In the structured
condition the word list was presented as lyrics for an
originally composed song. One-syllable words were
assigned one quarter note of 1 s duration, while twosyllable words were assigned one eighth note of 0.5 sec
(500ms) per syllable to generate a melodic-rhythmic
phrasing structure and to keep the sung condition at 15
s durations (with one second rest at the end), equal to
the spoken condition. We used an originally composed
melody that was not familiar but was simple and repetitive in structure (AABA form). We measured the size of
word chunks recalled in proper sequence, assessing
chunk lengths of 2, 3, 4, 5, 6, and 7 words.
Results
In the analysis of pairwise word order learning, a consistent trend emerged for better recall in music than spoken learning, reaching statistical significance at the end
of the learning and memory task, when comparing the
mean of the last learning trials (T6-10) and the two subsequent memory trials, F(1,18) = 4.51, p = .038 (see
Figure 2). Musical verbal learning induced greater
FIGURE 2. Music enhances pairwise word order learning and memory.
The x-axis shows performance across learning trials 1-10, distractor trial
(d), and memory trials 1 and 2. The percentage of word pairs recalled in
the correct order (y-axis) is change relative to trial 1. Standard error bars
are shown.
327
increases in word order recall in early and late phases of
learning, whereas spoken verbal learning induced the
greatest increases in word order recall during the middle phase of learning. The spoken verbal learners’ performance actually decreased slightly in the last two
learning trials, and remained relatively lower than the
musical verbal learners’ performance in the later recall
trials.
Two-tailed t-tests for differences in change of learning
performance between verbal and musical condition
(T6-10 vs. M1) for the higher word order sequences
(3-7 words) were all highly significant, 3: t(18) = 4.32,
p = .0004; 4: t(18) = 4.27, p = .0004; 5: t(18) = 4.08, p =
.0007; 6: t(18) = 3.89, p = .001; 7: t(18) = 2.40, p = .027.
Discussion
Participants in the music condition showed significantly
better word order memory than participants in the
spoken condition. The finding that music can improve
order memory is significant given the increasingly
recognized cognitive deficits in multiple sclerosis
(Amato et al., 2001; Peyser et al., 1980; Rao, 1990).
Approximately 50% of MS patients suffer cognitive
impairment (Rao, Leo, Bernardin, & Unverzagt, 1991),
and this commonly manifests in verbal memory impairment (Sweet, Rao, Primeau, Mayer, & Cohen, 2004).
This is the first known study to extend earlier work on
memory for temporal order in MS (Beatty & Monson,
1991) using an ecologically salient paradigm like the
AVLT.
Considering that the demyelination process of the disease will affect and interrupt network dynamics of neuronal cell assemblies required for learning, the results
provide evidence that melodic-rhythmic templates, as
commonly inherent in the structure of music as a temporal and nonverbal sensory language, may support verbal
learning and memory, in spite of an underlying disease
process that affects the neurobiological processes of
learning. From such circumstantial evidence one may
propose that music perception does affect neurobiological processes of learning in some compensatory way,
however, with physiological mechanisms to be determined. The differential effect of music may occur during
encoding rather than retrieval, because encoding is a
phase of memory processing associated with deficits in
MS (Marie & Defer, 2001).
While the exact nature of the neurophysiologic
mechanisms underlying the differential learning we
measured remains elusive, a few theories may be put
forth. Musical verbal learning may access compensatory
328
Michael H. Thaut, David A. Peterson, Kimberly M. Sena, & Gerald C. Mcintosh
pathways for memory functions during compromised
prefrontal cortical functions associated with learning
and recall. Musical learning may also confer a neurophysiological advantage through the stronger synchronization of the same neuronal cell assemblies
underlying conventional verbal learning and memory.
In both cases, the temporal structure implicit in musical
stimuli may sharpen the timing of neural dynamics in
brain networks degraded by demyelination in MS. Several researchers (Deutsch, 1982; Janata, Tillmann, &
Bharucha, 2002; Wallace, 1994) have—based on Gestalt
perception and learning principles—proposed that
music provides a highly effective mnemonic for learning by incorporating a temporal structure and redundancy that chunks information into more manageable
units ( Deutsch, 1999; Gfeller, 1983). “Chunking” is a
helpful mechanism not only in declarative learning and
recall, but also in motor learning (Verwey, 2001).
Indeed chunking is probably an innate feature across a
broad phylogenetic range of nervous systems (Matzel,
Held, & Miller, 1988). The intrinsic structure of sound
patterns in music is a highly effective mechanism to facilitate perceptual grouping and chunking. The present
study supports the notion that “musical chunking” can
be exploited to rehabilitate verbal learning and memory.
It extends recent research in our center regarding the
beneficial effect of musical template learning on verbal
learning in healthy adult participants ( Peterson & Thaut,
2003), as well as pilot research suggesting that music can
improve memory in MS patients and that music induced
enhancements were significantly correlated with
increases in severity of disease (Maeller, 1996).
There is a growing body of knowledge about the
neurobiological correlates of verbal memory, music,
chunking, and plasticity. Lesion (Halpern, 2001; Peretz,
2002), functional imaging (Parsons, Hodges, & Fox,
1998; Platel et al., 1997; Smith, Jonides, Marshuetz, &
Koeppe, 1998; Zatorre, Halpern, Perry, Meyer, & Evans,
1996), EEG (Peterson & Thaut, 2002; Ruchkin, Berndt,
Johnson, Ritter, Grafman, & Canoune, 1997) and MEG
(Maess, Koelsch, Gunter, & Friederici, 2001; Makeig &
Jung, 1996; Tecchio, Salustri, Thaut, Pasqualetti, &
Rossini, 2000) studies have illustrated that both music
and verbal memory recruit widespread networks
encompassing many brain regions. Theoretical work is
beginning to link the behavioral level phenomenon of
chunking to the dynamics of cell assemblies in cortex
(Wickelgren, 1999). System-level research into brain
plasticity has highlighted the importance of temporal
structure in stimuli (Merzenich et al., 1993; Pantev et al.,
1999) and associated cortical plasticity with verbal
learning (Tallal, 2000). Collectively, the research suggests
that physiological measures of brain network dynamics
(Fuster, 1997; Garrett, Peterson, Anderson, & Thaut,
2003), such as spectral analysis of the scalp EEG (Basar,
Basar-Eroglu, Karakas, & Schurmann, 1999; Lopes da
Silva, 1999), can provide a window into how musical
chunking may enhance verbal memory. Thus, simultaneous EEG would be a helpful adjunct to the methods
used in the present study by providing a measure of how
music modulates brain dynamics associated with the
learning process. In conclusion, we evaluated a specific
strategy for enhancing verbal memory in MS patients.
The results are suggestive of the therapeutic potential of
musical mnemonics in verbal learning and memory, an
area of dysfunction in MS that is definitely underserved
in basic research and therapeutic intervention.
Author Note
We are grateful to Geoffrey O’Shea for assistance with
data collection, and Kathrin Mertel for assistance with
data analysis. This research was funded by a Pilot
Research Grant from the National Multiple Sclerosis
Society (NMSS) to M. H. Thaut. The NMSS also assisted
with advertising the study to local patients.
Correspondence concerning this article should be
addressed to Michael H. Thaut, Center for Biomedical
Research in Music, Colorado State University, Fort
Collins, CO 80523 USA. E-MAIL: michael.thaut@
colostate.edu
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