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ADHD-related sex differences in frontal lobe white matter microstructure and associations with response control under conditions of varying cognitive load and motivational contingencies

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Abstract

Children with attention-deficit/hyperactivity disorder (ADHD) demonstrate reduced response inhibition, increased response time variability, and atypical frontal lobe white matter microstructure with emerging evidence of sex differences. This study aims to examine whether frontal lobe white matter microstructure is differentially impacted in ADHD by sex and whether this relates to Go/No-Go (GNG) task performance. Diffusion tensor imaging (DTI) from 187 children (8–12 years), including ADHD (n = 94) and typically developing controls (TD; n = 93). Participants completed three GNG tasks with varying cognitive demands and incentives (standard, cognitive, and motivational). Fractional anisotropy (FA) was examined as an index of white matter microstructure within bilateral frontal lobe regions of interest. Children with ADHD showed reduced FA in primary motor (M1) and supplementary motor area (SMA) regardless of sex. Sex-based dissociation for the effect of diagnosis was observed in medial orbitofrontal cortex (mOFC), with higher FA in girls with ADHD and lower FA in boys with ADHD. Both diagnosis and sex contributed to performance on measures of response inhibition and reaction time (RT) variability, with all children with ADHD demonstrating poorer performance on all GNG tasks, but boys with ADHD demonstrating more impulsivity on standard and motivational behavioral paradigms compared to girls with ADHD. Analyses revealed associations between reduced FA in M1, SMA, and mOFC and increased response inhibition and RT variability with some sex-based differences. These findings provide novel insights regarding the brain basis of ADHD and associated impairments in response inhibition and RT variability, and contribute to our understanding of sexual dimorphic behavioral outcomes.

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Data Availability

The datasets generated during and/or analyzed during the current study are available from the authors on reasonable request.

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Acknowledgements

We would like to thank the children and parents who participated in this research.

Funding

This work was supported by the NIH with grants awarded to KSR (K23-MH101322, R03-MH119457), SHM (R01-MH078160 and R01-MH085328), and P50HD103538. The MRI equipment in this study was funded by NIH grant 1S10OD021648. These sponsors had no role in the study design, collection of data, analysis of data, or interpretation of data.

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Authors and Affiliations

  1. Neuropsychology Department, Kennedy Krieger Institute, 1750 E. Fairmount Avenue, Baltimore, MD, 21231, USA

    Rachel K. Peterson & Keri S. Rosch

  2. Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Rachel K. Peterson, Stewart H. Mostofsky & Keri S. Rosch

  3. Center for Neurodevelopmental and Imaging Research, Kennedy Krieger Institute, Baltimore, MD, USA

    Philip Duvall, Deana Crocetti, Tara Palin, Joshua Robinson, Stewart H. Mostofsky & Keri S. Rosch

  4. Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Stewart H. Mostofsky

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  1. Rachel K. Peterson
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  2. Philip Duvall
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  3. Deana Crocetti
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  4. Tara Palin
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  5. Joshua Robinson
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  6. Stewart H. Mostofsky
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  7. Keri S. Rosch
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Contributions

Author contributions included conception and study design (DC, SHW, KSR), data collection or acquisition (PD, DC, TP, JR), statistical analysis (DC, SHM, KSR), interpretation of results (RKP, DC, SHM, KSR), drafting the manuscript work or revising it critically for important intellectual content (RKP, DC, SHM, KSR) and approval of final version to be published and agreement to be accountable for the integrity and accuracy of all aspects of the work (All authors).

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Correspondence to Rachel K. Peterson.

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The authors have no conflicts of interest to disclose.

Ethics approval

This study was approved by the Johns Hopkins Institutional Review Board.

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All study participants provided written informed consent prior to participation.

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All authors consented to this paper to be published in Brain imaging and behaviors.

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Peterson, R.K., Duvall, P., Crocetti, D. et al. ADHD-related sex differences in frontal lobe white matter microstructure and associations with response control under conditions of varying cognitive load and motivational contingencies. Brain Imaging and Behavior 17, 674–688 (2023). https://doi.org/10.1007/s11682-023-00795-1

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