Table 3.
Outcome measures and results for included studies
| Study | Intervention | Cognitive measures | Behavioral measures | Biological measures | Assessment times | Cognitive outcomes | Behavioral outcomes | Biological outcomes | Side-effects |
|---|---|---|---|---|---|---|---|---|---|
| Hupfeld et al., 2016 [35] | tDCS | Motor planning, balance course and black board tasks | - | - | Before and after treatment | Improved attention to the tasks, and superior direction-following behaviors after treatment | - | - | None |
| Wilson et al., 2018 [40] | tDCS | - | ATEC | - | Before, after, two months and one year after treatment | - | Improvement in all ATEC subscales, especially social domains | - | Not reported |
| Schneider and Hopp, 2011 [37] | tDCS | Bilingual Aphasia Test (BAT) | - | - | Before and after treatment | Significant increase in vocabulary and syntax scores after treatment | - | - | None |
| D’Urso et al., 2015 [36] | tDCS | - | ABC | - | Before and one week after treatment | - | Significant reduction in total score, irritability, lethargy/social withdrawal and hyperactivity subscales of ABC after treatment | - | Temporary skin irritation at the stimulation site |
| Van Steenburgh et al., 2014 [39] | tDCS | - | - | BOLD activity | Before and after treatment | Significant increase in anticorrelation after anodal tDCS over left DLPFC compared to sham. Significant increase in functional connectivity between posterior cingulate and mPFC after anodal tDCS over left or right DLPFC compared to sham | Not reported | ||
| Van Steenburgh et al., 2017 [38] | tDCS | n-back; brief test of attention (BTA) | - | - | Before and after treatment | Significant improvement in working memory performance with largest effects on spatial span and BTA function after balanced bilateral stimulation of DLPFC compared to sham | - | - | None |
| Amatachaya et al., 2014 [33] | tDCS | - | CARS; ATEC; CGAS; CGI-I | - | Before and one week after treatment | Significant improvement in total score of CARS; significant improvement in total score, health and behavioral problems, sociability and sensory/cognitive awareness subscales of ATEC; significant increase in CGAS score after active treatment compared to sham | - | None | |
| Amatachaya et al., 2015 [34] | tDCS | - | ATEC | Peak alpha frequency (PAF) | Before and one week after treatment | - | Significant improvement in health and behavioral problems and sociability subscales of ATEC after active treatment compared to sham | Significant increase in PAF at the stimulation site that was significantly related to improvements in the two subscales of ATEC | None |
| Enticott et al., 2011 [49] | Deep rTMS | - | IRI; AQ; RAADS | - | Before, after and one month after treatment | - | Reduction in all measures after treatment | - | None |
| Niederhofer, 2012 [53] | rTMS | - | ABC | - | Before and after treatment | - | Improvement in irritability and stereotypy subscales of ABC after treatment | - | Not reported |
| Cristancho et al., 2014 [47] | rTMS | - | Clinical examination | - | Before and after treatment | Improvement in patient’s mood, interpersonal communication, eye contact, concentration and verbal expression | - | Mild headaches, jaw twitching and transient dizziness | |
| Avirame et al., 2017 [43] | Deep rTMS | Mindstreams battery and Cambridge Mindreading (CAM) battery | IRI; AQ; Y-BOCS | - | Before, after and two months after treatment | Improvement in attention, speed processing, executive functions and motor skills | Slight improvement in autistic symptoms as measured by AQ and empathy as measured by IRI, and considerable improvement in OCD-like symptoms as measured by Y-BOCS after treatment | - | Not reported |
| Sokhadze et al., 2010 [55] | rTMS | Reaction time and %error in an oddball-type task | ABC; RBS-R; SRS | ERPs | Before and two weeks after treatment | Significant reduction in %error after treatment | Significant decrease in repetitive behavior subscale of RBS-R after treatment | Significant increase in the amplitude and latency of frontal and centro-parietal P50 to targets, decrease in the amplitude of centrio-parietal and parieto-occipital P50 to standard and novel distractors, decrease in the latency of frontal N200 to novel distracters and increase in centro-parietal P3b amplitude and P200 latency to targets after treatment | None |
| Casanova et al., 2014 [46] | rTMS | - | ABC; RBS-R; SRS | Autonomic measures | Before and two weeks after treatment | - | Significant decrease in irritability, lethargy/social withdrawal and hyperactivity subscales of ABC; significant decrease in total score and in stereotypy and ritualistic/sameness subscales of RBS-R after treatment | Significant increase in R-R cardiointervals and HF-HRV, and decrease in LF-HRV, LF/HF ratio and SCL after treatment | Not reported |
| Wang et al., 2016 [62] | rTMS | - | ABC; RBS-R | Autonomic measures | Before, during and after treatment | - | Significant decrease in stereotypy, hyperactivity and inappropriate speech subscales of ABC, and in total score, ritualistic/sameness, stereotypy and compulsive behavior subscales of RBS-R after treatment | Significant increase in R-R cardiointervals and HF-HRV, and decrease in LF-HRV, LF/HF ratio and SCL during treatment | Not reported |
| Sokhadze et al., 2017 [61] | rTMS | - | ABC; RBS-R; SRS | Autonomic measures | Before, during and after treatment | - | Significant decrease in lethargy/social withdrawal, hyperactivity and inappropriate speech subscales of ABC, in total score, stereotypy, ritualistic/sameness and compulsive behavior subscales of RBS-R, and in social cognition, social awareness and social motivation subscales of SRS after treatment | - | Not reported |
| Abujadi et al., 2018 [41] | iTBS | WSCT; Stroop | RBS-R; Y-BOCS | - | Before, after and three months after treatment | Improvement in perseverative errors of WSCT and in total time for completing Stroop test after treatment | Significant reduction in RBS-R mean scores and in compulsive behaviors of Y-BOCS after treatment | - | None |
| Sokhadze et al., 2009 [58] | rTMS | Reaction time and %error in an oddball-type task | ABC; RBS-R; SRS; CGI | Gamma activity; ERPs | Before and two weeks after treatment | No significant differences in reaction time and %error after treatment | Significant decrease in repetitive behavior of RBS-R | Decrease in gamma power, amplitude of the frontal P3a and latency of the centro-parietal P3b to non-targets after treatment | Not reported |
| Sokhadze et al., 2012 [56] | rTMS | Reaction time and %error in an oddball-type task | - | ERPs | Before and after treatment | Slowing of post-error reaction time in TMS group compared to waiting list, and significant decrease in omission error rate after treatment | - | Increased amplitude and reduced latency of ERN component after treatment | Not reported |
| Sokhadze et al., 2014 [60] | rTMS | Reaction time and %error in an oddball-type task | ABC; RBS-R | Gamma power; theta/beta ratio; ERPs | Before and after treatment | Slowing of post-error reaction time, significant decrease in total error and commission error rates after treatment | Significant decrease in lethargy and hyperactivity subscales of ABC, and in total score, stereotypy and ritualistic subscales of RBS-R after treatment | Increased relative power of gamma band and decreased theta/low beta ratio over 18 sessions of treatment, reduced amplitude and increased latency of the frontal and fronto-central N100, N200 and P3a to non-targets, increased amplitude of the centro-parietal P100 and P3b to targets, reduced latency and increased negativity of ERN during commission error | None |
| Sokhadze et al., 2014 [59] | rTMS | Reaction time and %error in an oddball-type task | ABC; RBS-R; SRS | ERPs | Before and after treatment | Slowing of post-error reaction time, significant decrease in commission error rates after treatment | Significant decrease in irritability, lethargy and hyperactivity subscales of ABC, and in total score, stereotypy and ritualistic subscales of RBS-R after treatment | Reduced amplitude and increased latency of the frontal and fronto-central N100, N200 and P3a to non-targets, increased amplitude of the centro-parietal P100 and P3b to targets, reduced latency and increased negativity of ERN during commission error | Not reported |
| Sokhadze et al., 2016 [57] | rTMS | Reaction time and %error in an oddball-type task | ABC; RBS-R | Gamma activity; ERPs | Before and two weeks after treatment | Slowing of post-error reaction time, significant decrease in total error rate mainly due to reduction in commission error rates after treatment | Significant decrease in irritability, lethargy and hyperactivity subscales of ABC, and in total score, stereotypy, ritualistic and compulsive behavior subscales of RBS-R after treatment | Reduced amplitude and increased latency of the frontal and fronto-central N100, N200 and P3a to non-targets, increased amplitude of the centro-parietal P100 and P3b to targets, reduced latency and increased negativity of ERN during commission error | Not reported |
| Baruth et al., 2010 [44] | rTMS | Reaction time and %error in an oddball-type task | ABC; RBS-R; SRS | Gamma activity | Before and two weeks after treatment | No significant differences in reaction time and %error after treatment | Significant decrease in irritability and repetitive behavior subscales of ABC, and in repetitive behavior subscale of RBS-R after treatment | Increased gamma power to targets and decreased gamma power to non-targets after treatment | 5 patients reported itching sensation at nose during stimulation and one reported mild headache after stimulation |
| Casanova et al., 2012 [45] | rTMS | Reaction time and %error in an oddball-type task | ABC; RBS-R; SRS | ERPs | Before and two weeks after treatment | Significant decrease in total error and omission error rates after treatment | Significant decrease in irritability subscale of ABC, and in repetitive behavior subscale of RBS-R after treatment | Increased amplitude of the frontal and parietal N200 and frontal P3a and reduced latency of the frontal N200 to targets after treatment | Not reported |
| Fecteau et al., 2011 [51] | rTMS | Boston Naming Test | - | - | Before and after treatment | Increased response latency after left pars opercularis stimulation and decreased response latency after left pars triangularis stimulation compared to sham | - | - | Many side-effects reported including sleepy, more emotional, stiff neck, headache and dizziness |
| Enticott et al., 2012 [50] | rTMS | Reaction time; movement time | - | MRCPs | Before and after treatment | No significant differences in reaction time and movement time after treatment | - | Improvement in gradient of the early component of MRCPs after SMA stimulation and in gradient of the late component after PMC stimulation compared to sham | Not reported |
| Enticott et al., 2014 [48] | Deep rTMS | Reading the mind in the eyes test and animations mentalizing test | RAADS; AQ; IRI | - | Before, after and one month after treatment | No significant differences in mentalizing measures | Significant decrease in social relatedness subscale of RAADS, and in personal distress subscale of IRI compared to sham | - | One reported light headedness and two reported facial discomfort during stimulation |
| Panerai et al., 2014 [54] | rTMS | Eye-hand integration in the Psycho-educatiol Profile−Revised (PEP-R) | - | - | Before and after treatment | Increased eye-hand integration following HF-rTMS to the left premotor cortex, and also following that + training program compared to sham and compared to each treatment alone, respectively | - | - | Not reported |
| Anninos et al., 2016 [42] | Pico-Tesla TMS | - | Clinical examination | - | Before and after treatment | - | four patients experienced major changes, three minor changes and one mixed changes in the list of disorders after active treatment, while no changes reported for the sham group | - | Not reported |
| Ni et al., 2017 [52] | iTBS | CCPT; WCST | Y-BOCS; SRS | - | Before, after, 8 hours and 2 days after treatment | Significant decrease in reaction time in the CCPT after DLPFC stimulation compared to sham | According to the parent-reports and in comparison to sham, significant reduction in compulsive behaviors subscale of Y-BOCS after pSTS stimulation, and improvement in social communication subscale of SRS after DLPFC stimulation | - | Three patients reported transient muscle twitches around the eyes during stimulation over the DLPFC |
| Desarkar et al., 2017 [63] | rTMS | - | - | cortico-spinal excitability | Before and after treatment | - | - | Lessened long term depression and long term potentiation-like neuroplasticity following high frequency rTMS compared to sham | Not reported |
| Gómez et al., 2017 [64] | tDCS/rTMS | - | ABC; ADI-R; ATEC; GCIS | Brain functional connectivity; ERPs | Before, after, one month and six months after treatment | - | Significant reduction in the total scores in all scales one month after treatment | Increase in functional connectivity of the brain, especially for alpha, beta and gamma frequency bands, with most significant changes caused by rTMS technique, and significantly shorter latency of the P300 with no changes in its amplitude after intervention | Not reported |
tDCS, transcranial direct current stimulation; rTMS, repetitive transcranial magnetic stimulation; iTBS, intermittent theta burst stimulation; MT, motor threshold; DLPFC, dorsolateral prefrontal cortex; SMA, supplementary motor area; TPJ, temporoparietal junction; mPFC, medial prefrontal cortex; pSTS, posterior superior temporal sulcus; dmPFC, dorsomedial prefrontal cortex; PrMC, premotor cortex; M1, primary motor cortex; ABC, Aberrant Behavior Checklist; RBS-R, Repetitive Behavior Scale-Revised; SRS, Social Responsiveness Scale; ATEC, Autism Treatment Evaluation Checklist; AQ, Autism Spectrum Quotient; RAADS, Ritvo Autism-Aspergers Diagnostic Scale; CARS, Childhood Autism Rating Scale; Y-BOCS, Yale-Brown Obsessive-Compulsive Scale; ADI-R, Autism Diagnostic Interview-Revised; IRI, Interpersonal Reactivity Index; CGAS, Children’s Global Assessment Scale; CGI, Clinical Global Impression; WCST, Wisconsin Card Sorting Test; CCPT, Conner’s Continuous Performance Test; BOLD, blood oxygenation level dependent; ERP, event-related potential; MRCP, movement-related cortical potential.