The Impact of Virtual Reality Intervention on Emotion Regulation and Executive Functions in Autistic Children

Abstract

Introduction:

Autistic children may encounter difficulties in managing emotions and executive functions (EFs), which can contribute to mental and health challenges. Recognizing physical activities as a potential strategy for enhancing emotion regulation (ER), this study aims to investigate the efficacy of a virtual reality (VR)-based physical exercise program in improving ER and EFs among children with autism spectrum disorder (ASD).

Materials and Methods:

Forty boys diagnosed with ASD, aged 7 to 10 years, were randomly assigned to two groups: a VR intervention group (n = 20) and a control group (n = 20). The intervention group participated in a VR program, while the control group solely concentrated on engaging in sedentary and inactive video gaming. EFs were evaluated through the utilization of both the flanker task and the Wisconsin card sorting task, both administered initially at baseline and subsequently after an 8-week interval. In addition, the parents of the children completed the Emotion Regulation Checklist to evaluate their ER skills.

Results:

According to the results, a significant difference was observed between the two groups in terms of EFs and the ability to regulate emotion (P < 0.05). The intervention group demonstrated a notable improvement in ER skills and exhibited superior executive functioning abilities compared with the control group.

Conclusion:

It appears that VR exercises can serve as a preliminary trial to enhance EFs and ER in children with autism. In addition, they may prove effective as complementary interventions to traditional educational strategies in preventing future challenges associated with ASD.

Introduction

Autism spectrum disorder (ASD) is a neurodiversity condition that occurs in childhood, with a growing prevalence rate. The prevalence is 1 in 36 children or 2.8% in the United States.¹ It has been observed that boys are four times more likely to be diagnosed than girls, and 44% of the diagnosed cases have medium to high IQ.² In addition, autistic individuals commonly experience co-occurring difficulties in social communication and interaction, coupled with restricted and repetitive behaviors.³ They may also exhibit challenges such as sleep problems and low working memory capacity.⁴ Evidence of inflexibility in set-shifting has been documented,⁵ alongside issues in response inhibition, as reported by Hopkins et al. and Lee et al.^6,7 As evidenced, autistic children often struggle with challenges in executive functions (EFs), particularly in areas such as working memory, inhibitory control, planning,^8,9 and emotion regulation (ER),¹⁰ impacting both their mental and physical health. Proficiency in EFs and ER plays a crucial role in determining an individual’s capacity for self-regulation.¹¹ Recognizing the significant impact of EFs and ER, targeted interventions become imperative. Motor activity interventions stand out among various approaches, potentially enhancing EFs and ER in children with autism. It is suggested that EFs act as mediators, facilitating the effects of exercise and motor activity on ER, thus promising improved outcomes and quality of life.

Emotions are indeed multidimensional, complex bodily responses to various factors or situations, leading to preparedness for action and a person’s adaptation to the situation. Emotional experiences elicit responses across multiple dimensions, encompassing emotional, physiological, behavioral, and cognitive domains in individuals. However, when these emotional responses become excessive and inappropriate, they can lead to issues such as heightened levels of anger, stress, and anxiety, increased respiration and heart rate, elevated temperature, intensified neuro- or musculoskeletal activity, eating or sleeping problems, substance abuse, conflicts, distractibility, mental rumination, and executive dysfunctions.^12,13 According to Gross’s process model, the generation of emotions involves the following four stages: (1) a factor or situation related to the individual’s goals, (2) attention, (3) cognitive appraisal, and (4) response.^13,14 The term “emotion regulation” signifies an individual’s ability to modulate the expression of feelings^13,15 and suggests that interventions and regulation of emotions can be applied at any stage of this emotion generation process,¹⁶ targeting one or several emotional responses. Indeed, the ability to regulate emotions, crucial for mental and physical health,^13,17 has been addressed through various interventions, such as regulating sensory arousal, managing mental rumination, and ER strategies (e.g., situational, cognitive reappraisal, and response suppression). As demonstrated by Cibralic et al., ER difficulties are linked with the severity of ASD symptoms, including social-communication impairments, repetitive behaviors, and sensory hypo/hypersensitivity. This reveals that autistic children face more problems than typical children in some developmental areas.¹⁸ Dysregulation of emotions is notably highly associated with the core features of autism, particularly impairments in social behaviors. For instance, when examining the role of ER on the autism spectrum, Mazefsky and colleagues identified underlying mechanisms contributing to poor ER in the autism spectrum, such as physiological arousal (both hyper- and hypoarousal), the co-occurrence of psychiatric disorders with varying degrees of positive and negative effects that interfere with adaptive ER, and abnormalities in the amygdala and prefrontal cortex connectivity.¹⁹ Moreover, Chandler et al. and Hosiri et al. emphasized that many destructive behaviors, impulsivity, and sleep problems in autistic children are linked to emotion problems.^20,21 These emotional and behavioral challenges present a significant obstacle to children’s daily functioning, leading to poor social development, depression, and anxiety.²² Similarly, Crouch et al., Batres, and Espinosa et al. have highlighted that developing the ability of ER is effective in improving EFs.^23–25

EFs encompass a set of interconnected cognitive skills that guide behaviors and thoughts toward specific and important goals.²⁶ These functions are broadly categorized into three types of brain functions as follows: working memory, cognitive flexibility, and inhibitory control.²⁷ EFs are associated with a network of brain regions, encompassing the prefrontal cortex, parietal lobes, anterior cingulate/supplementary motor area, putamen, thalamus, and various subcortical areas.²⁸

EFs enable individuals to regulate emotions effectively.²⁹ Inhibition, a component of EF, plays a crucial role in suppressing unwanted emotion responses, allowing for adaptive regulation.³⁰ Working memory aids in holding and manipulating emotional information, facilitating cognitive reappraisal and response modulation³¹ and decreasing of maladaptive ER such as mental rumination. In addition, cognitive flexibility allows individuals to shift between different ER strategies based on situational demands (dynamically ER strategy choosing).³² Research findings indicate that individuals with better EFs experience less difficulty in utilizing cognitive ER strategies, such as attentional deployment and cognitive reappraisal, and are more inclined to use antecedent-focused strategies.³³ In delineating the role of each component of EFs in ER, it can be argued that inhibitory control facilitates the suppression of predominant, impulsive, and situationally inappropriate emotional responses, thereby redirecting attention away from irrelevant stimuli and inhibiting their processing. Cognitive flexibility, on the contrary, reallocates attention among various tasks and stimuli according to their attentional demands. Consequently, automatic and impulsive emotional responses are attenuated, while emotional stability increases.^34,35 The functioning of working memory is associated with the maintenance, manipulation, and updating of information. Dysfunction in this process, particularly in maintaining or updating negative information, along with weakened inhibitory control and cognitive inflexibility, can lead to the continuous processing of irrelevant information and the depletion of attentional resources, often resulting in mental rumination.¹⁴ Moreover, the capacity of working memory contributes to individual emotional flexibility by enabling the selection and modification of ER strategies according to situational goals and needs.³⁶ Also, training working memory can reduce mental rumination tendencies by enhancing attentional control and cognitive flexibility, allowing individuals to better regulate their thoughts and emotions.³⁷ These components of executive functioning, through situational and cognitive strategies, alter attentional focus and the allocation of attentional resources to primary and relevant tasks, or by balancing attention between internal and external stimuli.³⁸ As a result, negative emotions are downregulated. However, when faced with various tasks or simultaneous processing of diverse stimuli, individuals may exhibit situationally inappropriate responses across emotional, behavioral, and physiological dimensions. Several clinical conditions, including depression, attention-deficit/hyperactivity disorder, and autism spectrum condition, have been linked to impairments in EFs.³⁹ Furthermore, emotions and cognition are intricately intertwined, each playing a role in information processing and performance. To sum up, there exists a potential for reciprocal influence between the processes of ER and EFs.¹⁶ Notably, impairment in executive control is associated with situationally inappropriate emotional responses and their regulation.^40,41 In addition, evidence indicates that, among the various aspects of EFs, cognitive flexibility (e.g., switching between thoughts and tasks) and behavioral inhibition (e.g., reducing mental rumination patterns, suppressing automated responses, and ignoring irrelevant stimuli) are impaired in autistic children.^7,42,43 While some repetitive and restricted behaviors (RRBs) in autistic individuals serve as coping mechanisms, contributing to ER, others are maladaptive, hindering overall well-being. Challenges in EFs are significantly associated with maladaptive RRBs in autistic individuals.⁴⁴ These weaknesses have been found to predict an increase in RRBs, indicating a strong correlation between the two.⁴⁵ Furthermore, a study on the effects of augmented reality (AR) using motivational games with cognitive-motor exercises demonstrated improvements in RRBs, EF, attention, and reaction time in patients with ASD. These findings suggest the potential effectiveness of cognitive-motor training as a complementary intervention for managing RRBs.⁴⁵

Consequently, challenges arising from difficulties in ER are not limited to autistic children; they extend to typical individuals as well. In conducted studies, interventions such as mindfulness, attention management, and ER have been used to enhance the ability to regulate emotions across diverse groups. In addition, akin to other interventions, exercise or physical activity is considered a preventive strategy for improving the capacity to regulate emotions when confronted with stressful factors and situations.¹⁴ Physical exercises have demonstrated efficacy in enhancing brain functions and structures.⁴⁶ Engaging in regular exercise, in particular, has been shown to improve flexibility and cognitive control.⁴⁷ Researchers such as Edwards et al., Gross, Giles et al., Augustine & Hemenover, Edwards et al., Ekkekakis et al., Liu et al., Bernstein & McNally, Bernstein et al., and Yuri have emphasized the beneficial effects of sports and physical activity on ER in typical individuals.^{13,14,48–55} Therefore, given the established effectiveness of physical exercise in enhancing emotional functioning in typically developing children, it is likely that children with ASD would also benefit.

In another aspect of the cognitive regulation ability, specifically the regulation of sensory arousal, studies have highlighted the significant impact of exercise training.^52,56 In a meta-analysis, Liu et al. emphasized the influence of exercise training on improving ER strategies.⁵² Their research findings suggested that neither the intensity nor duration of training, nor the health status of the participants, exerted a significant influence on the enhancement of ER abilities. Also, Tse et al. conducted a study on the effect of 12 weeks of jogging exercises on the ER ability of autistic children, confirming its effectiveness. They referred to the need for further research to elucidate the mechanisms of the impact of physical exercises on ER.²² In a separate study, Alderman et al. examined the combined training of meditation and aerobics among both healthy individuals and people with depression, observing a reduction in depression symptoms and mental rumination patterns in both groups.⁵⁷ In addition, Ferris et al. and Yanagisawa et al. have demonstrated the effectiveness of physical exercises on EFs.^58,59 Regarding autistic children, exercise training programs involving activities such as walking, running, playing in water, resistance training, and aerobic exercises have been used to enhance their motor skills.^58,59 However, due to their challenges with social interactions, activities requiring interpersonal engagement may induce significant stress in these children.⁶⁰ Recently, virtual reality (VR) has emerged as a valuable and an effective tool for identifying, treating, and addressing the psychoeducational needs of individuals with ASD in various studies.^61,62 Utilizing interactive games in VR, especially those customized to children’s interests, needs, and satisfaction, has been suggested as one of the most effective training methods.⁶³ VR introduces a novel technology where individuals use body movements within an interactive environment to participate in game visualization.⁶⁴

Evidence suggests that children engaging in physical activities within VR games experience increased cooperation and learning opportunities, as these games provide positive reinforcement through enjoyment and successful progress. This, in turn, facilitates the creation of new experiences.⁶⁰ In a meta-analysis study focused on the effects of AR and VR training for the rehabilitation of autistic children, Karami et al. demonstrated that VR training had a positive influence on social skills, cognitive functions, and emotional skills.⁶⁵ In addition, Vukicevic et al. explored the impact of VR games with Kinect sensors on the motor skills of autistic children, observing improvements in motor skills, positive emotions (e.g., smiles, laughs, shows positive excitement, jumps for joy, claps for joy, and adequately communicates with an adult), and a reduction in the rate of attention decrement.⁶⁶ In another systematic review and meta-analysis study evaluating the effectiveness of VR training programs for improving emotion recognition in autistic individuals, Farashi et al. suggested that VR training might activate the amygdala, a crucial component for ER.⁶⁷ Simultaneously, several studies have explored VR interventions, addressing motor imagery development,⁶⁸ enhancing agency and the feeling of presence,⁶⁹ cortical reorganization,⁷⁰ implicit imagery and visualization experiences in autistic children,⁷¹ enhancing interaction and response within virtual environments,⁷² EFs, social skills,⁷³ emotion recognition, and ER,^61,62 as well as sensorimotor rehearsal.⁷⁴ These benefits are attributed to its characteristics, including providing a safe and controllable environment, high interactivity with realistic scenes, attention-capturing elements, a sense of presence and immersion, and the incorporation of multisensory stimuli. Also, these studies provide support and evidence for the potential of VR in enhancing visualization ability and its application for motor imagery enhancement. Therefore, we hypothesize that VR interventions may also improve EFs and ER abilities, particularly in ASD children.

The stressors of contemporary life present challenges in regulating and managing emotions, potentially leading to psychological issues and various behavioral and functional disorders. While certain situations and events may be inevitable, regulating emotions is essential to prevent further damage. Difficulties in EFs and ER share common consequences such as impaired decision-making,⁷⁵ leading to behavioral problems,⁷⁶ cognitive inflexibility, and difficulty adapting to new situations. These challenges hinder academic and occupational performance, consequently contributing to heightened stress and anxiety levels,⁷⁵ and the therapeutic interventions targeting both areas may prove effective. Although the effects of aerobic exercise on physical health can extend to mental well-being, further research is needed to comprehend these mechanisms in autistic children, enabling more reliable exercise interventions. This study represents a novel approach by concurrently investigating ER and EF alongside the effects of VR interventions on these domains in autistic children. We have hypothesized that a VR intervention program may be an effective approach in this context. So, the main objective of this study is to investigate how a VR intervention program influences the regulation of emotions and EFs in autistic children.

Methods

Procedure

The present study used a semiexperimental research design with a pretest–posttest, including a control group. Participants were children aged 7 to 10 years recruited from two autism spectrum centers in Tabriz in the year 2023. Inclusion criteria consisted of being male (7–10 years old) and having a confirmed diagnosis of autism spectrum based on the diagnostic files of children in autism centers, verified by a child psychiatrist specialist. Also, participants who had mild autism conditions requiring support and substantial support (levels 1 and 2) were determined through autism severity diagnosis by a specialist psychologist using the Gilliam Autism Rating Scale (GARS-3)⁷⁷ and Diagnostic and Statistical Manual of Mental Disorders-5.⁷⁸ Other inclusion criteria were the absence of medical contraindications for exercise (such as epilepsy, orthopedic, and cardiovascular problems) and no hearing or visual impairments, confirmed by a pediatric specialist. The exclusion criteria encompassed individuals displaying the most severe autistic characteristics (e.g., requiring very substantial support/level 3), those undergoing specialized services beyond the standard care provided by the centers, individuals with an IQ below 80, and those participating in concurrent exercise activities. The study’s methodology involved coordination with welfare organizations and obtaining necessary permits for participation. Subsequently, the study’s goals and stages were explained to parents. After obtaining appropriate parental consent for their children’s participation in the study, the parents of the participants completed a satisfaction questionnaire. In addition, the medical records of the children, assessed by specialists, included evaluations of cardiovascular and musculoskeletal status, as well as assessments for hearing loss. Out of the 60 participants available, an expert psychologist assessed the level and intensity of the autism spectrum using the GARS-3. The Wechsler Intelligence Scale short form was used to determine the participants’ IQ. Twenty children were excluded due to accompanying physical problems, severe communication difficulties, and high severity of the condition. Forty children meeting the inclusion criteria with moderate and mild autism were selected for the study. Subsequently, autistic children with moderate levels were selected based on a cutoff score (71–100) on the GARS. The selected participants were randomly assigned into the experimental (n = 20) and control (n = 20) groups by the researcher. The ability to regulate emotions and EFs in both groups was evaluated in the pretest. The Emotion Regulation Checklist (ERC) was completed by the parents, and EF tests were administered to the children. The experimental group underwent VR training interventions for 16 sessions, lasting 30 minutes each, with two sessions per week. These interventions were conducted in a single-room setting. The control group simultaneously engaged in sedentary video gaming and did not receive any specific training instruction. After the completion of the training, both groups were tested. The interventions and data collection were carried out by the researcher and two specialists in the field of physical education. Throughout the study period, participants in both the experimental and control groups did not engage in sports or VR games during their leisure time or concurrent interventions that could potentially influence the study outcomes. Furthermore, they were unfamiliar with VR games. No participant missed more than one session and no children were excluded from the research after the initial training session. Following the VR interventions, a posttest was conducted for both groups. The researcher and two physical education professionals conducted the interventions and data collection, while they were not blind to the intervention assignment. Approval was obtained from the Ethics Committees of the University of Payame Noor and the Welfare Organization. The methods in this research follow the guidelines of the Declaration of Helsinki. In addition, the AI chatbot GPT-3.5 was used to ensure accurate and consistent translations of article text across languages, as well as for grammar-checking purposes.

Assessments

The GARS

The GARS-3,⁷⁹ designed for individuals aged 3 to 22 years, was used for ASD screening. This assessment comprises six subscales, encompassing a total of 58 questions. Each item is rated on a 4-point Likert scale, ranging from 0 to 3. The subscales cover the evaluation of social communication (9 items), repetitive behaviors (13 items), cognitive style (7 items), inconsistent speech (7 items), emotional response (8 items), and social interaction (14 items). Children selected for this study were those who were likely to have autism and required minimal support, with a score range of 71 to 100 on the GARS-3 examination. The interclass correlation coefficients for the subscales range from 0.71 to 0.85, and Cronbach’s alpha for internal consistency exceeds 0.9.^9,66,80

Emotion Regulation Checklist

This is a 24-item ERC, designed to measure children’s ER. It yields two scores: a subscale for ER (ERC-ER, eight items, α = 0.83) and a subscale for lability/negativity (ERC-LN, 16 items, α = 0.96). Parents and teachers rated the items on a 4-point Likert scale (ranging from 1 to 4, with 1 indicating “never” and 4 indicating “always”). In our study, only parents were responsible for completing the ERC. The ER subscale assesses self-awareness, emotion expression, and overall mood, with a higher score implying a greater level of ER. Similarly, the LN subscale evaluates anger dysregulation, lack of flexibility, and emotional lability, with a higher score indicating a higher level of emotion dysregulation.^15,81,82

Wisconsin card sorting test

It is a well-known and widely used neuropsychological test⁸³ that assesses a person’s cognitive flexibility when they are stuck in a specific set. A software version, which took approximately 20 minutes per person, was utilized.⁸⁴ The task involves four goal cards and 64 response cards, featuring dimensions such as shape, color, and numbers. Participants independently sort the cards based on their perspectives, receiving feedback on the correctness of their matches. Three undisclosed rules (color, shape, and number) guide the card sorting process. After successfully completing ten consecutive correct sets, the sorting rule is changed. Participants then receive binary “yes” or “no” feedback, and in this new rule, their previously correct answers are considered incorrect. The test concludes when participants accurately match six sets. The recorded measure of “perseverative errors” is a widely used metric for assessing cognitive flexibility. According to Chang and colleagues (2022), Lezak (1995) reported the validity of WCST for assessing cognitive deficits as 0.86, whereas Kaplan et al. (2021) estimated split-half reliabilities of approximately 0.9 and 0.95 for three primary WCST measures.⁸⁵ Naderi et al. (2006) established the validity of this test in the Iranian population using the test–retest method, yielding a coefficient of 0.85.^45,86

Short form of the Wechsler scale of intelligence

The Wechsler Intelligence Scale for Children (WISC) is an IQ test assessing cognitive abilities in children aged 6 to 16. In this study, the short form of the revised WISC, comprising the Vocabulary, Information, and Picture Completion subtests, was used to screen participants based on their intelligence scores. This short form has been translated and standardized by Shahim in Iran, with a reported validity coefficient of 0.92. The correlation coefficient between this form and the full version is reported to be 59%.^87,88 Children with IQs above 80, approved by a psychiatrist, were selected.

Flanker task test

To assess EFs, the flanker task, designed by the Psychology Experiment Building Language, was employed. This task measures inhibition control, assessing a subject’s ability to disregard irrelevant information, and cognitive flexibility, evaluating the ability to switch between two rules based on the situation.^89,90 In this task, a target in the form of an arrow appears in the center of the screen, flanked by arrows pointing in different directions (either right or left). This setup creates various conditions: (1) unflanked or flanked with unrelated stimuli (neutral flankers), (2) flanked by relevant stimuli pointing in the same direction as the target (congruent conditions), and (3) flanked by relevant stimuli but pointing in the opposite direction to the target (incongruent conditions). Participants respond by pressing the right or left shift buttons on the keyboard, corresponding to the orientation of the central arrow. Incongruent and congruent trials are presented randomly, and children respond to three blocks of 24 trials each. Before the main trials, each participant completes eight practice trials. A fixation point appears 700 ms before each trial, followed by a 1500-ms interval between trials. Participants have 1000 ms to respond. This measure encompasses various dimensions of EF. However, in this study, we utilized Conflict Cost as an outcome variable. This measure represents the increase in reaction time associated with incongruent stimuli, calculated as the incongruent mean minus the congruent mean.

Intervention

VR program

As per Vernadakis et al.’s study, the VR program utilized Xbox 360 Kinect Games.⁹¹ Each session held twice a week for eight weeks lasted 30 minutes. Initially, the children were unfamiliar with the selected games, namely Kinect Sports Season 2 and Kinect Adventures. Games inherently appeal to children, and VR games possess unique features for this purpose. The selection of VR games is intended to provide autistic children an opportunity to engage in physical exercises and interact with virtual agents and objects within virtual environments through body gestures and communication. After the pretest assessments, interventions occurred in a designated playroom equipped with a 40-inch TV monitor and an Xbox 360 Kinect game console. Four common Kinect sports games (baseball, basketball, bowling, and football) were used in the gaming room for this purpose. The chosen games aimed to challenge and enhance various fundamental motor skills in participants, encompassing the ability to manipulate and control objects through underhand and overhand throwing, striking, dribbling, catching, and kicking. Each game is characterized by features such as gameplay against the computer, gameplay against another player, or gameplay with other players at the beginner, amateur, professional, and championship levels. In addition, as the difficulty level of the game increased, options for accelerating game pace and complexity were provided. The experimental group played the games individually at the beginner and amateur levels, interacting with fictional teammates and opponents in virtual space. Nevertheless, due to the inherent challenges, children found it difficult to compete at the professional and championship levels. Players had the opportunity to gauge their performance against others by choosing between single-player, two-player, three-player, or four-player modes, or by challenging the computer, monitoring their advancements in both individual and team competitions. Despite the intended duration and nature of the games during training interventions, there were no data recorded regarding the children’s gameplay. To calibrate the Kinect camera, children stood two meters away from the TV screen during each session. The participant’s avatar on the TV display mirrored the child’s movements. The intervention was administered individually, and participants were required to select two games, playing each game for 12 minutes before moving on to the next. During the game, participants played selected games while their movements were monitored by the Kinect sensor. The training schedule included the following steps: (1) attending the training location, (2) warming up with stretching exercises (2–3 minutes), (3) practicing two games (24 minutes), and (4) concluding with a 2–3-minute stretching session. Children were also instructed on how to switch between games. In contrast, the control group did not receive any intervention, and pre- and postintervention evaluations were conducted.

Data Analysis

In this study, the dependent variables were EFs and ER skills, recorded at both pre- and poststages in both groups. Among EFs, cognitive flexibility was assessed using the Wisconsin Card Sorting Task (measured by perseverative errors) and the Flanker Task (measured by conflict cost scores). ER regulation skills were evaluated through measures of ER negativity and ER lability.

Differences in demographic characteristics, including age, height, weight, IQ, and GARS-3 scores, were assessed using independent t-tests. To evaluate the impact of the VR intervention on dependent variables, repeated-measures analyses of variance (ANOVA) and multivariate analyses of variance (MANOVA) were used. Assumptions essential to MANOVA and ANOVA, such as the normal distribution of residuals (Shapiro–Wilk test), homogeneity of variance (Levene’s test), equality of covariance matrices (Box’s Test), and randomness of residuals (Runs test), were checked and met (P > 0.05). All participants completed the intervention without dropouts, and there were no variables with missing data. Data analyses were conducted using SPSS 26, with a significance level set at P < 0.05.

Results

As indicated in Table 1, there were no statistically significant differences in the demographic characteristics of participants between the two groups at baseline. Table 1 illustrates the absence of significant differences in height, weight, age, IQ, and autism spectrum severity between the two groups. Furthermore, Tables 2 and 4 show no significant distinctions in the initial comparison of the groups regarding variables related to EFs and ER abilities during the pretest session. These findings suggest that the two groups did not exhibit a significant initial difference.

Table 1.

The Characteristics of the Participants by Group in Experimental and Control Groups. Expressed as Means (Standard Deviations) for Test Scores

	Experimental ASD group (M ± SD)	Control ASD group (M ± SD)	Statistics
Age (year)	8.89 (0.9)	8.94 (1.2)	t(38) = 0.167; P = 0.86
Height (cm)	135.4 (5.4)	136.1 (6.56)	t(38) = 0.36; P = 0.71
Weight (kg)	40.55 (5.85)	38.55 (7.85)	t(38) = −0.91; P = 0.36
IQ-SF (score)	101.75 (4.29)	104.85 (7.02)	t(38) = 1.68; P = 0.1
GARS-3 score	76.7 (11.45)	79.5 (10.92)	t(38) = −0.79; P = 0.43

Note. GARS, Gilliam Autism Rating Scale | third edition; ASD, autism spectrum disorder; IQ-SF, short form of the Wechsler scale of intelligence (consisting of the Vocabulary, Information, and picture completion subtests).

Table 2.

Comparisons of the Ability of Executive Functions Between and Within Groups at Different Times

	T1	T2	P value (time effect)	P value (interaction effect)
Executive functions (preservative errors)
VR intervention group (M ± SD)	18.25 (3.59)	15.9 (3.64)	0.001	0.001
Control group (M ± SD)	18.15 (3.97)	18.05 (2.97)	0.85	0.001
P value (group effect)	0.93	0.048
Executive functions (conflict cost)^a
VR intervention group(M ± SD)	268.15 (165.7)	213.6 (135.7)	0.001	0.001
Control group (M ± SD)	266.55 (185.47)	282.9 (163.4)	0.366	0.001
P value (group effect)	0.97	0.153

Conflict cost (incongruent mean–congruent mean).

Effect of VR intervention on EFs

For measuring cognitive flexibility, as indicated by perseverative errors, results of repeated-measures ANOVA (2 × 2) showed a significant interaction effect (P = 0.001). Follow-up analysis revealed that the groups did not differ significantly in the pretest stage (P = 0.93), but significant differences emerged between the groups in the posttest F(1, 39) = 4.175; P = 0.048). Pairwise comparison of measurement times within the control group showed no significance, while within the experimental group, pairwise comparison of measurement times was significant (t(19) = 7.37; P = 0.001), leading to decreased perseverative error scores (Table 2).

Similarly, for conflict cost, another measure of cognitive flexibility, results of repeated-measures ANOVA (2 × 2) indicated a significant interaction effect (group × time). Follow-up analysis demonstrated that the groups did not significantly differ in the pre/posttest stages. However, pairwise comparison of measurement times within the experimental group was significant $(t (19) = 5.99; P = 0.001)$ , resulting in reduced conflict costs due to the VR training intervention.

Effect of VR intervention on ER skills

Considering that here, the ERC comprised two components: ERC-ER and ERC-LN, MANOVA with repeated-measures (utilizing Greenhouse–Geisser corrections for Mauchly’s test violation) and planned contrasts were applied for data analysis. Results from the ERC task scores, as presented in Table 3, indicated significant main effects of group and time, along with an interaction effect between group and measurement times.

Table 3.

Main and Interaction Effects Related to Overall Emotion Regulation Skills

	Wilks lambda value	F	df	P	Partial $η^{2}$
Group	0.83	3.78	(2, 37)	0.032	0.17
Time	0.199	74.35	(2,37)	<0.001	0.8
Time*Group	0.223	64.4	(2,37)	<0.001	0.77

Due to the observed significance of the interaction effect, it is inferred that the VR intervention has influenced at least one component of ER skills across measurement times. Consequently, univariate ANOVA tests were conducted to assess the impact of the VR intervention on each ER skill component in children with ASD (refer to Table 4).

Table 4.

Comparisons of Emotion Regulation Between and Within Groups at Different Times

	T1	T2	P value (time effect)	P value (interaction effect)	η²
ERC- (ER)
VR intervention group (M ± SD)	17 (4.5)	21.3 (4.5)	<0.001	0.014	0.149
Control Group (M ± SD)	16.85 (4.7)	17.8 (3.6)	0.57	0.014	0.149
P value (group effect)	0.89	0.011
ERC-N/L
VR intervention group (M ± SD)	39.25 (6.03)	33.75 (5.5)	<0.001	<0.001	0.743
Control group (M ± SD)	41.35 (5.72)	41.25 (6.12)	0.7	<0.001	0.743
P value (group effect)	0.86	<0.001

As demonstrated in Table 4, statistically significant interaction effects between the group and the repeated time factor were observed for the two components of ER skills (ERC-ER and ERC-LN). Follow-up contrast tests, comparing interaction scores within time intervals, are presented in Table 5. Consequently, the interaction between the group and the repeated time factor is notably significant between the pretest and posttest stages for both ER factors and emotion lability/negativity.

Table 5.

Within-Group Repeated Contrasts for Each Measure of the Emotion Regulation Skills

Source	Time	Type III SS	df	Mean square	F	p	Partial $η^{2}$
Time^* Group
ERC-ER	Level 1 vs. Level 2	136.9	1	136.9	6.66	0.014	0.149
ERC-LN	Level 1 vs. Level 2	291.6	1	291.6	109.9	<0.001	0.74

Discussion

This research sought to examine the impact of VR interventions on EFs and ER capabilities in male autistic children between the ages of 7 and 10. Results revealed that engaging in physical activities through VR significantly impacted ER skills and EFs in autistic children.

In this study, our aim is to elucidate the outcomes resulting from the moderating influence of exercise and physical activities with VR on ER ability. Subsequently, we delve into several hypotheses regarding the mediating role of EFs in ER ability.

Among the studies conducted in this field, the findings of the current study, which imply improvements in ER ability, are supported by meta-analysis results from studies conducted by Farashi et al., Karami et al., and Vukićević et al.^65–67 All of these studies indicate the effectiveness of therapeutic interventions with VR in treating individuals with autism, particularly in enhancing motor skills and emotion recognition.

In line with Gross’s process model of ER, the utilization of situational strategies (i.e., situation modification and situation selection), cognitive strategies (i.e., attentional deployment and cognitive reappraisal), and behavioral strategies (i.e., response modulation) can enhance the regulation of emotion responses. One of the predictions of Gross’s process model is that the earlier a regulatory strategy intervenes in the initial stages of the emotion generation cycle, the more effective it is.³⁸ Results from functional magnetic resonance imaging studies have also indicated that activation of prefrontal cortical regions associated with cognitive control and emotional processing, which exhibit overlapping functions, increases during the utilization of antecedent-focused ER strategies.^92,93 Some studies have demonstrated that physical exercises are beneficial for working memory,⁹⁴ and individuals with better working memory performance are likely to exhibit improved downregulation of emotions.⁹⁵ Engaging in physical activities within a VR environment appears to use situational strategies through multiple mechanisms, including detachment from intrusive and emotionally challenging thoughts, and avoiding the repetition of neural pathways associated with negative emotions (e.g., inhibiting the reinforcement of mental ruts) for ER. In addition, cognitive strategies such as attentional shifting, involving altering the focus of attention, induce changes in information processing and downregulate negative emotions. Also, according to the neurotrophic hypothesis, physical exercises stimulate the release of neurotrophic factors and neurotransmitters such as serotonin, norepinephrine, and dopamine. Moreover, these exercises contribute to the growth of nerve cells in the hippocampus, facilitating brain vascularization and the production of protective monoamines (i.e., brain plasticity).^22,57,96,97 These changes are closely tied to ER and EFs.⁹⁷ Therefore, engaging in sports training or adopting new learning experiences through VR interventions, which demand effortful control, has the potential to induce enduring changes. These changes could lead to enhanced neural and functional integration, ultimately contributing to improved cognitive health in autistic children.

When studying and examining the mediating role of EFs on ER abilities, it is crucial to acknowledge that training through various methods affects EFs. The co-occurrence of challenges in emotional and cognitive functions in autistic children suggests a shared relationship between these processes, potentially involving common brain structures such as the dorsolateral prefrontal cortex and ventrolateral prefrontal cortex, dorsal anterior cingulate cortex, dorsomedial prefrontal cortex, and orbitofrontal cortex, as well as other regions, such as the supplementary motor cortex and posterior parietal cortex.^98,99 Development in EF domains, including inhibition, working memory, and decision-making, is crucial for effective ER¹⁰⁰ and the initial development of self-regulation.¹⁰¹ Moreover, Conner et al. have highlighted that difficulties in EFs, particularly cognitive flexibility, are closely linked to emotional dysregulation in autistic children.¹¹ Therefore, there is a likelihood that the enhancement of EFs facilitates the development of ER abilities.¹⁰² In this research area, the findings of the current study align with Liao et al.’s research on the “Impact of Virtual Reality-Based Physical Training on Executive Function in Older Adults,” Nekar et al.’s investigation into the “Influence of Augmented Reality Training on Executive Functions in ASD,” and Liang et al.’s systematic review addressing “The Effects of Exercise Interventions on Executive Functions in Children and Adolescents with ASD.”^45,103,104

Physical exercise contributes significantly to the development of ER abilities through its positive impact on attention, awareness, and EFs. In addition, it helps mitigate the tendency for mental rumination thinking patterns (e.g., The maintenance and manipulation of negative emotional information in working memory, along with the difficulty in updating them)¹⁴ and can effectively slow down the cycle of generating negative emotions in emotionally charged situations.¹⁴ Notably, certain studies have indicated that activities involving distinct sensory input from muscles and joints, such as adopting specific vertical positions or engaging in isometric hand contractions or whole-body movements, can profoundly enhance basic emotions such as anger, fear, happiness, and sadness.¹⁰⁵ In another study, it has also been demonstrated that improving gross motor skills through physical activities modulates EFs, which in turn significantly affects emotion cognition. Moreover, emotion cognition is closely associated with ER strategies.¹⁰⁶ Exercise and physical activities utilizing VR seem to expose individuals to various situations and stimuli, thereby enhancing different components of EFs. Strengthening working memory facilitates the retention and updating of information related to diverse stimuli. Moreover, the ability to dissociate from an emotion response and reevaluate a situation, followed by engaging in more adaptive emotional responses, contributes to better inhibitory control. In addition, the ability to shift attention from unwanted and intrusive stimuli and to flexibly switch between different thoughts, stimuli, and situations will foster cognitive flexibility.¹⁰⁷ The utilization of these functions involves the engagement of a control system known as effortful control. In accordance with the effortful control hypothesis, engaging in exercise and physical activities that demand effort can lead to an enhancement in the strength of neural network connections associated with EFs.⁸⁵ In addition, these activities contribute to an increase in the capacity of the effortful control system located within the prefrontal cortex.⁹⁷ This system allocates necessary cognitive resources from the nervous system to facilitate the execution of EFs, enabling individuals to sustain their activity and uphold their objectives even in the face of competing demands from their environment and various tasks.^85,97,107 Thus, it appears that the VR interventions used in this study, requiring both effort and the utilization of executive control alongside the effortful control system, have effectively facilitated the practice of EFs. This enhancement is expected to result in sustained participation and cohesive engagement in physical activities among autistic children.

In addition, another suggested method for regulating emotions involves the utilization of movement imagery.¹⁰⁸ According to studies conducted by Adamovich et al. (2009), EbrahimiSani et al. (2020), Badia et al. (2012), and Piccione et al. (2019), engaging in physical exercises and VR games has been shown to be beneficial for training and enhancing the ability of motor imagery.^68–70,74 Furthermore, compelling evidence suggests that motor imagery demonstrates both functional and computational equivalence in motor representations for motor planning. This includes the activation of analogous networks of interneurons, as observed during actual performance.^{70,96,108–110} In addition, motor imagery has been demonstrated to potentially engage comparable pathways of emotion processing.¹⁰⁸ Glover et al. (2020) have emphasized that motor imagery demands a greater utilization of executive resources compared with actual execution. Considering the inclusion of VR exercises in the current study, necessitating both practical implementation and the cultivation of motor imagery skills, it appears that EFs will be more prominently engaged, practiced, and developed compared with actual execution. So, when confronted with factors and situations that elicit incompatible emotional responses (e.g., specific situations), engaging in guided motion imagery can induce a shift in attention toward the emotional responses associated with the imagery, fostering adaptive responses. This aligns with the second phase of the process model of emotion generation proposed by Gross (1998). Building upon the proposition by Shafir et al. (2016),¹⁰⁵ engaging in and observing mentally simulating movements that elicit specific emotions can heighten the corresponding emotion responses, rendering them viable tools for ER. In general, the results of the present study support the hypothesis that improving EFs through exercise and physical activity in a VR environment likely contributes to the development of adaptive ER abilities in autistic children.

However, the current study has several limitations that warrant consideration. First, the collection of ER data through a parent-administered self-report scale poses a limitation. To enhance the depth of investigation and confirm the findings, future research should explore additional physiological and neurological responses associated with emotions. This would provide a more comprehensive understanding of the ER process. Furthermore, considering that the initiation and maintenance of behavioral changes are strongly associated with EFs,⁹⁶ it is crucial to determine how enhancing each component of EF through intervention programs can influence ER strategies.

In the present study, VR training interventions were used to investigate behavioral changes relevant to ER abilities. However, it is crucial to explore the stability and long-term durability of these behavioral and cognitive changes. Such insights are pivotal for understanding their influence on the adoption of healthy behaviors and the level of commitment to physical activities, particularly within the context of autistic children. Moreover, following Gross’s process model, the effectiveness of exercise and activity in enhancing ER is contingent on the activities being both demanding and enjoyable. Therefore, a separate study should be conducted to scrutinize the nature and intensity of these activities, contributing to a more nuanced understanding of their impact. Furthermore, the absence of an exploration into gender differences, due to limited access to female participants, is an important limitation. Since girls may encounter distinct challenges in executive and behavioral functions, future research should strive to address this gap. In addition, the awareness of parents regarding their child’s training group may introduce bias in their reported results concerning ER. This awareness could influence their interpretation of their child’s emotional progress, thus warranting caution in interpreting these findings. Given that in the present study, the effect of VR exercises on EFs and ER abilities was inferred based on the assumed mediating role of EFs, it is recommended that future studies separately examine both the mediating and moderating effects of EFs on the ER abilities of autistic children. Another limitation of this study is the absence of an active control condition. Including such a condition in future studies would allow for a comparison that could demonstrate the effectiveness of the investigated intervention in relation to an active control group. Lastly, although motor imagery likely contributes to the observed effects of VR exercises on ER, its specific impact on motor imagery ability in autistic children remains a subject for future investigation. Despite these limitations, the present study used an innovative training approach to investigate cognitive and behavioral variables in autistic children, marking a significant contribution to the field.

Conclusion

Autistic individuals are particularly susceptible to mental and physical health risks, emphasizing the importance of targeted interventions in this domain. The current study investigated the impact of VR interventions on the EFs and ER of male autistic individuals. The outcomes revealed a beneficial impact stemming from eight weeks of VR exercises, demonstrating a positive influence on EFs and ER, and a reduction in emotional instability among male autistic children. VR games, incorporating features such as attractiveness, enhanced feedback, interactivity, a strong sense of presence, and the cultivation of motor imagery skills, offer a multifaceted approach for autistic children. These games facilitate the acquisition of rewards, pleasure, and a diverse range of movement experiences, concurrently fostering the development of EFs. Beyond augmenting EFs through VR exercises, which promote the amalgamation of physical activity and the adoption of health-conscious behaviors, the orchestration and regulation of emotion responses are steered by the allocation of attentional resources to VR activities and games. Moreover, VR interventions, characterized by their accessibility, affordability, and lack of detrimental side effects, emerge as a valuable avenue for ER across various disorders. Although this approach holds the potential as an effective and convenient intervention to modulate emotions, thereby contributing to enhanced well-being, caution should be exercised when interpreting the results of this study. Data related to the adverse and detrimental side effects of VR technology were not collected or reported. Implementing a VR intervention program within a limited time frame, there is the possibility that excessive usage, when compared with traditional games for children, could lead to complications.

Footnotes

Acknowledgments

We would like to express our gratitude to the children who participated in our research, as well as to the parents, center staff, and authorities who granted permission for the study to be conducted. Furthermore, the study is supported by both the University of Payme Noor and the Ministry of Education, emphasizing the credibility of the research conducted within institutions dedicated to education or research.

Authors’ Contributions

H.S.B.: Conceptualization, methodology, writing—original draft preparation, writing—reviewing and editing, investigation, and project administration; S.E.S.: Data curation, writing—original draft preparation, methodology, software, and project administration; B.B.: Writing—supervision and data analyzing.

Confirmation Statement

H.S.B. is from Payame Noor University (Tehran, Iran); S.E.S. is from Ferdowsi University of Mashhad (Mashhad, Iran); and B.B. is from the University of Tabriz (Tabriz, Iran), all where education and research are the primary functions.

Compliance with Ethical Standards

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed Consent

Informed consent to participate and publication was obtained from all children and their parents included in the study.

Submission Declaration and Verification

By submitting this article, we affirm that the content presented has not been previously published and is not currently being considered for publication in any other venue. The publication of this work has been duly authorized by all authors and has received the necessary approvals from the responsible authorities at the institution where the research was conducted. Furthermore, if accepted, we commit to not publishing the same content elsewhere, in its current form, whether in English or any other language, including electronic formats, without obtaining written consent from the copyright holder.

Data Sharing

Authors will accommodate reasonable requests for materials, methods, or data essential for reproducing or validating the research findings whenever necessary.

Author Disclosure Statement

The authors declare that they have no conflict of interest.

Funding Information

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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