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A Simple Procedure Using Auditory Stimuli to Improve Movement in Parkinson’s
Disease: A Pilot Study
Fernandez del Olmo, M., Cudeiro, J.
Dpto. Medicina-NEUROcom, Facultad de Ciencias de la Salud, Campus de Oza, La Coruña, Spain
Corresponding Author
Javier Cudeiro, Dpto. Medicina-NEUROcom, Facultad de Ciencias de la Salud, Campus de Oza, 15006 La
Coruña, Spain,
jcud@udc.es
Key Words
Parkinson’s disease, motor control, motor performance, auditory stimulation
Abstract
It has been suggested that sequential movements in Parkinsonian patients might be improved by the effects
of external rhythmic cues, either visual or acoustic, acting as a sort of timekeeper. In line with that idea, we have
developed a portable system which allows the patient suffering from bradykinesia and rigidity to initiate appropriate
auditory stimulation when he/she is not able to move. Here we present data from six Parkinson’s Disease (PD)
patients studied with surface electromyography, while walking along an 8.5m walkway. All showed remarkable
improvement in the EMG parameters studied while using the device. The results are consistent with prior reports on
rhythmic auditory facilitation in Parkinson’s disease gait, and suggest that this represents a novel and inexpensive
tool to help people afflicted by PD in daily motor performance.
Introduction
Patients with Parkinson's disease (PD) have difficulty with self-initiating movements, such as walking, that
result in a slow, stumbling gait and even periods of complete akinesia. Parkinsonian hypokinesia renders difficult
the automatic execution of elementary movements and the specific performance of motor tasks; the harmony of
repetitive movements is disjointed in rhythm, speed and amplitude. However, motor performance can be improved
when external stimuli are provided, such as by lines on the floor
(Martin, 1967) or by acoustic cues (Georgiou et al,
1993; Thaut et al, 1996; McIntosh et al, 1997). The effectiveness of utilising sensory systems - for example vision -
to facilitate locomotor activity was first described by Martin
(1967) over 35 years ago. More recently, Richards et al
(1992) compared the effects of visual and auditory cues on various gait parameters in patients with Parkinson’s
disease on and off levodopa. In that study patients walked faster with both cues. These data strongly suggests that
the Parkinsonian brain may be capable of some reorganization (or re-routing) in order to initiate or facilitate
performance of volitional movements. In PD the widespread connections between polymodal cortical areas (motor,
visual, vestibular and auditory) and the basal ganglia seem to be functionally preserved (Alexander et al, 1986;
Playford et al, 1992; Bremmer et al, 2001), and the basal ganglia and cerebellum are good candidates for internal
timekeeping operations
(Rao et al, 2001). For this study, we reasoned that the availability of external cues (acting as
an external timekeeper), initiated by the PD patient, could be of benefit in overcoming problems of movement.
Methods
Six patients (between 58 and 65 years of age, 3 males, 3 females) with a clinical diagnosis of idiopathic
Parkinson’s disease were studied. Five healthy, age-matched, normal subjects were also studied. Informed consent
for participation was obtained from all individuals and protocol procedures were reviewed and approved by the
University of Coruña ethical board and were in accordance with The Declaration of Helsinki. All patients had a
normal neurological examination and none had a history of neurological, cardiovascular or psychiatric disturbance
Neurology and Clinical Neurophysiology 2003:2 (January 25, 2003)
other than Parkinson’s disease. All patients were on medication and rigidity and bradykinesia were major features of
the symptomatology. A Unified Parkinson’s Disease Rating Scale (UPRDS) motor score was recorded and the
average patient UPRDS was 50 (range 30-70). The average Hoehn and Yahr score was 3.2 (range 3-4).
Patients were tested in the morning always during the ON period, 60 minutes after medication. They walked
along an 8.5 m walkway, turned 180° at the walkway end and returning to starting position. Electromyographic
activity (EMG) of two leg muscles (Tibialis Anterior and Gastrocnemius) was recorded by mean of surface
electrodes following standard procedures
(Cram and Kasman, 1998). Quantification of the surface
electromyographic recording was done using the integral average (µV/sec) of the EMG raw signal
(Cram and
Kasman, 1998). Patients did not expect to obtain any direct and immediate benefit from this experiment, and it was
considered as a system to evaluate gait. We studied the following temporal parameters: interval between burst of
EMG activity, slope of each burst and its duration. In control trials, no external auditory cues were available. In test
trials, the patients were asked to proceed in the presence of an external rhythm (click tone) at fixed frequency of 100
click/min, a standard value for normal elderly walking cadence (Zatsiorky et al, 1994). The tone was delivered by a
device constructed in-house, consisting of a battery operated metronome and small headphones, that was controlled
by the patient. Patients were permitted a 10 minute rest between trial types. We compared performance during the
task with and without stimulation using the Mann-Whitney U and Wilcoxon tests for a p≤0.05.
Results
All patients showed significant improvement in the recorded EMG parameters while the device was in use.
Figure 1 illustrates the changes obtained in the surface electromyogram in one patient. The regularity of muscle
activation when the device is ON
shows a very clear change. The
sequential patterns that characterize
the agonist-antagonist activity are
clearly disrupted in the control
conditions and in particular,
activation of the gastrocnemius is
very poor. With acoustic
stimulation this activation clearly
improved. This is a very important
finding, because whatever
mechanisms are involved, this
suggests that our manipulation
(sensory stimulation) is affecting
the final output of the motor system
at the level of the motor unit,
which, in fact, has been
demonstrated to be affected in
patients with idiopathic PD
(Caviness et al, 2000).
2
The following changes in
measured EMG parameters were
found (expressed as % change for
all patients; significant for p≤0.05): the interval between EMG responses decreased with stimulation (20% TA; 38%
Figure 1 Representative segment of EMG activity recorded in one patient in
two different conditions: device providing acustic stimulation ON and
OFF. Note the different pattern of EMG activation when the stimulator
is ON specially for the gastrocnemius muscle.
Neurology and Clinical Neurophysiology 2003:2 (January 25, 2003)
G); the slope of EMG activation increased (32% TA, and 29% G); and the duration of each burst of EMG activation
decreased (23% TA and 20% G). Overall, it is very clear that the precise timing of activation improved because the
variability of each parameter significantly decreased and this is shown in Table 1. Here we report the changes
observed for each subject expressed as the mean, the standard deviation and the coefficient of variability (a
measurement for temporal stability
= standard deviation/mean*100)
(Hausdorff et al, 1998).
Interval between EMG responses (sec)
Mean/SD/Coefficient of variability
Slope of EMG:
Mean/SD/Coefficient of variability
Duration of EMG activation (sec):
Mean/SD/Coefficient of variability
Pt
#
Device OFF
Device ON
Device OFF
Device ON
Device OFF
Device ON
1 (TA):1.48/0.12/8.1
(G): 1.45/0.08/5.5
1.19/0.06/5.04
1.20/0.06/5
(TA):0.56/0.16/28.5
(G): 0.08/0.04/50
0.85/0.19/22
0.11/0.04/36
(TA):1.19/0.14/11.7
(G): 1.45/0.08/5.5
0.99/0.084/8
1.14/0.05/4.3
2 (TA):1.53/0.11/7.2
(G): 1.54/0.18/11.7
1.25/0.06/4.8
1.28/0.09/7
(TA):0.78/0.21/27
(G): 0.13/0.03/23
0.87/0.13/15
0.23/0.04/17
(TA):0.62/0.22/35.5
(G): 1.36/0.13/9
0.54/0.16/29.6
1.19/0.05/4.2
3 (TA):1.65/0.14//8.48
(G): 1.55/0.14/9
1.17/0.08/6.8
1.23/0.09/7.3
(TA):0.41/0.26/63
(G): 0.2/0.05/24
0.53/0.3/63
0.25/0.04/16
(TA):0.81/0.4/52
(G): 1.32/0.12/9.1
0.57/0.13/23
1.08/0.9/8.3
4 (TA):0.86/0.04/4.7
(G): 0.89/0.08/9
0.78/0.03/3.8
0.79/0.03/3.4
(TA):0.3/0.07/23
(G): 0.18/0.08/44
0.4/0.06/15
0.22/0.05/23
(TA):0.39/0.11/28.2
(G): 0.69/0.11/16
0.29/0.05/17
0.49/0.07/14
5 (TA):1.2/0.06/5
(G): 1.22/0.08/6.6
1.1/0.045/4
1.17/0.06/5.1
(TA):0.2/0.08/38
(G): 0.28/0.07/25
0.3/0.07/23
0.34/0.07/20
(TA):0.4/0.09/10.8
(G): 0.74/0.08/11
0.33/0.03/8
0.68/0.05/7.3
6 (TA):1.4/0.08/6.4
(G): 4/0.07/5
1.1/0.05/4.5
1.0/0.03/3
(TA):0.6/0.19/31
(G): 0.15/0.05/33
0.78/0.16/20
0.20/0.04/20
(TA):0.65/0.21/32.3
G): 1.00/0.13/13
0.55/0.12/18
0.65/0.05/7.6
TA = Tibialis anterior G = Gastrocnemius
Table 1 Changes observed for each patient in two different conditions: With and without stimulation
3
We investigated the effects of
using the device on the age-
matched normal control subjects.
After repeating the same protocols
we did not observe any significant
difference between the data
obtained with and without
stimulation. Figure 2 shows an
example from control subject
number one.
We have used the coefficient of
variability as a well known
indicator for temporal stability
(Hausdorff et al, 1998). Figure 3
Figure 2 Representative segment of EMG activity recorded in one healthy
control in two different conditions: device providing acoustic
stimulation ON and OFF. There is no difference between both
conditions.
Neurology and Clinical Neurophysiology 2003:2 (January 25, 2003)
illustrates how this indicator changes for patients with and without stimulation, and also in comparison to control
subjects. With acoustic stimulation,
the coefficient of variability
improved for each of the
parameters studied and reached
values very close to those recorded
for control subjects (for which
stimulation and control situations
were not statistically different).
4
Discussion
These data were in agreement
with findings by others (Thaut et al,
1996; McIntosh et al, 1997) who
used an auditory stimulation
training program of 3 weeks
duration, based upon rhythmic
stimuli embedded in a musical
structure (a technique called RAS).
These authors found that gait
velocity, cadence and stride length
improve in the vast majority of
patients. However, it is important
to note that in our study the patients
had never practiced protocol
described here prior to testing, and
therefore undertook no training
whatsoever. Furthermore, it is important to bear in mind that the patients did not expect any benefit from this
experiment, just a way to study gait. Also it is interesting that the external stimulation only improves the EMG
patterns and the internal timing of patients because experiments done in control healthy elderly, did not show any
difference. Similar results on electrical muscle activity were previously reported by Thaut and co-workers
(Miller et
al, 1996). They found a reduction in EMG shape variability in patients with Parkinson’s disease during RAS cued
walking, indicating, as we suggest, more consistent motor unit recruitment.
Figure 3. This figure shows the changes observed in the coefficient of
variabilty of the whole population of patients when the device is ON
(versus device OFF) and the comparison with the values obtained for
the control subjects. For the parkinsonian patients all the studied
parameters when the device was ON move toward normal values.
There is some evidence in the literature that rhythmic sound patterns can increase the excitabilty of spinal motor
neurons via the reticulospinal pathway reducing the time required for the muscle to respond to a given motor
command. It has been shown, for instance, that auditory signals reduced reaction time in a voluntary motor task
(Paltsev and Elner, 1967). Also auditory facilitation of the H-reflex has been shown (Rossignol and Jones, 1976)
and movement related gastrocnemius activity occurred during the period when the H-reflex was maximal, suggesting
that descending motor commands became entrained to the auditory pacing signal so as to make the best use of a
potential audiospinal facilitation effect.
Studies in monkeys have shown that movement related phasic discharge of pallidal neurons may serve as an
internal cue to the supplementary motor area signalling the end of one movement and allowing the onset of the next
(Brotchie et al, 1991). Several authors have suggested that external cues (e.g. sound) provide a trigger in Parkinson’s
disease to switch between the different components of a movement sequence, avoiding in this way the defective
internal pallidocortical projections
(Morris et al, 1994; Cunnington et al, 1995).
Neurology and Clinical Neurophysiology 2003:2 (January 25, 2003)
5
Based on clinical and experimental data, it has been suggested that bradykinesia or slow movement initiation in
Parkinson's disease (in general self-initiated movements) may reflect impaired input from cortical areas, more
specifically the medial premotor system centred around the putamen-thalamus-supplementary motor area loop
(Goldberg, 1985; Dick et al, 1989; Jahanshahi et al, 1995). However, the lateral premotor system involved in
externally triggered movements seems not to be impaired in Parkinson’s disease
(Jahanshahi et al, 1995). This
cortical zone, centered in the lateral premotor cortex receives its main input from the parietal cortex and cerebellum
(Goldberg, 1985
)
. We suggest that it is possible that the external stimulation works as a trigger, operating through the
intact lateral premotor system, which is able to overcome (partially at least) the motor program deficits due to
supplementary motor area malfunctioning. In fact, it is interesting to note that primary motor cortex itself functions
normally in Parkinson’s disease
(Dick et al, 1984; Jenkins et al, 1992; Playford et al, 1992). Our results highlight the
importance of external rhythmic stimulation as a putative tool for the management of patients with Parkinson’s
disease. However, the precise mechanisms underlying the positive effects shown here remain to be explored.
Conclusions
In addition to the typical neurochemical deficits, abnormal motor performance in Parkinson’s Disease results
from impaired motor programming, with functional alterations of the supplementary motor area and pre-motor
cortex resulting in a failure of the internal rhythm formation process. Our most important finding is that individuals
with Parkinson’s disease improved the temporal motor parameters studied during walking when receiving external
auditory cues. These results are consistent with prior reports of rhythmic auditory facilitation in Parkinson’s disease
gait, and suggest that auditory paced stimulation is likely to be a novel and inexpensive tool for improving important
gait parameters and for gait rehabilitation.
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