Majid Naeeimi; Seyed Ali Hosseini; Akbar Biglarian; Nasrin Amiri; Ebrahim Pishyareh* Pediatric Neurorehabilitation Research center the University of Social Welfare and Rehabilitation Sciences, Tehran, Iran
Introduction Autism is one subset of pervasive developmental disorders that are characterized by abnormal behaviors and verbal communication (1). High-functioning autism is a group of children with autism that have sustained impairment in nonverbal behaviors, using repetitive patterns in favorite things and interpersonal relationship dysfunction (2). Statistics obtained from research centers in the US imply an increase of 10% to 17% annual risk of this disorder (3).
However, the core impairment in autism is a communication disorder. In recent years, the reason for this communication disorder has been developed for determining executive function in autism (4, 5). Executive functions is an umbrella term for cognitive processes that regulate, control, and manage other cognitive processes such as planning, working memory, attention, problem solving, verbal reasoning, inhibition, mental flexibility, task switching, initiation and monitoring of actions (6-8).
Executive dysfunction not only causes difficulty in communication skills to children with autism but can also destroy activities of daily living in this group of children (9). In 2009, the results of a study conducted by Kenworthy on children with high-functioning autism indicated a significant relationship between executive dysfunction and symptoms of autism (impaired communication skills, social skills, and repetitive behaviors). In this study, planning, shifting, and inhibition abilities were more emphases (10). Therefore, in this study, these three variables have been studied. Despite this research has been conducted in the field of executive dysfunction in children with autism spectrum disorder preschoolers and its interventions (11). During a recent investigation, it has been demonstrated that effective behavioral interventions for children with high-
functioning autism such as Applied Behavior Analysis and developmental interventions such as sensory integration therapy has positive effects on children’s cognitive skills, such as working memory, planning, and decision-making (12). Alternatively, a new form of treatment for children with high-functioning autism is neurofeedback that aims to influence or change irregular activities of brain waves. Neurofeedback is designed to train individuals to enhance poorly regulated brainwave patterns by using sophisticated computer technology (13).
The beneficial effects of neurofeedback on shifting, working memory, attention control, and reduction of negative behaviors in children with high-functioning autism have been reported (14). While interventions based on education through rehabilitation approaches can be effective in improving impaired executive functioning in autistic children, Pharmacotherapy and psychosocial interventions such as family therapy and behavior therapy for improving social deficits and reduce impulsive behavior would be useful in this group of children (14, 15). But audiovisual stimulation has been selected as an intervention in this study, using entrainment would Try to change the brain’s response to external changes and would do this by changing the link between different areas of the cortex (16). AVE consists of constant, repetitive stimuli of the proper frequency and sufficient strength to “excite” the thalamus and neocortex.
These stimuli do not transfer energy directly into the cortex. The direct transmission of energy from AVE only goes so far as to excite retinal cells in the eyes and pressure-sensitive cilia within the cochlea in the ears. The nerve pathways from the eyes and ears carry the elicited electrical potentials into the thalamus. From there, the entrained electrical activity within the thalamus is “amplified” and distributed throughout other limbic areas and the cerebral cortexes via the cortical thalamic loop. AVS involves the continuous electrical response of the brain in relation to the stimulus frequency plus the mathematical representation (harmonics) of the stimulus wave shape (17). AVS is believed to achieve its effects through several mechanisms simultaneously. These include altered EEG activity, dissociation / hypnotic induction, limbic stabilization, improved neurotransmitter production, and altered cerebral blood flow (17). Previous studies with Audiovisual stimulation has been conducted mostly in children with ADHD (18). The results in these researches indicated a significant improvement in the children’s working memory, sustain attention, and planning (16).
In another study of audiovisual stimulation effects on school-age children with autism, the results cleared a significant increase in attention, shifting, and decrease repetitive movements (16). The present study investigated the effects of audiovisual stimulation on executive functioning in high function autistic children. It appears that due to the growing and unpredictability prevalence of the autistic disorder, damaging effects on quality of life (especially the activities of daily living), the lack of a specific treatment plan and executive difficulties of previous methods, Using a low-cost approach, specific, measurable, and fewer complications such as audiovisual stimulation, could affect the areas of executive function in autistic disorder improving underlying impairments in social skills, communication skills and reducing repetitive behaviors in these children (16, 18). Methods This study is a clinical trial. The participants in this study consist of 41 high-functioning autism spectrum disorders in children 5 to 8 years old who were referred to Tehran’s Autism Charity. After the selection of the patients referred to Tehran’s Autism Charity, the participants were randomly assigned to a specific category. The independent variable in this study was audiovisual stimulation; on the other hand, the dependent variables were increasing three main subgroups of executive function (inhibition, shifting, and planning).
All children who participated in the study needed to 5 to 8 years old diagnosed as high-functioning autism by a verified child psychiatrist. On the other hand, after a clear description of the research objectives, parents were asked to complete a consent survey form to have their children participate in the research. It is worth noting that the authorization of this study was under supervision and verification of the University of Social Welfare and Rehabilitation Sciences. Autism Charity Foundation announced readiness to cooperate with the researcher for this study. There is no limit to the use of the drug and the researcher was committed if manifest of beneficial effects of audiovisual stimulation were observed in the experimental group, this intervention will be performed free of charge for the control group as well. However, children who had participated in similar studies, a history of seizures, neurological disorders, IQs lower 70, and lack of cooperation during the assessment and treatment, were excluded from the study. Data were collected using’ Behavioral Ratings of executive function (parent form) “. The evaluation was conducted in two stages, prior to and after the intervention.
The Behavior Rating Inventory of Executive Function (BRIEF) developed by Gerard Gioia, Ph.D., Peter Isquith, Ph.D., Steven Guy, Ph.D., and Lauren Kenworthy, Ph.D., is an assessment of executive function behaviors at home and at school for children and adolescents aging 5 to 18. The 86-item questionnaire has separate forms for parents and teachers, and typically takes 10–15 minutes to administer and 15–20 minutes to score. The BRIEF is useful for evaluating children with a variety of disorders and disabilities. Specifically, it is often used for assessing executive functioning in children with developmental and/or acquired neurological conditions including learning disabilities, Tourette syndrome, traumatic brain injury, pervasive developmental disorders, high functioning autism, low birth weight. The BRIEF is most often used to assess Attention-Deficit/Hyperactivity Disorder (19). Each form of the BRIEF parent- and teacher- rating form contains 86 items in eight non-overlapping clinical scales and two validity scales.
These are theoretically and statistically derived scales form two indexes: a) Behavioral Regulation (Inhibit, Shifting and Emotional Control), and b) Metacognition (Initiate, Working memory Plan/Organize, Organization of materials, Monitor). An experimental instrument in this study was David Pal’s unit that is manufactured by Mind Alive Inc. This device consists of a main controller, a headset, a forward glasses a wire, and a power supply interface. There are buttons on the unit to adjust the power button, select button (to select the type of incentive program), light intensity and volume buttons, as well as a part input adapter to connect with. It has 18 default programs of audiovisual stimulation that have been used in children with ADHD or LD. The audiovisual stimulation plan in this study was A 5 program with volume 2 and light intensity 3. It includes 35 minutes of decreasing Stimulation 19 to 10 Hz frequencies which have been extremely effective in increasing the ability to control attention and planning in children with attention deficit disorder, according to recent research (17). Following that, the children are referred to the Autism Charity Foundation in which they would be prepared with a soft toy phone and glasses during two sessions to be conducted for constant 35 minutes use of the audiovisual units in each session. The intervention procedure consisted of 18 sessions of 35-minute long over 6 weeks by 3 sessions per week.
As can be seen from the mean of each variable, inhibition, shifting, and planning, have been significantly reduced in the experimental group. Table (2) presents the results of covariance analysis in order to prove the research hypothesis. The followings are the results of covariance analysis to test each of the research hypotheses: 1. Audiovisual stimulation used in this study increases inhibition ability in high-functioning autism children based on the Behavior Rating Inventory of Executive Functioning measures.
Both intervention and control groups continued their usual rehabilitation programs such as occupational therapy, speech therapy, education, and play therapy during the conduction of audiovisual stimulation sessions. Data were analyzed using SPSS.20 software. After testing Kolmograph-Smirnov and ensure normal distribution of the data, parametric tests were used. Descriptive statistics (mean and SD) in each group were reported. In the following section, multivariate analysis was used to compare significant advances in executive function progress. Results In this research, for the quantitative data collection and testing the hypothesis, descriptive and inferential statistical methods were used. To demonstrate the variable frequency table was also used showing the frequency, mean, standard deviation, and descriptive diagrams. The mean and standard deviation of the test subjects in both groups, before and after the intervention are shown in Table (1).
Audiovisual stimulation used in this study, increase shifting ability in high-functioning autism children based on the Behavior Rating Inventory of Executive Functioning measures. 3. Audiovisual stimulation used in this study, increase planning ability in high-functioning autism children based on the Behavior Rating Inventory of Executive Functioning measures.
Based on the results shown in Table (2), the F between-group variable for inhibition, shifting, and planning are respectively 5/55 ،24/587, 15/28. Considering the significance level, the outcome indicates that audiovisual stimulation used in the present study increased inhibition, shifting and planning ability based on the Behavior Rating Inventory of Executive Functioning measures (F= 5/55, P<0/05, F= 24/587, P< 0/05, F= 15/28, p<0/05). As can be seen in Figure (1) inhibition, shifting and planning ability scores in the experimental group had declined and this means that audiovisual stimulation used in this study, increase inhibition, shifting and planning ability in high-functioning autism children based on Behavior Rating Inventory of Executive Functioning measures while the control group had not.
Discussion This study is among the first studies in the field of audiovisual stimulation to enhance the capabilities of executive function in children with high-functioning autism. Audiovisual stimulation is fully configurable by therapists that use repeated, instant and safe stimulation for effectiveness in inhibition, shifting, and planning abilities. After 18 sessions of intervention by the audiovisual stimulation, according to the significant differences in pre-test and post-test scores of the variables, considerable progress on all three variables (the ability to inhibit the ability to shift and ability to plan) has been made. These findings indicate the potential utility of this stimulus to test the possibility of using other subsets of executive function such as working memory, organization of material, and emotional control in children with high functioning autism.
Similar to previous research, the results of this study suggest audiovisual stimulation is effective in enhancing inhibition ability in children with high-functioning autism. As Woodbury in 1996 stated this stimulation increases the ability to inhibit and control impulsivity in children with high functioning autism, the findings of this study also showed the same results (16). Similarly, Damasio in his studies cited that one of the reasons for, impaired inhibition ability in autism disorder would be the poor performance of the prefrontal region of the brain that audiovisual stimulation also impacts this area (20). In addition, the findings in this study show the ability to shift in children participating in the study increased as a result of audiovisual stimulation and this is consistent with results in Olmstead’s study 2005, in children with attention deficit hyperactivity disorder and learning disability (16).
Of course Interventions including 12 sessions, two times a week, were conducted by Olmstead in comparison with intervention in this study was long and expensive to the researcher. On the other hand, it was found reducing the length of time in intervention sessions would not be a barrier to the effectiveness of audiovisual stimulation. Another important subset of executive function was examined in the present study, planning ability; there was a significant improvement in results. Carter and Russell In 1994, a study was done on children with learning disorders, have also achieved such results (21). In addition to the results in the shifting ability in children with attention deficit hyperactivity disorder and learning, disorder had taken by Olmstead, in 2005, satisfying results on planning ability also reported in her study (16). Conclusion Overall, the interventions were used in this study as a method of rehabilitation programs and software to improve the executive function of autistic children.
Limitations of the study included differences in symptoms, age, and cultural conditions of each of the participants that complicated the generalizability of results to other autistic children. Because children with autism have sensory problems, wearing sunglasses and headphones in a certain period of time in initial sessions seemed to be difficult. Moreover, the original study with more control is needed to validate the findings. In future research, it is better to use the larger sample sizes for the intervention of the new methods that can be varied according to patient age and diagnosis. Also, conducting a follow-up study on the effects of such interventions could help to register the sustainability of results. However, regarding the mechanism of audiovisual stimulation conducting this research in other disorders such as cerebral palsy, neurological, brain damage, and mental retardation considered to be useful. Furthermore, the use of more precise assessment measures such as QEEG during audiovisual stimulation intervention can prove essential in providing additional useful information on the mechanism of action of these stimuli to the researcher. Overall the current investigation provides preliminary evidence for the feasibility and use of audiovisual stimulation intervention in children with high functioning autism. Similarly, the use of such technology that is user-friendly appears to prevent the onset of early behavioral problems, cognitive and executive dysfunction in children with autism. Acknowledgments The authors would like to appreciate the efforts of the Autism Charity Foundation President and all families and colleagues who have helped in this research. In addition, special thanks go to Dr. Harold Russell and Dr. Patricia Woodbury for sharing valuable information.
References 1. Brzezinski R, Huerta M, Lord C. DSM-5, and autism spectrum disorders (ASDs): An opportunity for identifying ASD subtypes. Molecular autism. 2013;4(1):1-6. 2. Baumer-Zviely N. Social and academic abilities in children with high-functioning autism spectrum disorders: Guilford Press; 2013. 3. Harpaz R, Ortega-Sanchez I, Seward J. The United States Centers for Disease Control and Prevention. Prevention of Herpes Zoster: Recommendations of the Advisory Committee on Immunization Practices. 2013. 4. Hill EL. Executive dysfunction in autism. Trends in Cognitive Sciences. 2004;8(1):26-32. 5. Ozonoff S. Components of executive function in autism and other disorders. 1997. 6. Elliott R. Executive functions and their disorders Imaging in clinical neuroscience. British Medical Bulletin. 2003; 65(1):49-59. 7. Monsell S. Task switching. Trends in Cognitive Sciences. 2003;7(3):134-40. 8. Chan RC, Shum D, Toulopoulou T, Chen EY. Assessment of executive functions: Review of instruments and identification of critical issues. Archives of Clinical Neuropsychology. 2008;23(2):201-16. 9. Pennington BF, Ozonoff S. Executive functions and developmental psychopathology. Journal of Child Psychology and Psychiatry. 1996;37(1):51-87. 10. Kenworthy L, Black DO, Harrison B, Della Rosa A, Wallace GL. Are executive control functions related to autism symptoms in high-functioning children? Child Neuropsychology. 2009;15(5):425-40. 11. Colón-Torres M. Executive Functions of Preschool Children with Autism Spectrum Disorders: Indiana University of Pennsylvania; 2011. 12. Hormones N. Early comprehensive interventions for children with autism| A meta-analysis: the university of UTAH; 2006. 13. Coben R, Linden M, Myers TE. Neurofeedback for autistic spectrum disorder: a review of the literature. Applied Psychophysiology and Biofeedback. 2010;35(1):83-105. 14. Kouijzer ME, van Schie HT, de Moor JM, Gerrits BJ, Buitelaar JK. Neurofeedback treatment in autism. Preliminary findings in behavioral, cognitive, and neurophysiological functioning. Research in Autism Spectrum Disorders. 2010;4(3):386-99. 15. Barkley RA, Grodzinsky G, DuPaul GJ. Frontal lobe functions in attention deficit disorder with and without hyperactivity: A review and research report. Journal of abnormal child psychology. 1992;20(2):163-88. 16. Olmstead R. Use of auditory and visual stimulation to improve cognitive abilities in learning-disabled children. Journal of Neurotherapy. 2005;9(2):49-61. 17. Siever D, Evans J. Audio-visual entrainment: History, physiology, and clinical studies. Handbook of neurofeedback: Dynamics and clinical applications. 2007:155-83. 18. Siever D. Applying audio-visual entrainment technology for attention and learning (Part 3). Biofeedback Magazine. 2008;31(4). 19. Gioia GA, Isquith PK, Retzlaff PD, Espy KA. Confirmatory factor analysis of the Behavior Rating Inventory of Executive Function (BRIEF) in a clinical sample. Child Neuropsychology. 2002;8(4):249-57. 20. Damasio AR, Maurer RG. A neurological model for childhood autism. Archives of neurology. 1978;35(12):777. 21. Carter J, Russell H. An audio-visual stimulation unit with EEG biofeedback for the treatment of learning disabilities: Final report. Washington, DC: US Department of Education SBIR Phase I Contract Number: RN. 1994;93082027.