Reduced Tic Symptomatology in Tourette Syndrome After an Acute Bout of Exercise

Abstract

In light of descriptive accounts of attenuating effects of physical activity on tics, we used an experimental design to assess the impact of an acute bout of aerobic exercise on tic expression in young people (N = 18) with Tourette Syndrome (TS). We compared video-based tic frequency estimates obtained during an exercise session with tic rates obtained during pre-exercise (baseline) and post-exercise interview-based sessions. Results showed significantly reduced tic rates during the exercise session compared with baseline, suggesting that acute exercise has an attenuating effect on tics. Tic rates also remained reduced relative to baseline during the post-exercise session, likely reflecting a sustained effect of exercise on tic reduction. Parallel to the observed tic attenuation, exercise also had a beneficial impact on self-reported anxiety and mood levels. The present findings provide novel empirical evidence for the beneficial effect of exercise on TS symptomatology bearing important research and clinical implications.

Keywords

Tourette syndrome tic frequency exercise anxiety mood observational methodology

In his assembled vignettes, The Man Who Mistook His Wife for A Hat, the famed neurologist Oliver Sacks (1985) introduced the notion that leisure physical activity has a beneficial impact or “liberating” (p. 102) effect on tic symptomatology in Tourette Syndrome (TS). Nevertheless, research on the impact of physical activity on TS symptomatology has been limited. Given the significant burden of TS, evaluating the influence of factors such as physical activity that can lead to tic attenuation is imperative, in terms of both understanding and implementing symptom management.

TS is a neurodevelopmental disorder characterized by the presence of involuntary motor and phonic tics that can be simple (e.g., blinking) or complex (Robertson, 2011). Diagnostic criteria for TS include multiple motor tics and one or more phonic tics lasting for at least 1 year (American Psychiatric Association, 2000; World Health Organization, 1992). While 10% of the TS population are “uncomplicated” cases, (i.e., comorbidity-free), the rest present with comorbid neuropsychiatric conditions or symptoms, the most common being attention-deficit hyperactivity disorder (ADHD) and obsessive-compulsive disorder (OCD). Depression and anxiety, among other problems, are also common (Robertson, 2011). Tic severity increases in early childhood to late adolescence and then decreases or remits into adulthood (Leckman et al., 1998). Tics tend to fluctuate or “wax and wane” in type and anatomical location, complexity, frequency, and intensity (S. Chang & Piacentini, 2002; Leckman & Cohen, 1999). There is a long-standing research and clinical consensus that variation in tic expression is attributed mainly to neurobiological factors (e.g., Baym, Corbett, Wright, & Bunge, 2008; Diler, Reyhanli, Toros, Kibar, & Avci, 2002; Gates et al., 2004; Jeffries et al., 2002; Kawohl, Bruhl, Krowatschek, Ketteler, & Herwig, 2009; Leary, Reimschisel, & Singer, 2007; Peterson, Skudlarski, et al., 1998; Peterson, Staib, et al., 2001; Swain, Scahill, Lombroso, King, & Leckman, 2007); however, it is becoming increasingly recognized that tic variability can also be attributed to contextual influences (i.e., environmental or intrinsic factors that can act either as antecedents or consequences to tics; Conelea & Woods, 2008).

Experimental manipulations of contextual factors have primarily employed tic suppression paradigms investigating the role of reinforcement in tic reduction (Himle & Woods, 2005; Himle, Woods, & Bunaciu, 2008; Himle, Woods, Conelea, Bauer, & Rice, 2007; Meidinger et al., 2005; Woods et al., 2008; Woods & Himle, 2004; Woods, Walther, Bauer, Kemp, & Conelea, 2009) or stress in tic exacerbation (Conelea, Woods, & Brandt, 2011). Other factors assumed to be moderating tics include intrinsic states such as premonitory urges (i.e., sensations preceding tics; Leckman, Walker, & Cohen, 1993; Woods, Piacentini, Himle, & Chang, 2005) and attentional resources (e.g., Conelea & Woods, 2008; Woods et al., 2008). Although the body of research is growing, experimental work on the relationship between tic frequency and contextual factors remains surprisingly scarce given the plethora of contextual factors that have been reported in descriptive studies to exacerbate or attenuate tics. According to a comprehensive review conducted by Conelea and Woods (2008), whereas factors such as anxiety or stress and fatigue have predominantly been associated with tic exacerbation, passive or relaxed states, concentration and physical activity, have been mostly reported to lead to tic attenuation. The implications of such findings are important, particularly if engagement in specific activities can lead to tic attenuation and in turn to alleviation of tic-related distress. Notably, the tic attenuation derived from physical activity or exercise is thought to result from automatic or effortless tic regulation. This contrasts with the tic suppression research paradigms and current behavioral therapies, such as habit reversal training (HRT; Azrin & Nunn, 1973; for a review see Himle, Woods, et al., 2006), Cognitive-Behavioral Intervention for Tics (CBIT; Piacentini et al., 2010; Wilhelm et al., 2012), and Exposure and Response Prevention (ERP; Verdellen, Hoogduin, & Keijsers, 2007), which focus on enhancing voluntary tic control ability.

The assumption that physical activity may aid in symptom management for a range of neurodevelopmental disorders associated with self-regulatory control problems has only been recently explored. The impetus for this line of research has been the accumulated multidisciplinary evidence indicating that aerobic exercise, when it involves flexible and goal-directed actions, can have beneficial effects on cognition and especially executive function across the life span (e.g., Barenberg, Berse, & Dutke, 2011; Chaddock et al., 2012; Tomporowski, Lambourne, & Okumura, 2011). Evidence from experimental and meta-analytic studies in children suggests that moderate to vigorous aerobic exercise can facilitate executive control, with effects seen both after chronic training (e.g., Davis et al., 2007; Hinkle, Tuckman, & Sampson, 1993) as well as after single bouts of exercise (e.g., Budde, Voelcker-Rehage, Pietrabyk-Kendziorra, Ribeiro, & Tidow, 2008; Y. K. Chang, Labban, Gapin, & Etnier, 2012; Ellemberg & St. Louis-Deschênes, 2010; Hillman et al., 2009; Pesce, Crova, Cereatti, Casella, & Bellucci, 2009). In addition, it has been suggested that the more cognitively demanding the exercise is, the greater impact there is on executive function (Best, 2010). A growing literature has also shown that higher levels of physical fitness have been associated with enhanced cognitive abilities and superior brain function in children (e.g., Chaddock, Erickson, Prakash, Kim, et al., 2010; Chaddock, Erickson, Prakash, VanPatter, et al., 2010; Chaddock, Hillman, Buck, & Cohen, 2011; Davis et al., 2011; Pontifex et al., 2011). Importantly, the execution of complex motor action requires recruitment of prefrontal corticostriatal neural circuitry, which also supports executive function (e.g., Diamond, 2009). Apart from changes in heart rate (HR; for example, Davranche, Burle, Audiffren, & Hasbroucq, 2005, 2006; Hillman, Snook, & Jerome, 2003; Kamijo et al., 2004), exercise-induced physiological changes at brain level (e.g., changes in cellular development and morphology; Churchill et al., 2002; Colcombe et al., 2006) have in turn been assumed to lead to cognitive improvements.

In line with these neurobiological changes, a few studies have shown post-exercise improvements in cognition in children with ADHD as well as behavioral improvements in core symptoms, including reduced impulsivity and inattentiveness levels (e.g., Archer & Kostrzewa, 2012; Gapin & Etnier, 2010; Gehan & Samiha, 2011; Medina et al., 2009; see also review by Gapin, Labban, & Etnier, 2011). To the best of the authors’ knowledge, there is only one published case report of a physical therapy evaluation with a child with TS, which reported not only the predicted post-exercise improvements in physical fitness and motor function but also the unexpected finding of a reduction in the child’s tic and urge severity (Liu et al., 2011).

Improved outcomes in several other aspects of mental health have also been found to be resulting from exercise, including reductions in psychological indices of anxiety and depressed mood as well as improvements in quality of life (e.g., Berger, 1996; Biddle, Fox, & Boutcher, 2000; Field, 2012). Acknowledging the limited number and methodological weaknesses of studies included in systematic reviews, meta-analyses have reported small-to-moderate effects of physical activity on depression and anxiety levels in adolescents aged 11 to 19 years (Larun, Nordheim, Ekeland, Hagen, & Heian, 2006) and 11 to 21 years (Calfas & Taylor, 1994). Interestingly, the reported exercise-induced effects of decreased depression and anxiety levels did not vary as a function of exercise intensity (Larun et al., 2006).

Aims of Current Study

The present study is the first attempt to experimentally assess the effect of acute aerobic exercise on tic expression in a group of young individuals with TS. Using a recently emerged videogame design (i.e., “exergame”; Best, 2010) that requires whole-body physical exertion while playing, we compared tic frequency rates during engagement in a physical activity task, kickboxing, with tic rates during pre-exercise (baseline) and post-exercise interview-based tasks. In light of the reported attenuating effects of exercise on tics (Conelea & Woods, 2008) and the limited empirical evidence suggesting that physical activity can result in reduced tics (Liu et al., 2011) and ADHD symptoms (e.g., Archer & Kostrzewa, 2012; Gapin & Etnier, 2010; Gehan & Samiha, 2011; Medina et al., 2009), the main hypothesis was that tic rates would be significantly reduced during the exercise session compared with baseline. Driven from reported findings of single-bout post-exercise effects on executive function, including self-regulatory control (Budde et al., 2008; Ellemberg & St. Louis-Deschênes, 2010; Hillman et al., 2009; Pesce et al., 2009), a second hypothesis was that tic rates would be significantly lower in the post-exercise interview session compared with baseline, reflecting a sustained effect of exercise on tic reduction.

Given the evidence showing enhanced executive function performance associated with higher cognitively demanding tasks (Best, 2010), an exploratory aim examined whether a physical activity session of increased difficulty level (hard) would lead to a reduction or an increase in tics relative to a less cognitively demanding (easy) physical activity session. We also wanted to explore whether tic ratings would correlate positively with perceived stress and anxiety levels at both baseline and during the exercise sessions, based on the assumption that stress has an exacerbating effect on tic expression (Conelea & Woods, 2008).

In light of evidence supporting the alleviating effects of exercise on depressed mood and anxiety levels and the global exercise-induced improvements in physical and psychological well-being (e.g., Berger, 1996; Biddle et al., 2000; Field, 2012), a secondary aim of this investigation was to determine whether exercise has a beneficial effect on self-reported well-being. It was therefore anticipated that after the exercise session, perceived levels of cheerfulness would be higher and anxiety levels would be lower than those reported at baseline. Finally, given the reported beneficial effects of physical fitness on well-being, we intended to explore whether physical activity levels would correlate with self-report measures of physical and psychological well-being, including mood and stress measures.

Method

Participants

A total of 18 young participants with “uncomplicated” TS (13 male/5 female), aged 10 to 20 years (M age = 14.48; SD = 2.47; range = 10.60-20.1) took part in the study (see Table 1 for participant characteristics). Participants were recruited through the U.K. charity Tourettes Action (TA). Clinical diagnosis of TS and absence of comorbid disorders was confirmed in writing by the participants’ general practitioner, pediatrician, or psychiatrist. Guided by the evidence that TS symptoms peak early in the second decade of life (Leckman, 2002; Robertson, 2011), age exclusion criteria included a lower cutoff of 10 years and a higher cutoff of 20 years (oldest participant included in the study was 20.1 years; see Table 1) to include any late-onset cases with TS. Other exclusion criteria included the following: a clinical diagnosis of a comorbid psychiatric or mental disorder (e.g., ADHD or OCD), serious physical illness or handicaps, major neurological disease, and presence of severe learning disabilities.

Table 1.

Participant Characteristics.

			Tic severity^a			Pattern of current tics^b
Participant number	Sex (M/F)	Age (y/m)	Global	Motor	Phonic	Presence of complex tics (yes/no);	presence and characteristics of motor and phonic tics
1	M	16.4	53	24	9	Yes	Motor: Eye blinking, eye movement/closure, facial grimacing, mouth movement, head tilting, shoulder shrugging/gyrating, waist gyrating, hand movement Phonic: Throat clearing
2	M	12.9	40	18	12	Yes	Motor: Eye blinking, eye rolling, eye wide-opening, head tilting, shoulder stretching, waist/back gyrating, nose twitching, mouth/tongue movements, facial grimacing Phonic: Grunting (with “ah” sound)
3	F	13.0	22	12	0	No	Motor: Eye blinking, eye rotating, eye wide-opening/eyebrow raising, head tilting, nose twitching, mouth movement, facial grimacing Phonic: None
4	M	15.6	32	13	9	Yes	Motor: Eye blinking, eye movement/upward or to the side, eye wide-opening/eyebrow raising, nose twitching, mouth movement, neck tensing, facial grimacing Phonic: Coughing
5	F	10.6	50	16	14	Yes	Motor: Eye blinking, eye darting/scanning, eye wide-opening/eyebrow raising, nose witching, mouth movement, rotating (when eye scanning), head shaking/tensing, neck tensing Phonic: Gulping
6	F	16.6	78	24	24	Yes	Motor: Eye blinking, mouth/tongue movements, body clicking, abdominal tensing, pulling clothes, bouncing on chair, hair flipping, copropraxia Phonic: High-pitch screeching, muttering, coprolalia
7	M	10.8	19	9	0	No	Motor: Eye blinking, eye movement/closure, eye wide-opening/eyebrow raising, mouth movement, frowning, head shaking, shoulder shrugging Phonic: None
8	M	13.5	31	12	9	No	Motor: Eye blinking, eye movement/closure, eye wide-opening/eyebrow raising, mouth movement, frowning, head shaking, shoulder shrugging Phonic: None
9	M	17.10	44	13	11	No	Motor: Eye blinking, eye movement/closure, eye wide-opening/eyebrow raising, frowning, mouth movement, head shaking, shoulder shrugging Phonic: None
10	F	16.11	73	21	22	Yes	Motor: Eye blinking, eye movement/closure, mouth movement, head shaking, neck tensing, abdominal tensing, Phonic: Grunting
11	M	16.8	57	19	18	Yes	Motor: Eye blinking, eye movement/closure, eye wide-opening/eyebrow raising, eye rolling, eye rotating, mouth/tongue, movement Phonic: None
12	M	15.9	34	12	12	No	Motor: Eye blinking, eye movement/closure, eye rolling, mouth movement, head tilting Phonic: Coughing, sniffing, grunting
13	M	13.0	42	16	16	Yes	Motor: Eye blinking, eye wide-opening/eyebrow raising, mouth movement, head tilting, arm/hand movement, brushing hair Away Phonic: Low-pitch screeching, coughing, throat clearing
14	M	13.7	44	20	14	Yes	Motor: Eye blinking, eye rolling, eye movement/upward or to the side, mouth movement, facial grimacing, head tilting, shoulder shrugging, hand movement Phonic: Grunting
15	F	12.9	32	12	0	No	Motor: Eye blinking, eye wide-opening/eyebrow raising, nose twitching, mouth movement, facial grimacing, head shaking Phonic: None
16	M	12.11	66	21	15	Yes	Motor: Eye movement/closure, eye wide-opening/eyebrow raising, mouth/tongue movements, frowning, facial grimacing, head tilting, hand movements, lip pulling (with hand) Phonic: Coughing/throat clearing
17	M	20.10	56	18	18	Yes	Motor: Winking, head movement/upward or downward, head shaking, mouth/tongue movements, nose twitching, facial grimacing, hand movements, copropraxia Phonic: Saying words (e.g., “aha”), palilalia, coprolalia
18	M	13.5	60	21	19	Yes	Motor: Eye blinking, eye movement/closure, eye wide-opening/eyebrow raising, mouth movement, facial grimacing, head tilting, shoulder shrugging Phonic: Grunting (with “eh” sound)

Note. All participants exhibited on the day their current major tics as identified on the Yale Global Tic Severity Scale.

Tic severity as indexed by Global scores and Motor and Phonic subscale scores on the Yale Global Tic Severity Scale (Leckman et al., 1989).

Pattern of current tics as exhibited on the day of the testing session.

Apart from a clinical diagnosis of TS, inclusion criterion was a minimum of one discernible tic per minute (e.g., Himle, Chang, et al., 2006). Participants underwent a clinical assessment interview on the day of their testing session. Twelve of the 18 participants displayed complex tic patterns in addition to simple motor and/or phonic tics. Of the 18 participants, 6 were on medication, 4 were on clonidine (Participants 8, 11, 17, and 18), 3 on aripiprazole (Participants 1, 6, and 18), and 1 on risperidone and sertraline (Participant 6).

The study was approved by the University of Nottingham Medical School Ethics Committee, in accordance with the ethical standards specified in the 1964 Declaration of Helsinki. Written consent and assent was provided by parents/carers and participants, after they were informed about the nature of the study. Parents/carers and participants were informed prior to the session that they could withdraw from the study at any time without affecting receipt of their inconvenience allowance. All participants completed the full session and upon completion parents/carers received £10 to cover travel expenses, while participants received an inconvenience allowance of £10 in shopping vouchers.

Materials and Testing Equipment

Assessment

Clinical measures of symptom severity administered on the day of the session included the following:

The Yale Global Tic Severity Scale (YGTSS; Leckman et al., 1989) is used to rate the type, frequency, duration, intensity, and complexity of motor and vocal tics, and also provides an overall impairment score and a global (motor + vocal + overall impairment) tic severity score. Good psychometric properties have been reported for the use of YGTSS in children and adolescents with TS, including internal consistency, convergent validity and association with clinician ratings of TS impairment (Leckman et al., 1989; Storch, Murphy, Geffken, Sajid, & Allen, 2005).

The Children’s Yale–Brown Obsessive-Compulsive Scale (CY-BOCS; Scahill et al., 1997) is a 10-item obsession-compulsion screening scale, each item rated from 0 (no symptoms) to 40 (extreme symptoms); it includes questions on the amount of time the patient spends on obsessions and compulsions, the amount of distress they experience and the extent to which they can exert control over such thoughts. It has been well validated in children and adolescents with OCD, demonstrating high internal consistency for the total CY-BOCS score as well as good convergent and divergent validity (Scahill et al., 1997; Storch et al., 2006).

In addition, an estimate of general cognitive ability was administered using the following:

The Wechsler Abbreviated Scale of Intelligence (WASI-II; The Psychological Corporation, 1999), two-subset form: vocabulary testing and matrix reasoning, yielding a full scale IQ score. The WASI-II has excellent internal consistency and inter-rater and test–retest reliability (Garland, 2005).

Patient- and Parent-rated Questionnaires

A short physical activity readiness assessment was used as a mandatory screen to check that participation in exercise should not pose any problems to the young person’s physical health.

The Social Communication Questionnaire (SCQ; Rutter, Bailey, & Lord, 2003) provides screening for autism spectrum disorders; the lifetime form used in the present study consists of 40 yes or no questions focusing on the child’s developmental history. The SCQ has been widely used with both adults and children and has shown fairly good psychometric properties, including high convergent validity and increased sensitivity and specificity (Berument, Rutter, Lord, Pickles, & Bailey, 1999; Chandler, Charman, Baird, & Simonoff, 2007; Charman et al., 2007).

The Conners–3rd Edition–Parent (CONNERS; Conners, 2008) assesses the likelihood of whether a child has ADHD or ADHD-related problems by including questions on home, social, and school life; the Global Index total score was included in the present study. The authors report high internal consistency and test–retest validity and good discriminative and construct validity.

The Strengths and Difficulties Questionnaire (SDQ; Goodman, 1997) contains 25 items that are grouped around the following psychological attributes: emotional symptoms, conduct problems, hyperactivity/inattention, peer relationship problems and pro-social behavior. The sum of the scores on the first four attributes makes up a Total Difficulties score that provides an estimate of psychological adjustment and psychopathology. Studies with clinical and non-clinical samples have established satisfactory reliability and validity for use of this measure with children and adolescents (Goodman, 2001).

The Physical Activity Questionnaire for Adolescents (PAQ-A; Kowalski, Crocker, & Kowalski, 1997) is a nine-item questionnaire that measures moderate to vigorous physical activity levels during the school year, with a 7-day recall. It has shown good internal consistency and test–retest reliability, and satisfactory validity (Janz, Lutuchy, & Levy, 2008; Kowalski et al., 1997).

The Depression Anxiety Stress Scales (DASS; S. H. Lovibond & Lovibond, 1995) used in this study are made up of 21 items (short version), each rated on a 4-point Likert-type scale that assesses the degree of depression, anxiety and tension or stress symptoms over the last week; scores range from 0 = did not apply at all to 3 = apply to them most of the time. Although the DASS scales have been validated for use with clinical and non-clinical adult populations (P. F. Lovibond, 1998; S. H. Lovibond & Lovibond, 1995; Taylor, Lovibond, Nicholas, Cayley, & Wilson, 2005), there is limited evidence for their validity in adolescent populations (Szabo, 2010; Tully, Zajac, & Venning, 2009; Willemsen, Markey, Declercq, & Vanheule, 2010). Nevertheless, the scale was chosen for its brief administration time and its advantage over other scales for its inclusion of three dimensions of negative emotionality (S. H. Lovibond & Lovibond, 1995) and was completed with the help of the parent/carer to minimize any comprehension difficulties.

The KIDSCREEN-52 quality-of-life measure for children and adolescents (KIDSCREEN-52 HRQoL; Ravens-Sieberer et al., 2005) assesses children’s and adolescents’ subjective health and well-being, with a 7-day recall, on a 5-point Likert-type scale ranging from 1 = never to 5 = always; the questionnaire is categorized into 10 HRQoL subscales, 2 of which (included in the present study) are physical and psychological well-being. Psychometric results from a cross-cultural survey in 13 European countries indicate acceptable levels of reliability and validity (Ravens-Sieberer et al., 2008).

The Perceived Stress Scale–10 (PSS-10; Cohen, Kamarck, & Mermelstein, 1983) is a 10-item questionnaire designed to measure, on a Likert-type scale, ranging from 0 = never to 4 = very often, the extent to which an individual perceives certain life situations as stressful. The PSS-10 has demonstrated adequate reliability and has shown satisfactory validity when compared with stressful life events and negative affect (Cohen et al., 1983; Cohan, Tyrrell, & Smith, 1993).

Patient ratings

The Pictorial Children’s Effort Rating Table (PCERT; Eston et al., 1994) has been validated for use in children and adolescents for perceived effort estimation and production (Yelling, Lamb, & Swaine, 2002). It uses a numerical scale from 1 to 10, and pictographs to represent the corresponding perceived exertion levels, as an index of perceived tiredness, with Level 1 being very, very easy, Level 5 starting to get hard, and 10 so hard I’m going to stop.

The Mood Sheet was a devised Likert-type scale containing the following two questions: (a) “How anxious are you feeling at the moment?” and (b) “How cheerful are you feeling at the moment?” Participants rated their responses on a scale ranging from 1 = not at all cheerful/anxious to 10 = extremely cheerful/anxious.

Testing equipment

The exercise session was delivered through the X-Box 360 Kinect, using the kickboxing exercise-based routine included in the “Your Shape” DVD, projected through a 23-inch Full HD 1080p Samsung widescreen LCD monitor. This mode was well suited for use with video-based recordings; it ensured that participants’ face and upper body would face the camera most of the time as participants had to follow the instructions of the virtual coach on the screen and remain in the target space to engage in the appropriate execution of the desired kickboxing movements. A SONY DCR-DVD150E digital video-camera recorder was placed at a 2-m distance from the point where the participant stood (while performing the physical activity session) or sat (during the pre- and post-exercise interviews). Participants were also fitted with a transmitter belt of a polar FT7 Heart Rate Monitor (Electro, Finland), which measured the average HR per minute throughout the whole session.

Data Collection and Analysis Procedures

Session recordings

All sessions took place in a U.K. University hospital (Queen’s Medical Centre, Nottingham) and lasted 2 to 2.5 hr including breaks. The session recording started with participants engaging in a clinical assessment interview that included administration of the YGTSS, the CY-BOCS, and the WASI. This was followed by a non-clinical pre-exercise interview (approximately 45 min after the participants’ arrival) that included the administration of the PAQ-A and questions about hobbies and other leisure activities. On completion of the pre-exercise interview session, participants rated their perceived tiredness, anxiety, and mood levels on the designated scales (i.e., PCERT and Mood Sheet; in Materials section).

Prior to the exercise session, participants had the chance to practice some of the kickboxing routine (2-3 min) before they started the first session, which was always the “easy” exercise session, followed by the second or “hard” session. This order was maintained to optimize training adaptation, that is, muscle preparation and skills development. Although both sessions were of moderately vigorous intensity, the second session was more cognitively demanding in that it required greater coordination and speed. Each exercise session lasted approximately 5 min and there was a break (approximately 2 min) between them. At the end of each session, participants were asked to rate their perceived tiredness, anxiety, and mood levels. Following the exercise session (approximately 30 min after the end of exercise), participants engaged in a post-exercise interview session about their impressions of the task and their associated feelings. In addition, perceived tiredness, anxiety, and mood ratings were recorded. At the end of the post-exercise session, participants were debriefed and thanked for their participation.

Tic coding procedure

Tic classification and counting was performed using a professional video-editing tool (Ultimate Corel VideoStudio Pro x4) that allowed the marking of tics as logged events with a start and end time. Importantly, such software allows the “playback” of tic occurrences so that even subtle tics or components of complex tics could be detected in slow or repeated “playback” motion. A continuous 5-min time segment was sampled from the pre-exercise, exercise, and post-exercise sessions. Baseline tic frequency was assessed during the non-clinical pre-exercise interview rather than the clinical interview, to avoid the issue of tic-related conversation elevating tic frequencies (O’Connor, Brisebois, Brault, Robillard, & Loiselle, 2003; Silva, Munoz, Barickman, & Friedhoff, 1995; Woods, Watson, Wolfe, Twohig, & Friman, 2001). Motor and vocal tics were counted and averaged per minute for each 5-min segment for each condition, in accordance with previous protocols (e.g., Himle, Chang, et al., 2006). A second rater independently counted 24% of observation segments (see “Results” section).

Results

Participant Scores on Physical and Psychological Measures

Table 2 contains the initial scores on all physical and psychological measures. Of particular note, the mean global YGTSS score was 46.28 (SD = 16.73; range = 19-78), indicating moderate tic severity in the group as a whole. Notably, although participants only had a clinical diagnosis of TS, the group means indicated elevated levels of ADHD (CONNERS) symptomatology (M = 66.83, SD = 16.08).

Table 2.

Participant Scores (M ± SD) on Measures of Clinical Symptomatology, Psychological Functioning, and Physical Fitness.

Measure	Minimum	Maximum	M (SD)
BMIa	10.60	30.52	20.91 (4.85)
PAQ Physical activity levelb	1.40	4.27	2.49 (0.86)
YGTSS Global tic severityc	19.00	78.00	46.28 (16.73)
WASI Intellectual functioning (t scores)d	76.00	120.00	99.50 (12.03)
SDQ Strengths and difficultiese	4.00	28.00	13.17 (7.25)
SCQ Social communication–autistic symptom severityf	.00	10.00	4.56 (3.09)
CONNERS Attention-hyperactivity symptom severityg	40.00	90.00	66.83 (16.08)
CY-BOCS Obsessive-compulsive symptom severityh	.00	21.00	6.22 (7.08)
DASSi Stress	2.00	16.00	7.00 (3.63)
Anxiety	.00	8.00	3.00 (2.85)
Depression	.00	14.00	2.22 (4.04)
PSSj Perceived Stress	8.00	34.00	19.17 (5.89)
KIDSCREENk Physical well-being	29.63	64.30	48.17 (9.00)
Psychological well-being	28.36	68.49	50.27 (11.24)

Note. BMI = Body Mass Index; PAQ = Physical Activity Questionnaire; YGTSS = The Yale Global Tic Severity Scale; WASI = The Wechsler Abbreviated Scale of Intelligence; SDQ = Strengths and Difficulties Questionnaire; SCQ = Social Communication Questionnaire; CONNERS = Conners–3rd Edition; CY-BOCS = Children’s Yale–Brown Obsessive-Compulsive Scale; DASS = Depression Anxiety Stress Scale; PSS = Perceived Stress Scale.

Body mass index categories: Underweight ≤ 18.5; Normal weight = 18.5-24.9; Overweight = 25-29.9; Obesity ≥ 30.

A score of 1 indicates low physical activitywhereas a score of 5 indicates high physical activity levels.

A global tic severity score is the summation of the total motor tic score, total phonic tic score and overall impairment rating; range = 0-100, with higher scores indicating greater frequency/severity of symptoms.

Classifications (t scores): Extremely low ≤ 70; borderline = 70-79; low average = 80-89; average = 90-109; high average = 110-119; superior ≥ 120.

Total Difficulties score: Normal = 0-15; Borderline = 16-19; Abnormal = 20-40.

Lifetime Form-range = 0-39, with higher scores indicating greater frequency/severity of symptoms; A cutoff score of ≥ 15 indicates possible Autistic Spectrum Disorder.

Parent-rated Global Index Total score: Classifications (t scores): average ≤ 60; mildly atypical = 61-65; moderately atypical = 66-70; markedly atypical ≥ 70.

Severity rating range = 0-40: subclinical = 0-7; mild = 8-15; moderate = 16-23; severe = 24-31; extreme = 32-40.

Stress severity rating: normal = 0-14; mild = 15-18; moderate = 19-25; severe = 26-33; extremely severe ≥ 34 Anxiety severity rating: normal = 0-7; mild = 8-9; moderate = 10-14; severe = 15-19; extremely severe ≥ 20 Depression severity rating: normal = 0-9; mild = 10-13; moderate = 14-20; severe = 21-27; extremely severe ≥ 28.

Severity rating range = 0-40, with higher scores indicating greater symptom frequency/severity.

Severity ratings for Physical well-being, Psychological well-being (t scores): below average ≤ 29; average = 40-69; above average ≥ 80.

Tic Ratings

Tic frequency scores during the exercise session and during the pre- and post-exercise interviews were subjected to a repeated-measures ANOVA, with condition (pre-exercise interview, exercise session, post-exercise interview) as the within-subjects factor. Results showed that tic occurrence significantly differed across the different types of sessions, F(2) = 12.99, p < .001, $η_{p}^{2}$ = .517 (see Figure 1 for mean tic rates per condition).

Figure 1.

Mean tic rates during the pre-exercise (M = 20.44, SD = 17.08) and post-exercise (M = 16.05, SD = 15.58) interviews; and during the easy-exercise (M = 4.93, SD = 6.03) and hard-exercise (M = 7.11, SD = 7.66) sessions.

To test the a priori hypotheses that tic rate would be significantly reduced during the exercise session compared with baseline, that is, during the pre-exercise interview as well as during the post-exercise interview compared with baseline, post hoc paired t tests were performed. Effect sizes were calculated using Cohen’s d and were corrected for dependence between means using Morris and DeShon’s (2002) equation. The mean tic rate during the exercise session (M = 6.05, SD = 6.64) was significantly lower than that shown during the pre-exercise interview (M = 20.44, SD = 17.08), t(17) = 4.24, p = .001, d = 1.299, indicating that exercise had an attenuating effect on tic expression (Note: One participant did not show a tic reduction while two participants showed 100% tic reduction in the exercise session vs. baseline comparison). Tic frequency in the post-exercise interview (M = 16.05, SD = 15.58) was significantly higher than in the exercise session, t(17) = 3.203, p = .005, d = .935, but the mean tic rate during the post-exercise session was significantly lower than at baseline, t(17) = 2.24, p = .039, d = .536, in support of our hypothesis that tic frequency would remain below baseline following exercise.

To explore whether task difficulty would have a differential impact on tic expression, tic rate during the easy-exercise session was compared with tic rate during the hard-exercise condition; it was found that the hard session produced a significantly higher mean number of tics (M = 7.11, SD = 7.66) relative to the easy session (M = 4.93, SD = 6.03), t(17) = 2.53, p = .022, d = .661. When compared separately, tic rates during the pre-exercise interview were significantly higher than during either the hard-exercise, t(17) = 4.17, p = .001, d = 1.263, or easy-exercise, t(17) = 4.26, p = .001, d = 1.258, sessions. Therefore, the finding that level of difficulty may play a role in tic expression during exercise—that is, the harder the level of difficulty, the higher the tic rate—does not influence our main expectation that exercise would attenuate tic frequency.

Given the uneven distribution of tic data across participants (e.g., high SDs), we also used non-parametric statistical methods to test the above hypotheses and obtained similar results to the parametric statistical estimates.

Inter-rater reliability

Inter-rater reliability was calculated based on procedures used in previous studies (e.g., Himle, Chang, et al., 2006; Piacentini et al., 2006; Woods et al., 2009). Twenty-four percent of all the conditions were sampled and scored by an independent rater (G.M.J.), who had received training in the observation and coding procedures by the main coder (E.N.), using an interval-sampling procedure established in previous studies (e.g., Himle et al., 2006; Piacentini et al., 2006; Woods et al., 2009). The 5-min video-recorded segments in each condition were divided into 10-s intervals, noting the number of tics detected by each observer. Inter-rater agreement was established at 87% (range = 76%-89%) indicating acceptable reliability.

Other Ratings

Physical exertion

To check physical exertion levels, mean HR as indexed by beats per minute (BPM) registered on a HR monitor and subjective ratings of perceived tiredness were obtained. Based on their age-adjusted maximum HR (male maximum HR = 220 − age; female maximum HR = 226 − age), 12 participants performed at 51% to 63% of their estimated maximum HR, while the rest performed at a submaximal 43% to 49% of their maximum HR intensity (collapsed across both exercise sessions). Compared with mean HR at baseline (M = 79.78, SD = 8.40; minimum = 63, BPM maximum = 89 BPM), mean HR measurements obtained during the easy-exercise session (M = 103.94, SD = 12.85; minimum = 89 BPM, maximum = 129 BPM), t(17) = 7.36, p < .001, d = 1.789, and the hard-exercise session (M = 108.72, SD = 10.44; minimum = 93 BPM, maximum = 128 BPM), t(17) = 10.78, p < .001, d = 2.567, were significantly higher, reflecting the change in the physical effort exerted in the exercise-based task relative to the seat-based interview. HR was significantly increased during the hard-exercise session compared with the easy session, t(17) = 2.70, p = .015, d = .668. Mean HR at the post-exercise interview (M = 82.72, SD = 7.28; minimum = 66 BPM, maximum = 89 BPM) was decreased relative to the exercise session, although it was found to be significantly higher than that at baseline, t(17) = 3.26, p = .005, d = .800. Finally, exercise was shown to have a similar effect on tic frequency whether participants performed at maximal or submaximal HR intensity, F(1, 16) = 2.89, p = .109, ns.

Perceived exertion ratings (PCERT) were significantly higher toward the end of the session, that is, in the post-exercise interview (M = 6.72, SD = 1.44) compared with baseline (M = 3.14, SD = 1.33), t(17) = 8.90, p < .001, d = 2.092. PCERT mean scores at baseline indicated that participants felt the task at hand was “easy” (Level 3). PCERT ratings were higher for the hard- (M = 6.44, SD = 1.54) than the easy- (M = 4.83, SD = 1.63) exercise session, t(17) = 7.09, p < .001, d = 1.679, as a result of increasing task difficulty. Perceived tiredness was significantly higher than baseline at the end of both the easy-, t(17) = 4.13, p = .001, d = .978, and the hard-, t(17) = 9.31, p < .001, d = 2.207, exercise sessions, hence reflecting participants’ increased physical exertion levels during the exercise sessions.

Psychological and physical well-being

Ratings of perceived cheerfulness were found to be significantly higher following exercise (i.e., during the post-exercise interview) than at baseline, t(17) = 3.66, p = .002, d = .869, indicating that exercise had a beneficial effect on mood, an effect which was also shown at the end of both the easy-, t(17) = 3.61, p = .002, d = .875, and the hard-, t(17) = 4.93, p < .001, d = 1.232, exercise sessions (see Figure 2a). Likewise, as shown in Figure 2b, exercise was shown to have a beneficial effect on self-reported anxiety levels, leading to significantly reduced anxiety ratings at the end of both the easy-, t(17) = 3.93, p = .001, d = .942, and the hard-, t(17) = 4.47, p < .001, d = 1.256, exercise sessions, an effect that was retained toward the end of the testing session (i.e., at the post-exercise interview), t(17) = 4.49, p < .001, d = 1.312.

Figure 2.

Self-reported ratings of (a) mood (i.e., cheerfulness) and (b) anxiety levels at baseline (i.e., during the pre-exercise interview), at the end of the easy- and hard-exercise sessions and at the post-exercise interview.

Interestingly, mean tic ratings during the exercise session correlated with perceived stress (PSS-10) scores (r = .508, p = .031), as well as with perceived anxiety ratings reported at the end of both easy- (r = .620, p = .006) and hard- (r = .518, p = .027) exercise sessions. However, this relationship between tic frequency and perceived state as well as long-term anxiety was not found to be significant at baseline. Perceived stress scores on PSS-10 also correlated negatively with psychological well-being scores on the KIDSCREEN-52 (r = −.558, p = .016). Moreover, global YGTSS tic severity correlated with stress (r = .734, p = .001) and depression (r = .620, p = .006) DASS scores, indicating a likely long-term relationship between tic severity and stress and depressed mood.

In exploring the potential relationship between general physical fitness and tic severity, PAQ-A scores reflecting physical activity levels did not show a significant correlation with tic severity on the YGTSS (r = −.191, p = .448). However, PAQ-A scores correlated negatively with body mass index (BMI) measurements (r = −.618, p = .006) and BMI measurements correlated positively with global (r = .472, p = .048) and motor (r = .540, p = .021) YGTSS tic severity, as well as with age (r = .569, p = .014). BMI measurements also correlated with stress (r = .477, p = .045) and depression (r = .478, p = .045) DASS scores, implicating an indirect relationship between BMI fitness level and tic, stress, and depression symptomatology. Finally, a significant relationship between physical fitness on the PAQ-A and physical well-being on the KIDSCREEN-52 (r = .484, p = .042) depicted the expected physical benefits of physical fitness too.

Discussion

The present findings provide novel empirical data demonstrating the beneficial effect of an acute bout of exercise on TS symptomatology in a lab-based controlled setting. Using an exergame that engaged young participants with “uncomplicated” TS in moderately vigorous aerobic exercise, we observed that tic frequency rates during the exercise-based session were significantly reduced compared with baseline. These results are consistent with the self/parental reports of attenuating effects of physical activity on tics (Eapen, Fox-Hiley, Banerjee, & Robertson, 2004; O’Connor et al., 2003; Robertson, Banerjee, Eapen, & Fox-Hiley, 2002; see Conelea & Woods, 2008, for a review) and provide additional empirical evidence to the limited literature showing exercise-induced symptom reductions in TS (Liu et al., 2011) as well as ADHD (e.g., Archer & Kostrzewa, 2012; Gapin & Etnier, 2010; Gehan & Samiha, 2011; Medina et al., 2009). We also demonstrated that tic frequency rates were lower in a post-exercise session than at baseline, indicating that tic rates remained decreased (for approximately 30 min) after the end of the exercise session, hence reflecting a sustained effect of exercise on tic reduction that might have important clinical implications.

There are a number of possible explanations for the present findings. First, based on experimental evidence that acute as well as chronic participation in moderately vigorous aerobic exercise can facilitate superior executive control functions in children and adults (e.g., Chaddock, Erickson, Prakash, Kim, et al., 2010; Colcombe & Kramer, 2003; Etnier, Nowell, Landers, & Sibley, 2006; Hillman et al., 2009; Pontifex et al., 2011; Tomporowski, Davis, Miller, & Naglieri, 2008; Tomporowski, 2003), it is possible that tic reduction was brought about by a transient activation of executive control circuits through exercise. A second, and perhaps related, explanation is that the chosen task operated as a distraction task, taking attention (e.g., focus on premonitory urges) away from the tics and therefore leading to tic reduction due to the execution of an alternative purposeful movement. A third possibility is that exercise may function as a competing motor response to tics. Current clinical therapies successfully achieving tic reduction, such as HRT and CBIT (Piacentini et al., 2010; Wilhelm et al., 2012), similarly involve performing motor actions to replace tics; however, specific antagonistic actions are trained to interrupt or inhibit specific tics (Azrin & Nunn, 1973; Azrin & Peterson, 1990; Woods & Miltenberger, 1995). In this respect, an exercise component involving purposeful motor action that is not aimed at replacing specific tics may be a useful adjunction to such behavioral treatments. Exploring ways in which this could be successfully achieved would potentially lead to enhanced treatment benefits for individuals with TS, particularly for those whose tics are not easy to target with a specific antagonistic response or are not preceded by a premonitory urge.

In manipulating task difficulty, we found that the hard-exercise session produced higher tic rates than the easy-exercise session, contrary to the presumed intensity-related superior effects of aerobic exercise on executive function (Best, 2010). However, a plausible explanation could be that the observed tic patterns during the hard task may have been modulated by other contextual factors, such as increased concentration demands, or accumulated stress or fatigue levels, which notably have been shown to exacerbate tics (see Conelea & Woods, 2008, for a review). Because the hard-exercise session always followed the easy session—to ensure optimal muscle preparation and skill adaptation—the differential impact of the two tasks on tic expression is difficult to establish.

Participants’ self-reported anxiety and mood ratings were significantly improved following both exercise tasks, compared with baseline, and remained improved at the end of the session (post-exercise interview), despite accumulated levels of perceived tiredness. These findings are in line with previous reviews and meta-analytic studies showing that physical activity can reduce depressive symptoms as well as anxiety levels (Field, 2012; Jerstad, Boutille, Ness, & Stice, 2010; Larun et al., 2006). However, the decreased levels of anxiety and increased levels of mood toward the end of the session could also reflect elevated levels of cheerfulness due to the ending of the session or habituation to the environment, especially in light of evidence that context familiarity plays a role in tic attenuation (Conelea & Woods, 2008). Given the concurrent tic attenuation at the end of the session, it is unclear whether an acute bout of physical activity has an attenuating effect on tics that is independent of the observed reductions in anxiety or mood elevation. These relationships could be better explored in future research that uses a covariate approach to examine tic frequency as a function of anxiety and mood severity. Notably, global (YGTSS) tic severity scores correlated with both stress and depression (DASS) scores indicating a likely relationship between anxiety and depressive symptoms and tic severity, as previously suggested (Lewin et al., 2011). Also, tic frequency during the exercise sessions correlated positively with state anxiety ratings obtained at the end of each exercise session, in line with a purported tic and stress relationship (Conelea et al., 2011).

The significant correlations between BMI measurements and tic, stress, and depression symptomatology point toward a potential relationship between physical fitness and TS symptomatology. Not surprisingly, perceived long-term stress (PSS) scores correlated negatively with scores on psychological well-being measures, reflecting the detrimental effect of stress on general well-being (e.g., Cooper, 2009), while PAQ-A physical fitness level correlated positively with physical well-being scores on a quality of life questionnaire (KIDSCREEN-52) showing the impact of physical activity on physical health. Such exercise-induced health-related benefits involving both physical and psychological well-being, coupled with exercise-induced improvements in clinical symptomatology, highlight the likely global beneficial effects of physical activity in TS; however, the aforementioned correlations should be treated with caution given the limitations of the present study.

Finally, the limited power of our study did not allow us to explore whether medication effects or age differences may have contributed to the pattern of the present findings. In any context, it is crucial that future studies use controlled designs with bigger samples to further examine the potential impact of such factors on the mediating relationship between exercise and tic expression, also considering other potentially important conditions such as comorbidity and tic complexity. Future research aiming at an improved understanding of the mechanisms involved in exercise-induced benefits in young people with TS may ultimately lead to the development of efficient exercise-based programs that can be applied in clinical settings, either as an alternative intervention, or in conjunction with current behavioral therapies.

Footnotes

Acknowledgements

A special thank you goes to all the young participants and their families who took part in this study. We also wish to thank Jane Fowlie, our dedicated research nurse, for her valuable help throughout this project.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research was funded by a grant awarded to Tourettes Action from the Big Lottery Fund, UK [C1677A1405].

Author Biographies

Elena Nixon recently took up a lectureship in applied neuropsychology at Nottingham University, United Kingdom, following a PhD award and subsequent research and teaching posts in psychiatry. Her current research interests focus on the impact of behavioral interventions on clinical symptomatology and executive function, mainly in depressive and neurodevelopmental disorders.

Cris Glazebrook initially took up a lectureship in behavioral sciences in the School of Nursing at Nottingham University, United Kingdom, after receiving a PhD award in child health psychology. She is now professor of health psychology and her research work focuses on promoting physical activity and well-being in children at risk of mental or chronic health conditions as well as in children with neurodevelopmental disorders.

Chris Hollis completed his PhD at the Institute of Psychiatry in London, United Kingdom, and is now professor of child and adolescent psychiatry at Nottingham University, United Kingdom. He is a lead clinician for the Developmental Neuropsychiatry service at Nottingham University Queen’s Medical Centre, with special research interests in neurodevelopmental disorders and psychopharmacology.

Georgina M. Jackson completed her PhD in psychology at Sheffield University, United Kingdom, and is now professor of cognitive neuropsychology at Nottingham University, United Kingdom. Her research expertise lies in the study of the development of self-regulation, the associated behavioral and brain level changes and how these are affected by intrinsic and environmental factors in neurodevelopmental disorders, particularly in Tourette syndrome.

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