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Treatment Response of Transcranial Magnetic Stimulation in Intellectually Capable Youth and Young Adults with Autism Spectrum Disorder: A Systematic Review and Meta-Analysis

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Abstract

To examine current clinical research on the use of transcranial magnetic stimulation (TMS) in the treatment of pediatric and young adult autism spectrum disorder in intellectually capable persons (IC-ASD). We searched peer-reviewed international literature to identify clinical trials investigating TMS as a treatment for behavioral and cognitive symptoms of IC-ASD. We identified sixteen studies and were able to conduct a meta-analysis on twelve of these studies. Seven were open-label or used neurotypical controls for baseline cognitive data, and nine were controlled trials. In the latter, waitlist control groups were often used over sham TMS. Only one study conducted a randomized, parallel, double-blind, and sham controlled trial. Favorable safety data was reported in low frequency repetitive TMS, high frequency repetitive TMS, and intermittent theta burst studies. Compared to TMS research of other neuropsychiatric conditions, significantly lower total TMS pulses were delivered in treatment and neuronavigation was not regularly utilized. Quantitatively, our multivariate meta-analysis results report improvement in cognitive outcomes (pooled Hedges’ g = 0.735, 95% CI = 0.242, 1.228; p = 0.009) and primarily Criterion B symptomology of IC-ASD (pooled Hedges’ g = 0.435, 95% CI = 0.359, 0.511; p < 0.001) with low frequency repetitive TMS to the dorsolateral prefrontal cortex. The results of our systematic review and meta-analysis data indicate that TMS may offer a promising and safe treatment option for pediatric and young adult patients with IC-ASD. However, future work should include use of neuronavigation software, theta burst protocols, targeting of various brain regions, and robust study design before clinical recommendations can be made.

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Availability of Data and Materials

Data regarding systematic review is attached to the submission. Further meta-analytic data than presented in this manuscript is available upon request.

Abbreviations

rTMS :

Repetitive transcranial magnetic stimulation

MDD :

Major depressive disorder

HF-rTMS :

High frequency rTMS

LtDLPFC :

Left dorsolateral prefrontal cortex

TMS :

Transcranial magnetic stimulation

LF-rTMS :

Low frequency rTMS

RtDLPFC :

Right dorsolateral prefrontal cortex

TBS :

Theta burst stimulation

cTBS :

Continuous theta burst stimulation

iTBS :

Inhibitory theta burst stimulation

dTMS :

Deep TMS

OCD :

Obsessive compulsive disorder

mPFC :

Medial prefrontal cortex

ACC :

Anterior cingulate cortex

ASD :

Autism spectrum disorder

RRB :

Restricted/repetitive behaviors

EF :

Executive functioning

IC-ASD :

Autism spectrum disorder in intellectually capable persons

PRISMA:

Preferred Reporting Items for Systematic Reviews and Meta-Analyses

SMD :

Standardized mean differences

REML :

Restricted maximum likelihood

I2 JWR :

Jackson-White-Riley I2 index

NT :

Neurotypical

ADI-R :

Autism diagnostic interview-revised

ADOS :

Autism diagnostic observation schedule

SCL :

Skin conductance level

HRV :

Heart rate variability

BiDLPFC :

Bilateral DLPFC

M1:

Primary motor cortex

SMA :

Supplemental motor area

pSTS :

Posterior superior temporal sulcus

FDI :

First dorsal interossei muscle

SRS-2:

Social responsiveness scale

RBS-R :

Repetitive behavioral scale-revised

ABC:

Aberrant behavioral checklist

ERP :

Event related potentials

BRIEF:

Behavioral Rating Inventory for Executive Function

SR:

Self-Report

VABS-II:

Vineland Adaptive Behavior Scale–II

MRCP:

Movement-related cortical potentials

PV:

Parvalbumin

E/I:

Excitation-to-inhibition

EEG:

Electroencephalogram

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Funding

This work is funded in part by the National Institute of Mental Health (NIMH) of the National Institutes of Health (NIH) under award numbers T32HD007475 in the Eunice Kennedy Shriver National Institute of Child Health and Human Development, K23MH100450, and the Alan and Lorraine Bressler Clinical and Research Program for Autism Spectrum Disorder. Dr. Joshi is specifically supported by the NIMH of the NIH under Award Number K23MH100450. Dr. Anteraper receives grant support from NIMH of the NIH under award number 1R03MH121879-01A1. Dr. Croarkin receives funding from the NIH under grants R01 MH113700 and R01 MH124655. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the NIMH or the NIH.

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Authors and Affiliations

  1. Division of Child and Adolescent Psychiatry, Department of Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center at Village of Vanderbilt, 1500 21st Avenue South, Suite 2200, Nashville, TN, 37212, USA

    Joshua R. Smith

  2. Vanderbilt Kennedy Center, 110 Magnolia Circle, Nashville, TN, 37203, USA

    Joshua R. Smith

  3. Division of Child and Adolescent Psychiatry, Department of Psychiatry, Massachusetts General Hospital, 55 Fruit Street, Boston, MA, 02114, USA

    Joshua R. Smith, Tolga Atilla Ceranoglu & Gagan Joshi

  4. Department of Psychiatry, Harvard Medical School, 25 Shattuck Street, Boston, MA, 02115, USA

    Joshua R. Smith, Tolga Atilla Ceranoglu & Gagan Joshi

  5. Clinical and Research Programs in Pediatric Psychopharmacology, and Adult ADHD, Massachusetts General Hospital, 55 Fruit Street, Boston, MA, 02114, USA

    Maura DiSalvo, Allison Green, Tolga Atilla Ceranoglu & Gagan Joshi

  6. Alan and Lorraine Bressler Clinical and Research Program for Autism Spectrum Disorder, Massachusetts General Hospital, 55 Fruit Street, Boston, MA, 02114, USA

    Maura DiSalvo, Allison Green, Tolga Atilla Ceranoglu & Gagan Joshi

  7. Department of Psychological and Brain Sciences, Indiana University, 1101 East 10th Street, Bloomington, IN, 47405, USA

    Allison Green

  8. Carle Foundation Hospital, 611 West Park Street, Urbana, IL, 61801, USA

    Sheeba Arnold Anteraper

  9. Department of Psychiatry and Psychology, Mayo Clinic, 1216 2nd Street Southwest, Rochester, MN, 55902, USA

    Paul Croarkin

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  1. Joshua R. Smith
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  2. Maura DiSalvo
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  3. Allison Green
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  7. Gagan Joshi
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Contributions

JS: Conceptualization, Methodology, Investigation, Data Curation, Formal Analysis, Writing—Original Draft. MD: Conceptualization, Methodology, Investigation, Data Curation, Formal Analysis, Writing – Review and Editing. AG: Conceptualization, Methodology, Investigation, Writing – Review and Editing. AC: Conceptualization, Methodology, Investigation, Data Curation, Writing – Review and Editing. SA: Conceptualization, Writing – Review and Editing. PC: Conceptualization, Supervision, Writing – Review and Editing. GJ: Conceptualization, Methodology, Investigation, Data Curation, Formal Analysis, Supervision, Writing – Review and Editing.

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Correspondence to Joshua R. Smith.

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Competing Interests

JRS is employed by Vanderbilt University Medical Center as a child and adolescent psychiatrist with no other financial relationships to disclose. AG and MD do not have financial relationships to disclose. AC reports personal fees from Massachusetts Department of Mental Health, non-financial support from NIH, personal fees from Pamlab, Inc., personal fees from US Department of Defense, non-financial support from Neurocentria, Inc., personal fees from Food and Drug Administration, non-financial support from Pfizer Pharmaceuticals, Inc., personal fees from Sunovion Pharmaceuticals, Inc., non-financial support from Roche TCRC, Inc. SA is employed by the Carle Foundation Hospital in Urbana, Illinois with no other financial relationships to disclose. PC has received research support from Pfizer, Inc. and equipment support from Neuronetics, Inc. and MagVenture, Inc. He has received grant in kind support from AssureRX for supplies and genotyping. He has been the primary investigator for a multicenter study funded by Neuronetics, Inc. and a site primary investigator for a study funded by NeoSync, Inc. He has served as a paid consultant for Engrail Therapeutics, Myriad Neuroscience, Procter and Gamble Company, and Sunovion. In the last year, GJ has received research support from the Demarest Lloyd, Jr. Foundation as a primary investigator (PI) for investigator-initiated studies. Additionally, GJ receives research support F. Hoffmann-La Roche Ltd. as a site PI for multi-site trials. In the past three years, GJ has received research support from Pfizer and the Simons Center for the Social Brain. In addition, GJ has received honorarium from the Governor's Council for Medical Research and Treatment of Autism in New Jersey and from NIMH for grant review activities. Finally, he received speaker’s honorariums from the American Academy of Child and Adolescent Psychiatry, The Israeli Society of ADHD, the Canadian Academy of Child and Adolescent Psychiatry, and the University of Jülich.

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Smith, J.R., DiSalvo, M., Green, A. et al. Treatment Response of Transcranial Magnetic Stimulation in Intellectually Capable Youth and Young Adults with Autism Spectrum Disorder: A Systematic Review and Meta-Analysis. Neuropsychol Rev 33, 834–855 (2023). https://doi.org/10.1007/s11065-022-09564-1

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