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Sensory Training for Patients with Focal

Hand Dystonia
Kirsten E. Zeuner, MD,1 William Bara-Jimenez, MD,1 Patricia S. Noguchi,1 Susanne R. Goldstein, MD,1
James M. Dambrosia, PhD,2 and Mark Hallett, MD1

Some patients with focal hand dystonia have impaired sensory perception. Abnormal sensory processing may lead to
problems with fine motor control. For patients with focal hand dystonia who demonstrate sensory dysfunction, sensory
training may reverse sensory impairment and dystonic symptoms. We studied the efficacy of learning to read braille as
a method of sensory training for patients with focal hand dystonia. Sensory spatial discrimination was evaluated in 10
patients who had focal hand dystonia and 10 age- and gender-matched controls with a spatial acuity test (JVP domes
were used in this test). Clinical dystonia evaluation included the Fahn dystonia scale and time needed to write a standard
paragraph. Each individual was trained in braille reading at the grade 1 level for 8 weeks, between 30 and 60 minutes
daily, and was monitored closely to ensure that reading was done regularly. Both controls and patients demonstrated
improvement on the spatial acuity test. Patients showed a significant mean difference from baseline to 8 weeks on the
Fahn dystonia scale. Sixty percent of the patients shortened the time they needed to write a standard paragraph. Improved sensory perception correlated positively with improvement on the Fahn dystonia scale. We conclude that training
in braille reading improves deficits in spatial discrimination and decreases disability in patients with focal hand dystonia.
Ann Neurol 2002;51:593598

Focal dystonia of the hand can appear as task-specific


dystonia in musicians, writers, typists, athletes, and
others whose work involves frequent repetitive movements.13 It is a movement disorder characterized by
sustained contractions of agonist and antagonist muscles that lead to abnormal twisting movements and
postures. Initially, only the skilled task is involved;
later, the dystonia can become more generalized, affecting other tasks and parts of the body. Task-specific
dystonia is chronic and difficult to treat.
Focal hand dystonia may result from sensory dedifferentiation.4 In animal models of hand dystonia, owl
monkeys were trained to grasp a handgrip that repeatedly opened and closed. After months of training, they
developed a focal dystonia-like disorder.5 Electrophysiological mapping showed enlarged receptive fields with
the breakdown of normally separated representations of
different hand digits. It was presumed that stereotyped,
repetitive inputs, such as those of musicians, could
cause this enlargement of the receptive fields and dedifferentiation of representations in the sensory cortex
in humans, which would lead to a motor disorder.5 8
Increased cortical representation of the digits of the left

hand in string players has been shown on magnetic


source imaging.9 An abnormality of the homuncular
organization of the finger representation in the primary
somatosensory cortex in patients with focal hand dystonia has previously been described.10 12
Several experiments have demonstrated sensory dysfunction in patients with focal hand dystonia. An impaired capacity to integrate sensory information into
motor programming has been described.13 Grunewald
and colleagues showed that in focal dystonia there is an
abnormal perception of the tonic vibration reflex and
of motion, but not of position, suggesting an abnormal
perception of movement.14 Murase and colleagues assumed that the sensitivity of sensory input channels
from the hand is possibly not correctly set by the central command to move.15 They concluded that dystonic patients might, therefore, have difficulties in interpreting sensory input that occurs before movement
and, in more severely affected patients, even during
movement.15 Difficulty in interpreting tactile stimuli
(graphesthesia and manual form perception) has been
detected in both hands of patients with focal dystonia.6
Such patients have also shown decreased performance

From the 1Medical Neurology Branch and 2Biostatistics Branch,


Human Motor Control Section, National Institute of Neurological
Disorders and Stroke, Bethesda, MD.

Address correspondence to Dr Hallett, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Building
10, Room 5N226, 10 Center Drive, MSC 1428, Bethesda, MD
20892-1428. E-mail: hallettm@ninds.nih.gov

Received Jun 4, 2001, and in revised form Jan 10, 2002. Accepted
for publication Jan 16, 2002.
Published online Apr 23, 2002 in Wiley InterScience
(www.interscience.wiley.com). DOI: 10.1002/ana.10174

This article is a US Government work and, as such, is in the public domain of the United States of America.

Published 2002 by Wiley-Liss, Inc.

593

in tactile spatial acuity and localization compared with


controls.16 Abnormal temporal discrimination of somatosensory stimuli has been noted as well.17,18 Because a major role of the sensory system is to drive the
motor system, a sensory disorder may contribute significantly to disordered movements such as focal hand
dystonia.19
The extent of the change in somatosensory cortical
representation of the digits depends on the amount,
simultaneity, rate, and timing of sensory input.7 Intense braille reading can influence cortical representation20 22 and produce superior tactile spatial acuity in
blind braille readers.23
Treatment of hand dystonia is difficult. Patients
with mild symptoms are often advised to reduce their
task-specific activity or to consult an occupational therapist. Current treatment involves botulinum toxin injections; the response rate is generally good, except for
patients with musicians cramp,3 but improvement is
generally far from perfect and repeated treatment is required every 3 months. Drug therapy, with agents such
as anticholinergics, baclofen, and benzodiazepines, is of
limited benefit.
On the basis of the hypothesis that abnormal sensory
processing could cause a motor disorder, the use of
sensory training has been suggested to treat focal hand
dystonia.3,7,8,12,16 18 In 1997, Byl and colleagues proposed that sensory training should not be stereotyped
and that repetitive motion events should be spaced
apart to ensure differentiated sensory inputs.7,8 In this
study, we tested the hypothesis that sensory training
could improve sensory perception and, consequently,
dystonia. For our test, we selected braille reading as a
sensory training method to improve patients spatial
discrimination and localization.
Subjects and Methods
We studied 10 patients with focal hand dystonia (1 man and
9 women) and 10 normal volunteers (2 men and 8 women).
The average age of the patient group was 50.1 7.36 years;
the average age of the normal volunteers was 44.7 10.7
years. This difference was not significant. Two patients had
simple writers cramp only, whereas in 8 patients dystonia
was present at rest or during more than one action (dystonic
writers cramp).24 One patient also had spasmodic dysphonia. One patient was left-handed; after developing writers
cramp in her left hand, she switched to her right hand and
developed writers cramp there as well.
The diagnosis of focal hand dystonia was made by medical
history and the National Institute of Neurological Disorders
and Stroke standard neurological examination. Patients were
asked not to receive any change in treatment for dystonia
during the study. Botulinum toxin injections were not given
for at least 3 months before enrollment in the study.
Sensory perception was evaluated in each individual with a
grating orientation discrimination test, which involved using
the entire set of eight commercially available plastic hemi-

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spheric JVP domes (Stoelting, Wood Dale, IL). The domes


have gratings of equal ridge and gap widths cut into their
faces with gap values of 0.35, 0.5, 0.75, 1.0, 1.2, 1.5, 2.0,
and 3.0mm. The threshold is defined as the dome with
which the patient achieves a 75% correct response rate. Patients who were unable to reach the threshold for 3.0mm
were considered to have an arbitrary threshold at 4.0mm, so
that these results could be compared with those of the following weeks. The arm and hand were held in a supine position; the right index finger was tested for about 1 second,
and the test was repeated 20 times with each dome. Each
individual had to identify the orientation of the gaps, which
were presented in order of decreasing gap values and randomly positioned either vertically or horizontally. This test
has been described in detail previously.2530 Only minor
learning effects have been reported.26,28,30,31
For clinical evaluation of the dystonia, each patient was
monitored according to the Fahn dystonia scale and was
asked questions about the severity of the dystonia in their
everyday lives.32 The average arm dystonia disability score on
the Fahn dystonia scale was 41.1%. Arm dystonia disability,
according to Fahn, is described as follows: 100%, unaware of
any difficulty; 95%, aware of some finger, hand, or arm
movements that cause some annoyance but no limitations of
activities; and 90%, completely independent and no limitations of activities but socially affected. If there were any limitations of functional activities, the patient had to check specific items on a list. All patients in this study were limited in
their functional activities and had to check listed items. The
scale uses a range of points from 0 to 3 for each of 7 questions. The total number of points scored for each patient was
divided by the maximum possible points for each patient,
the quotient was multiplied by 90, and the result was subtracted from 90%. The final score represents the percentage
of normal activity. Therefore, an increase in score represented an improvement in arm dystonia.32
In addition, each patient wrote a standard paragraph, with
the time in seconds for completion recorded. Patients were
asked to rate themselves on a visual analog (ranging from
0 no improvement to 100 full recovery) and a verbal
scale with four levels (ranging from 0 no improvement to
3 major improvement) for improvement of the dystonia.
All testing and evaluations were done at baseline and at
weeks 4, 8, 12, and 20.
For 8 weeks, patients and volunteers were trained in
braille reading at the grade 1 level with standardized books
from the American Printing House for the Blind.33 Patients
were asked to practice with the finger clinically most affected
and then continue with the two fingers on either side of it.
Fingers were always trained individually. The investigators
followed the instructions given by a braille teacher and the
print teachers edition of The Braille Connection.33 Patients
were taught to move both hands from left to right, with one
hand detecting the lines and the other hand reading the cells,
and to use only a light touch. They were reminded to move
their fingers lightly across the dots and not vertically or in
circles.
Patients practiced 1 hour each day for the first 5 days and
30 minutes per day for the remaining 7 weeks. Five patients
continued practicing after week 8, and 4 patients continued
after week 20. In the 1st week, the practice was done entirely

under supervision, and in the remaining weeks, practice was


supervised once or twice a week; patients were blindfolded.
For homework, specific exercises from the The Braille Connection workbook were assigned with copies from the print
teachers edition, so that each individual could check his or
her own work for mistakes. Subjects practiced blindfolded
but were allowed to look at the printed copy to verify words
or letters. At each visit to the National Institutes of Health,
they were given new exercises from the workbook as exams,
along with feedback about their progress. Normal volunteers
were only paid for the time they had practiced. The target
goal was to read the given exercises without errors being
made. Everybody learned the complete alphabet (including
exercise B24 in the workbook and pages 19 27 in the practice book). The number of exercises patients could do was
independent of their baseline performance on the grating orientation task. All individuals signed an informed consent
form for this study protocol, which had been approved by
the National Institute of Neurological Disorders and Stroke
Institutional Review Board.

Statistical Analysis
The dependant variables in this study were the thresholds in
the grating orientation task, the scores on the Fahn dystonia
scale, and the time needed to write a standard paragraph.
The change scores were compared with Mann-Whitney U
statistics. A comparison of performances during weeks 1 to 8
by patients and controls was made with the nonparametric
Wilcoxon signed rank test for matched pairs. Spearman rank
correlations were computed to assess relationships among the
various patient measurements and to assess relationships between the dependant variables. Nonparametric statistics were
selected because of the small group size and the skewness of
the distribution for the dependent variables.

Results
The mean value (plus or minus the standard deviation)
for the grating orientation task at baseline was 2.38
1.09mm for patients and 1.95 1.01mm for normal
volunteers. This difference was not significant ( p
0.54). Both groups improved; at week 8, the mean
value was 1.75 0.69mm for patients and 1.38
0.61mm for normal volunteers. Improvement was significant in both groups ( p 0.03 for patients, p
0.01 for normal volunteers; Fig 1). Patients who were
unable to reach the threshold of 3.0mm were considered to have an arbitrary threshold at 4mm so that
comparisons could be made with results of the following weeks. After 8 weeks, all subjects had reached a
threshold of at least 3mm. The standard deviation,
therefore, decreased after 8 weeks. Patients who had
higher thresholds in the grating orientation task improved more than those who had lower baseline scores.
The amount of mean improvement did not differ between the two groups.
On the Fahn scale, which represents the severity of
focal hand dystonia in patients, 5 of 10 patients improved, whereas 4 showed no change. The improve-

Fig 1. Thresholds, in millimeters, in the grating orientation


task at baseline and after week 8 for 10 patients (left) and 10
normal volunteers (right). Two patients and 1 normal volunteer could not recognize the grating with 3mm at baseline;
they were given an arbitrary number of 4mm.

ment on the Fahn scale was significant ( p 0.046; Fig


2). Patients who improved their spatial acuity also improved on the Fahn scale (correlation coefficient,
0.27); however, the correlation coefficient was low.
Six of 10 patients shortened the time they needed to
write a standard paragraph (see Fig 2). Two of 10 patients were unable to finish writing the standard paragraph (Patients 4 and 8). Patients 4 and 8 were included in the nonparametric statistical test with an
arbitrary, unchanged number of 300 seconds. Improvement in the time needed to write a standard paragraph
was not significant ( p 0.12). There was no improvement on either the visual analog scale or the verbal
scale.
Patient 6 stopped practicing between weeks 8 and
12. Her performances in the areas of the grating orientation task, the Fahn dystonia scale, and the writing
of a standard paragraph decreased. She restarted again
after week 12 and practiced regularly through week 20.
She improved again on all three tests, although her
writing was not quite as good as after week 8. Patient
10 continued up to week 12 and stopped practicing
between weeks 12 and 20. Her writing remained the
same, but her performance on the grating orientation
task and the Fahn scale decreased. Three of 4 patients
had diminished writing performance after they stopped
practicing at week 8; 1 patient stayed at the same level.
Three of 4 patients who continued after week 8 further
improved their writing. Patient 8 temporarily discontinued after week 20 (the study was already finished)
but restarted training again after 3 weeks because she
found that her dystonia and writing difficulties worsened after the interruption. Her writing example is
shown in Figure 3. Changes in percentages from baseline to week 20 for the grating orientation task and the
writing of a standard paragraph are shown in Figure 4.

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595

Fig 2. (A) Fahn dystonia scale scores for


10 dystonia patients at baseline and at
week 8. A score of 100% meant lack of
awareness of any disability. (B) Time
taken to write a standard paragraph, recorded in seconds, for 10 patients at baseline and at week 8. Patients 4 and 8
could not complete the writing. They were
given an arbitrary, unchanged number of
300 seconds.

Discussion
We asked two principal questions in this study: (1)
does braille reading improve sensory discrimination
and (2) does sensory training lead to improvement in
focal hand dystonia? Although our patients showed decreased performance on the grating orientation task at

baseline, confirming recent reports,16 the difference between patients and controls was not significant. This
might be because we investigated only 10 subjects in
each group, whereas Bara-Jimenez and colleagues16
tested 17 patients and 13 normal volunteers. Our primary outcome was improvement after 8 weeks of sen-

Fig 3. Attempts by Patient 8 to write a


standard paragraph. The patient was originally left-handed. She switched to writing
with her right hand 10 years ago, after
developing writers cramp in her left hand;
she now has writers cramp in both hands.
Sensory training was done with her left
hand only. At baseline, she was unable to
write the paragraph with either her right
or left hand. After 6 months of regular
sensory training, she could finish the paragraph with either hand.

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Fig 4. Changes in performance, as percentages,


in (A) the grating orientation task (GOT) and
(B) the writing of a standard paragraph between weeks 1 and 20, depending on each
patients amount of practice. The filled columns represent patients who continued to practice at week 20. The white columns show patients who stopped practicing at week 8 or 12.
0 no change; n.a. (not applicable) patients who did not come for follow-up or who
received alternative treatments after week 8.

sory training for each individual, with no significant


differences in the thresholds between the groups. The
differences were within the standard deviations described by Bara-Jimenez and colleagues.16 The significant differences in threshold between writers cramp
patients and controls reported by Sanger and colleagues18 might have been influenced by the age difference between patients and controls, who were 10 17
years younger. Age influences spatial acuity and could
have contributed to their findings.28
Our study shows that spatial acuity improved significantly in patients and controls after 8 weeks of daily
practice. Therefore, we conclude that braille reading
improves tactile spatial acuity and is a method of overcoming this deficiency in patients with focal hand dystonia. This is consistent with findings of van Boven
and colleagues,23 who described a significantly better
threshold in the spatial acuity test in braille-reading
blind subjects than in a control group of sighted subjects. Braille reading does meet the requirements of
sensory training, such as ensuring differentiated inputs
without repetitive or stereotyped features, as suggested
by Byl and colleagues.7,8 In addition, it requires a high
level of concentration. This is consistent with the report by Braun and colleagues,34 who showed that after
only 4 weeks of training with a tactile discriminating
stimulus, active discrimination training with a certain
degree of difficulty and attention led to alterations in
the functional organization of the human sensory cortex. This group described a difference between passive
tactile stimulation and stimulus discrimination. Representations of fingers D1 and D5 in the somatosensory
cortex were closer together after passive tactile stimulation than after a stimulus discrimination task, after
which digital representations were further apart. They
concluded that differential activation in the same somatosensory area was specific to different tasks.
Three of four patients who continued practicing up
to week 20 further improved in the grating orientation
task. The fourth patient of this patient group, Patient
5, did not improve, and his performance on the grating

orientation task decreased at week 20. He practiced


only two or three times per week after week 12, compared with every day up to week 12; therefore, practice
was probably insufficient to maintain the initial improvement that he demonstrated after week 12.
The second question in which we were interested
was whether sensory training could improve focal hand
dystonia. Patients who improved in the grating orientation task also improved on the Fahn dystonia scale.
This scale includes questions not only about writing
but also about tasks that are influenced by focal hand
dystonia in daily living.32 Improvement on the Fahn
scale was significant between weeks 1 and 8. Those patients who continued practicing until week 20 had the
same scores as after week 8. Two patients who discontinued after week 8 had scores that continuously decreased; one remained at the same level, whereas the
other improved.
The verbal and visual analog scales showed no subjective improvement during the first 8 weeks. This indicates that the patients themselves, as a group, believed that there was no marked improvement in their
dystonia. However, 2 of 3 patients who continued with
their sensory training after week 20 noticed clear improvement, which motivated them to continue for an
observation period of up to 1 year. It is probable that
the training has to continue for more than 8 weeks for
clinical improvement to be sufficiently substantial and
recognized subjectively.
It appears that continuing, regular practice beyond 8
weeks leads to further improvement not only in spatial
discrimination but also in dystonia in some patients. In
interpreting our results, we believe that sensory training
possibly results in redifferentiation in the sensory cortex and improved output to the motor cortex and,
therefore, leads to improved spatial acuity and focal
hand dystonia. Improvement in sensory discrimination
and hand dystonia apparently diminishes after patients
stop practicing, indicating that there is no long-lasting
effect without daily, regular practice.
Our results are consistent with findings of Byl and

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597

colleagues,35,36 who described improvement in patients


with focal hand dystonia after multimodal retraining
designed to excite cortical areas associated with 3b (somatosensory) and 3a (proprioception, vibration, and
muscle afferents). Therapeutic retraining for patients
with focal dystonia possibly needs to be more complex
to represent the normal variability and flexibility of the
nervous system and ultimately restore normal targetspecific fine motor activities.
We thank our patients for participating in this study. We are grateful for the support of Patricia Droppers, a braille teacher at Volunteers for the Visually Handicapped in Silver Spring, MD, who designed the sensory training program with us. We also appreciate the
skillful editing of Devera G. Schoenberg.

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