Attenuation of the contingency detection effect in the extrastriate body area in autism spectrum disorder

Yuko Okamoto; Ryo Kitada; Hiroki C Tanabe; Masamichi J Hayashi; Takanori Kochiyama; Toshio Munesue; Makoto Ishitobi; Daisuke N Saito; Hisakazu T Yanaka; Masao Omori; Yuji Wada; Hidehiko Okazawa; Akihiro T Sasaki; Tomoyo Morita; Shoji Itakura; Hirotaka Kosaka; Norihiro Sadato

doi:10.1016/j.neures.2014.06.012

Attenuation of the contingency detection effect in the extrastriate body area in autism spectrum disorder

Neurosci Res. 2014 Oct:87:66-76. doi: 10.1016/j.neures.2014.06.012. Epub 2014 Jul 24.

Authors

Yuko Okamoto¹, Ryo Kitada², Hiroki C Tanabe³, Masamichi J Hayashi⁴, Takanori Kochiyama⁵, Toshio Munesue⁶, Makoto Ishitobi⁷, Daisuke N Saito⁸, Hisakazu T Yanaka⁹, Masao Omori¹⁰, Yuji Wada¹¹, Hidehiko Okazawa⁸, Akihiro T Sasaki¹², Tomoyo Morita¹³, Shoji Itakura¹⁴, Hirotaka Kosaka¹⁵, Norihiro Sadato¹⁶

Affiliations

¹ Division of Cerebral Integration, Department of Cerebral Research, National Institute for Physiological Sciences, Japan; Department of Physiological Sciences, The Graduate University for Advanced Studies (Sokendai), Japan; Department of Education, Faculty of Regional Sciences, Tottori University, Japan.
² Division of Cerebral Integration, Department of Cerebral Research, National Institute for Physiological Sciences, Japan; Department of Physiological Sciences, The Graduate University for Advanced Studies (Sokendai), Japan.
³ Division of Cerebral Integration, Department of Cerebral Research, National Institute for Physiological Sciences, Japan; Department of Social and Human Environment, Graduate School of Environmental Studies, Nagoya University, Japan.
⁴ Division of Cerebral Integration, Department of Cerebral Research, National Institute for Physiological Sciences, Japan; Department of Physiological Sciences, The Graduate University for Advanced Studies (Sokendai), Japan; Institute of Biomedicine, Physiology, University of Helsinki, Finland; Brain Research Unit, O.V. Lounasmaa Laboratory, Aalto University School of Science, Finland.
⁵ Advanced Telecommunications Research Institute International, Brain Activity Imaging Center, Kyoto, Japan.
⁶ Research Center for Child Mental Development, Kanazawa University, Japan.
⁷ Department of Neuropsychiatry, Faculty of Medical Sciences, University of Fukui, Japan; Department of Child and Adolescent Mental Health, National Institute of Mental Health, National Center of Neurology and Psychiatry, Japan.
⁸ Biomedical Imaging Research Center, University of Fukui, Japan; Research and Education Program for Life Science, University of Fukui, Japan; Research Center for Child Mental Development, University of Fukui, Japan.
⁹ Department of Education, Faculty of Regional Sciences, Tottori University, Japan; Biomedical Imaging Research Center, University of Fukui, Japan; Research and Education Program for Life Science, University of Fukui, Japan.
¹⁰ Faculty of Nursing and Social Welfare Sciences, Fukui Prefectural University, Japan.
¹¹ Department of Neuropsychiatry, Faculty of Medical Sciences, University of Fukui, Japan; Research Center for Child Mental Development, University of Fukui, Japan.
¹² Division of Cerebral Integration, Department of Cerebral Research, National Institute for Physiological Sciences, Japan; Department of Physiological Sciences, The Graduate University for Advanced Studies (Sokendai), Japan; Department of Physiology, Osaka City University Graduate School of Medicine, Japan; Pathophysiological and Health Science Team, RIKEN Center for Life Science Technologies, Japan.
¹³ Division of Sensori-Motor Integration, Department of Integrative Physiology, National Institute for Physiological Sciences, Japan; Department of Adaptive Machine System, Graduate School of Engineering, Osaka University, Japan.
¹⁴ Department of Psychology, Graduate School of Letters, Kyoto University, Japan; Advanced Telecommunications Research Institute International, Intelligent Robotics and Communication Laboratories, Japan.
¹⁵ Department of Neuropsychiatry, Faculty of Medical Sciences, University of Fukui, Japan; Biomedical Imaging Research Center, University of Fukui, Japan; Research Center for Child Mental Development, University of Fukui, Japan.
¹⁶ Division of Cerebral Integration, Department of Cerebral Research, National Institute for Physiological Sciences, Japan; Department of Physiological Sciences, The Graduate University for Advanced Studies (Sokendai), Japan; Biomedical Imaging Research Center, University of Fukui, Japan. Electronic address: [email protected].

PMID: 25066523
DOI: 10.1016/j.neures.2014.06.012

Abstract

Detection of the contingency between one's own behavior and consequent social events is important for normal social development, and impaired contingency detection may be a cause of autism spectrum disorder (ASD). To depict the neural underpinnings of this contingency effect, 19 adults with ASD and 22 control participants underwent functional MRI while imitating another's actions and their actions being imitated by the other. As the extrastriate body area (EBA) receives efference copies of one's own movements, we predicted that the EBA would show an atypical response during contingency detection in ASD. We manipulated two factors: the congruency of the executed and observed actions, and the order of action execution and observation. Both groups showed the congruency effect in the bilateral EBA during imitation. When action preceded observation, the left EBA of the control group showed the congruency effect, representing the response to being imitated, indicating contingency detection. The ASD group showed a reduced contingency effect in the left EBA. These results indicate that the function of the EBA in the contingency detection is altered in ASD.

Keywords: Autism spectrum disorders; Being imitated; Extrastriate body area.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Brain / physiopathology
Brain Mapping
Child Development Disorders, Pervasive / physiopathology*
Female
Humans
Imitative Behavior / physiology*
Magnetic Resonance Imaging
Male
Occipital Lobe / physiopathology*
Psychomotor Performance / physiology
Self Concept*
Social Behavior*
Young Adult