Differential Fairness Decisions and Brain Responses After Expressed Emotions of Others in Boys with Autism Spectrum Disorders

Journal of Autism and Developmental Disorders, May 2017

Little is known about how emotions expressed by others influence social decisions and associated brain responses in autism spectrum disorders (ASD). We investigated the neural mechanisms underlying fairness decisions in response to explicitly expressed emotions of others in boys with ASD and typically developing (TD) boys. Participants with ASD adjusted their allocation behavior in response to the emotions but reacted less unfair than TD controls in response to happiness. We also found reduced brain responses in the precental gyrus in the ASD versus TD group when receiving happy versus angry reactions and autistic traits were positively associated with activity in the postcentral gyrus. These results provide indications for a role of precentral and postcentral gyrus in social-affective difficulties in ASD.

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Differential Fairness Decisions and Brain Responses After Expressed Emotions of Others in Boys with Autism Spectrum Disorders

J Autism Dev Disord Differential Fairness Decisions and Brain Responses After Expressed Emotions of Others in Boys with Autism Spectrum Disorders Eduard T. Klapwijk 0 1 2 4 5 6 Moji Aghajani 0 1 2 4 5 6 Gert‑Jan Lelieveld 0 1 2 4 5 6 Natasja D. J. van Lang 0 1 2 4 5 6 Arne Popma 0 1 2 4 5 6 Nic J. A. van der Wee 0 1 2 4 5 6 Olivier F. Colins 0 1 2 4 5 6 Robert R. J. M. Vermeiren 0 1 2 4 5 6 0 Institute of Psychology, Leiden University , Leiden , The Netherlands 1 Department of Psychiatry, VU University Medical Center , Amsterdam , The Netherlands 2 Department of Child and Adolescent Psychiatry, Curium - Leiden University Medical Center , Postbus 15, 2300 AA Leiden , The Netherlands 3 Eduard T. Klapwijk 4 Department of Psychiatry, Leiden University Medical Center , Leiden , The Netherlands 5 Institute of Criminal Law & Criminology, Faculty of Law, Leiden University , Leiden , The Netherlands 6 Department of Child and Adolescent Psychiatry, VU University Medical Center , Amsterdam , The Netherlands Little is known about how emotions expressed by others influence social decisions and associated brain responses in autism spectrum disorders (ASD). We investigated the neural mechanisms underlying fairness decisions in response to explicitly expressed emotions of others in boys with ASD and typically developing (TD) boys. Participants with ASD adjusted their allocation behavior in response to the emotions but reacted less unfair than TD controls in response to happiness. We also found reduced brain responses in the precental gyrus in the ASD versus TD group when receiving happy versus angry reactions and autistic traits were positively associated with activity in the postcentral gyrus. These results provide indications for a role of precentral and postcentral gyrus in social-affective difficulties in ASD. Social decision-making; Autism spectrum disorders; Interpersonal effects of emotions; Dictator game; fMRI - Leiden Institute for Brain and Cognition (LIBC), Leiden, The Netherlands Introduction Difficulties in reciprocal social interactions and communication are among the core features of autism spectrum disorders (ASD), along with a restricted repertoire of activities and interests (American Psychiatric Association 2013) . These social deficits have been documented in numerous studies showing that individuals with ASD have impairments in the ability to represent other people’s mental states (i.e., mentalizing; Baron-Cohen et  al. 1985; Kaland et  al. 2008) and in processing emotions of others (Adolphs et al. 2001; Hobson 1986; Uljarevic and Hamilton 2013) . Neuroimaging studies have also revealed differences between individuals with ASD compared to typically developing (TD) individuals in brain areas relevant for social-affective functioning (Di Martino et  al. 2009; Fishman et  al. 2014; Frith 2001; Pelphrey et  al. 2011; Philip et  al. 2012; White et  al. 2014) . These studies suggest that social deficits in ASD are associated with atypical activation in brain areas involved in mentalizing, such as hypoactivation in the medial prefrontal cortex (mPFC) and temporoparietal junction (TPJ) (e.g., Castelli et al. 2002; Wang et al. 2007; Watanabe et al. 2012) , as well as in brain areas relevant for processing and resonating with others’ emotions such as hypoactivation in the inferior frontal gyrus and both underand overactivation in the amygdala (e.g., Greimel et  al. 2010; Klapwijk et  al. 2016a; Monk et  al. 2010; Pelphrey et al. 2007; Swartz et al. 2013) . In most of the neuroimaging studies on social processing in ASD, participants are merely required to observe others or to think about their mental states (e.g., Kana et  al. 2015; Schulte-Ruther et al. 2011; Vander Wyk et al. 2014) . Although these studies have greatly advanced the understanding of the neurocognitive mechanisms associated with social deficits in ASD, most do not take more interactive elements of social exchange into account. Studying such elements, however, is essential, as responding towards others involves different cognitive processes than merely observing others’ behavior (Schilbach et  al. 2013) . This is especially important because a discrepancy has been reported between potentially normative performance on explicit social tasks in ASD versus difficulties in applying social abilities during social interactions (Klin et al. 2003) . For example, although adults with ASD do not spontaneously attribute mental states to others, they are able to understand mental states of others when they are explicitly encouraged to mentalize (Moran et  al. 2011; Senju et  al. 2009) . Paradigms inspired by behavioral economics are increasingly used to investigate social cognitive processes underlying social interactions in psychiatric populations (Hasler 2012; Sharp et al. 2012) including ASD (Chiu et al. 2008; Sally and Hill 2006; Yoshida et al. 2010) . These paradigms not only offer simplicity and experimental control, but (...truncated)


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Eduard T. Klapwijk, Moji Aghajani, Gert-Jan Lelieveld, Natasja D. J. van Lang, Arne Popma, Nic J. A. van der Wee, Olivier F. Colins, Robert R. J. M. Vermeiren. Differential Fairness Decisions and Brain Responses After Expressed Emotions of Others in Boys with Autism Spectrum Disorders, Journal of Autism and Developmental Disorders, 2017, pp. 2390-2400, Volume 47, Issue 8, DOI: 10.1007/s10803-017-3159-4