G illes de la Tourette disorder has long been regarded as a disorder of involuntary movement. However, the great majority of patients of Tourette's reported premonitory urges; many stated that without the premonitory sensation, there would be no tics. It has been suggested that the tics are merely a voluntary response to these involuntary sensations. Performance of the tic releases the urge and emotional tension, analogous to a compulsory behavior undoing an obsessive thought in patients with obsessive-compulsive disorder (OCD). Patients with Tourette's disorder, OCD, or both disorders oftentimes repeat such compulsions until they feel “just right.” 1 Such conceptualization suggests that tics occur not because patients with Tourette's are impaired in inhibiting such a prepotent movement tendency; rather, they choose not to inhibit the urge to move or vocalize because of the mounting tension associated with such inhibition. The question of whether Tourette's disorder can better be viewed as an obsessive-compulsive spectrum rather than as an involuntary movement disorder is important, as it would have implications for its pathogenic mechanisms as well as for suggesting different treatment options for this condition.
To examine how “internally” generated movements, such as tics, are controlled is intrinsically difficult. However, a laboratory-based cognitive motor paradigm can be used as a behavioral proxy to investigate how movements are initiated and countermanded. The current study used a tracking stop-signal task to examine whether children with Tourette's are impaired in motor response inhibition. 2 We hypothesized that if the “urge-undo” mechanism played a major role in the generation of tics, these children would show no difference in response inhibition from healthy comparison subjects as they would be able to prevent prepotent movement tendency from developing into a motor response.
METHOD
Subjects
Thirty children (24 boys and six girls, 12 [SD=1.4] years old) with Tourette's disorder, according to DSM-IV, were recruited from a Pediatric Neurology or Child Psychiatry clinic of the Chang Gung Memorial Hospital. Children with Tourette's were rated on the Yale Global Tic Severity Scale (YGTSC). 3 The reliability and validity of this Chinese version of the YGTSC is currently being assessed. Thirty healthy children were also recruited, two of whom met criteria for attention deficit hyperactivity disorder (ADHD) upon diagnostic interview and were excluded from the study. The sample size was estimated on the basis of a previous study where 20 adolescents, each of high and low schizotypy, showed an effect size greater than 1.0 for group difference. Table 1 summarizes the demographics of the subjects. All of the participants and their parents gave written consent after they were given a detailed description of the study, according to institute guidelines.
TABLE 1. Clinical Characteristics and Stop Signal Performance of Children With Tourette's Disorder and Healthy Comparison Subjects
Behavioral Task and Experimental Procedures
There were two trial types, “go” and “stop,” in the stop-signal paradigm. A small dot appeared on the computer screen to engage attention at the beginning of a go trial. After a randomized time interval between 1 and 2 seconds (the fore-period), the dot turned into a circle (2° visual angle), which served as an imperative stimulus and instructed the subjects to press a mouse button quickly. The circle vanished at button press or after 1 second had elapsed, whichever came first, and the trial terminated. A premature button press before the circle appeared also terminated the trial. The go trials constitute the majority of trials (75%) and set up a prepotent response tendency. In a stop trial, an additional “X,” the “stop” signal, appeared after the go signal. The subjects were told to withhold button press if they saw the stop signal. Clearly it would be easier for the subject to withhold the response if the stop signal appeared immediately or early after the go signal, and the reverse applied if the time interval between the stop and go signals (or the stop-signal delay) was extended. The stop-signal delay started at 200 msec and varied from one stop trial to the next, according to a staircase procedure: if the subject succeeded in withholding the response, the stop-signal delay increased by 50 msec; conversely, if they failed, stop-signal delay decreased by 50 msec. Subjects were instructed to respond to the go signal quickly while keeping in mind that a stop signal could come up in a small number of trials. There were 225 go and 75 stop trials randomly intermixed in an experiment. With the staircase procedure we anticipated that the subjects would succeed in withholding their response in approximately 50% of the stop trials. 4
Data Analysis
The stop-signal reaction time was computed for each individual subject based on the horse race model. 2 We also examined a fore-period (FP) effect on go trial reaction time (RT) by dividing the trials into those with an FP of less than 1,500 msec and the others with one equal to or longer than 1,500 msec: FP effect = mean RT for short FP (<1,500 msec) – mean RT for long FP (≥1,500 msec). The FP effect indexes the level of response readiness and thus the prepotency to make a response. 5
RESULTS
As seen in Table 1 there were no differences between Tourette's disorder and healthy comparison children in general task performance, including average percentages of correct go and stop trials, suggesting that they were equally engaged in the behavioral task. 6 More importantly, they did not differ in the fore-period effect, suggesting that the response prepotency elicited during the wait period did not differ between Tourette's and healthy comparison children. The most important result is that children with Tourette's did not differ from healthy comparison children in stop-signal reaction time. This result also stands in a covariance analysis with the fore-period effect as a covariate (F 1,55 =0.019, p=0.890). Similar negative results were obtained when Tourette's children with ADHD or OCD comorbidity or when Tourette's children without these comorbid diagnoses were compared with healthy children.
DISCUSSION
The stop-signal task has been used to explore response inhibition in patients with Tourette's disorder, with mixed results: patients with chronic tic disorders appeared to be impaired in stopping a simple, automated movement, 7 while a more recent study did not find a difference between Tourette's disorder patients and healthy comparison subjects. 8 Moreover, with 50% of the trials being stop trials, the former study failed to set up a prepotent response tendency, and with the number of commission errors as the sole outcome measure, the latter study may have missed the difference in temporal dynamics during stop-signal inhibition.
The current finding suggests that children with Tourette's are not impaired in the suppression of voluntary motor acts. This result cannot be accounted for by different level of motor prepotency between Tourette's patients and healthy comparison subjects, since they demonstrate similar fore-period effects. Moreover, covariance analysis showed that they did not differ in stop-signal inhibition, even when the fore-period effect was taken into account. The current results are thus consistent with the “urge-undo” mechanism of tic generation, suggesting that the premonitory sensations or greater attention to these sensations rather than the tic movements are involuntary in Tourette's disorder.
Note, however, that the stop-signal task, as any laboratory-based cognitive motor paradigm, examines externally guided movements. Therefore, one might question whether Tourette's disorder patients are impaired in suppressing the internally generated tendency to move, despite their intact performance in the stop-signal task. Moreover, the current findings do not suggest that tics are solely compulsions. Indeed, tic movements are preceded by a premonitory sensation in Tourette's disorder patients, but patients with OCD rarely reported such sensations prior to repetitive behaviors. 9 Further studies would also need to examine whether Tourette's disorder patients engage different neural circuitry during stop-signal inhibition in order to achieve performance equitable to healthy comparison subjects. 6
Acknowledgments
This study was carried out at the Chang Gung Memorial Hospital. The authors thank the children and their parent(s) for their participation in the study, Monchu Chen and Jet Lan for their technical assistance at various stages of the study, and two anonymous reviewers for their most helpful comments on the manuscript. A grant from the National Science Council of Taiwan (NSC93-2314-B-182A-189, H.L. Chang) supported the study. The authors have no financial interest in the current work.
Footnote
Received November 29, 2005; revised March 14, 2006; accepted April 8, 2006. Dr. Li is affiliated with the Department of Psychiatry Yale University School of Medicine, New Haven, Connecticut. Drs. Chang, Hsu, and Ko are affiliated with the Department of Child Psychiatry, Chang Gung Memorial Hospital, Tao-yuan, Taiwan. Dr. Wang is affiliated with the Department of Pediatric Neurology, Chang Gung Memorial Hospital, Tao-yuan, Taiwan. Address correspondence to Dr. Chiang-shan Ray Li, Connecticut Mental Health Center, Rm. S103, Department of Psychiatry, Yale University, 34 Park St., New Haven, CT 06519; [email protected] (E-mail), or to Dr. Hsueh-Ling Chang, Dept. of Child Psychiatry, Chang Gung Memorial Hospital, 123 Dung Hou Road, Tao-yuan, Taiwan; [email protected] (E-mail).
Leckman JF, Walker DE, Goodman WK, et al: “Just right” perceptions associated with compulsive behavior in Tourette's syndrome. Am J Psychiatry 1994; 151:675–680
Logan GD: On the ability to inhibit thought and action: a user's guide to the stop signal paradigm, in Inhibitory Processes in Attention, Memory and Language. Edited by Dagenbach D, Carr TH. San Diego, Academic Press, 1994, pp 189–239
Leckman JF, Riddle MA, Hardin MT, et al: The Yale Global Tic Severity Scale: initial testing of a clinician-rated scale of tic severity. J Am Acad Child Adolesc Psychiatry 1989; 28:566–573
Li C-SR, Huang C, Constable RT, et al: Imaging response inhibition in a stop-signal task—neural correlates independent of signal monitoring and postresponse processing. J Neurosci 2006, 26:186–192
Serrien DJ, Orth M, Evans AH, et al: Motor inhibition in patients with Gilles de la Tourette syndrome: functional activation patterns as revealed by EEG coherence. Brain 2005; 128:116–125
Miguel EC, Coffey BJ, Baer L, et al: Phenomenology of intentional repetitive behaviors in obsessive-compulsive disorder and Tourette's disorder. J Clin Psychiatry 1995; 56:246–255
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