Neural correlates of moral reasoning in autism spectrum disorder

doi:10.1093/scan/nss051 SCAN (2013) 8, 702^710 Neural correlates of moral reasoning in autism spectrum disorder Karla Schneider,1,2 Katharina D. Pauly,1,2 Anna Gossen,1,2 Lea Mevissen,1 Tanja M. Michel,1,4 Ruben C. Gur,3 Frank Schneider,1,2,3 and Ute Habel1,2 1 Department of Psychiatry, Psychotherapy, and Psychosomatic Medicine, Medical School, RWTH Aachen University, 52074 Aachen, Germany, JARA-Brain Jülich Aachen Research Alliance, Translational Brain Medicine, Forschungszentrum Jülich GmbH, 3Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia Veterans Administration Medical Center, and 4Department of Psychiatry and Psychotherapy, Medical School, University of Rostock, 18147 Rostock 2 In our study, we tried to clarify whether patients with autism spectrum disorder (ASD) reveal different moral decision patterns as compared to healthy subjects and whether common social interaction difficulties in ASD are reflected in altered brain activation during different aspects of moral reasoning. 28 patients with high-functioning ASD and 28 healthy subjects matched for gender, age and education took part in an event-related functional magnetic resonance imaging study. Participants were confronted with textual dilemma situations followed by proposed solutions to which they could agree or disagree. On a neural level, moral decision making was associated with activation in anterior medial prefrontal regions, the temporo-parietal junction and the precuneus for both groups. However, while patients and healthy controls did not exhibit significant behavioral differences, ASD patients showed decreased activation in limbic regions, particularly the amygdala, as well as increased activation in the anterior and the posterior cingulate gyrus during moral reasoning. Alterations of brain activation in patients might thus indicate specific impairments in empathy. However, activation increases in brain regions associated with the default mode network and self-referential cognition also provide evidence for an altered way of patients cerebral processing with regard to decision making based on social information. Keywords: autism spectrum disorder; decision making; morality; neuroimaging; fMRI INTRODUCTION Although it is a relatively new field of research, already a wealth of studies approaching behavioral characteristics and neural underpinnings of moral cognition has accumulated (e.g. Moll et al., 2002; Schleim et al., 2010; Bzdok et al., in press). In solving moral tasks, the ventromedial prefrontal cortex (VMPFC), lateral orbitofrontal cortex, temporal and limbic regions seem to play a key role (Moll et al., 2002; Hiraishi et al., 2007; Young et al., 2007; Zahn et al., 2009; Schleim et al., 2010). Additionally, a recent study (Young et al., 2010) could show a reduced capacity of moral decision making based on the comprehension of the mental states of other individuals, especially in case of attempted harms, if the right temporo-parietal junction (TPJ) was temporarily inhibited by transcranial magnetic stimulation in healthy participants. Moral reasoning as a sophisticated element of social cognition requires a broad understanding of social contexts. Correspondingly, mental disorders, which are related to deficits in empathy and Theory of Mind (ToM), might interfere with adequate moral decision making (de Oliveira-Souza et al., 2008). For autism spectrum disorders (ASDs), this linkage was already suggested in a few behavioral studies (Blair, 1996; Moran et al., 2011; Zalla et al., 2011; Shulman et al., 2012) andto the authors’ knowledgein only one (case) study using functional magnetic resonance imaging (fMRI; Hiraishi et al., 2007). Particularly, Moran et al. (2011) revealed subtle weaknesses in moral decisions in patients with ASD with regard to the ability to differentiate between intentional and attempted harms. Likewise, Zalla et al. (2011) reported impairments of ASD patients with regard to provide welfare-based moral justifications. Advance Access publication 7 May 2012 We would also like to thank all our subjects, the participating self-help groups and therapy centers. Correspondence should be addressed to Ute Habel, Department of Psychiatry, Psychotherapy, and Psychosomatic Medicine, RWTH Aachen University, Pauwelsstraße 30, 52074 Aachen, Germany. E-mail: According to the main diagnostic classification systems of ICD-10 and DSM-IV, ASDs as pervasive developmental disorders are characterized by the three core features of deficits in communication, repetitive stereotyped behavior and impaired social interaction. While the literature is indecisive regarding the question of global ToM- and empathy-deficits in ASD (Frith and Happé, 1994; Castelli, 2005; Silani et al., 2008; Senju et al., 2009; Bird et al., 2010; Chevallier, 2012), there seems to be substantial convergence that also highfunctioning adults with ASD exhibit at least subtle deficits in empathy (Schulte-Rüther et al., 2010; Zalla et al., 2011) and/or ToM (Kana et al., 2009; Senju et al., 2009; Moran et al., 2011), which also seem to affect patients’ ability to make adequate moral decisions (Hiraishi et al., 2007; Moran et al., 2011; Zalla et al., 2011; Shulman et al., 2012). Furthermore, most of the recent studies examining moralityassociated aspects of social cognition, such as ToM (Kana et al., 2009) and empathy (Schulte-Rüther et al., 2010), revealed dysfunctions in respective brain networks in ASD patients, which have been related to patients’ social impairments (Lombardo et al., 2011). Anatomical and functional alterations were mainly found in the prefrontal cortex (PFC), particularly the medial PFC and in the TPJ (Kana et al., 2009; Martineau et al., 2010; Schulte-Rüther et al., 2010; Lombardo et al., 2011). Common dysfunctions in these areas in ASD might well come along with deficits in moral reasoning (Blair, 1996; Moran et al., 2011; Zalla et al., 2011; Shulman et al., 2012), and hence result in altered brain activation during moral tasks. Nonetheless, so far studies on moral understanding in clinical samples mainly focused on patients with psychopathy (e.g. de Oliveira-Souza et al., 2008), who were said to exhibit a contrariwise profile of empathy deficits as compared to patients with ASD, namely intact cognitive elements, but impairments in affective aspects of empathy (Blair, 2008; Krippl and Karim, 2011). However, at the same time potential overlaps between Asperger’s syndrome and sociopathy/ psychopathy were suggested (Anckarsäter et al., 2008). More, though there is no evidence for a general overrepresentation of patients with ß The Author (2012). Published by Oxford University Press. For Permissions, please email: Moral reasoning in autism spectrum disorder ASD in forensic settings, a first long-term study on deviant behavior in pervasive developmental disorders (Mouridsen et al., 2008) revealed a tendency in patients with ASD to particular cri (...truncated)