Biological Psychology 103 (2014) 125–134 Contents lists available at ScienceDirect Biological Psychology jo ur nal home p age: www.elsevier.com/locate/biopsycho Altered neurophysiological responses to emotional faces discriminate children with ASD, ADHD and ASD + ADHD Charlotte Tye a,d,* , Marco Battaglia b , Eleonora Bertoletti c , Karen L. Ashwood d , Bahare Azadi d , Philip Asherson a , Patrick Bolton a,d , Gráinne McLoughlin a,e a MRC Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, King’s College London, UK b Laval University and Institut Universitaire en Santé Mentale de Québec, Québec, Canada c Academic Centre for the Study of Behavioural Plasticity, Vita-Salute San Raffaele University, Milan, Italy d Child and Adolescent Psychiatry, Institute of Psychiatry, King’s College London, UK e Swartz Center for Computational Neuroscience, Institute for Neural Computation, University of California San Diego, USA a r t i c l e i n f o Article history: Received 25 April 2014 Accepted 25 August 2014 Available online 30 August 2014 Keywords: ASD ADHD Comorbidity Emotion Event-related potentials (ERP) a b s t r a c t There are high rates of overlap between autism spectrum disorder (ASD) and attention deficit hyper- activity disorder (ADHD). Emotional impairment in the two disorders, however, has not been directly compared using event-related potentials (ERPs) that are able to measure distinct temporal stages in emotional processing. The N170 and N400 ERP components were measured during presentation of emo- tional face stimuli to boys with ASD (n = 19), ADHD (n = 18), comorbid ASD + ADHD (n = 29) and typically developing controls (n = 26). Subjects with ASD (ASD/ASD + ADHD) displayed reduced N170 amplitude across all stimuli, particularly for fearful versus neutral facial expressions. Conversely, subjects with ADHD (ADHD/ASD + ADHD) demonstrated reduced modulation of N400 amplitude by fearful expressions in parietal scalp regions and happy facial expressions in central scalp regions. These findings indicate a dissociation between disorders on the basis of distinct stages of emotion processing; while children with ASD show alterations at the structural encoding stage, children with ADHD display abnormality at the contextual processing stage. The comorbid ASD + ADHD group presents as an additive condition with the unique deficits of both disorders. This supports the use of objective neural measurement of emotional processing to delineate pathophysiological mechanisms in complex overlapping disorders. © 2014 Elsevier B.V. All rights reserved. 1. Introduction Many of the characteristic social impairments of autism spectrum disorder (ASD) are likely to involve the ability to pro- cess socio-emotional signals including information from faces (Baron-Cohen, 1995; Baron-Cohen, Tager-Flusberg, & Cohen, 1993), particularly as there is consistent evidence of face processing deficits among these subjects (Dawson, Webb, & McPartland, 2005). Deficits are reported for the recognition of emotional expres- sions in ASD (Harms, Martin, & Wallace, 2010), with the greatest deficits shown for negative expressions (Ashwin, Chapman, Colle, & Baron-Cohen, 2006; Boraston, Blakemore, Chilvers, & Skuse, 2007; Uljarevic & Hamilton, 2012; Wallace, Coleman, & Bailey, 2008). Recent findings suggest there is substantial co-occurrence between * Corresponding author at: MRC SGDP Centre, Institute of Psychiatry, De Crespigny Park, London SE5 8AF, UK. Tel.: +44 207 848 5272; fax: +44 207 848 0866. E-mail address: charlotte.tye@kcl.ac.uk (C. Tye). ASD and attention deficit hyperactivity disorder (ADHD) that can be largely accounted for by overlapping genetic influences (Rommelse, Franke, Geurts, Hartman, & Buitelaar, 2009; Rommelse, Geurts, Franke, Buitelaar, & Hartman, 2011). Although the majority of research in ADHD has focused on the core symptoms of inatten- tion, hyperactivity and impulsivity, there is accumulating evidence to suggest emotional impairment in the disorder (Castellanos, Sonuga-Barke, Milham, & Tannock, 2006; Uekermann et al., 2010). In the limited studies available, deficits are reported in recognising and identifying emotion both generally (across different emotions) and for specific emotional expressions, as well as understanding their contextual meaning (Dickstein & Castellanos, 2012), although inconsistencies pertaining to methodological differences by age and intellectual ability are apparent. Similar performance on emotion identification tasks (labelling or matching emotional faces) has been reported in direct compar- isons of ASD and ADHD (Buitelaar, Van der Wees, Swaab-Barneveld, & van der Gaag, 1999; Fine, Semrud-Clikeman, Butcher, & Walkowiak, 2008), although some studies demonstrate poorer http://dx.doi.org/10.1016/j.biopsycho.2014.08.013 0301-0511/© 2014 Elsevier B.V. All rights reserved.