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Extrastriatal dopamine D2/3 receptor binding, functional connectivity, and autism socio-communicational deficits: a PET and fMRI study

Molecular Psychiatry volume 27, pages 2106–2113 (2022)Cite this article

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Abstract

The social motivation hypothesis of autism proposes that social communication symptoms in autism-spectrum disorder (ASD) stem from atypical social attention and reward networks, where dopamine acts as a crucial mediator. However, despite evidence indicating that individuals with ASD show atypical activation in extrastriatal regions while processing reward and social stimuli, no previous studies have measured extrastriatal dopamine D2/3 receptor (D2/3R) availability in ASD. Here, we investigated extrastriatal D2/3R availability in individuals with ASD and its association with ASD social communication symptoms using positron emission tomography (PET). Moreover, we employed a whole-brain multivariate pattern analysis of resting-state functional magnetic resonance imaging (fMRI) to identify regions where functional connectivity atypically correlates with D2/3R availability depending on ASD diagnosis. Twenty-two psychotropic-free males with ASD and 24 age- and intelligence quotient-matched typically developing males underwent [11C]FLB457 PET, fMRI, and clinical symptom assessment. Participants with ASD showed lower D2/3R availability throughout the D2/3R-rich extrastriatal regions of the dopaminergic pathways. Among these, the posterior region of the thalamus, which primarily comprises the pulvinar, displayed the largest effect size for the lower D2/3R availability, which correlated with a higher score on the Social Affect domain of the Autism Diagnostic Observation Schedule-2 in participants with ASD. Moreover, lower D2/3R availability was correlated with lower functional connectivity of the thalamus-superior temporal sulcus and cerebellum–medial occipital cortex, specifically in individuals with ASD. The current findings provide novel molecular evidence for the social motivation theory of autism and offer a novel therapeutic target.

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Fig. 1: [11C]FLB457 binding potential (BPND) values of all 10 regions of interest in autism-spectrum disorder (ASD) and typically developing (TD) individuals.
Fig. 2: Correlations between [11C]FLB457 binding potential (BPND) values in the posterior subregion of the thalamus and social affect (SA)-revised scores of the Autism Diagnostic Observation Schedule Second Edition (ADOS-2) in individuals with autism-spectrum disorder (ASD).
Fig. 3: Results of the multivariate pattern analysis (MVPA) of resting-state functional MRI data.

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Acknowledgements

We thank all the study participants and staff of Hamamatsu Medical Imaging Center, Hamamatsu Medical Photonics Foundation, the Global Strategic Challenge Center, Hamamatsu Photonics K.K., and the Department of Psychiatry, Hamamatsu University School of Medicine for their assistance with data collection. This research was supported by the Strategic Research Program for Brain Sciences of the Japan Agency for Medical Research and Development (JP16dm0107134). We thank Sarina Iwabuchi, Ph.D., and Sydney Koke, MFA, from Edanz (https://jp.edanz.com/ac) for editing a draft of this paper.

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Authors and Affiliations

  1. Department of Psychiatry, Hamamatsu University School of Medicine, Hamamatsu, Japan

    Chihiro Murayama, Yasuhiko Kato, Masamichi Yokokura, Takafumi Goto, Taishi Tamayama, Yosuke Kameno, Tomoyasu Wakuda, Hitoshi Kuwabara & Hidenori Yamasue

  2. United Graduate School of Child Development, Hamamatsu University School of Medicine, Hamamatsu, Japan

    Toshiki Iwabuchi, Masamichi Yokokura, Taeko Harada, Hitoshi Kuwabara, Atsushi Senju & Hidenori Yamasue

  3. Research Center for Child Mental Development, Hamamatsu University School of Medicine, Hamamatsu, Japan

    Toshiki Iwabuchi, Taeko Harada & Atsushi Senju

  4. Centre for Brain and Cognitive Development, Birkbeck, University of London, London, UK

    Atsushi Senju

  5. Hamamatsu Medical Imaging Center, Hamamatsu Medical Photonics Foundation, Hamamatsu, Japan

    Sadahiko Nishizawa

  6. Global Strategic Challenge Center, Hamamatsu Photonics K.K., Hamamatsu, Japan

    Yasuomi Ouchi

  7. Department of Biofunctional Imaging, Hamamatsu University School of Medicine, Hamamatsu, Japan

    Yasuomi Ouchi

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  1. Chihiro Murayama
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Contributions

HY had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: MY, YO, and HY. Acquisition, analysis, or interpretation of data: CM, YaK, MY, TI, TH, TG, TT, YoK, TW, HK, SB, AS, YO, and HY. Drafting of the paper: CM, TI, HY. Critical revision of the paper for important intellectual content: TI, MY, TH, TG, TT, YoK, TW, HK, SB, AS, SN, and YO. Statistical analysis: CM, TI, and HY. Obtained funding: HY. Administrative, technical, or material support: SN, YO. Study supervision: YO, HY.

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Correspondence to Hidenori Yamasue.

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Murayama, C., Iwabuchi, T., Kato, Y. et al. Extrastriatal dopamine D2/3 receptor binding, functional connectivity, and autism socio-communicational deficits: a PET and fMRI study. Mol Psychiatry 27, 2106–2113 (2022). https://doi.org/10.1038/s41380-022-01464-3

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