The purpose of this preliminary study was to examine whether an aquatic exercise intervention that involves both aerobic and coordinative exercises influences restraint inhibition in children with ADHD. Thirty participants were assigned to either an aquatic exercise or a wait-list control group. Participants were assessed by Go/Nogo Task and motor ability prior to and after an 8-week exercise intervention (twice per week, 90 min per session) or a control intervention. Significant improvements in accuracy associated with the Nogo stimulus and the coordination of motor skills were observed over time in the exercise group compared with the control group. Only main effects of group were found for reaction time and accuracy associated with the Go stimulus. These findings suggest that an exercise program that involves both quantitative and qualitative exercise characteristics facilitates the restraint inhibition component of behavioral inhibition in children with ADHD.

Introduction

Attention/deficit hyperactivity disorder (ADHD) is a common childhood neurobehavioral disorder that is typically characterized by inattention, overactivity, and impulsiveness (Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision [DSM-IV-TR]; American Psychiatric Association, 2000). Symptoms of ADHD are related to functional impairments in social interaction, family, and academic settings, as well as the presence of multiple comorbid disorders. ADHD has a prevalence of ∼7.2% in school-aged children between 4 and 17 years of age, resulting in a high social burden with a cost of up to $52 billion per year in the USA (Visser, Bitsko, Danielson, Perou, & Blumberg, 2010).

Based on a prominent top-down model proposed by Barkley (1997), it has been argued that behavioral inhibition is the primary deficit underlying dysfunction in ADHD and causes deficits in sustained attention and executive functions. Specifically, ADHD is negatively related to multiple subcomponents of behavioral inhibition such as restraint inhibition (i.e., success in withholding motor actions before a response occurs) and cancellation inhibition (i.e., success in withholding motor actions during a response; Schachar et al., 2007). Deficient inhibition has recently been negatively linked to brain structures and neural networks. Specifically, compared with normal peers, children with ADHD have been found to show smaller prefrontal and basal ganglia volumes, corresponding to interference control and response inhibition, respectively (Halperin & Healey, 2011). Decreased activation in the fronto-striatal region, the network between the prefrontal area and the basal ganglia, has also been reported (Booth et al., 2005). Additionally, although the activations of restraint and cancellation inhibition share similar networks (e.g., the inferior frontal cortex, dorsal anterior cingulate cortex), restraint inhibition exhibits bilateral/more activation of several brain regions (e.g., the dorsolateral prefrontal cortex and inferior parietal cortex; Eagle, Bari, & Robbins, 2008) and therefore receives particular emphasis in the present study.

Recent research indicates that fitness, believed to result from regular exercise, is associated with improved performance in inhibitory control and greater activation of the prefrontal cortex during performance of an inhibition task (Pontifex et al., 2011) and a larger basal ganglia volume (Chaddock et al., 2010). Along with the underlying mechanism of ADHD proposed above, these results suggest that possessing a high level of fitness or participating in long-term exercise may benefit inhibitory control in children with ADHD. Indeed, Gapin and Etnier (2010) first observed a positive relationship between the level of physical exercise and multiple aspects of executive function. Several reviews have subsequently proposed potential biological mechanisms linking physical exercise and executive function in ADHD (Berwid & Halperin, 2012; Gapin, Labban, & Etnier, 2011).

It should be noted that previous research studies examining exercise and ADHD utilized either a cross-sectional design (Gapin & Etnier, 2010; Hung et al., 2013) or emphasized the effects of acute exercise (Chang, Liu, Yu, & Lee, 2012; Pontifex, Saliba, Raine, Picchietti, & Hillman, 2013). Furthermore, the majority of exercise and cognition research has primarily focused on aerobic exercise. The effects on cognition of other types of exercise, such as exercise programs involving forms of coordinative exercise, are still unknown and should be considered. Indeed, Pesce (2012) argued that the design of an exercise program should shift from quantitative (e.g., exercise intensity, duration, and frequency) to qualitative (e.g., a combination of complex skills, motor coordination, and cognitive training) exercise characteristics. To date, only two pilot ADHD studies have explored a physical activity program that involved moderate- to vigorous-intensity exercise for 30–45 min for 8–10 weeks, and these programs were found to improve inhibitory control, motor skills, sustained attention, visual search speed, disruptive behaviors, and other social problems (Smith et al., 2013; Verret, Guay, Berthiaume, Gardiner, & Beliveau, 2012). To corroborate these initial promising findings, further evidence that multiple exercise modalities affect inhibitory control in the ADHD population is needed.

The purpose of this preliminary study was to expand current knowledge by examining the effects of an 8-week aquatic exercise intervention program, which combined both aerobic and coordinative exercise characteristics, on the restraint inhibition component of behavioral inhibition in children with ADHD.

Method

Participants

Thirty children between 5 and 10 years of age were recruited from two local elementary schools in New Taipei City, Taiwan. Participants met the following inclusion criteria: (a) diagnosis of ADHD by a psychiatrist based on the DSM-IV-TR (American Psychiatric Association, 2000); (b) the absence of neurological disorders; (c) right-hand dominance; (d) normal or corrected-to-normal vision; and (e) the ability to safely conduct the exercise program based on an assessment of the Physical Activity Readiness Questionnaire. The (b) and (c) criteria were included to avoid any potential confounding factors associated with brain activity and underlying cognitive performance (Chaudhary, Narkeesh, & Gupta, 2009).

Eligible participants were then assigned to either the aquatic exercise group (n = 15) or the wait-list control group (n = 15) based on their school. One participant in the exercise group and two participants in the control group were excluded in the final analysis due to their absence during the aquatic exercise programs (more than four times) or their absence during the 8-week post-test, respectively (Table 1). All participants' parents provided written informed consent in accordance with the Institutional Review Board of the National Taiwan Sport University.

Table 1.

Participant demographic characteristics according to group

Variable Wait-list control (n = 13; M [SD]) Aquatic exercise (n = 14; M [SD]) Total (N = 27; M [SD]) 
Gender (Male:Female) 13:0 10:4 23:4 
Age (years) 8.78 [8.33] 8.19 [7.65 8.44 [8.29] 
Height (cm) 132.00 [11.04] 126.67 [6.50] 128.95 [8.91] 
Weight (kg) 28.11 [5.40] 28.67 [7.06] 28.40 [6.19] 
BMI (kg/m216.42 [1.53] 17.70 [3.10] 17.03 [2.50] 
BMAT variable 
 Target throwing (score) 12.46 [4.50] 15.07 [4.55] 13.81 [4.63] 
 Bead moving (number/40 s) 30.54 [4.09] 33.57 [7.01] 32.11 [5.89] 
 n n N 
ADHD Type 
 ADHD-I 
 ADHD-HI 
 ADHD-C 10 18 
Treatment 
 Medication (methylphenidate) 13 
 Behavior 
 None 11 
Variable Wait-list control (n = 13; M [SD]) Aquatic exercise (n = 14; M [SD]) Total (N = 27; M [SD]) 
Gender (Male:Female) 13:0 10:4 23:4 
Age (years) 8.78 [8.33] 8.19 [7.65 8.44 [8.29] 
Height (cm) 132.00 [11.04] 126.67 [6.50] 128.95 [8.91] 
Weight (kg) 28.11 [5.40] 28.67 [7.06] 28.40 [6.19] 
BMI (kg/m216.42 [1.53] 17.70 [3.10] 17.03 [2.50] 
BMAT variable 
 Target throwing (score) 12.46 [4.50] 15.07 [4.55] 13.81 [4.63] 
 Bead moving (number/40 s) 30.54 [4.09] 33.57 [7.01] 32.11 [5.89] 
 n n N 
ADHD Type 
 ADHD-I 
 ADHD-HI 
 ADHD-C 10 18 
Treatment 
 Medication (methylphenidate) 13 
 Behavior 
 None 11 

Notes: BMI = body mass index; ADHD-I = predominantly inattentive subtype; ADHD-HI = predominantly hyperactive-impulsive subtype; ADHD-C = combined hyperactive-impulsive and inattentive subtype; N/n = number of participants; BMAT = Basic Motor Ability Test-Revised.

Aquatic Exercise Program

The aquatic exercise program was conducted by an instructor with a professional background in water exercise. The program was implemented with an instructor-to-student ratio of 1:10. The program consisted of 8 consecutive weeks of 2 sessions per week (16 sessions in total) at a local swimming pool. Each session lasted 90 min and consisted of four stages: (a) a 5-min warm-up period; (b) moderate-intensity water aerobic exercise for 40 min; (c) perceptual-motor water exercise for 40 min; and (d) a 5-min cool-down period.

The moderate-intensity exercise program was chosen based on evidence that moderate-intensity exercise may improve cardiovascular fitness, one of the potential mechanisms associated with exercise and cognition, as well as the appropriateness of the intensity for children with ADHD (Smith et al., 2013). The perceptual-motor water exercise included games designed to incorporate coordination, balance, and power to reinforce different aspects of motor skills. The exercise program emphasized enjoyment and safety to maximize the children's motivation.

Motor Ability Assessment

Participants' motor abilities were assessed using the Basic Motor Ability Test-Revised (BMAT; Arnheim & Sinclair, 1979). The BMAT is a motor ability assessment designed specifically for children that measures small and large muscle control, static and dynamic balance, and hand–eye coordination. The test–retest reliability of the BMAT was 0.93. The present study applied two subtests that specifically examined the coordination aspects of motor skills. These subtests included the following: (a) target throwing to test hand–eye coordination associated with throwing and (b) bead moving to test bilateral hand–eye coordination and dexterity.

Go/Nogo Task

The Go/Nogo Task is believed to reflect the restraint inhibition component of response inhibition and is, therefore, emphasized in the present study. Stimuli for the Go/Nogo Task were displayed on an IBM-compatible personal computer, and the visual Go/Nogo Task was presented using STIM 2 software (Neuroscan Inc., USA). During the Go/Nogo Task, each participant was instructed to press a button for a frequent stimulus (i.e., GO stimulus, 70% probability) or to withhold a response for an infrequent stimulus (i.e., Nogo stimulus, 30% probability). The stimulus, sized 3 × 3 cm, was presented in the center of the 15-inch screen with a black background. In each trial, a cue consisting of a yellow square was first presented for 500 ms to attract the participant's attention. This cue was followed by either the target Go stimulus (i.e., green circle) or the target Nogo stimulus (i.e., red octagon) for 200 ms. The participant was asked to press or withhold the button with his/her right index finger as quickly and accurately as possible, according to the type of target stimulus, within the next 1500 ms. A reaction time between 400 and 800 ms for the Go stimulus was considered a correct response.

The participant was instructed to perform a practice block of 10 practice trials. The formal test was conducted only when the criterion of achievement of 80% correct responses in the practice block was met. The task was administered in 8 blocks of 160 target stimuli. Three indices were derived from the Go/Nogo Task, including reaction time and accuracies associated with the Go and Nogo stimuli. Including the short break between each block, the total duration of the Go/Nogo Task was ∼15–20 min.

Experimental Procedures

The participants were invited to come individually to the laboratory on 2 separate days. The children who were undergoing medical treatment were asked to remain free of medication for at least 24 h prior to the experiment. On the first visit, the participant's parent and the participant signed an informed consent form, provided a health history, and filled out a demographics questionnaire. Each eligible participant then entered the pre-test stage, which consisted of performing the Go/Nogo Task and a motor ability assessment according to the BMAT protocol.

Participants in the aquatic exercise group underwent an 8-week water exercise program that consisted of two 90-min sessions per week as an after school program. Participants in the wait-list control group maintained their normal after school activities. While 1 participant who was absent more than twice during the exercise program was allowed to continue participating in the program, his data were excluded from further analysis. Within 1 week of completing the exercise or wait-list treatment, each participant was asked to return to the laboratory to complete the Go/Nogo Task and the BMAT again for the comparison of pre- and post-test scores.

Statistical Analysis

A non-randomized control trial design was used for this pilot study. Independent t-tests and chi-square tests were performed to compare the demographic variables between the aquatic exercise and wait-list control groups where appropriate. In addition, independent t-tests were separately applied for a subset of the BMAT in both the pre- and post-tests. Two-way repeated-measure analysis of variance (ANOVA), with group as the between-subject (aquatic exercise vs. wait-list control) factor and time as the within-subject (pre-test vs. post-test) factor, was separately conducted for indices of the Go/Nogo Task with respect to reaction time and response accuracy. Following the ANOVAs, multiple comparisons with Bonferroni–Holm adjustments were applied to control for experiment-associated inflation of type 1 error for small sample sizes. For all statistical analyses, a significance level of .05 was used prior to the adjustment (SPSS 18.0).

Results

Demographic Analyses

Independent t-tests confirmed that there were no differences in age, height, weight, BMI, or the two subsets of BMAT variables—t's(25) < 1.30, p > .05. However, the chi-square tests revealed significant differences with respect to gender (p = .04), ADHD type (p = .04), and treatment (p = .04) between the groups.

Motor Ability Assessment

An independent t-test revealed no significant difference in target throwing between the two groups in the pretest (p > 0.05); however, the aquatic exercise group achieved a higher target throwing score (18.28 ± 3.54) compared with the wait-list control group in the post-test (14.38 ± 3.69)—t(25) = 2.81, p = .01. Similarly, Although no difference was found in the bead moving score in the pretest, there was an increase in the bead moving score in the aquatic exercise group (35.79 ± 4.87) compared with the wait-list control group (32.38 ± 3.69) in the post-test—t(25) = 2.17, p = .04.

Go/Nogo Task

Go stimulus

With regard to reaction time, there was a significant main effect of group, F(1, 25) = 10.36, p = .004, partial eta square = 0.29, where reaction time in the aquatic exercise group (509.39 ± 21.07 ms) was longer than that in the wait-list control group (411.66 ± 21.86 ms). However, there was no main effect of time or an interaction between group and time (p > .05). Similarly, the analysis of accuracy revealed that there was only a significant main effect of group, F(1, 25) = 5.23, p = .03, partial eta square = 0.17, where accuracy in the aquatic exercise group was lower (94.16 ± 1.26%) than that in the wait-list control group (98.30 ± 1.30%; Fig. 1a).

Fig. 1.

Response accuracy as a function of time and group: (a) Go stimulus and (b) Nogo stimulus (mean ± 1 SE). # represents a significant difference between the two groups.

Fig. 1.

Response accuracy as a function of time and group: (a) Go stimulus and (b) Nogo stimulus (mean ± 1 SE). # represents a significant difference between the two groups.

Nogo stimulus

There was a significant main effect of time, F(1, 25) = 6.00, p = .02, partial eta square = 0.19, and a significant interaction effect of group and time, F(1, 25) = 8.30, p = .001, partial eta square = 0.25. The follow-up analysis revealed that there was no difference between the two groups in the pretest (88.64 ± 7.03%, 88.85 ± 9.75%), but the exercise group had a higher accuracy than the control group in the post-test (94.31 ± 4.88%, 88.39 ± 12.10%; Fig. 1b). On the other hand, the effect size (ES) between post- and pretest is 0.9 (Cohen's d) in the exercise group and −0.04 in the control group.

Discussion

This study examined the effects of an exercise program on response inhibition in children diagnosed with ADHD. This study provides further support for the growing body of evidence that suggests a relationship between exercise intervention, inhibition, and ADHD. Our results indicate that children with ADHD demonstrated an improvement in accuracy for the Nogo stimulus, a widely used index that assesses the restraint inhibition component of behavioral inhibition. Specifically, children in the exercise group exhibited substantial inhibition enhancement over time (ES = 0.9), whereas inhibition in children in the wait-list control group remained unchanged (ES = −0.04). Our positive findings are in accordance with previous studies that demonstrated the beneficial effects of a physical activity program on response inhibition in children with ADHD (Smith et al., 2013; Verret et al., 2012). Coordination aspects of motor skills were also improved following the 8-week, multifaceted exercise program. Notably, the present study extended previous research by utilizing an aquatic-based moderate-intensity exercise program that involved both aerobic and perceptual-motor exercises during 90-min sessions.

In addition to the exercise-associated increases in prefrontal cortex activation and basal ganglia volume discussed above (Chaddock et al., 2010; Pontifex et al., 2011), other biological mechanisms have been proposed. For instance, ADHD has been linked to dysregulated levels of dopamine, serotonin, and norepinephrine, which are essential to arousal in fronto-striato-cerebellar circuits as well as the control of executive function (e.g., serotonin is predominantly linked to restraint inhibition; del Campo, Chamberlain, Sahakian, & Robbins, 2011; Eagle et al., 2008). Animal studies have shown that exercise training of different types (i.e., treadmill- and wheel-running) changes the dopamine system by up-regulating dopamine and enhancing dopamine and dopamine receptor binding; changes have also been reported in the serotonin and norepinephrine systems based on elevated expression in cognitive-related brain regions, particularly in the hippocampus (see reveiw in Lin & Kuo, 2013). Although confirmation of these findings in human studies is still required, these studies speculated that a multifaceted exercise program may alter dopaminergic and noradrenergic neurotransmission, which may in turn result in improved cognitive function in ADHD.

Another possibility is that exercise improves executive function by regulating attention and information processing. Using a neuroelectrical technique, Hung and colleagues (2013) observed that ADHD children with greater motor ability demonstrated larger P3 amplitudes and shorter P3 latencies during the performance of an inhibitory response compared with ADHD children with lower motor ability. Using an intervention design, Chang, Tsai, Chen, and Hung (2013) reported that an 8-week coordinative exercise program not only increased inhibitory responses behaviorally but also induced similar neuroelectrical patterns in healthy children, regardless of whether the exercise was of low or moderate intensity. These findings imply that the motor ability level or participation in chronic exercise involved coordinative characteristics associated with attentional resource allocation facilitation and stimulus classification efficiency.

Reaction time and accuracy for the Go stimulus only confirmed the main effects for group but not for intervention, suggesting that exercise has a limited influence on basic information processing such as attention ability. Although these findings need to be replicated in a larger sample with homogeneous variables incorporating the demographic characteristics of the exercise and control groups, these results are consistent with previous literature indicating that exercise has disproportionate effects on cognition, where larger effects are observed in tasks requiring a larger amount of executive control (Pontifex et al., 2011). Our study extended the observation of this phenomenon from healthy children to children with ADHD.

Some limitations of this preliminary study warrant consideration and should inform future research directions. The relatively small sample size and the unbalanced gender proportions (i.e., primarily boys) limited the statistical power and increased the likelihood of sampling biases. Furthermore, given the non-randomized control trial design, the two groups had a slightly heterogeneous background in terms of gender, ADHD type, and status of attention ability (i.e., go stimulus performance). Accordingly, the precise causal effects of exercise on executive function in ADHD require further assessment to include these factors. A study with the cross-over design has countered some confounders and may be considered for conducting such research in the future. Furthermore, along with reaction times and accuracy, an index of variability that is relevant to the ADHD population is suggested in order to enhance a full understanding between exercise and cognition in the special population. Finally, further studies are also encouraged to control the level of physical activity outside the exercise intervention (e.g., keeping a daily exercise log) and to apply cognitive and behavioral perspectives to the examination of ADHD symptoms (Smith et al., 2013).

The primary strength of this preliminary study is the use of a long-term exercise program that included both quantitative and qualitative exercise characteristics. It is particularly significant that exercise incorporating appropriate intensity, qualitative characteristics, and enjoyment may attract children with ADHD and increase long-term adherence to such programs. Furthermore, this study is one of only a few studies that have investigated response inhibition aspects of executive function in ADHD. To date, psychostimulant medications appear to be the principal option for individuals with ADHD; other options, such as psychotherapy, cognitive rehabilitation, or physical exercise, which have fewer side effects are recommended as additional options. Notably, psychosocial treatments tend to address some of the additional social-emotional/behavioral difficulties but not necessarily the core symptoms of ADHD (e.g., attention deficit); cognitive rehabilitation requires intensive effort for extended periods of time, yet generalizability to daily life has been a concern. Thus, exercise therapies is highly recommended and should be further explored because the therapy may result in long-term lifestyle changes (e.g., greater participation in physical exercise) and may also lower the risk of comorbid issues such as oppositional behavior or substance abuse problems. In summary, although our findings support ongoing research in the field, our novel data suggest that the increased inhibitory performance in children with ADHD can be improved by engaging in a multifaceted exercise program. Given that alterations in inhibition are a critical aspect of the dysfunction associated with ADHD, these findings regarding the positive effect of an aquatic exercise program provide preliminary support for therapeutic interventions that can be used by researchers, parents, educators, and clinicians.

Funding

The present work was partially supported by the “Aim for the Top University Plan” of the National Taiwan Normal University and the Ministry of Education, Taiwan, Republic of China. The work was also supported by Grant of “he Graduate Students Study Abroad Program” from the National Science Council (Taiwan) (NSC 101-2917-I-003-005).

Conflict of Interest

None declared.

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