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Altered neurovascular coupling in the children with attention-deficit/hyperactivity disorder: a comprehensive fMRI analysis

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Abstract

The coupling between resting-state cerebral blood flow (CBF) and blood oxygenation level-dependent (BOLD) signals reflects the mechanism of neurovascular coupling (NVC), which have not been illustrated in attention-deficit/hyperactivity disorder (ADHD). Fifty ADHD and 42 age- and gender-matched typically developing controls (TDs) were enrolled. The NVC imaging metrics were investigated by exploring the Pearson correlation coefficients between CBF and BOLD-derived quantitative maps (ALFF, fALFF, DCP maps). Three types of NVC metrics (CBF-ALFF, CBF-fALFF, CBF-DCP coupling) were compared between ADHD and TDs group, and the inner association between altered NVC metrics and clinical variables in ADHD group was further analyzed. Compared to TDs, ADHD showed significantly reduced whole-brain CBF-ALFF coupling (P < 0.001). Among regional level (all PFDR < 0.05), ADHD showed significantly lower CBF-ALFF coupling in bilateral thalamus, default-mode network (DMN) involving left anterior cingulate (ACG.L) and right parahippocampal gyrus (PHG.R), execution control network (ECN) involving right middle orbital frontal gyrus (ORBmid.R) and right inferior frontal triangular gyrus (IFGtriang.R), and increased CBF-ALFF coupling in attention network (AN)-related left superior temporal gyrus (STG.L) and somatosensory network (SSN))-related left rolandic operculum (ROL.L). Furthermore, increased CBF-fALFF coupling was found in the visual network (VN)-related left cuneus and negatively correlated with the concentration index of ADHD (R = − 0.299, PFDR = 0.035). Abnormal regional NVC metrics were at widespread neural networks in ADHD, mainly involved in DMN, ECN, SSN, AN, VN and bilateral thalamus. Notably, this study reinforced the insights into the neural basis and pathophysiological mechanism underlying ADHD.

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Data availability

Data generated or analyzed during the study are available from the corresponding author by request.

Abbreviations

ADHD:

Attention-deficit/hyperactivity disorder

TD:

Typically developing

NVC:

Neurovascular coupling

BOLD:

Blood oxygenation level dependent

ASL:

Arterial spin labeling

CBF:

Cerebral blood flow

ALFF:

Amplitude of low-frequency fluctuation

fALFF:

Fractional amplitude of low-frequency fluctuation

DC:

Degree centrality

DMN:

Default-mode network

AN:

Attention network

SN:

Salience network

SSN:

Somatosensory network

VN:

Visual network

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Acknowledgements

This work was supported by the Natural Science Fund Youth Science Fund Project of China [grant number 82001439], the Natural Science Fund Project of Guangdong Province [grant numbers 2022A1515011910] and the Guangdong Basic and Applied Basic Research Foundation, China (No.2020A1515011436). We would like to thank the participants and their families and the staff at the MRI at the First Affiliated Hospital of Sun Yat-sen University for all their help and support.

Funding

This work was supported by the Natural Science Fund Youth Science Fund Project of China [grant numbers 82001439], the Natural Science Fund Project of Guangdong Province [grant numbers 2022A1515 011910], and the Guangdong Basic and Applied Basic Research Foundation, China (No.2020A1515011436).

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Author notes

  1. Shu Su, Jing Zhao and Yan Dai contributed equally to this work.

Authors and Affiliations

  1. Department of Radiology, First Affiliated Hospital, Sun Yat-Sen University, Guangzhou, China

    Shu Su, Jing Zhao, Yan Dai, Liping Lin, Qin Zhou, Zi Yan, Zhiyun Yang & Yingqian Chen

  2. Department of Biomedical Engineering, College of Engineering, Peking University, Beijing, China

    Long Qian & Wei Cui

  3. Department of Pediatric, First Affiliated Hospital, Sun Yat-Sen University, Guangzhou, China

    Meina Liu & Hongyu Zhang

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  1. Shu Su
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Contributions

Shu Su, Yingqian Chen, Jing Zhao and Zhiyun Yang wrote the main manuscript text. Shu Su, Yingqian Chen, Yan Dai, Long Qian, Wei Cui and Liping Lin prepared figures 1-5. Qin Zhou, Zi Yan, Hongyu Zhang and Meina Liu collected the imaging and clinical data. All authors reviewed the manuscript.

Corresponding authors

Correspondence to Zhiyun Yang or Yingqian Chen.

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Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Ethical approval and consent to participate

This study was approved by the institutional review board of our institution (No. [2019]328). Written informed consent was obtained from the guardians of all the subjects and their guardians in this study.

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Su, S., Zhao, J., Dai, Y. et al. Altered neurovascular coupling in the children with attention-deficit/hyperactivity disorder: a comprehensive fMRI analysis. Eur Child Adolesc Psychiatry 33, 1081–1091 (2024). https://doi.org/10.1007/s00787-023-02238-0

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