Transcranial direct current stimulation and cognitive stimulation therapy in children with autism spectrum disorder: randomized, sham-controlled, double-blind, crossover, clinical trial
Keywords:Autism spectrum disorder, Transcranial direct current stimulation, Social cognition, Executive functions, Neuromodulation
BACKGROUND: Transcranial direct current stimulation (tDCS) is a non-invasive neuromodulation technic that has been researched as a therapeutic alternative to reduce symptoms and improve cognitive functioning in many disorders, including autism spectrum disorder (ASD), a neurodevelopmental disorder in which functional changes are observed in some brain structures, damaging different areas of the individual’s lives. OBJECTIVE: To compare the effects of active and sham transcranial direct current stimulation during cognitive stimulation tasks training in children with an autism spectrum disorder. METHODS: A randomized, sham-controlled, double-blind, crossover clinical trial was conducted. Twelve children with ASD underwent ten cognitive training sessions combined with active and sham tDCS. Anodal tDCS was administered over the left dorsolateral prefrontal cortex (DLPFC). Executive functions and social cognition were evaluated before, after, and three months after (follow-up) the intervention. RESULTS: No differences were found in the effects between the two interventions. Considering the mean results before and after active tDCS, improvements were seen in the theory of mind function (pre-intervention: 14.58 ± 5.04; post-intervention: 17.08 ± 5.21 [d2 = 0.51)]; follow-up: 16.92 ± 5.52 [d2 = 0.46]) and inhibitory control (pre-intervention: -1.31 ± 1.90; follow-up: 0.25 ± 1.14, d2 = 1.04). CONCLUSION: The administration of active tDCS over the left DLPFC during the training of cognitive stimulation tasks did not result in superior effects compared to sham tDCS combined with training in children with an autism spectrum disorder.
(1) APA. AMERICAN PSYCHIATRIC ASSOCIATION. Manual Diagnóstico e Estatístico de Transtornos Mentais - DSM-5. 5th ed. Porto Alegre: Artmed; 2014.
(2) Baldimtsi E, Nicolopoulou A, Tsimpli IM. Cognitive and Affective Aspects of Theory of Mind in Greek-Speaking Children with Autism Spectrum Disorders. J Autism Dev Disord. 2021;51:1142–56. https://doi.org/10.1007/s10803-020-04595-0.
(3) Berenguer C, Roselló B, Colomer C, Baixauli I, Miranda A. Children with autism and attention deficit hyperactivity disorder. Relationships between symptoms and executive function, theory of mind, and behavioral problems. Res Dev Disabil. 2018;83:260–9. https://doi.org/10.1016/j.ridd.2018.10.001.
(4) Kouklari E-C, Tsermentseli S, Monks CP. Developmental trends of hot and cool executive function in school-aged children with and without autism spectrum disorder: Links with theory of mind. Dev Psychopathol. 2019;31(2):541–56. https://doi.org/10.1017/S0954579418000081.
(5) Peterson CC, Wellman HM, Slaughter V. The Mind Behind the Message: Advancing Theory-of-Mind Scales for Typically Developing Children, and Those With Deafness, Autism, or Asperger Syndrome. Child Dev. 2012;83(2):469–85. https://doi.org/10.1111/j.1467-8624.2011.01728.x.
(6) Valeri G, Casula L, Napoli E, Stievano P, Trimarco B, Vicari S, et al. Executive Functions and Symptom Severity in an Italian Sample of Intellectually Able Preschoolers with Autism Spectrum Disorder. J Autism Dev Disord. 2020;50:3207–15. https://doi.org/10.1007/s10803-019-04102-0.
(7) Happé F, Cook JL, Bird G. The Structure of Social Cognition: In(ter)dependence of Sociocognitive Processes. Annu Rev Psychol. 2017;68:243–67. https://doi.org/10.1146/annurev-psych-010416-044046.
(8) Pinkham AE, Penn DL, Green MF, Buck B, Healey K, Harvey PD. The Social Cognition Psychometric Evaluation Study: Results of the Expert Survey and RAND Panel. Schizophr Bull. 2014;40(4):813–23. https://doi.org/10.1093/schbul/sbt081.
(9) Diamond A. Executive functions. Annu Rev Psychol. 2013;64:135–68. https://doi.org/10.1146/annurev-psych-113011-143750.
(10) Carlson SM, Zelazo PD, Faja S. Executive function. In: Zelazo PD. The Oxford handbook of developmental psychology, Vol. 1. 1st ed.. Oxford: Oxford University Press; 2013. p. 706–43.
(11) Dias NM, Seabra AG. Intervention for executive functions development in early elementary school children: effects on learning and behaviour, and follow-up maintenance. Educ Psychol (Lond). 2017;37(4):468–86. https://doi.org/10.1080/01443410.2016.1214686.
(12) Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. The Unity and Diversity of Executive Functions and Their Contributions to Complex “Frontal Lobe” Tasks: A Latent Variable Analysis. Cogn Psychol. 2000;41(1):49–100. https://doi.org/10.1006/cogp.1999.0734.
(13) Brignell A, Chenausky KV, Song H, Zhu J, Suo C, Morgan AT. Communication interventions for autism spectrum disorder in minimally verbal children. Coch Datab Syst Rev. 2018;11:CD012324. https://doi.org/10.1002/14651858.CD012324.pub2.
(14) Liang X, Li R, Wong SHS, Sum RKW, Wang P, Yang B, et al. The Effects of Exercise Interventions on Executive Functions in Children and Adolescents with Autism Spectrum Disorder: A Systematic Review and Meta-analysis. Sports Med. 2022;52:75–88. https://doi.org/10.1007/s40279-021-01545-3.
(15) Sharma S, Hucker A, Matthews T, Grohmann D, Laws KR. Cognitive behavioural therapy for anxiety in children and young people on the autism spectrum: a systematic review and meta-analysis. BMC Psychol. 2021;9:151. https://doi.org/10.1186/s40359-021-00658-8.
(16) Tan BWZ, Pooley JA, Speelman CP. A Meta-Analytic Review of the Efficacy of Physical Exercise Interventions on Cognition in Individuals with Autism Spectrum Disorder and ADHD. J Autism Dev Disord. 2016;46:3126–43. https://doi.org/10.1007/s10803-016-2854-x.
(17) Virues-Ortega J, Julio FM, Pastor-Barriuso R. The TEACCH program for children and adults with autism: A meta-analysis of intervention studies. Clin Psychol Rev. 2013;33(8):940–53. https://doi.org/10.1016/j.cpr.2013.07.005.
(18) Weston L, Hodgekins J, Langdon PE. Effectiveness of cognitive behavioural therapy with people who have autistic spectrum disorders: A systematic review and meta-analysis. Clin Psychol Rev. 2016;49:41–54. https://doi.org/10.1016/j.cpr.2016.08.001.
(19) Amatachaya A, Auvichayapat N, Patjanasoontorn N, Suphakunpinyo C, Ngernyam N, Aree-Uea B, et al. Effect of anodal transcranial direct current stimulation on autism: A randomized double-blind crossover trial. Behav Neurol. 2014;2014:173073. https://doi.org/10.1155/2014/173073.
(20) Costanzo F, Menghini D, Casula L, Amendola A, Mazzone L, Valeri G, et al. Transcranial Direct Current Stimulation Treatment in an Adolescent with Autism and Drug-Resistant Catatonia. Brain Stimul. 2015;8(6):1233–5. https://doi.org/10.1016/j.brs.2015.08.009.
(21) Wilson JE, Trumbo MC, Wilson JK, Tesche CD. Transcranial direct current stimulation (tDCS) over right temporoparietal junction (rTPJ) for social cognition and social skills in adults with autism spectrum disorder (ASD). J Neural Transm. 2018;125:1857–66. https://doi.org/10.1007/s00702-018-1938-5.
(22) Wilson JE, Quinn DK, Wilson JK, Garcia CM, Tesche CD. Transcranial Direct Current Stimulation to the Right Temporoparietal Junction for Social Functioning in Autism Spectrum Disorder. J ECT. 2018;34(1):e10–3. https://doi.org/10.1097/YCT.0000000000000445.
(23) Gómez L, Vidal B, Maragoto C, Morales L, Berrillo S, Cuesta HV, et al. Non-Invasive Brain Stimulation for Children with Autism Spectrum Disorders: A Short-Term Outcome Study. Behav Sci. 2017;7(3):63. https://doi.org/10.3390/bs7030063.
(24) Schneider HD, Hopp JP. The use of the Bilingual Aphasia Test for assessment and transcranial direct current stimulation to modulate language acquisition in minimally verbal children with autism. Clin Linguist Phon. 2011;25(6-7):640–54. https://doi.org/10.3109/02699206.2011.570852.
(25) Steenburgh JJ, Varvaris M, Schretlen DJ, Vannorsdall TD, Gordon B. Balanced bifrontal transcranial direct current stimulation enhances working memory in adults with high-functioning autism: a sham-controlled crossover study. Mol Autism. 2017;8:40. https://doi.org/10.1186/s13229-017-0152-x.
(26) Zhou T, Kang J, Li Z, Chen H, Li X. Transcranial direct current stimulation modulates brain functional connectivity in autism. Neuroimage Clin. 2020;28:102500. https://doi.org/10.1016/j.nicl.2020.102500.
(27) Wilson J, Andrews G, Hogan C, Wang S, Shum DHK. Executive function in middle childhood and the relationship with theory of mind. Dev Neuropsychol. 2018;43(3):163–82. https://doi.org/10.1080/87565641.2018.1440296.
(28) Costanzo F, Varuzza C, Rossi S, Sdoia S, Varvara P, Oliveri M, et al. Reading changes in children and adolescents with dyslexia after transcranial direct current stimulation. Neuroreport. 2016;27(5):295–300. https://doi.org/10.1097/WNR.0000000000000536.
(29) Soff C, Sotnikova A, Christiansen H, Becker K, Siniatchkin M. Transcranial direct current stimulation improves clinical symptoms in adolescents with attention deficit hyperactivity disorder. J Neural Transm. 2017;124:133–44. https://doi.org/10.1007/s00702-016-1646-y.
(30) Sotnikova A, Soff C, Tagliazucchi E, Becker K, Siniatchkin M. Transcranial Direct Current Stimulation Modulates Neuronal Networks in Attention Deficit Hyperactivity Disorder. Brain Topogr. 2017;30:656–72. https://doi.org/10.1007/s10548-017-0552-4.
(31) Amatachaya A, Jensen MP, Patjanasoontorn N, Auvichayapat N, Suphakunpinyo C, Janjarasjitt S, et al. The short-term effects of transcranial direct current stimulation on electroencephalography in children with autism: A randomized crossover controlled trial. Behav Neur. 2015;2015:928631 . https://doi.org/10.1155/2015/928631.
(32) Schneider HD, Hopp JP. The use of the Bilingual Aphasia Test for assessment and transcranial direct current stimulation to modulate language acquisition in minimally verbal children with autism. Clin Linguist Phon. 2011;25:640–54. https://doi.org/10.3109/02699206.2011.570852.
(33) Nejati V, Salehinejad MA, Nitsche MA, Najian A, Javadi A-H. Transcranial Direct Current Stimulation Improves Executive Dysfunctions in ADHD: Implications for Inhibitory Control, Interference Control, Working Memory, and Cognitive Flexibility. J Atten Disord. 2017;24(13):1928–43. https://doi.org/10.1177/1087054717730611.
(34) Brooks BL, Sherman EMS, Strauss E. NEPSY-II: A Developmental Neuropsychological Assessment, Second Edition. Child Neuropsychology 2009;16(1):80–101. https://doi.org/10.1080/09297040903146966.
(35) Trevisan BT, Dias NM, Seabra AG. Teste Infantil de Nomeação. Avaliação Neuropsicológica Cognitiva: Linguagem Oral . 1st ed. São Paulo: Memnon; 2012.
(36) Sedó M, Paula JJ, Malloy-Diniz LF. FDT - Teste dos Cinco Dígitos. São Paulo: Hogrefe; 2015.
(37) Brunoni AR, Amadera J, Berbel B, Volz MS, Rizzerio BG, Fregni F. A systematic review on reporting and assessment of adverse effects associated with transcranial direct current stimulation. Inter J Neuropsychopharm. 2011;14(8):1133–45. https://doi.org/10.1017/S1461145710001690.
(38) Gill J, Shah-Basak PP, Hamilton R. It’s the Thought That Counts: Examining the Task-dependent Effects of Transcranial Direct Current Stimulation on Executive Function. Brain Stimul. 2015;8(2):253–9. https://doi.org/10.1016/j.brs.2014.10.018.
(39) Segrave RA, Arnold S, Hoy K, Fitzgerald PB. Concurrent Cognitive Control Training Augments the Antidepressant Efficacy of tDCS: A Pilot Study. Brain Stimul. 2014;7(2):325–31. https://doi.org/10.1016/j.brs.2013.12.008.
(40) Claro R. Onde está o absurdo? Cartas para identificar situações fora do comum. 1st ed. São Paulo: Matrix; 2017.
(41) Claro R. Que emoção é esta? Cartas com desenhos para criança identificar as emoções. 1st ed. São Paulo: Matrix; 2018.
(42) Luckhardt C, Boxhoorn S, Schütz M, Fann N, Freitag CM. Brain stimulation by tDCS as treatment option in Autism Spectrum Disorder—A systematic literature review. Prog Brain Res. 2021;264:233–57. https://doi.org/10.1016/bs.pbr.2021.03.002.
(43) Khaleghi A, Zarafshan H, Vand SR, Mohammadi MR. Effects of Non-invasive Neurostimulation on Autism Spectrum Disorder: A Systematic Review. Clin Psychopharma Neuro. 2020;18(4):527–52. https://doi.org/10.9758/cpn.2020.18.4.527.
(44) Hadoush H, Nazzal M, Almasri NA, Khalil H, Alafeef M. Therapeutic Effects of Bilateral Anodal Transcranial Direct Current Stimulation on Prefrontal and Motor Cortical Areas in Children with Autism Spectrum Disorders: A Pilot Study. Autism Res. 2020;13(5):828–36. https://doi.org/10.1002/aur.2290.
(45) García-González S, Lugo-Marín J, Setien-Ramos I, Gisbert-Gustemps L, Arteaga-Henríquez G, Díez-Villoria E, et al. Transcranial direct current stimulation in Autism Spectrum Disorder: A systematic review and meta-analysis. Euro Neuropsychopharma. 2021;48:89–109. https://doi.org/10.1016/j.euroneuro.2021.02.017.
(46) Pineda-Alhucema W, Aristizabal E, Escudero-Cabarcas J, Acosta-López JE, Vélez JI. Executive Function and Theory of Mind in Children with ADHD: a Systematic Review. Neuropsychol Rev 2018;28:341–58. https://doi.org/10.1007/s11065-018-9381-9.
(47) Mahmoodifar E, Sotoodeh MS. Combined Transcranial Direct Current Stimulation and Selective Motor Training Enhances Balance in Children With Autism Spectrum Disorder. Percept Mot Skills. 2020;127(1):113–25. https://doi.org/10.1177/0031512519888072.
(48) Panikratova YR, Vlasova RM, Akhutina T v., Korneev AA, Sinitsyn VE, Pechenkova E v. Functional connectivity of the dorsolateral prefrontal cortex contributes to different components of executive functions. Int J Psychophys. 2020;151:70–9. https://doi.org/10.1016/j.ijpsycho.2020.02.013.
(49) Soltaninejad Z, Nejati V, Ekhtiari H. Effect of Anodal and Cathodal Transcranial Direct Current Stimulation on DLPFC on Modulation of Inhibitory Control in ADHD. J Atten Disord. 2015;23(4):325–32. https://doi.org/10.1177/1087054715618792.
(50) Cristofori I, Cohen-Zimerman S, Grafman J. Executive functions. Hand Clin Neuro. 2019;163:197–219. https://doi.org/10.1016/B978-0-12-804281-6.00011-2.
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Copyright (c) 2023 Patricia Vieira de Oliveira, Mariana Lessa de Castro, Luanda André Collange-Grecco, Sueli Rizzutti, Mauro Muszkat
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This work is licensed under a Creative Commons Attribution 4.0 International License.