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The structural neural correlates of atypical facial expression recognition in autism spectrum disorder

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Abstract

Previous studies have demonstrated that individuals with autism spectrum disorder (ASD) are worse at recognizing facial expressions than are typically developing (TD) individuals. The present study investigated the differences in structural neural correlates of emotion recognition between individuals with and without ASD using voxel-based morphometry (VBM). We acquired structural MRI data from 27 high-functioning adults with ASD and 27 age- and sex-matched TD individuals. The ability to recognize facial expressions was measured using a label-matching paradigm featuring six basic emotions (anger, disgust, fear, happiness, sadness, and surprise). The behavioural task did not find deficits of emotion recognition in ASD after controlling for intellectual ability. However, the VBM analysis for the region of interest showed a positive correlation between the averaged percent accuracy across six basic emotions and the grey matter volume of the right inferior frontal gyrus in TD individuals, but not in individuals with ASD. The VBM for the whole brain region under each emotion condition revealed a positive correlation between the percent accuracy for disgusted faces and the grey matter volume of the left dorsomedial prefrontal cortex in individuals with ASD, but not in TD individuals. The different pattern of correlations suggests that individuals with and without ASD use different processing mechanisms for recognizing others’ facial expressions.

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Data availability

The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to information that could compromise research participant privacy/consent.

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Acknowledgements

We thank ATR Brain Activity Imaging Center for their support in acquiring the data. We also thank Kazusa Minemoto, Emi Yokoyama and Akemi Inoue for their technical support.

Funding

This study was supported by the JSPS Funding Program for Next Generation World-Leading Researchers (LZ008), Grant-in-Aid for Young Scientists (B) (16K17360), and Grant-in-Aid for Scientific Research (C) (20K03478). The funding sources had no involvement in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.

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Authors and Affiliations

  1. Graduate School of Medicine, Kyoto University, Shogoin-Kawahara-cho, Sakyo-ku, Kyoto, 606-8507, Japan

    Shota Uono, Sayaka Yoshimura, Reiko Sawada & Motomi Toichi

  2. Department of Developmental Disorders, National Institute of Mental Health, National Center of Neurology and Psychiatry, 4-1-1 Ogawa-higashi, Kodaira, 187-8551, Japan

    Shota Uono

  3. Guardian Robot Project, RIKEN, 2‑2‑2, Hikaridai, Seika‑cho, Souraku‑gun, Kyoto, 619-0288, Japan

    Wataru Sato

  4. Brain Activity Imaging Center, Advanced Telecommunications Research Institute International, 2-2-2, Hikaridai, Seika-cho, Souraku-gun, Kyoto, 619-0288, Japan

    Takanori Kochiyama

  5. The Organization for Promoting Neurodevelopmental Disorder Research, 40 Shogoin-Sannocho, Sakyo-ku, Kyoto, 606-8392, Japan

    Reiko Sawada & Motomi Toichi

  6. Health and Medical Services Center, Shiga University, 1-1-1, Baba, Hikone, Shiga, 522-8522, Japan

    Yasutaka Kubota

  7. Rakuwa-Kai Otowa Hospital, 2 Otowa Chinji-cho, Yamashina-ku, Kyoto, 607-8062, Japan

    Morimitsu Sakihama

Authors
  1. Shota Uono
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  2. Wataru Sato
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  3. Takanori Kochiyama
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  4. Sayaka Yoshimura
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  5. Reiko Sawada
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  6. Yasutaka Kubota
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  7. Morimitsu Sakihama
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  8. Motomi Toichi
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Contributions

SU, WS, TK, SY, RS, YK, MS, and MT conceived and designed the experiments. SU, WS, TK, SY, RS and YK performed the experiments. SU, WS, and TK analysed the data. SU and WS wrote the first draft of the manuscript, and all authors contributed to the writing of the manuscript.

Corresponding author

Correspondence to Shota Uono.

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Ethical approval

The experiment was approved by the local ethics committee of the Primate Research Institute, Kyoto University. The experiment was conducted in accordance with the guidelines of the Declaration of Helsinki 1964 and its later amendments.

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All participants provided written informed consent prior to participation.

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Not applicable.

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The authors declare that they have no conflict of interest.

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Uono, S., Sato, W., Kochiyama, T. et al. The structural neural correlates of atypical facial expression recognition in autism spectrum disorder. Brain Imaging and Behavior 16, 1428–1440 (2022). https://doi.org/10.1007/s11682-021-00626-1

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