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Improving social cognition following theta burst stimulation over the right inferior frontal gyrus in autism spectrum: an 8-week double-blind sham-controlled trial

Published online by Cambridge University Press:  06 September 2024

Hsing-Chang Ni Open the ORCID record for Hsing-Chang Ni [Opens in a new window] ,
Yi-Lung Chen ,
Meng-Ying Hsieh ,
Chen-Te Wu ,
Rou-Shayn Chen ,
Chi-Hung Juan ,
Cheng-Ta Li ,
Susan Shur-Fen Gau  and
Hsiang-Yuan Lin
Hsing-Chang Ni*
Affiliation:
Department of Psychiatry, Chang Gung Memorial Hospital at Linkou, Taoyuan, Taiwan College of Medicine, Chang Gung University, Taoyuan, Taiwan
Yi-Lung Chen
Affiliation:
Department of Healthcare Administration, Asia University, Taichung, Taiwan Department of Psychology, Asia University, Taichung, Taiwan
Meng-Ying Hsieh
Affiliation:
Deparment of Pediatrics, Chang Gung Memorial Hospital at Taipei, Taipei, Taiwan Department of Pediatric Neurology, Chang Gung Memorial Hospital at Linkou, Taoyuan, Taiwan
Chen-Te Wu
Affiliation:
Department of Medical Imaging and Intervention, Chang Gung Memorial Hospital at Linkou, Taoyuan, Taiwan
Rou-Shayn Chen
Affiliation:
Department of Neurology, Chang Gung Memorial Hospital at Linkou, Taoyuan, Taiwan
Chi-Hung Juan
Affiliation:
Institue of Cognitive Neuroscience, National Central University, Jhongli, Taiwan
Cheng-Ta Li
Affiliation:
Department of Psychiatry, Taipei Veterans General Hospital, Taipei, Taiwan
Susan Shur-Fen Gau
Affiliation:
Graduate Institute of Brain and Mind Sciences, College of Medicine, National Taiwan University, Taipei, Taiwan Neurobiology and Cognitive Science Center, National Taiwan University, Taipei, Taiwan Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan
Hsiang-Yuan Lin*
Affiliation:
Azrieli Adult Neurodevelopmental Centre, Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, Ontario, Canada Department of Psychiatry, Temerty Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
*
Corresponding author: Hsing-Chang Ni; Email: alanni@cgmh.org.tw; alanni0918@yahoo.com.tw; Hsiang-Yuan Lin; Email: Hsiang-Yuan.Lin@camh.ca; hsiangyuan.lin@utoronto.ca
Corresponding author: Hsing-Chang Ni; Email: alanni@cgmh.org.tw; alanni0918@yahoo.com.tw; Hsiang-Yuan Lin; Email: Hsiang-Yuan.Lin@camh.ca; hsiangyuan.lin@utoronto.ca
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Abstract

Background

The right inferior frontal gyrus (RIFG) is a potential beneficial brain stimulation target for autism. This randomized, double-blind, two-arm, parallel-group, sham-controlled clinical trial assessed the efficacy of intermittent theta burst stimulation (iTBS) over the RIFG in reducing autistic symptoms (NCT04987749).

Methods

Conducted at a single medical center, the trial enrolled 60 intellectually able autistic individuals (aged 8–30 years; 30 active iTBS). The intervention comprised 16 sessions (two stimulations per week for eight weeks) of neuro-navigated iTBS or sham over the RIFG. Fifty-seven participants (28 active) completed the intervention and assessments at Week 8 (the primary endpoint) and follow-up at Week 12.

Results

Autistic symptoms (primary outcome) based on the Social Responsiveness Scale decreased in both groups (significant time effect), but there was no significant difference between groups (null time-by-treatment interaction). Likewise, there was no significant between-group difference in changes in repetitive behaviors and exploratory outcomes of adaptive function and emotion dysregulation. Changes in social cognition (secondary outcome) differed between groups in feeling scores on the Frith-Happe Animations (Week 8, p = 0.026; Week 12, p = 0.025). Post-hoc analysis showed that the active group improved better on this social cognition than the sham group. Dropout rates did not vary between groups; the most common adverse event in both groups was local pain. Notably, our findings would not survive stringent multiple comparison corrections.

Conclusions

Our findings suggest that iTBS over the RIFG is not different from sham in reducing autistic symptoms and emotion dysregulation. Nonetheless, RIFG iTBS may improve social cognition of mentalizing others' feelings in autistic individuals.

Keywords

autismright inferior frontal gyrustheta burst stimulation
Type
Original Article
Information
Psychological Medicine , First View , pp. 1 - 12
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Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

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References

Altman, D. G. (1985). Comparability of randomised groups. Journal of the Royal Statistical Society. Series D (The Statistician), 34(1), 125–136.Google Scholar
Altschuler, M. R., & Faja, S. (2022). Brief report: Test-retest reliability of cognitive, affective, and spontaneous theory of mind tasks among school-aged children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 52(4), 1890–1895. doi: 10.1007/s10803-021-05040-6CrossRefGoogle ScholarPubMed
Ameis, S. H., Blumberger, D. M., Croarkin, P. E., Mabbott, D. J., Lai, M. C., Desarkar, P., … Daskalakis, Z. J. (2020). Treatment of executive function deficits in autism spectrum disorder with repetitive transcranial magnetic stimulation: A double-blind, sham-controlled, pilot trial. Brain Stimulation, 13(3), 539–547. doi: 10.1016/j.brs.2020.01.007CrossRefGoogle ScholarPubMed
Austin, P. C., Manca, A., Zwarenstein, M., Juurlink, D. N., & Stanbrook, M. B. (2010). A substantial and confusing variation exists in handling of baseline covariates in randomized controlled trials: A review of trials published in leading medical journals. Journal of Clinical Epidemiology, 63(2), 142–153. doi: 10.1016/j.jclinepi.2009.06.002CrossRefGoogle ScholarPubMed
Barahona-Correa, J. B., Velosa, A., Chainho, A., Lopes, R., & Oliveira-Maia, A. J. (2018). Repetitive transcranial magnetic stimulation for treatment of autism spectrum disorder: A systematic review and meta-analysis. Frontiers in Integrative Neuroscience, 12, 27. doi: 10.3389/fnint.2018.00027CrossRefGoogle ScholarPubMed
Barch, D. M., Burgess, G. C., Harms, M. P., Petersen, S. E., Schlaggar, B. L., Corbetta, M., ... Consortium, W. U.-M. H. (2013). Function in the human connectome: task-fMRI and individual differences in behavior. Neuroimage, 80, 169–189. doi: 10.1016/j.neuroimage.2013.05.033CrossRefGoogle ScholarPubMed
Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., & Plumb, I. (2001). The “Reading the Mind in the Eyes” test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry, 42(2), 241–251.CrossRefGoogle ScholarPubMed
Barstow, C., Shahan, B., & Roberts, M. (2018). Evaluating medical decision-making capacity in practice. American Family Physician, 98(1), 40–46.Google ScholarPubMed
Blumberger, D. M., Mulsant, B. H., Thorpe, K. E., McClintock, S. M., Konstantinou, G. N., Lee, H. H., … Downar, J. (2022). Effectiveness of standard sequential bilateral repetitive transcranial magnetic stimulation vs bilateral theta burst stimulation in older adults with depression: The FOUR-D randomized noninferiority clinical trial. JAMA Psychiatry, 79(11), 1065–1073. doi: 10.1001/jamapsychiatry.2022.2862CrossRefGoogle ScholarPubMed
Blumberger, D. M., Vila-Rodriguez, F., Thorpe, K. E., Feffer, K., Noda, Y., Giacobbe, P., … Downar, J. (2018). Effectiveness of theta burst versus high-frequency repetitive transcranial magnetic stimulation in patients with depression (THREE-D): A randomised non-inferiority trial. Lancet (London, England), 391(10131), 1683–1692. doi: 10.1016/S0140-6736(18)30295-2CrossRefGoogle ScholarPubMed
Bodfish, J. W., Symons, F. J., Parker, D. E., & Lewis, M. H. (2000). Varieties of repetitive behavior in autism: Comparisons to mental retardation. Journal of Autism and Developmental Disorders, 30(3), 237–243. doi: 10.1023/a:1005596502855CrossRefGoogle ScholarPubMed
Bottema-Beutel, K., Kim, S. Y., & Crowley, S. (2019). A systematic review and meta-regression analysis of social functioning correlates in autism and typical development. Autism Research, 12(2), 152–175. doi: 10.1002/aur.2055CrossRefGoogle ScholarPubMed
Burke, M. J., Romanella, S. M., Mencarelli, L., Greben, R., Fox, M. D., Kaptchuk, T. J., … Santarnecchi, E. (2022). Placebo effects and neuromodulation for depression: A meta-analysis and evaluation of shared mechanisms. Molecular Psychiatry, 27(3), 1658–1666. doi: 10.1038/s41380-021-01397-3CrossRefGoogle ScholarPubMed
Casanova, M. F., Hensley, M. K., Sokhadze, E. M., El-Baz, A. S., Wang, Y., Li, X., & Sears, L. (2014). Effects of weekly low-frequency rTMS on autonomic measures in children with autism spectrum disorder. Frontiers in Human Neuroscience, 8, 851. doi: 10.3389/fnhum.2014.00851CrossRefGoogle ScholarPubMed
Cash, R. F. H., Weigand, A., Zalesky, A., Siddiqi, S. H., Downar, J., Fitzgerald, P. B., & Fox, M. D. (2021). Using brain imaging to improve spatial targeting of transcranial magnetic stimulation for depression. Biological Psychiatry, 90(10), 689–700. doi: 10.1016/j.biopsych.2020.05.033CrossRefGoogle ScholarPubMed
Castelli, F., Frith, C., Happe, F., & Frith, U. (2002). Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain, 125(Pt 8), 1839–1849. doi: 10.1093/brain/awf189CrossRefGoogle ScholarPubMed
Chung, S. W., Hill, A. T., Rogasch, N. C., Hoy, K. E., & Fitzgerald, P. B. (2016). Use of theta-burst stimulation in changing excitability of motor cortex: A systematic review and meta-analysis. Neuroscience & Biobehavioral Reviews, 63, 43–64. doi: 10.1016/j.neubiorev.2016.01.008CrossRefGoogle ScholarPubMed
Cole, E. J., Enticott, P. G., Oberman, L. M., Gwynette, M. F., Casanova, M. F., Jackson, S. L. J., … r, T. M. S. i. A. S. D. C. G. (2019). The potential of repetitive transcranial magnetic stimulation for autism spectrum disorder: A consensus statement. Biological Psychiatry, 85(4), e21–e22. doi: 10.1016/j.biopsych.2018.06.003CrossRefGoogle ScholarPubMed
Corp, D. T., Bereznicki, H. G. K., Clark, G. M., Youssef, G. J., Fried, P. J., Jannati, A., … Big, T. M. S. D. C. (2020). Large-scale analysis of interindividual variability in theta-burst stimulation data: Results from the ‘Big TMS Data Collaboration’. Brain Stimulation, 13(5), 1476–1488. doi: 10.1016/j.brs.2020.07.018CrossRefGoogle ScholarPubMed
Dapretto, M., Davies, M. S., Pfeifer, J. H., Scott, A. A., Sigman, M., Bookheimer, S. Y., & Iacoboni, M. (2006). Understanding emotions in others: Mirror neuron dysfunction in children with autism spectrum disorders. Nature Neuroscience, 9(1), 28–30. doi: 10.1038/nn1611CrossRefGoogle ScholarPubMed
Dayan, E., Censor, N., Buch, E. R., Sandrini, M., & Cohen, L. G. (2013). Noninvasive brain stimulation: From physiology to network dynamics and back. Nature Neuroscience, 16(7), 838–844. doi: 10.1038/nn.3422CrossRefGoogle ScholarPubMed
De Carli, P., Bakermans-Kranenburg, M. J., Parolin, L., Lega, C., Zanardo, B., Cattaneo, Z., & Riem, M. M. E. (2019). A walk on the dark side: TMS over the right inferior frontal gyrus (rIFG) disrupts behavioral responses to infant stimuli. Social Neuroscience, 14(6), 697–704. doi: 10.1080/17470919.2019.1574891CrossRefGoogle ScholarPubMed
Dichter, G. S., & Belger, A. (2007). Social stimuli interfere with cognitive control in autism. Neuroimage, 35(3), 1219–1230. doi: 10.1016/j.neuroimage.2006.12.038CrossRefGoogle ScholarPubMed
Dippel, G., & Beste, C. (2015). A causal role of the right inferior frontal cortex in implementing strategies for multi-component behaviour. Nature Communications, 6, 6587. doi: 10.1038/ncomms7587CrossRefGoogle ScholarPubMed
Duque, J., Greenhouse, I., Labruna, L., & Ivry, R. B. (2017). Physiological markers of motor inhibition during human behavior. Trends in Neurosciences, 40(4), 219–236. doi: 10.1016/j.tins.2017.02.006CrossRefGoogle ScholarPubMed
Eliasova, I., Anderkova, L., Marecek, R., & Rektorova, I. (2014). Non-invasive brain stimulation of the right inferior frontal gyrus may improve attention in early Alzheimer's disease: A pilot study. Journal of the Neurological Sciences, 346(1-2), 318–322. doi: 10.1016/j.jns.2014.08.036CrossRefGoogle ScholarPubMed
Elmaghraby, R., Sun, Q., Ozger, C., Shekunov, J., Romanowicz, M., & Croarkin, P. E. (2022). A systematic review of the safety and tolerability of theta burst stimulation in children and adolescents. Neuromodulation, 25(4), 494–503. doi: 10.1111/ner.13455CrossRefGoogle ScholarPubMed
Enticott, P. G., Fitzgibbon, B. M., Kennedy, H. A., Arnold, S. L., Elliot, D., Peachey, A., … Fitzgerald, P. B. (2014). A double-blind, randomized trial of deep repetitive transcranial magnetic stimulation (rTMS) for autism spectrum disorder. Brain Stimulation, 7(2), 206–211. doi: 10.1016/j.brs.2013.10.004CrossRefGoogle ScholarPubMed
Faul, F., Erdfelder, E., Buchner, A., & Lang, A. G. (2009). Statistical power analyses using G*power 3.1: Tests for correlation and regression analyses. Behavior Research Methods, 41(4), 1149–1160. doi: 10.3758/BRM.41.4.1149CrossRefGoogle Scholar
Gau, S. S. F., Liu, L. T., Wu, Y. Y., Chiu, Y. N., & Tsai, W. C. (2013). Psychometric properties of the Chinese version of the Social Responsiveness Scale. Research in Autism Spectrum Disorders, 7(2), 349–360. doi: 10.1016/j.rasd.2012.10.004CrossRefGoogle Scholar
Geurts, H. M., Corbett, B., & Solomon, M. (2009). The paradox of cognitive flexibility in autism. Trends in Cognitive Sciences, 13(2), 74–82. doi: 10.1016/j.tics.2008.11.006CrossRefGoogle ScholarPubMed
Gollo, L. L., Roberts, J. A., & Cocchi, L. (2017). Mapping how local perturbations influence systems-level brain dynamics. Neuroimage, 160, 97–112. doi: 10.1016/j.neuroimage.2017.01.057CrossRefGoogle ScholarPubMed
Harrison, P. L., & Oakland, T. (2003). Adaptive behavior assessment system® second edition ABAS®-II. San Antonio: Harcourt.Google Scholar
Hoekert, M., Vingerhoets, G., & Aleman, A. (2010). Results of a pilot study on the involvement of bilateral inferior frontal gyri in emotional prosody perception: An rTMS study. BMC Neuroscience, 11, 93. doi: 10.1186/1471-2202-11-93CrossRefGoogle ScholarPubMed
Hogeveen, J., Obhi, S. S., Banissy, M. J., Santiesteban, I., Press, C., Catmur, C., & Bird, G. (2015). Task-dependent and distinct roles of the temporoparietal junction and inferior frontal cortex in the control of imitation. Social Cognitive and Affective Neuroscience, 10(7), 1003–1009. doi: 10.1093/scan/nsu148CrossRefGoogle ScholarPubMed
Hong, Y. H., Wu, S. W., Pedapati, E. V., Horn, P. S., Huddleston, D. A., Laue, C. S., & Gilbert, D. L. (2015). Safety and tolerability of theta burst stimulation vs. single and paired pulse transcranial magnetic stimulation: A comparative study of 165 pediatric subjects. Frontiers in Human Neuroscience, 9, 29. doi: 10.3389/fnhum.2015.00029CrossRefGoogle ScholarPubMed
Huang, Y. Z., Edwards, M. J., Rounis, E., Bhatia, K. P., & Rothwell, J. C. (2005). Theta burst stimulation of the human motor cortex. Neuron, 45(2), 201–206. doi: 10.1016/j.neuron.2004.12.033CrossRefGoogle ScholarPubMed
Huang, Y. Z., Rothwell, J. C., Chen, R. S., Lu, C. S., & Chuang, W. L. (2011). The theoretical model of theta burst form of repetitive transcranial magnetic stimulation. Clinical Neurophysiology, 122(5), 1011–1018. doi: 10.1016/j.clinph.2010.08.016CrossRefGoogle ScholarPubMed
Hus, V., & Lord, C. (2014). The autism diagnostic observation schedule, module 4: Revised algorithm and standardized severity scores. Journal of Autism and Developmental Disorders, 44(8), 1996–2012. doi: 10.1007/s10803-014-2080-3CrossRefGoogle ScholarPubMed
Jannati, A., Block, G., Ryan, M. A., Kaye, H. L., Kayarian, F. B., Bashir, S., … Rotenberg, A. (2020). Continuous theta-burst stimulation in children with high-functioning autism spectrum disorder and typically developing children. Frontiers in Integrative Neuroscience, 14, 13. doi: 10.3389/fnint.2020.00013CrossRefGoogle ScholarPubMed
Kana, R. K., Keller, T. A., Minshew, N. J., & Just, M. A. (2007). Inhibitory control in high-functioning autism: Decreased activation and underconnectivity in inhibition networks. Biological Psychiatry, 62(3), 198–206. doi: 10.1016/j.biopsych.2006.08.004CrossRefGoogle ScholarPubMed
Kaokhieo, J., Tretriluxana, J., Chaiyawat, P., Siripornpanich, V., Permpoonputtana, K., Tretriluxana, S., & Nanbancha, A. (2023). Effects of repetitive transcranial magnetic stimulation combined with action-observation-execution on social interaction and communication in autism spectrum disorder: Feasibility study. Brain Research, 1804, 148258. doi: 10.1016/j.brainres.2023.148258CrossRefGoogle ScholarPubMed
Karlson, C. W., & Rapoff, M. A. (2009). Attrition in randomized controlled trials for pediatric chronic conditions. Journal of Pediatric Psychology, 34(7), 782–793. doi: 10.1093/jpepsy/jsn122CrossRefGoogle ScholarPubMed
Kennedy, D. P., & Courchesne, E. (2008). The intrinsic functional organization of the brain is altered in autism. Neuroimage, 39(4), 1877–1885. doi: 10.1016/j.neuroimage.2007.10.052CrossRefGoogle ScholarPubMed
Kenworthy, L., Case, L., Harms, M. B., Martin, A., & Wallace, G. L. (2010). Adaptive behavior ratings correlate with symptomatology and IQ among individuals with high-functioning autism spectrum disorders. Journal of Autism and Developmental Disorders, 40(4), 416–423. doi: 10.1007/s10803-009-0911-4CrossRefGoogle ScholarPubMed
King, B. H., Dukes, K., Donnelly, C. L., Sikich, L., McCracken, J. T., Scahill, L., … Hirtz, D. (2013). Baseline factors predicting placebo response to treatment in children and adolescents with autism spectrum disorders: A multisite randomized clinical trial. JAMA Pediatrics, 167(11), 1045–1052. doi: 10.1001/jamapediatrics.2013.2698CrossRefGoogle ScholarPubMed
Klomjai, W., Katz, R., & Lackmy-Vallee, A. (2015). Basic principles of transcranial magnetic stimulation (TMS) and repetitive TMS (rTMS). Annals of Physical and Rehabilitation Medicine, 58(4), 208–213. doi: 10.1016/j.rehab.2015.05.005CrossRefGoogle ScholarPubMed
Konstantin, G. E., Nordgaard, J., & Henriksen, M. G. (2023). Methodological issues in social cognition research in autism spectrum disorder and schizophrenia spectrum disorder: A systematic review. Psychological Medicine, 53(8), 3281–3292. doi: 10.1017/S0033291723001095CrossRefGoogle ScholarPubMed
Kosaka, H., Omori, M., Munesue, T., Ishitobi, M., Matsumura, Y., Takahashi, T., … Wada, Y. (2010). Smaller insula and inferior frontal volumes in young adults with pervasive developmental disorders. Neuroimage, 50(4), 1357–1363. doi: 10.1016/j.neuroimage.2010.01.085CrossRefGoogle ScholarPubMed
Kuang, S. (2016). Two polarities of attention in social contexts: From attending-to-others to attending-to-self. Frontiers in Psychology, 7, 63. doi: 10.3389/fpsyg.2016.00063CrossRefGoogle ScholarPubMed
Lee, C. W., Chu, M. C., Wu, H. F., Chung, Y. J., Hsieh, T. H., Chang, C. Y., … Lin, H. C. (2023). Different synaptic mechanisms of intermittent and continuous theta-burst stimulations in a severe foot-shock induced and treatment-resistant depression in a rat model. Experimental Neurology, 362, 114338. doi: 10.1016/j.expneurol.2023.114338CrossRefGoogle Scholar
Leekam, S. (2016). Social cognitive impairment and autism: What are we trying to explain? Philosophical Transactions of the Royal Society B, 371(1686), 20150082. doi: 10.1098/rstb.2015.0082CrossRefGoogle ScholarPubMed
Li, C. T., Huang, Y. Z., Bai, Y. M., Tsai, S. J., Su, T. P., & Cheng, C. M. (2019). Critical role of glutamatergic and GABAergic neurotransmission in the central mechanisms of theta-burst stimulation. Human Brain Mapping, 40(6), 2001–2009. doi: 10.1002/hbm.24485CrossRefGoogle ScholarPubMed
Li, Y., Li, W., Zhang, T., Zhang, J., Jin, Z., & Li, L. (2021). Probing the role of the right inferior frontal gyrus during pain-related empathy processing: Evidence from fMRI and TMS. Human Brain Mapping, 42(5), 1518–1531. doi: 10.1002/hbm.25310CrossRefGoogle ScholarPubMed
Livingston, L. A., Shah, P., White, S. J., & Happe, F. (2021). Further developing the frith-happe animations: A quicker, more objective, and web-based test of theory of mind for autistic and neurotypical adults. Autism Research, 14(9), 1905–1912. doi: 10.1002/aur.2575CrossRefGoogle ScholarPubMed
Lord, C., Elsabbagh, M., Baird, G., & Veenstra-Vanderweele, J. (2018). Autism spectrum disorder. Lancet (London, England), 392(10146), 508–520. doi: 10.1016/S0140-6736(18)31129-2CrossRefGoogle ScholarPubMed
Lord, C., Risi, S., Lambrecht, L., Cook, E. H. Jr., Leventhal, B. L., DiLavore, P. C., … Rutter, M. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223.CrossRefGoogle ScholarPubMed
Lord, C. R. M., DiLavore, P. C., Risi, S., Gotham, K., & Bishop, S. L. (2012). Autism diagnostic observation schedule, second edition (ADOS-2) manual (part I): Modules 1–4. Torrance, CA: Western Psychological Services.Google Scholar
Masi, A., Lampit, A., Glozier, N., Hickie, I. B., & Guastella, A. J. (2015). Predictors of placebo response in pharmacological and dietary supplement treatment trials in pediatric autism spectrum disorder: A meta-analysis. Translational Psychiatry, 5(9), e640. doi: 10.1038/tp.2015.143CrossRefGoogle ScholarPubMed
Massey, S. H., Stern, D., Alden, E. C., Petersen, J. E., Cobia, D. J., Wang, L., … Smith, M. J. (2017). Cortical thickness of neural substrates supporting cognitive empathy in individuals with schizophrenia. Schizophrenia Research, 179, 119–124. doi: 10.1016/j.schres.2016.09.025CrossRefGoogle ScholarPubMed
Mazefsky, C. A. (2021). Encyclopedia of autism Spectrum disorders. Cham, Switzerland: SpringerLink.Google Scholar
Mazefsky, C. A., Day, T. N., Siegel, M., White, S. W., Yu, L., Pilkonis, P. A., … Developmental Disabilities Inpatient Research, C. (2018a). Development of the emotion dysregulation inventory: A PROMIS(R)ing method for creating sensitive and unbiased questionnaires for autism spectrum disorder. Journal of Autism and Developmental Disorders, 48(11), 3736–3746. doi: 10.1007/s10803-016-2907-1CrossRefGoogle Scholar
Mazefsky, C. A., Herrington, J., Siegel, M., Scarpa, A., Maddox, B. B., Scahill, L., & White, S. W. (2013). The role of emotion regulation in autism spectrum disorder. Journal of the American Academy of Child Psychiatry, 52(7), 679–688. doi: 10.1016/j.jaac.2013.05.006CrossRefGoogle ScholarPubMed
Mazefsky, C. A., Yu, L., White, S. W., Siegel, M., & Pilkonis, P. A. (2018b). The emotion dysregulation inventory: Psychometric properties and item response theory calibration in an autism spectrum disorder sample. Autism Research, 11(6), 928–941. doi: 10.1002/aur.1947CrossRefGoogle Scholar
Moher, D., Hopewell, S., Schulz, K. F., Montori, V., Gotzsche, P. C., Devereaux, P. J., … Consolidated Standards of Reporting Trials, G. (2010). CONSORT 2010 Explanation and elaboration: Updated guidelines for reporting parallel group randomised trials. Journal of Clinical Epidemiology, 63(8), e1–37. doi:10.1016/j.jclinepi.2010.03.004CrossRefGoogle ScholarPubMed
Newman-Norlund, R. D., Gibson, M., McConnell, P. A., & Froeliger, B. (2020). Dissociable effects of theta-burst repeated transcranial magnetic stimulation to the inferior frontal gyrus on inhibitory control in nicotine addiction. Frontiers in Psychiatry, 11, 260. doi: 10.3389/fpsyt.2020.00260CrossRefGoogle Scholar
Ni, H. C., Chao, Y. P., Tseng, R. Y., Wu, C. T., Cocchi, L., Chou, T. L., … Lin, H. Y. (2023a). Lack of effects of four-week theta burst stimulation on white matter macro/microstructure in children and adolescents with autism. NeuroImage: Clinical, 37, 103324. doi: 10.1016/j.nicl.2023.103324CrossRefGoogle ScholarPubMed
Ni, H. C., Chen, Y. L., Chao, Y. P., Wu, C. T., Chen, R. S., Chou, T. L., … Lin, H. Y. (2023b). A lack of efficacy of continuous theta burst stimulation over the left dorsolateral prefrontal cortex in autism: A double blind randomized sham-controlled trial. Autism Research, 16(6), 1247–1262. doi: 10.1002/aur.2954CrossRefGoogle ScholarPubMed
Ni, H. C., Chen, Y. L., Chao, Y. P., Wu, C. T., Wu, Y. Y., Liang, S. H., … Lin, H. Y. (2021). Intermittent theta burst stimulation over the posterior superior temporal sulcus for children with autism spectrum disorder: A 4-week randomized blinded controlled trial followed by another 4-week open-label intervention. Autism, 25(5), 1279–1294. doi: 10.1177/1362361321990534CrossRefGoogle ScholarPubMed
Ni, H. C., Hung, J., Wu, C. T., Wu, Y. Y., Chang, C. J., Chen, R. S., & Huang, Y. Z. (2017). The impact of single session intermittent theta-burst stimulation over the dorsolateral prefrontal cortex and posterior superior temporal sulcus on adults with autism spectrum disorder. Frontiers in Neuroscience, 11, 255. doi: 10.3389/fnins.2017.00255CrossRefGoogle ScholarPubMed
Ni, H. C., Lin, H. Y., Chen, Y. L., Hung, J., Wu, C. T., Wu, Y. Y., … Huang, Y. Z. (2022). 5-day multi-session intermittent theta burst stimulation over bilateral posterior superior temporal sulci in adults with autism-a pilot study. Biomedical Journal, 45(4), 696–707. doi: 10.1016/j.bj.2021.07.008CrossRefGoogle ScholarPubMed
Oberman, L. M., Pascual-Leone, A., & Rotenberg, A. (2014). Modulation of corticospinal excitability by transcranial magnetic stimulation in children and adolescents with autism spectrum disorder. Frontiers in Human Neuroscience, 8, 627. doi: 10.3389/fnhum.2014.00627CrossRefGoogle ScholarPubMed
Pavlova, M. A., & Sokolov, A. A. (2022). Reading language of the eyes. Neuroscience & Biobehavioral Reviews, 140, 104755. doi: 10.1016/j.neubiorev.2022.104755CrossRefGoogle ScholarPubMed
Peled-Avron, L., Glasner, L., Gvirts, H. Z., & Shamay-Tsoory, S. G. (2019). The role of the inferior frontal gyrus in vicarious social touch: A transcranial direct current stimulation (tDCS) study. Developmental Cognitive Neuroscience, 35, 115–121. doi: 10.1016/j.dcn.2018.04.010CrossRefGoogle Scholar
Penuelas-Calvo, I., Sareen, A., Sevilla-Llewellyn-Jones, J., & Fernandez-Berrocal, P. (2019). The “Reading the Mind in the Eyes” test in autism-spectrum disorders comparison with healthy controls: A systematic review and meta-analysis. Journal of Autism and Developmental Disorders, 49(3), 1048–1061. doi: 10.1007/s10803-018-3814-4CrossRefGoogle Scholar
Rossi, S., Antal, A., Bestmann, S., Bikson, M., Brewer, C., Brockmoller, J., … basis of this article began with a Consensus Statement from the Ifcn Workshop on “Present, F. o. T. M. S. S. E. G. S. O. u. t. A. (2021). Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: Expert guidelines. Clinical Neurophysiology, 132(1), 269–306. doi: 10.1016/j.clinph.2020.10.003CrossRefGoogle ScholarPubMed
Sandercock, R. K., Lamarche, E. M., Klinger, M. R., & Klinger, L. G. (2020). Assessing the convergence of self-report and informant measures for adults with autism spectrum disorder. Autism, 24(8), 2256–2268. doi: 10.1177/1362361320942981CrossRefGoogle ScholarPubMed
Schurz, M., Radua, J., Aichhorn, M., Richlan, F., & Perner, J. (2014). Fractionating theory of mind: A meta-analysis of functional brain imaging studies. Neuroscience & Biobehavioral Reviews, 42, 9–34. doi: 10.1016/j.neubiorev.2014.01.009CrossRefGoogle ScholarPubMed
Sokhadze, E., Baruth, J., Tasman, A., Mansoor, M., Ramaswamy, R., Sears, L., … Casanova, M. F. (2010). Low-frequency repetitive transcranial magnetic stimulation (rTMS) affects event-related potential measures of novelty processing in autism. Applied Psychophysiology and Biofeedback, 35(2), 147–161. doi: 10.1007/s10484-009-9121-2CrossRefGoogle ScholarPubMed
Sokhadze, E. M., El-Baz, A., Baruth, J., Mathai, G., Sears, L., & Casanova, M. F. (2009). Effects of low frequency repetitive transcranial magnetic stimulation (rTMS) on gamma frequency oscillations and event-related potentials during processing of illusory figures in autism. Journal of Autism and Developmental Disorders, 39(4), 619–634. doi: 10.1007/s10803-008-0662-7CrossRefGoogle ScholarPubMed
Sokhadze, E. M., Lamina, E. V., Casanova, E. L., Kelly, D. P., Opris, I., Tasman, A., & Casanova, M. F. (2018). Exploratory study of rTMS neuromodulation effects on electrocortical functional measures of performance in an oddball test and behavioral symptoms in autism. Frontiers in Systems Neuroscience, 12, 20. doi: 10.3389/fnsys.2018.00020CrossRefGoogle Scholar
Sundby, K. K., Jana, S., & Aron, A. R. (2021). Double-blind disruption of right inferior frontal cortex with TMS reduces right frontal beta power for action stopping. Journal of Neurophysiology, 125(1), 140–153. doi: 10.1152/jn.00459.2020CrossRefGoogle ScholarPubMed
Tettamanti, M., Vaghi, M. M., Bara, B. G., Cappa, S. F., Enrici, I., & Adenzato, M. (2017). Effective connectivity gateways to the theory of mind network in processing communicative intention. Neuroimage, 155, 169–176. doi: 10.1016/j.neuroimage.2017.04.050CrossRefGoogle Scholar
Tsujii, T., Sakatani, K., Masuda, S., Akiyama, T., & Watanabe, S. (2011). Evaluating the roles of the inferior frontal gyrus and superior parietal lobule in deductive reasoning: An rTMS study. Neuroimage, 58(2), 640–646. doi: 10.1016/j.neuroimage.2011.06.076CrossRefGoogle ScholarPubMed
Udden, J., Folia, V., Forkstam, C., Ingvar, M., Fernandez, G., Overeem, S., … Petersson, K. M. (2008). The inferior frontal cortex in artificial syntax processing: An rTMS study. Brain Research, 1224, 69–78. doi: 10.1016/j.brainres.2008.05.070CrossRefGoogle ScholarPubMed
Upton, S., Brown, A. A., Golzy, M., Garland, E. L., & Froeliger, B. (2023). Right inferior frontal gyrus theta-burst stimulation reduces smoking behaviors and strengthens fronto-striatal-limbic resting-state functional connectivity: A randomized crossover trial. Frontiers in Psychiatry, 14, 1166912. doi: 10.3389/fpsyt.2023.1166912CrossRefGoogle ScholarPubMed
Vellante, M., Baron-Cohen, S., Melis, M., Marrone, M., Petretto, D. R., Masala, C., & Preti, A. (2013). The “Reading the Mind in the Eyes” test: Systematic review of psychometric properties and a validation study in Italy. Cognitive Neuropsychiatry, 18(4), 326–354. doi: 10.1080/13546805.2012.721728CrossRefGoogle Scholar
Villalobos, M. E., Mizuno, A., Dahl, B. C., Kemmotsu, N., & Muller, R. A. (2005). Reduced functional connectivity between V1 and inferior frontal cortex associated with visuomotor performance in autism. Neuroimage, 25(3), 916–925. doi: 10.1016/j.neuroimage.2004.12.022CrossRefGoogle ScholarPubMed
White, S. J., Coniston, D., Rogers, R., & Frith, U. (2011). Developing the frith-happe animations: A quick and objective test of theory of mind for adults with autism. Autism Research, 4(2), 149–154. doi: 10.1002/aur.174CrossRefGoogle ScholarPubMed
Wilson, A. C. (2021). Do animated triangles reveal a marked difficulty among autistic people with reading minds? Autism, 25(5), 1175–1186. doi: 10.1177/1362361321989152CrossRefGoogle ScholarPubMed
Winhuisen, L., Thiel, A., Schumacher, B., Kessler, J., Rudolf, J., Haupt, W. F., & Heiss, W. D. (2007). The right inferior frontal gyrus and poststroke aphasia: A follow-up investigation. Stroke, 38(4), 1286–1292. doi: 10.1161/01.STR.0000259632.04324.6cCrossRefGoogle ScholarPubMed
Yang, Y. C., Lu, L., Jeng, S. F., Tsao, P. N., Cheong, P. L., Li, Y. J., … Wu, Y. T. (2019). Multidimensional developments and free-play movement tracking in 30- to 36-month-old toddlers with autism spectrum disorder who were full term. Physical Therapy, 99(11), 1535–1550. doi: 10.1093/ptj/pzz114CrossRefGoogle ScholarPubMed
Zeidan, J., Fombonne, E., Scorah, J., Ibrahim, A., Durkin, M. S., Saxena, S., … Elsabbagh, M. (2022). Global prevalence of autism: A systematic review update. Autism Research, 15(5), 778–790. doi: 10.1002/aur.2696CrossRefGoogle ScholarPubMed
Zhao, H., Mao, X., Zhu, C., Zou, X., Peng, F., Yang, W., … Cui, R. (2021). GABAergic system dysfunction in autism Spectrum disorders. Frontiers in Cell and Developmental Biology, 9, 781327. doi: 10.3389/fcell.2021.781327CrossRefGoogle ScholarPubMed
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