muscle control in chronic tic disorders

Biofeedback and Self-Regulation, Vol. 20, No. 2, 1995

Muscle Control in Chronic Tic Disorders

Kieron O'Connor, Daniele Gareau, and Francois Borgeat 1 Fernand-Seguin Research Center, Montreal

EMG was recorded in nine subjects suffering from chronic tic disorder. Six subjects suffered asymmetrical tics and three had symmetrical tics. EMG in tic-affected and contralateral nonaffected sites was recorded at rest, during a baseline period, and at postbiofeedback training. All subjects received 2-4 biofeedback training sessions aimed at enhancing their ability to control levels of muscle contraction in both affected and nonaffected sites. All nine subjects met the criterion of discriminating unaided between levels of O, 25%, 50%, and 75% of their fullest contraction. Five of the six people with asymmetrical tics showed lower resting EMG on the affected side at baseline, but EMG significan@ increased in tic-affected but not nonaffected muscles after exercises aimed at enhancing muscle control. Six subjects reported a clinical!y significant >40% decrease in tic frequency. The reflexlike quality of tic muscles can be modified by biofeedback training, and this constitutes a useful and relatively quickly acquired aid to tic management.

Descriptor Key Words: tics; EMG feedback; muscle control.

Tics are defined as repetitive involuntary contractions of functionally re- lated groups of skeletal muscles. Tics seem mainly confined to the upper body, and the most common occur in the eye, head, shoulders, and face, and may include excessive blinking, cheek twitches, nose twitches, grimaces, shoulder shrugs, and head and neck contractions. Tics can also be vocal and include coughs, sniffs, barking, and throat clearing. In Gilles de la Tourette syndrome (TS) multiple tics, both vocal and muscular, are frequently found together along with other behavioral and attentional problems. TS is recognized in the DSM-III-R as an organic diagnostic, whereas

1Address all correspondence to K. O'Connor, Fernand-Seguin Research Center, Louis-H. Lafontaine Hospital, 7331 Hochelaga Street, Montreal, Canada HIN 3V2.

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0363-3586/95/0600-0111507.50/0 © 1995 Plenum Publishing Corporation

112 O'Connor, Gareau, and Borgeat

some complex tics (e.g., trichotilomania) are recognized as impulse disorders (Shapiro, Shapiro, Young, & Feinberg, 1988). In fact tics show both compulsive and impulsive characteristics.

COMPULSIVE ASPECTS

Tics can superficially resemble compulsive movements. In a compul- sion the person feels unable to resist performing an action. People with tics do show higher than normal levels of perfectionism, and also show a tendency toward hyperactivity (Trimble, 1989; O'Connor, Gareau, & Blow- ers, 1994). Clinically speaking, the client with a tic orten claims that the tic relieves a vaguely defined subjective tension, and the tic may have initial tension-reducing properties, which are reinforced through repetition of the habit. In this sense, tics, in particular complex tics (those involving more than one movement), can resemble the automated rituals of the obsessive-compulsive, where the person feels obliged to perform a purpose- less action in order to "neutralize" aversive feelings. Furthermore the person with a tic, like the person with a compulsive disorder, can orten report that they are unable to break out of a series of repetitive movements once they are begun. Similar aspects of behavioral treatments have proved effective in treatments of tics and compulsions. Among these, response prevention and habit reversal plus exposure seem the treatments of choice. However, several behavioral treatments have proved helpful in tic management, and the lack of large-scale studies does not permit us to isolate one aspect of treatment as the most useful. In a recent study Pe- terson and Azrin (1992) compared the efficacy of awareness, relaxation, and habit reversal for tics in people with TS, and found no significant difference between treatments. All treatments were equally successful in reducing tic occurrence by between 32-55% over a six week period. A problem for a purely compulsive model of tic disorders is that the psy- chotropic medications most effective for tics are not the most effective in treating obsessive compulsions.

IMPULSIVE ASPECTS

Data supporting the impulsive nature of tics include findings of elevated dopamine in tic disorders. In particular dopamine neurons are found in midbrain structures implicated in motor regulation an elevated levels might be expected to lead to a state of heightened motor activation. Neuroleptic treatments of tic disorders have been developed on the basis

Muscle Control in Chronic Tic Disorders 113

that such medication acts as a dopamine antagonist. But not all patients respond to neuroleptics and double-blind placebo-controlled designs have found tic frequencies reduced by only an average of 50% with unwanted side effects in 80% (Shapiro, Shapiro, Young, & Feinberg, 1988). Signifi- cant support for the impulse interpretation of tics comes with the finding that in some patients tics resemble a powerful polysynaptic startle response (Commander, Corbett, Prendergast, & Ridley, 1991). Corbett (1976) has in fact proposed that tics represent conditioned startle responses. Corbett's reflex model also proposes an interaction in tic onset between environ- mental and biological factors, with a genetically determined vulnerability of dopamine modulation producing an excessive startle to stressful stimuli. If tics have come to resemble reflexes, one might expect a difference in ability to control tension levels between tic affected and unaffected muscle groups.

Some tics are markedly asymmetrical; for example, shoulder, neck, face, and sometimes eye tics can occur only on one side. In our clinical treatment of these problems we have frequently noted that the person experiencing a tic has difficulty in contracting the affected muscle or muscles slowly. In the case of a unilateral tic s/he is less able to modulate the level of contraction on the tic-affected side than on the contralateral nonaffected side between completely contracted and completely relaxed. The tic-affected muscle when contracted to any degree immediately jumps to a full contraction. No level of tension other than a full contraction can be sus- tained and the muscle appears to have reflexlike qualities.

The present study had three principal aims. The first aim was to see if in asymmetrical cases of tic disorders there were quantifiable electromyographic differences in muscle contraction as measured by EMG between affected and contralateral nonaffected muscles. The second aim was to see whether learning to systematically control tension levels in affected muscle sites through biofeedback-assisted exercises would increase the person's voluntary control over the tic and increase the ability to perform step- wise contraction and relaxation. And the third aim was to see if biofeedback training in muscle control would have an effect on tic production outside of the biofeedback session.

SUBJECTS

The criteria for patient selection were as follows: a motor tic over which the person had little or no control and which was debilitating and chronic (over a period of several years) and which was not part of another identifiable neurological problem or of pharmacological origin. Patients


were all diagnosed as having idiopathic tic disorders, and none had tics secondary to other disorders; those with TS were not included. Patients were screened neurologically and psychiatrically and none of the patients included had other major problems. Fourteen patients were recruited rang- ing in age from 23 to 49 years. The age of tic onset varied, and several patients had a history of tic disorder prior to the present tic. None of the patients had vocal tics and so were not TS, and patients were not receiving other treatments at the time. The results on nine of the patients who had tics in easily identifiable groups of muscles on the face or neck are pre- sented here (see Table I). The other five were excluded either because they had multiple tics or because their tics were not easily identifiable as symmetrical or asymmetrical. Of the nine subjects selected, six had tics that were clearly asymmetrical, while tics in the other three were symmetrical.

METHOD

Electromyographic (EMG) recordings were taken (scored as root mean square level) from three muscle sites: the affected muscle group, the contralateral nonaffected group, a "neutral" site (a site distant from the tic group). The back of the neck (spinalis capitis) was chosen as a "neutral" site. In the event of the neck site being implicated by the tic (2 subjects), the frontalis site was chosen as an alternative. Heart rate (HR) in beats per minute was recorded as an independent measure of autonomic arousal. Its role was to monitor changes in general levels of activation that might influence any changes in muscle state. The EMG and HR recording and feedback were carried out using IBM Biotext 1.2 (Eschbach, 1987) on Autogenic Systems Instruments using Cyborg M130 amplifier modules. The characteristics of this module are band pass 100 to 250 Hz, with high- and low-pass filters at 48 dB/octave and time constant at 0.022 s. The sensors used were 4-mm stainless steel and were applied with Spectra 360 electro- lytic gel after cleansing and abrasion of the skin, at sites one third and two thirds of muscle length.

PROCEDURE

The subject was required to keep an initial base line diary of tics over a period of two weeks prior to the study. The subjects recorded tics in a specially prepared booklet, where they marked the exact time and nature of the tic during hourly periods throughout the day. If the tic occurred as a series then the series was recorded as a unit. The subjects were given


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instructions in developing awareness and detection of tic onset at the initial meeting. Subjects monitored tics during this baseline period. On a sub- sequent meeting two weeks later psychophysiological measures were taken in an isolated laboratory with a two-way window. The subject reclined in a comfortable chair and was asked to relax with eyes open and more as little as possible while 10 minutes of tonic resting measures of EMG and HR were taken (baseline).

A week later the subjects attended again and began the biofeedback- assisted discrimination exercises to teach them to identify levels of EMG recorded muscle tension. These exercises involved identifying, with the aid of auditory feedback, different levels of muscle contraction (i.e., when the muscle was a quarter contracted, half contracted, three quarters contracted, and fully contracted). The procedure was introduced to the subjects as a means to assist them in becoming more aware of "tension" levels. The subject was placed in a comfortable reclining chair and the electrodes attached. Subjects with asymmetrical tics began the exercises with the nonaffected side. They were asked to contract the muscle as slowly as possible to a point they felt was full contraction, without forcing, while listening to an auditory signal fed back to them through an 8-ohm speaker mounted on the laboratory wall. The subject was asked to isolate the target muscle and ensure that only this muscle was contracted. It was explained that the higher the EMG level of the muscle the higher the frequency of the signal. Initially the assistant indicated verbally to the person whether their EMG level showed 0.25%, 50%, 75% or total contraction. Once the subject had associated their muscle contraction with the auditory signal they were left to practice modulating their contraction and linking this with the auditory signal. After this practice period subjects were asked to say out loud when they detected their muscle as being 0.25%, 50%, 75% or fully contracted, and the experimenter corrected them if they were not within 10% of the target level. Subjects mostly found gradually relaxing the muscle from full contraction through the different levels to zero more difficult than gradually contracting from zero to full contraction. This procedure was repeated until the subject could identify the 0, 25%, 50%, and 75% levels of contraction by themselves without feedback. This was the criterion for successful com- pletion of the procedure. After subjects had mastered the discrimination exercise with the nonaffected side, we began with the affected side, which all subjects found more difficult to control than the nonaffected side. In the case of subjects with symmetrical tics, we began with the biceps as a nonaffected site and subsequently practiced on both affected sites at the same time. Subjects were given home practice exercises and asked to repeat slow contractions and decontractions of the muscle at home in both affected and nonaffected muscles six times each, twice a day for the next


two weeks. On the second discrimination session, one week after the first session (i.e. after one week of practice) subjects followed the same procedure, this time mostly with the tic-affected muscle and continued the home practice. A week later, after the second week of practice, all subjects were tested to see if they reached the criterion of unaided identification (i.e., with no verbal or auditory feedback) of EMG level in the tic-affected site. In this third session the subjects continued the exercises if they could not identify without the aid of the feedback the four degrees of contraction in both the tic-affected and the contralateral nonaffected muscles. Seven of the subjects had achieved the criterion level of unaided identification of the tension level associated with their degree of contraction after two weeks of practice, and two subjects reached this criterion after four weeks of practice.

After the person's ability to produce and to accurately report levels of tension in both sides was verified in this last training session, the subjects attended, one week later, for another EMG recording session during which tonic resting levels were recorded for 10 minutes (post-test).

ANALYSIS

EMG trials were sampled at 30-second intervals giving approximately 20 trials for each 10-minute tonic resting session. Each trial contained 480 data points, each point representing 62.5 ms. Mean levels of the trials were computed over the first and last (artifact-free) minute of each session recorded at baseline, and at post-test. Trials with actual tics or movement artifacts were eliminated. However, in the current analysis (one minute at the beginning, one minute at the end), there was no artifact present in the original trials chosen of four subjects. In three subjects (J.V., J.B., F.R.) one trial was rejected and substituted for the adjacent trial (either the pre- ceding trial, in the case of the last minute, or succeeding trial, in the case of the first minute). In subject S.M. two trials and in subject G.C. three trials were substituted. There was little variability within trials within recording sessions. The variance measures given in Table III are computed across trials. Clinical measures of tic frequency were computed from the subject's diary for the two-week period at the baseline, the week between initial attendance and first training session, and the week after the final training session. The effects of training were evaluated by looking at baseline-post changes in tic frequency within each single case (Table II). Dif- ferences in EMG levels in tic and nonaffected sides were examined both within and across subjects within the asymmetrical and symmetrical groups. The mean EMG levels of tic and opposite sites were compared at baseline


Table Il. Self-Reported Tics

Mean baseline Mean Change in intensity Subject frequency postdiscrimination from pre- to code ~ (SDn.1) frequency ~ (SDn_I) postdiscrimination

J.V. Per hour 13.5 (6.7) 8.8 (5.5), No change M.P. Series per day 2.9 (3.0) 1.0 (0) a'° Decrease J.B. Per day 5.4 (1.7) 2.0 (1.6) Decrease N.D. Series per day 2.0 (0) 01 Decrease S.L. Series per day 2.3 (1.5) 1.1 (0.3) No change S.M. Per hour 5.8 (2.2) 3.6 (1.9) Decrease G.L. Per hour 9.7 (2.5) 2.0 (0) No change G.C, Per hour 52.4 (8.8) 47.1 (2.0) Decrease F.R. Series per day 5.4 (1.5) 8.8 (1.3) No change

aTic no longer present bReplaced by feeling of tension.

and at post-training across subjects using the Wilcoxon matched-pairs signed ranks test (Table III).

RESULTS

In five of the six cases where there was a clear asymmetrical tic, the tic-affected side showed less tension at baseline than the opposite unaffected side. The odd case out was a subject (S.L.) with an asymmetrical leftward head tilt involving contraction of the neck muscles on the left side, but which may have also implicated the right side. The Wilcoxon test showed no significant difference between tic-affected and opposite muscles for the asymmetrical group at baseline but a difference at post-test (Z = -1,99;p < 0.05; two-tailed). There was a significant increase in EMG values from baseline to post-test in the tic-affected muscle only (Z = 2,20; p < 0.03). In the three subjects with bilateral tics, there was no consistent difference between sides at baseline and two of the three subjects showed an increase in tension post-training. The neutral site and the heart rate showed no pattern of change over sessions, and the generally low EMG level in this neutral site suggested that the subjects were indeed at rest during these recording sessions. The effect of the discrimination training then was to generally increase tension on the tic-affected side. All subjects found the discrimination exercises much harder for affected than nonaffected muscles.

We considered any decrease in tic frequencies greater than 40% as a clinically significant improvement. There was a decrease in the frequency

Muscle Control in Chronic Tic Disorders

Table III. Root Mean Square EMG Values (Microvolts)

119

Subject code a Baseline Postdiscrimination

J.V. Tie 0.82 (1.2) 1.04 (0.4) Opp 2.35 (1.8) 1.10 (0.6) Neut 1.10 (2.1) 1.00 (0.9) HR 66.95 (0.9) 71.93 (3.6)

M.P. b Tic 0.35 (0.4) 3.55 (1.5) Opp 4.63 (0.6) 0.80 (1.5) Neut 0 (0.1) 0 (0.1) HR 69.10 (1.0) 69.10 (1.2)

J.B. b Tic 3.67 (2.2) 5.45 (6.6) Opp 4.50 (2.9) 4.67 (3.6) Neut 0.87 (0.8) 0.50 (0.7) HR 75.97 (6.0) 82.60 (4.7)

N.D. b Tic 0.93 (0.6) 1.75 (1.2) Opp 1.99 (1.2) 1.65 (1.3) Neut 2.67 (2.4) 2.38 (2.6) n R 61.07 (6.5) 70.32 (6.0)

S.L. b Tic 3.47 (2.3) 3.60 (1.1) Opp 1.47 (1.0) 1.25 (1.0) Neut 0.47 (0.4) 0.45 (0.4) HR 81.02 (2.4) 76.20 (2.4)

S.M. ö Tic 1.90 (3.3) 5.35 (5.5) Opp 3.15 (3.3) 4.90 (5.2) Neut 1.70 (0.9) 3.40 (2.9) HR 78.95 (1.6) 74.02 (3.0)

G.L. » Tic 7.30 (11.8) 3.02 (1.5) 9.52 (11.3) 5.17 (2.7)

Neut 2.0 (0.8) 1.15 (0.6) HR 77.52 (4.5) 70.82 (2.6)

G.C. Tic 3.00 (1.1) 3.50 (2.1) 4.15 (1.4) 7.05 (4.1)

Neut 0.20 (0.3) 0.92 (2.5) HR 79.87 (6.0) 85.50 (7.0)

F.R. Tic 3.00 (4.1) 7.50 (4.3) 3.80 (5.6) 2.82 (3.1)

Neut 0.30 (0.5) 0.37 (0.6) HR 83.95 (6.6) 93.37 (7.0)

aTic, tic-affected muscle; Opp, contralaterally opposite site; Neut, neutral site; HR, Heart rate.

bDenotes subject showing clinically significant improvement in tic frequency.

of reported tic in six subjects following the exercises, with cessation of the tic in two subjects (subjects with least tics at baseline). In two subjects there was no decrease in frequency but a decrease in reported intensity. In one subject there was no change in either intensity or frequency.


DISCUSSlON

Our first aim in this study was to look for EMG differences between tic-affected and nonaffected sites. At baseline there was no overall difference between the two sites, but in live of the six cases where tic disorders were asymmetrical the tic-affected muscle generally had a lower resting EMG level than the contralateral nonaffected muscle. There was, however, a significant increase in EMG level at post-test in affected but not nonaffected sites. These findings might appear counterintuitive, since evidently, during tic production, the tic-affected muscles must contract and might be expected to show higher EMG than the nonaffected sides. However, the present recordings were at rest, and during the recording the subjects were in general not producing tics. We did eliminate trials with tics and movement artifacts, but there were relatively few and certainly not enough to bias the trial selection. In everyday life people with tics are able to control their tics, either by physicaUy preventing the tic, by relaxing, or by delaying the tic to a later more appropriate time. Since the differences were present when the subjects were relaxing, the lower EMG level might simply reflect less variation in range available for the tic-affected muscle as a result of its all-or-nothing state of contractibility. The discrimination training may have increased EMG since it is not identical to relaxation training and the exercises involved creating an awareness and a control of different levels of contraction rather than relaxing the muscle. Subjectively subjects gen- eraUy report experiencing increased "tension" following the exercises. How- ever, although the differences were statistically significant the quantitative changes are not great and the finding clearly requires independent repli- cation before it can be considered other than serendipitous. As regards our second aim of investigating the effect of increasing the person's control over muscle contraction on EMG levels, the tic-affected muscle was clearly less controllable than the nonaffected muscle and subjects had more difficulty learning to discriminate and control contraction level. But increasing control over contraction did increase degree of control over the tic in the majority of subjects.

Successful control over muscle contraction was followed in eight subjects by a decrease of varying degrees in tic occurrence and in six cases by a clinically significant decrease (>40% of initial value). Increased awareness of a tic induced by self-report can either increase or decrease reported frequency, but we controlled for this effect by recording the tic over a baseline of two weeks and a further week prior to discrimination training. There was no difference between these two self-report measures and hence the first baseline is reported here. The lack of change in the other two measures


(neutral site and heart rate) suggested that changes in the tic-affected mus- des were not due to general state changes in arousal or habituation.

Two subjects (G.C. and F.R.) appeared not to show much benefit clinically in terms of reduced tic frequency from the procedure, and the most parsimonious explanation is that the exercises in these cases were not practiced long enough or applied thoroughly enough. As noted in the meth- odology, most subjects (7) were able to learn the discrimination procedure to criterion within two weeks, and 2 subjects (G.C. and S.M.) after four weeks. All subjects achieved the discrimination criterion of identifying unaided degrees of muscle contraction, but subsequently we have refined this criterion as the ability to smoothly and continuously increase and decrease EMG level between 0 and full-scale contraction. We now also use a visually displayed graphic as feedback to give an indication of the con- tinuity of contraction. Our clinical experience has suggested that it is im- por tant to achieve isolation of the muscle or muscle group from surrounding groups affected during the discrimination exercise. And this point particularly applies to blinking and other facial tics where several muscles mostly irrelevant to the tic-affected muscle function can be implicated in the blinking action (e.g., in the tic involving excessive blinking (G.C.) the normal blinking movement of the subject implicated not just the eyelid but all the muscles surrounding the eye).

In conclusion our findings provide some psychophysiological evidence for Corbett's proposal that the muscles implicated in simple tics exhibit a reflexlike quality in that they are under less voluntary control than nonaffected sites, and that modifying the "reflexive" nature of the muscle does have some immediate effect on tic frequency. Replacing the tic with a soft response over a period of several weeks has been reported in the literature as a form of competing response, which, when practiced contingently with the tic, can reverse the tic habit when it occurs (Azrin & Peterson, 1989). But in our case the exercises were noncontingent and simply involved increasing control of the muscle contraction with the aid of biofeedback. Our study, though preliminary, suggests that increasing control over tic-affected muscles may be an important factor in augmenting control over the tic.

REFERENCES

Azrin, N. H., & Peterson, A. L. (1989). Reduction of an eye tic by controlled blinking. Behavior Therapy, 20, 467-473.

Commander, M., Corbett, J., Prendergast, M., & Ridley, C. (1991). Reflex tics in two patients with Gilles de la Tourette syndrome. British Journal of Psychiatry, 159, 877-879.


Corbett, J. A. (1976). The nature of tics and Gilles de la Tourette syndrome. In F. Abuzzahab & F. Anderson (Eds.), Gilles de la Tourette's Syndrome (Vol. 1, pp. 26-32). St. Paul, Minnesota: Mason.

Eschbach, A. A (1987). IBMBiotext User's Manual. Autogenic Systems Instrument, 1350 South Kostner Ave, Chicago, IL.

O'Connor, K. P., Gareau, D., & Blowers, G.(1994). Personal constructs associated with tics. British Joumal of Clinical Psychology, 33, 151-158.

Peterson, A. L., Azrin, N. H. (1992). An evaluation of behavioral treatments for Tourette syndrome. Behavior Research and Therapy, 30, 167-174.

Shapiro, A. K., Shapiro, E. S., Young, J. G., & Feinberg, T. E. (1980). Gilles de la Tourette Syndrome. New York: Raven Press.

Trimble, M. (1989). Psychopathology and movement disorders: A new perspective on Gilles de la Tourette syndrome. Joumal of Neurology, Neurosurgery and Psychiatry, 52, 90-95.

muscle control in chronic tic disorders

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