Archives of Physical Medicine and Rehabilitation

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ORIGINAL ARTICLE

Effect of Rhythmic Auditory Cueing on Gait in People

Abstract
Objective: To determine whether rhythmic music and metronome cues alter spatiotemporal gait measures and gait variability in people with
Alzheimer disease (AD).
Design: A repeated-measures study requiring participants to walk under different cueing conditions.
Setting: University movement laboratory.
Participants: Of the people (NZ46) who met study criteria (a diagnosis of probable AD and ability to walk 100m) at routine medical review, 30
(16 men; mean age
SD, 80
6y; revised Addenbrooke’s Cognitive Examination range, 26e79) volunteered to participate.
Interventions: Participants walked 4 times over an electronic walkway synchronizing to (1) rhythmic music and (2) a metronome set at
individual mean baseline comfortable speed cadence.
Main Outcome Measures: Gait spatiotemporal measures and gait variability (coefficient of variation [CV]). Data from individual walks under
each condition were combined. A 1-way repeated-measures analysis of variance was used to compare uncued baseline, cued, and retest measures.
Results: Gait velocity decreased with both music and metronome cues compared with baseline (baseline, 110.5cm/s; music, 103.4cm/s;
metronome, 105.4cm/s), primarily because of significant decreases in stride length (baseline, 120.9cm; music, 112.5cm; metronome, 114.8cm)
with both cue types. This was coupled with increased stride length variability compared with baseline (baseline CV, 3.4%; music CV, 4.3%;
metronome CV, 4.5%) with both cue types. These changes did not persist at (uncued) retest. Temporal variability was unchanged.
Conclusions: Rhythmic auditory cueing at comfortable speed tempo produced deleterious effects on gait in a single session in this group with
AD. The deterioration in spatial gait parameters may result from impaired executive function associated with AD. Further research should
investigate whether these instantaneous cue effects are altered with more practice or with learning methods tailored to people with cognitive
impairment.
Archives of Physical Medicine and Rehabilitation 2013;94:718-24
ª 2013 by the American Congress of Rehabilitation Medicine

Alzheimer disease (AD) is characterized by deterioration of Motor deficits (including gait) in people with AD contribute to
physical function including gait, as well as cognitive decline. functional impairment independently of cognitive impairment,11
Typical gait changes associated with AD include decreased speed with functional impairment being a primary risk factor for insti-
and greater temporal and spatial variability.1-4 Gait deterioration tutionalization in this population.12 The projected worldwide rise
starts early in the course of the disease1,2,4 and is associated with in the number of people with AD to 81 million people by 204013 is
an increased rate of falling5 compared with cognitively intact intensifying the need to find effective management strategies to
older people.6,7 This increased rate of falling is associated with maintain quality of life and reduce burden of care. Recent
a greater likelihood of mortality8 or severe injury9 with subse- systematic reviews14-16 have shown that people with dementia can
quent institutionalization.10 improve their physical function with training.
Physical training programs that target motor deficits caused by
Presented in poster format to the Joint World Congress of the International Society of Posture the disease process as well as secondary physical problems of
and Gait Research and Gait & Mental Function, June 24e28, 2012, Trondheim, Norway. weakness and loss of flexibility resulting from reduced activity
No commercial party having a direct financial interest in the results of the research supporting
this article has or will confer a benefit on the authors or on any organization with which the authors
levels have been shown to improve walking in people with AD.17,18
are associated. An alternative approach builds on work demonstrating the role of

0003-9993/13/$36 - see front matter ª 2013 by the American Congress of Rehabilitation Medicine
http://dx.doi.org/10.1016/j.apmr.2012.11.009

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Auditory cueing in Alzheimer disease 719

executive function in walking19 and has used methods of improving when they attended for a routine medical review: (1) a diagnosis
executive function such as medication20,21 and cognitive training22 of probable AD according to published consensus guidelines32
to improve gait control in people with dementia. (including neuropsychological testing and functional imaging
A method of improving disordered walking that has been used studies such as single photon emission computed tomography
effectively with other neurologic disorders, some characterized by or 18F-fluorodeoxyglucoseepositron emission tomography); (2)
cognitive impairment such as Parkinson’s disease (PD) and stroke,23,24 adequate hearing (able to engage in conversation); (3) aged 65
is rhythmic auditory cueing. Auditory cues range from simple years; and (4) the ability to walk at least 100m on a level surface
metronome beats to specifically composed music with enhanced without a gait aid. Exclusion criteria were uncorrected visual
beats, and aim to regulate and increase gait speed by exploiting the disorders or significant musculoskeletal and neurologic disorders
strong connection between rhythmic sound and human movement. that would affect walking, including pain. The study was approved
Increased gait variability, which is strongly related to the risk of falling by the university ethics committee, and informed consent was
in people with AD,5 has also been shown to improve with rhyth- obtained for all participants.
mic auditory cueing in a group with PD.25 The effects of rhythmic
auditory cues (RACs) on the walking patterns of people with dementia Apparatus
have been evaluated in only 1 previous study.26 No significant
improvement in gait measures was found with either rhythmic music A GAITRite electronic walkwaya (830cm long and 89cm wide with
or metronome cues; however, participants were severely impaired an active sensor area of 732cm long and 61cm wide) recorded
nursing home residents who may have had only a limited ability to spatial and temporal gait measures. Data were sampled at 80Hz.
benefit from the cues. Gait variability measures were not reported. The system has high test-retest reliability for gait measures of
Neural pathways that mediate auditory-motor synchronization are people with AD.33 The auditory cues were a metronome beat and
not yet fully understood; however, connections between auditory and a musical piece (“Pomp and Circumstance March No. 1” in D, by
motor regions are known to be extensive and include the supple- Sir Edward Elgar),34 each in Musical Instrument Digital Interface
mentary and presupplementary motor areas, the cerebellum, and the (MIDI) format and played through bookshelf speakers connected to
basal ganglia,27,28 with the posterior superior temporal gyrus and a computer using commercial software (PowerTracks Pro Audiob).
premotor cortex identified as key structures.28 The ability of auditory The musical piece was chosen for its clearly discernible and
cues to improve different types of gait deficits caused by a range of unchanging rhythm, its usual performance tempo close to that of
different disorders may be attributable to their ability to access an normal walking cadence, and its familiarity to participants.
auditory-premotor circuit that remains functional.28 Furthermore, in Speakers were positioned next to the walkway with the sound
people with disorders such as PD and stroke, the effects of cues on volume individually set to be “easily audible” for each participant.
gait have been shown to persist after their removal, suggesting that
they may induce plasticity in auditory-motor networks.29-31
Procedure
Given the rapidly increasing prevalence of AD, and the contri-
bution of its associated decline in gait speed and stability to
Testing occurred in the university movement laboratory. Mood and
increased cost of care and decreased quality of life, interventions
cognitive function (including orientation/attention, memory, verbal
aimed at improving walking in this population should be explored.
fluency, language, and visuospatial domains) were assessed with
Therefore, the aims of this study were to evaluate whether rhythmic
the Geriatric Depression Scale (GDS)35 and the revised Adden-
auditory cueing alters spatiotemporal gait measures and gait vari-
brooke’s Cognitive Examination (ACE-R), respectively.36 Partici-
ability in people with AD, and whether different cue types produce
pants then walked in their own low-heeled shoes 6 to 8 times along
different effects. Based on previous findings in healthy and clinical
the walkway. This included 2 to 4 familiarization walks and 4
groups, we hypothesized that (1) people with AD would walk faster
walks from which mean walking cadence was calculated (base-
compared with baseline when timing gait to RACs; and (2) gait
line). This value was used as the tempo for both metronome and
variability would decrease during cued walking.
music cues. A further 12 walks were completedd4 in time to each
of the music and metronome cues set at individual, mean self-
selected, comfortable speed cadence (in random order), and
Methods a further 4 uncued walks (retest) to determine any carryover of
effects, with rests between each condition.
Participants Before each cued walk the auditory cue was played, and
participants were instructed to walk on the spot in time to the beat.
Eligible patients were identified from the private caseload of Synchronized stepping was demonstrated together with extra
a geriatrician (also Director of Aged Care at a large teaching and reinforcement of cue timing using handclapping or rhythmic
research hospital). All patients who satisfied the following inclu- counting (“1, 2”). Once each participant’s gait cadence appeared
sion criteria were invited to participate by a researcher (J.E.W.) to be synchronized, the extra timing reinforcement was ceased,
and instruction was given to continue walking in time to the beat
List of abbreviations: of the cue along the walkway. Walks were started and finished 2m
beyond each end of the electronic walkway to ensure that constant
ACE-R revised Addenbrooke’s Cognitive Examination
AD Alzheimer disease speed walking was recorded.
CV coefficient of variation
GDS Geriatric Depression Scale Data analysis
MDC minimum detectable change
PD Parkinson’s disease
Gait measures were chosen to adequately characterize 5 previously
RACs rhythmic auditory cues
identified domains of walking: (1) pacedvelocity and stride length;

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720 J.E. Wittwer et al

(2) rhythmdswing time, stride time, and cadence; (3) base of sup-
Table 1 Participant characteristics (nZ30)
portdstride width; (4) phaseddouble support percentage; and (5)
variabilitydstride length (spatial) and stride time (temporal) vari- Characteristic Mean
SD Range
ability.37 Swing time variability is also included because it is not Age (y) 80
6 66e92
confounded by walking speed.38 Variability was calculated using the Height (m) 1.66
0.11 1.49e1.86
coefficient of variation (CV). Data from individual walks were Weight (kg) 69.8
14.4 45e105
combined for each condition for each participant. Walks were ACE-R (total score, 100)* 59.9
15.8 26e79
removed if the participant had talked or become obviously distracted, ACE-R fluency (total score, 14)y 5.7
3.1 0e13
to reduce the likelihood of secondary tasks affecting gait measures. GDSz 2.2
2.1 0e8
When separate walks are combined for analysis, the assumption Median Range
is that they are similar and can be treated as though they make up (Interquartile
one longer walk. Inspection of mean velocity values for individual Range)
walks under each condition revealed that in some cases, the mean Time since diagnosis (wk) 25 (6e53) 1e667
velocity of one walk for a participant was markedly different from No. of medications 3 (2e4.75) 1e10
others under the same condition. Because gait variability is related
* Higher score indicates better performance; score of 84 is lower
to velocity, “outlier” walks were removed to minimize their limit of normal.36
potential to confound comparison of gait variability under different y
Score of 9 is lower limit of normal.36
cue conditions. A previous conservative estimate of the minimum z
Score 5 suggests depression.35
detectable change (MDC) score for gait velocity in people with AD
is 10cm/s,33 so if a participant had recorded individual walk speeds
An average of 25 (range, 14e38) strides per participant was
under one condition that were different from each other by more
used for analysis for each condition (this exceeds a recently rec-
than this value, the walk most distant in value from the mean speed
ommended minimum of 1241). Table 2 shows means and SDs for
for the group of walks was discarded. This resulted in the removal
baseline and cued spatiotemporal gait measures, and their vari-
of 10% of walks, and the resultant mean difference between the
ability and change scores with each cue. Mean stride length and
fastest and slowest walks for all participants under all conditions
velocity values decreased significantly compared with baseline
was 5.1
3.3cm/s. Total stride numbers per condition (baseline,
values with both music and metronome cues. This was coupled
cued music, cued metronome, and retest) were then matched for
with a significant increase compared with baseline in mean stride
each condition using a previously reported method.39
length variability, also with both cue types. Baseline and retest
Baseline (uncued), cued, and retest (uncued) measures were
measures were not significantly different from each other. While
compared using a 1-way repeated-measures analysis of variance.
group mean values showed slower gait speed and increased spa-
Effect sizes were calculated using partial h2. In order to examine
tial variability with cues, there were individual differences in
the relationship between executive function and the effect of cues
responses, with some participants walking faster to music (nZ9;
on gait speed, the verbal fluency component of the ACE-R was
median increase in velocity, 3.9cm/s) and metronome cues (nZ7;
correlated with change in velocity from baseline with each cue type,
median increase in velocity, 5.2 cm/s), and some participants
using the Pearson product-moment correlation coefficient. Statis-
walking with decreased spatial variability with music (nZ9;
tical analysis was conducted using IBM SPSS softwarec (version
median decrease in CV, 0.7%) and some with metronome cues
19), and statistical significance was set to P.05.
(nZ7; median decrease in CV, 0.6%).
In view of the deterioration of gait measures with cues, addi-
Sample size determination tional post hoc analysis explored the relationship between this
adverse change and a measure of executive function. There was
Sample size calculation indicated that with statistical significance a moderate positive correlation between verbal fluency and change
set at a 2-sided level of .05, a power of 0.9, and the correlation from baseline in gait velocity scores with music (rZ.37, nZ30,
among repeated measures of 0.5, a minimum of 30 participants P<.05), but not with metronome cueing (rZ.25, nZ30, PZ.18).
was required to detect a moderate to large effect (partial h2 values Lower verbal fluency scores were associated with larger decreases
of .06 indicate a moderate effect and >.14, a large effect).40 from baseline in gait speed when cued with music (fig 1).

Results Discussion

Of 44 patients who were eligible to participate, 12 declined. In this group of people with probable AD, not only did RACs fail to
Reasons included no interest in the project (7), unavailability of produce faster, less variable walking as we had hypothesized, both
a familiar accompanying family member/carer (3), distress in types of cue produced temporary deleterious effects on gait speed
unfamiliar settings (1), and too busy (1). Two other patients agreed and spatial variability, at least within the single testing session.
to participate but were subsequently not tested because of sudden Since cue tempo was matched to baseline cadence, the expected
changes in personal circumstances. Characteristics of 30 partici- unchanged temporal gait parameters combined with change in
pants (16 men) who attended are detailed in table 1. Twenty-three spatial measures suggest that participants were not simply ignoring
participants were taking acetylcholine esterase inhibitor medica- the cues, which might be suspected if all measures were unchanged.
tion, and 2 were taking psychotropic medication. Seven partici- Although the magnitude of the unexpected decrease in stride length
pants had fallen once in the previous year, and 5 had fallen 2 or and velocity with cues was smaller than previously published MDC
more times, with information unavailable for 1 participant. GDS values (9cm for stride length and 11cm/s for velocity)33 under the
scores 5 were recorded for 6 participants. All were community circumstances of this study, on average there appeared to be a cost in
dwelling except 1 nursing home resident. responding to the cues.

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Auditory cueing in Alzheimer disease 721

Table 2 Effects of music and metronome cues on gait spatiotemporal measures and variability
Mean Change From
Baseline Effect Size Baseline
Gait Measure (Uncued) Music Metronome Wilks l (P) (Partial h2) Music Metronome
Velocity (cm/s) 110.5
25.4 103.4
27.8* 105.4
26.1* .004 .382 7.1
10.7 5.1
7.8
Stride length (cm) 120.9
20.9 112.5
22.9* 114.8
22.6* .003 .406 8.4
10.9 6.1
9.1
Swing time (s) 0.386
0.042 0.385
0.043 0.385
0.042 .955 .012
Stride time (s) 1.11
0.11 1.11
0.12 1.11
0.11 .325 .118
Stride width (cm) 8.96
3.74 9.14
3.84 8.96
3.78 .239 .142
Double support (% gait cycle) 30.68
5.54 30.80
6.55 30.53
5.82 .203 .154
Cadence (steps/min) 109.2
11.3 109.4
11.8 109.7
11.1 .307 .123
Stride length variability (%) 3.39
1.27 4.30
1.46* 4.45
2.17* .002 .414 0.91
1.75 1.06
1.92
Stride time variability (%) 2.32
0.70 2.28
0.70 2.21
0.68 .912 .019
Swing time variability (%) 5.05
1.77 5.04
1.31 4.78
1.16 .344 .114
NOTE. Values are mean
SD or as otherwise indicated.
* Significant differences from baseline measures.

Our results are in contrast to findings from most other gait speed in the group with PD whose gait speed had declined
studies23,24 of the effects of RACs in clinical (excluding dementia) during an initial single session of exposure to cues.42 Studies43
and healthy groups, which report either improvement in gait have demonstrated intact motor learning ability in people with
parameters or no effect. These contrasts may be partly explained by dementia using a tailored approach, so it is possible that practice
variation in study design and protocols. For example, some studies over a longer period than 1 session may have produced different
report comparisons of uncued and cued trials, and others report effects on gait measures in our group. Cue frequency may also be
retention (ie, uncued trials) after a period of training with cues. an important contributor to the effects of RACs on gait measures.
Studies similar to ours that use the former design are measuring the In our study, cue frequency was matched to baseline cadence, so
instantaneous effects of cues rather than learning, and are typically our design focused on potential spatial effects of cues when
used as an initial gauge of the response to cued gait. Previous stepping tempo was controlled. Other studies have manipulated
studies23,24 of this type have commonly reported either modest cue frequency to test whether participants can alter their usual gait
improvement or no effect of cueing on stride length or gait speed. cadence to match different cue frequencies. Practice of walking
Only 1 other study42 has reported a decline similar to ours in cued with stepping rates cued higher than comfortable speed cadence
gait speed within a single session in a group with PD. may be more likely to result in increased walking speed both in
As well as measurement conditions, variables such as RAC the presence of cues and in retention trials.
dosage may influence the effects of cues on gait. Effects of RACs Cognition, or more specifically cognitive reserve, may be
may be related to exposure so that more practice with cues may another salient mediator of the effect of RACs on walking. Even
lead to enhanced24 or even different effects. A week of home routine walking has been shown to rely on executive function, which
practice with metronome cues produced a subsequent increase in includes complex cognitive processes that are necessary for
successful goal-directed actions and appropriate allocation of
attention.44 The slowed and more variable gait typically seen in
AD1,2 has been associated with deterioration of executive function,45
which is present from the early stages of the disease.46 Baseline gait
speed of people with AD in this study was lower than previously
published values for cognitively healthy people of similar age,2,47
and all gait measures (including variability) for this group were
similar to previously published values for groups with AD of similar
severity.3,33,47 They also performed more poorly on a test of exec-
utive function than cognitively intact older people (see table 1).
The degree of executive function involvement in motor tasks
depends on their complexity and novelty. When motor tasks become
more complex or novel, or both, the progressive decline in executive
function associated with AD means capacity may be more easily
exceeded, which may result in deterioration of motor task perfor-
mance.45 The relationship between cognitive reserve and walking is
typically investigated using dual-task designs, where walking is
combined with a secondary task such as counting backward. Gait
studies using dual-task paradigms in people with AD have shown
decreased gait speed48-50 and increased temporal variability.48,50,51
These changes are similar to the decline in gait speed and stability
Fig 1 Association between executive function and change in gait found with RACs in this study, suggesting that cueing, while not
velocity with rhythmic music cues. designed to be a dual or competing task, may have created a similar

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722 J.E. Wittwer et al

drain on cognitive reserve at least within a single session. Even related to walking ability, future studies could narrow inclusion
though RACs can operate at automatic levels (eg, unconscious foot criteria based on these characteristics or compare cue effects across
tapping to the beat of ambient music), we increased the cognitive different subgroupings, with larger numbers required for adequate
load of the walking task by asking participants to consciously attend statistical power. Future work should also include more extensive
to cues and match their stepping, rather than simply playing the cues neuropsychologic testing to permit greater elucidation of relation-
without any instructions when participants walked. This suggested ships between gait changes with cues and executive function. The
adverse effect of cognitive impairment on the response to RACs is participation of volunteers may limit generalization of findings to
supported by results of a previous study of a cognitively healthy older more confident, physically able people with AD. GDS scores
group, who walked faster with music cues using the same cueing suggest depression in some participants, which increases the
protocol, and their low baseline gait variability did not increase. diagnostic challenge of AD; however, the diagnosis was made by an
The 1 previous study26 of people with dementia found no experienced geriatrician according to a wide range of recognized
significant change in spatiotemporal gait measures with either criteria. Only the instantaneous and short-term retention of cue
music or metronome cues at a comfortable speed cadence after effects was tested and only with cue frequency matched to baseline
a period of training. There are, however, a number of differences cadence. Longer-term training programs using cues have been
from our study that may account for the different results. In successful in other clinical groups, some with cognitive impair-
addition to greater disease severity, participants in the previous ment.31 Studies have also demonstrated intact motor learning
study26 received physical assistance to walk, and the authors ability in people with dementia by using implicit methods where
suggested that participants may actually have matched their gait to learning occurs from repeated exposure to the task without
the rhythmic sway of the aides. A single-session study52 of people conscious effort, as opposed to explicit or declarative methods.43
with less severe cognitive decline resulting from Huntington Before use of RACs is deemed ineffective or even counterproduc-
disease found improved gait measures in the presence of cues. In tive for people with dementia, further work should establish
a group with PD and cognitive impairment, metronome cues whether more practice with a tailored learning approach and
improved gait speed and stride length when combined with a greater variety of cue frequencies produces different results.
a spatial cue,53 suggesting that timing cues alone were not enough
to improve gait, unlike in cognitively intact PD groups. While Conclusions
these disorders have cognitive decline as a common factor, their
differing underlying pathologic processes may result in different
Rhythmic auditory cueing at a comfortable speed tempo produced
effects of RACs on gait. If the effects of AD on gait are not just
deleterious effects on gait in a single session in this group of
attributable to a decline in executive function but also because of
people with AD. The deterioration in spatial gait parameters may
damage to specific motor and auditory pathways from the disease
be attributable to the impaired executive function associated with
process, this may explain differences in response to cueing in
AD. Further research should explore relationships between
people with cognitive impairment from other disorders.
cognition and cue effects, and also whether instantaneous effects
Even though the average group response to RACs was decreased
of cues are altered with greater amounts of practice or with
stride length and speed, and increased variability, there were indi-
learning methods tailored to people with cognitive impairment.
vidual differences, with some participants walking with increased
speed similar to cognitively healthy people in a previous study.39
We examined the relationship between executive function and the Suppliers
effect on gait of cues and found that impaired executive function
was moderately related to gait deterioration with music but not a. CIR Systems Inc, 69 Garlor Dr, Havertown, PA 19083.
metronome cues. While music cues have been found to produce b. PG Music Inc, 29 Cadillac Ave, Victoria BC V8Z 1T3, Canada.
faster walking in some instances,39,54 it has also been suggested that c. IBM Corp, 294 Rte 100, Somers, NY 10589-3202.
cognitive impairment may impair the ability to extract beat infor-
mation from the more complex aural texture of the music.52 Keywords
It is interesting that despite the decreased speed and increased
spatial variability, timing variability did not increase. It might be Alzheimer disease; Auditory stimulation; Gait; Rehabilitation
expected that if gait was deteriorating in the cued conditions
because of an overload of executive function capacity, timing
variability would also increase. An alternative explanation may be Corresponding author
that participants were able to respond to the temporal cues but
chose a conservative spatial response of decreasing stride length Joanne E. Wittwer, BAppSc(Phty), Musculoskeletal Research
(and thus speed) to preserve stability. The increased spatial vari- Centre, La Trobe University, Victoria 3086, Australia. E-mail
ability, while statistically significant, was relatively small in address: [email protected].
magnitude and may simply be a byproduct of the slower speed.3
Acknowledgment
Study limitations
We thank Associate Professor Michael Woodward, MB, BS,
The findings of this study should be interpreted in light of FRACP for providing assistance with patient recruitment.
its limitations. It was designed as an initial exploration in people
with mild to moderate AD of the effect of RACs on gait, so References
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