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A simple procedure using auditory stimuli to improve movement in Parkinson's disease: A pilot study


Abstract and Figures

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.
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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,
Key Words
Parkinson’s disease, motor control, motor performance, auditory stimulation
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.
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.
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 p0.05.
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).
The following changes in
measured EMG parameters were
found (expressed as % change for
all patients; significant for p0.05): 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
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
(G): 0.08/0.04/50
(G): 1.45/0.08/5.5
2 (TA):1.53/0.11/7.2
(G): 1.54/0.18/11.7
(G): 0.13/0.03/23
(G): 1.36/0.13/9
3 (TA):1.65/0.14//8.48
(G): 1.55/0.14/9
(G): 0.2/0.05/24
(G): 1.32/0.12/9.1
4 (TA):0.86/0.04/4.7
(G): 0.89/0.08/9
(G): 0.18/0.08/44
(G): 0.69/0.11/16
5 (TA):1.2/0.06/5
(G): 1.22/0.08/6.6
(G): 0.28/0.07/25
(G): 0.74/0.08/11
6 (TA):1.4/0.08/6.4
(G): 4/0.07/5
(G): 0.15/0.05/33
G): 1.00/0.13/13
TA = Tibialis anterior G = Gastrocnemius
Table 1 Changes observed for each patient in two different conditions: With and without stimulation
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
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).
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)
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.
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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Neurology and Clinical Neurophysiology 2003:2 (January 25, 2003)
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... Researcher will use these devices (decibel meter, and metronome) to keep IV in control, measurement of volume, and music tempo will be collected and reported as part of the results of the experiment. Similarly, the instrument used to measure the DV is used extensively as supported in the literature [11,21,22]. It does not seem necessary to validate the instrument statistically. ...
... The degree of osseointegration and the initial bone quality evaluated by many methods, including histology and histomorphometry, [58] removal torque analysis [59], pull-and push-through tests, and radiographic examination, However, these methods are not accurate for long-term clinical assessment due to problems of invasiveness. So a noninvasive device called the Periotest was introduced and used to evaluate the implant stability [60]. The range in Periotest values (PTV) evaluated by clinically osseointegrated implants depends on the surrounding tissues damping characteristics, fibrous tissues in failed implants and bone in successful implants. ...
... In addition, the regularity of RAS leads to the recruitment of more motor neurons by modifying their activity, resulting in more regular and synchronised patterns of neural activation [16]. The complete specification of the dynamics of the movement over the entire movement cycle has been demonstrated in optimization models using rhythmic cues as predictive time constraints [17]. ...
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Background Gait disorders which caused by stroke are one of the most common causes of functional disabilities in hemiparetic stroke patients that leads to significant impact on quality of life and financial cost. In this study, we focused on how certain gait metrics in stroke patients were affected by rhythmic auditory stimulation and treadmill training. Results In this randomized controlled experiment, which involved 30 male stroke patients, there was a significant increase in post treatment walking speed, step cycle, step length, percent of time on each foot and ambulation index in both groups. The post treatment improvement in gait parameters was significantly higher in the study group compared to the controls. Conclusions Combination of rhythmic auditory stimulation with treadmill training enhances the gait performance.
... Clinician-patient interaction via telehealth provides an additional advantage on PD symptoms (e.g., bradykinesia, freezing phenomenon and tremor) [7,8]. For instance, the mobile phone providing auditory and tactile external stimuli can effectively reduce the symptoms of "bradykinesia" and "freezing of walking phenomenon" [9,10]. In addition, the mobile phone's inertial sensor provides spatiotemporal data for practical movement analysis [11,12]. ...
Objective: Mobile app-based telerehabilitation is practical and cost-effective in neurological rehabilitation. The present systematic review aimed to investigate the effectiveness of mobile application-based rehabilitation in patients with Parkinson’s Disease. Methods: Literature was searched via databases of "Web of Science (WoS), PubMed, Cochrane, Scopus and ScienceDirect”. Physiotherapy Evidence Database (PEDro) and Revised Cochrane risk-of-bias tool for randomized trials (RoB2) were used to evaluate the quality analysis and risk of bias evaluation. Both narrative and quantitative synthesis were carried out. Results: A total of 2175 articles were screened (WoS=41, PubMed=42, Cochrane=84, Scopus=114, ScienceDirect=1894). A total of 5 studies were included in the systematic review following the screening and eligibility procedures. Two studies were enrolled in meta-analysis regarding the data homogeneity. PEDro scores of the trials ranged from 4 to 7 (median:6), indicating good quality. All studies were in the “some concerns” category. The mobile application-based intervention yielded better results on quality of life and patient adherence in two studies. Application-based rehabilitation was not superior to standard treatment on MiniBESTest (ES:0.15, 95% CI: -0.33-0.26) and UPDRS III (ES:0.86, 95% CI: -0.94-2.46) scores. Conclusion: Mobile application-based rehabilitation is not superior to standard treatments in balance and disease severity. However, mobile technologies could be preferred to increase patient adherence and quality of life. The limited study and the low number of cases in the review may reduce the level of evidence for the results.
... The basal ganglia receive sensory information and improvements in movement have occurred with auditory facilitation as the external cues have been reported to improve the impaired internal motor response. [10,11] In an attempt to bypass the dysfunction, the input system receives auditory information through the striatum to ultimately project to the premotor cortex. [12][13][14][15][16] Auditory information has been shown to impact sequencing, timing, and behavioral response selection of movement. ...
Parkinson disease (PD) leads to neurological impairments yet the auditory system remains intact. Rhythmic Auditory Stimulation (RAS) and Patterned Sensory Enhancement (PSE) have been shown to impact gait in PD. Music therapists (MT) can individualize auditory protocols but for a physical therapist (PT) to incorporate PSE into treatment, a new tool is needed. The Synchronized Optimization Auditory Rehabilitation (SOAR) tool is a new software created to simulate PSE techniques and allow for customization depending on the individual’s reaction to the cue. The purposes were to evaluate the validity of the SOAR tool with RAS and the interrater reliability between disciplines’ application of the SOAR tool. Day one - MT measured gait parameters during no cue, RAS, and SOAR tool. Day two - PT measured gait parameters while using the SOAR tool. A moderate to high correlation between RAS and the SOAR tool on gait was found. The interrater reliability between the MT and PT was high. These finding suggest the SOAR tool is an additional auditory cue delivery tool that PTs could use in the treatment of individuals with PD when auditory cues are deemed appropriate and a MT is not an available member of the interdisciplinary rehabilitation team.
... By reviewing the literature, there was no study which investigates the effect of the auditory cue on the EMG of the elderly while pedaling and the results of the current study are reporting for the first time. In the previous study by Fernández-del-Olmo (2003), (37) the burst of EMG in tibialis anterior and gastrocnemius muscles, slope of each burst and the its duration were studied in Parkinson disease during gait with and without external rhythm (click tone). In agreement with our results, they found that with stimulation, the slope of the EMG activation increased. ...
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Rhythmic auditory cue is one of the accepted techniques for the rehabilitation and improvement of motor control in the healthy elderly and with movement disorders. The aim of this study was to determine the effects of the auditory cue on the EMG activity of the elderly subjects during cycling. 10 healthy elderly males participated in this study. The EMG activity of rectus femoris (RF), biceps femoris (BF), and tibialis anterior (TA) muscles were recorded using an EMG-USB2+ multichannel system (Bioelettronica Italy) (sampling frequency of 1000 Hz) and bipolar surface electrodes. Using OT BioLab software the signals were processed and the RMS of signals was obtained. For the tests, the subjects were asked to pedal with the preferred speed with and without a rhythmic auditory cue. Each condition was repeated three times, and each test lasts for one minute. There were three 3-minutes rest between repetitions. Data were analyzed using SPSS software (version 24) and repeated measure analysis of variance and paired sample t-tests with a significance level of 0.05. The results showed that the normalized muscle activity in pedaling with an auditory cue was significantly higher than that of pedaling without an auditory cue (P=0.05). During pedaling with an auditory cue, the normalized EMG activity of right RF and left TA muscles were approximately 1.25 (p=0.03) and 1.22 (p=0.04) significantly greater than the un-cued condition, respectively. In conclusion, rhythmic auditory cue increased the EMG activity of the lower extremity muscles among the elderly. So, in designing an appropriate training and rehabilitation program for the lower extremity muscles in the elderly, the use of auditory cue while pedaling as an easy and low-cost training method can be recommended.
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BACKGROUND AND OBJECTIVES: Stroke is among the commonest causes of adult-onset disability. Six months after the stroke, only 50% of the patients achieve functional independence in ADLs and walk short distances. In research studies over the past ten years, exercise and rehabilitation strategies to improve walking ability have become more intensive and progressive, like rhythmic auditory stimulation, task-oriented circuit training, dual-task exercises, etc. Gains in the walking ability attained by the interventions as mentioned above within three months of stroke. Some evidence-based studies proved that RAS and TOCT effectively improve gait parameters like Stride length, Cadence, and Velocity in subjects with hemiparetic stroke. However, there is no comparative study of these two protocols. Hence, the purpose of this study is to compare the effects of RAS and TOCT on improving walking ability in subjects with hemiparetic stroke. METHODS: Quasi experimental design. A total of 68 subjects, 64 of them met selection criteria for the study, and 4 of them dropped from the study. Therefore, 60 subjects divided into two groups, 30 members in group A (RAS), 30 members in group B (TOCT). Both groups performed intervention for 1 hour a day, five days a week for six weeks. The outcomes of the study were Stride length, Cadence, and Velocity. They were measured using the ink foot method with 10 meters walk test. RESULTS: Paired T-test used to access the statistical significance between pre and post-test scores within the group, Independent T-test was used to access the statistical significance between pre and post-test scores between the groups, Statistical analysis of the data revealed that the RAS group has more difference when compared to TOCT group. CONCLUSION: In this study, six weeks of treatment duration for RAS and TOCT showed significant effective changes in Stride length, Cadence, and Velocity. However, RAS has shown more effective when compared to TOCT in improving walking ability in subjects with hemiparetic stroke.
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Purpose: This study was conducted to investigate whether the effect of rhythmic auditory stimulation, which consists of different rhythm patterns, on the walking ability of children with Cerebral Palsy, creates a difference on walking ability in terms of biomechanics and what the effect degrees are on this difference. Materials and Method: The study is an experimental research design conducted on 12 male spastic quadriplegia children with a mean age of 13 ± 3.5. Applications were made in the motion analysis laboratory to test the walking ability. The subjects were asked to walk freely and according to rhythm respectively. Images were recorded and analyzed with 10 cameras (330 fps) using the three-dimensional motion analysis system Vicon Motion Capture and Nexus2 as pre and post test. Rhythmic auditory stimulus walking test was performed in Bounce Metronom software program with 2, 4 and 6 beat (moderato) rhythms. SPSS 22 software program was used for statistical analysis, paired sample t-Test for comparison of differences between tests, and ANOVA test for repeated measures. Results were evaluated at the (p <0.05) significance level. Findings: In our study, according to the paired sample t-test results, significant differences were found in terms of adaptation and application to the rhythms of children with Cerebral Palsy in walking skill (p<0.05). The subjects showed improvements in gait parameters with 4 and 6 beat rhythms. It was observed that 2-beat rhythms were less effective on the walking ability of the subjects than the 4 and 6-beat rhythms. With 6-beat rhythms; Significant improvement was detected in limp index, single and double support phases. With 4-beat rhythms; Significant improvements were observed in the parameters of double step duration, double support, single support and limp index. In addition, according to the repeated measurements ANOVA test results, it was seen that 4 and 6-beat rhythms positively affect the gait parameters of the subjects. Results: It was determined that rhythmic auditory stimulation had a positive biomechanical effect on the gait parameters of children with Cerebral Palsy, compared to 2-beat rhythm, 4 and 6-beat rhythmic auditory stimulation had a positive effect on the spatial and temporal parameters of CP children's walking ability.
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Gait asymmetry in lower-limb amputees can lead to several secondary conditions that can decrease general health and quality of life. Including augmented sensory feedback in rehabilitation programs can effectively mitigate spatiotemporal gait irregularities. Such benefits can be obtained with non-invasive haptic systems representing an advantageous choice for usability in overground training and every-day life. In this study, we tested a wearable tactile feedback device delivering short-lasting (100 ms) vibrations around the waist syncronized to gait events, to improve the temporal gait symmetry of lower-limb amputees. Three above-knee amputees participated in the study. The device provided bilateral stimulations during a training program that involved ground-level gait training. After three training sessions, participants showed higher temporal symmetry when walking with the haptic feedback in comparison to their natural walking (resulting symmetry index increases of +2.8% for Subject IDA, +12.7% for Subject IDB and +2.9% for Subject IDC). One subject retained improved symmetry (Subject IDB, +14.9%) even when walking without the device. Gait analyses revealed that higher temporal symmetry may lead to concurrent compensation strategies in the trunk and pelvis. Overall, the results of this pilot study confirm the potential utility of sensory feedback devices to positively influence gait parameters when used in supervised settings. Future studies shall clarify more precisely the training modalities and the targets of rehabilitation programs with such devices.
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Though its existence has been known for well over 30 years, only recently has the supplementary motor area (SMA) and its role in the cortical organization of movement come to be examined in detail by neuroscientists. Evidence from a wide variety of investigational perspectives is reviewed in an attempt to synthesize a conceptual framework for understanding SMA function. It is suggested that the SMA has an important role to play in the intentional process whereby internal context influences the elaboration of action. It may be viewed as phylogenetically older motor cortex, derived from anterior cingulate periarchicortical limbic cortex, which, as a key part of a medial premotor system, is crucial in the “programming” and fluent execution of extended action sequences which are “projectional” in that they rely on model-based prediction. This medial system can be distinguished from a lateral premotor system postulated to have evolved over phylogeny from a different neural source. An anatomico-physiologic model of the medial premotor system is proposed which embodies the principles of cyclicity and reentrance in the process of selecting those neural components to become active in conjunction with the performance of a particular action. The postulated dynamic action of this model in the microgenesis of a discrete action is outlined. It is concluded that although there is a great deal to be learned about the SMA, a convergence of current evidence can be identified. Such evidence suggests that the SMA plays an important role in the development of the intention-to-act and the specification and elaboration of action through its mediation between medial limbic cortex and primary motor cortex.
We investigated the functional anatomy of self-initiated and externally triggered movements. Six patients with Parkinson's disease off medication and six age-matched normals were assessed All subjects had regional cerebral blood pow (rCBF) measurement with PET and recording of movement-related cortical potentials (MRPs) from frontal (F), fronto-central (FC), central (C) and parietal (P) sites to obtain measures of the Bereitschaftspotential (BP). The tasks were (i) self-initiated extension of the right index finger on average once every 3 s, (ii) externally triggered finger extension with the rate yoked to the self-initiated task, and (iii) rest condition with tones presented at a rate yoked with the self-initiated task. For the self-initiated movements, the amplitude of the early and peak BP were lower in Parkinson's disease relative to normals. For the externally triggered movements, the patients and the normals did not differ on any of the measures of cortical negativity prior to movement For both groups, the late and peak BP components, but not the early component, had a lower amplitude in the externally triggered than the self-initiated movements. In normals, the left primary sensorimotor cortex, the supplementary motor area bilaterally anterior cingulate, the lateral premotor cortex bilaterally the insular cortex bilaterally, the left thalamus and the left putamen, parietal area 40 bilaterally and the right dorsolateral prefrontal cortex (DLPFC) were significantly activated during the self-initiated movements relative to rest. For the normals, greater activation of the right DLPFC during the self-initiated movements was the only area that significantly differentiated them from the externally triggered movements. When Parkinson's disease patients and normals were compared for the self-initiated movements relative to rest, normals showed greater activation of the supplementary motor area and anterior cingulate, left putamen, left insular cortex, right DLPFC and right parietal area 40. When the groups were compared for the externally triggered movements relative to rest the global pattern of blood pow and rCBF change in the two groups did not differ, confirming the absence of group differences in BPs for the externally triggered movements. During the self-initiated movements, the lower amplitude of the early BP in patients with Parkinson's disease as well as the underactivation of the supplementary motor area relative to normals support the premises that (i) the supplementary motor area contributes to the early BT: and (ii) the deficit in self-initiated movements in Parkinson's disease is due to supplementary motor area underactivation. The DLPFC is activated in situations requiring non-routine decision making as in the self-initiated movements.
The basal ganglia are thought to play an important role in regulating motor programs involved in gait and in the fluidity and sequencing of movement. We postulated that the ability to maintain a steady gait, with low stride-to-stride variability of gait cycle timing and its subphases, would be diminished with both Parkinson's disease (PD) and Huntington's disease (HD). To test this hypothesis, we obtained quantitative measures of stride-to-stride variability of gait cycle timing in subjects with PD (n = 15), HD (n = 20), and disease-free controls (n = 16). All measures of gait variability were significantly increased in PD and HD. In subjects with PD and HD, gait variability measures were two and three times that observed in control subjects, respectively. The degree of gait variability correlated with disease severity. In contrast, gait speed was significantly lower in PD, but not in HD, and average gait cycle duration and the time spent in many subphases of the gait cycle were similar in control subjects, HD subjects, and PD subjects. These findings are consistent with a differential control of gait variability, speed, and average gait cycle timing that may have implications for understanding the role of the basal ganglia in locomotor control and for quantitatively assessing gait in clinical settings.
To identify the fundaamentall deficit in gait hypokinesia in Parkinson's disease (PD) we conducted a series of experiments that compared PD subjects with age- and height- matched controls in their capacity to regualte either stride length, cadence (steps per minute) or both parameters to three conditions. In the first condition the spatial and temporal parameters of gait were documented for slow, normal and fast walking. The seconde condition compared parkinsonian gait with the walking pattern of elderly controls whilst controlling for two movement speeds: fast (control preferred) speed and slow (PD preferred) speed. In the third condition we examined the ability of PD subjects to regulate one parameter (e.g. stride length) when the other two parameters (e.g. velocity and cadence) were held at control values. A total of 34 PD subjects and 34 matched controls were tested using a footswitch stride analysis system that measured the spatial and temporal parameters of gait for a series of 10 m walking trials. Parkinsonian subjects exhibited marked gait hypokinesia in each of the experiments. Although they retained the capacity to vary their gait velocity in a similar manner to controls, their range of response was reduced. Within the lower velocity range, PD subjects could vary their speed of walking by adjusting cadence and, to a lesser extent, stride length. However, when the speed of walking was controllled, the stride length was found to be shorter and the cadence higher in PD subjects than in controls. Stride length could not be upgraded by internal control mechanisms in response to a fixed cadence set for age and height-matched velocity. In contrast, cadence was readily modulated by external cues and by internal control mechanisms when stride length was fixed to the values obtained for age-and height-matched controls. It was concluded that regualation of stride length is the fundamental problem in gait hypokinesia and the relative increase in cadence exhibited by PD subjects is a compensatory mechanism for the difficulty in regulating stride length. These findings are discussed in the context of the hypothesized role of the basal ganglia in generating internal cues for the maintenance of the gait sequence and in relation to the structuring of movement rehabilitation strategies.
An investigation was made of the time course of audio-spinal influences in man using the H-reflex technique and non-startling sounds. It was found that in all subjects the sound potentiated the H-reflex at a central latency of 80 msec, the peak facilitation (185%) being attained at 110--130 msec. The mean duration of this facilitation was 200 msec ranging from 120 to 460 msec. No inhibition was seen to follow the excitatory period. An habituation study showed a significant drop in peak facilitation after exposure to ten conditioning stimuli but a constant increase of the H-reflex above control level even after 60 presentations. The time course of this audiospinal facilitation was superposed over the EMG events during hopping to a simplified musical stimulus. In this situation, landing occurred some 50 msec prior to the ON beat or strong beat of the music. With this mode of synchronization, the timing of the ON and OFF beats of the musical stimulus would be suitable to potentiate the EMG events related respectively to the peak upwards acceleration determining the take-off and to the landing. It is inferred that during synchronized stereotyped movements to repetitive auditory stimuli, the motor events are timed to make best use of a potential audio-spinal facilitation.
Using positron emission tomography (PET) we previously showed that activation of the putamen, supplementary motor area, and cingulate cortex is impaired in patients with Parkinson's disease (PD) when they are off treatment and perform volitional motor tasks. Evidence suggests that these areas are involved in the generation of internally cued movements in normal subjects. We have now studied the effect of the dopamine agonist apomorphine on cerebral activation when used to treat the akinesia of PD. Regional cerebral blood flow was measured using C15O2 PET in PD patients at rest and when performing paced joystick movements with the right hand in one of four freely chosen directions. All patients used apomorphine regularly, and were studied before treatment, while still "off" but receiving a subcutaneous apomorphine infusion, and when switched "on" with apomorphine. Significant increases in regional cerebral blood flow were determined using statistical parametric mapping. Under resting conditions apomorphine had no effect on focal or global cerebral blood flow. Seven patients with PD performed the motor task adequately in the "off" and "on" states. This group of subjects demonstrated impaired activation of the supplementary motor area and contralateral putamen in the "off" state. Activation of the supplementary motor area significantly improved when the akinesia was reversed with apomorphine. We conclude that the concomitant improvement of supplementary motor area activation and motor function in apomorphine-treated patients with PD provides further evidence for the role of this structure in generating motor programs.