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  • Differences in Neural Activity When ProcessingEmotional Arousal and Valence in Autism

    Spectrum Disorders

    Angela Tseng,1 Zhishun Wang,1 Yuankai Huo,1 Suzanne Goh,1

    James A. Russell,2 and Bradley S. Peterson1,3*

    1Department of Psychiatry, Columbia University College of Physicians and Surgeons andNew York State Psychiatric Institute, New York, NY, USA

    2Department of Psychology, Boston College, Chestnut Hill, MA, USA3Childrens Hospital Los Angeles and the Keck School of Medicine at the University of

    Southern California, Institute for the Developing Mind, Childrens Hospital Los Angeles, KeckSchool of Medicine at the University of Southern California, Los Angeles, CA, USA

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    Abstract: Individuals with autism spectrum disorders (ASD) often have difficulty recognizing andinterpreting facial expressions of emotion, which may impair their ability to navigate and communicatesuccessfully in their social, interpersonal environments. Characterizing specific differences betweenindividuals with ASD and their typically developing (TD) counterparts in the neural activity subserv-ing their experience of emotional faces may provide distinct targets for ASD interventions. Thus weused functional magnetic resonance imaging (fMRI) and a parametric experimental design to identifybrain regions in which neural activity correlated with ratings of arousal and valence for a broad rangeof emotional faces. Participants (51 ASD, 84 TD) were group-matched by age, sex, IQ, race, and socioe-conomic status. Using task-related change in blood-oxygen-level-dependent (BOLD) fMRI signal as ameasure, and covarying for age, sex, FSIQ, and ADOS scores, we detected significant differences acrossdiagnostic groups in the neural activity subserving the dimension of arousal but not valence. BOLD-signal in TD participants correlated inversely with ratings of arousal in regions associated primarilywith attentional functions, whereas BOLD-signal in ASD participants correlated positively with arousalratings in regions commonly associated with impulse control and default-mode activity. Only minordifferences were detected between groups in the BOLD signal correlates of valence ratings. Our find-ings provide unique insight into the emotional experiences of individuals with ASD. Although behav-ioral responses to face-stimuli were comparable across diagnostic groups, the corresponding neuralactivity for our ASD and TD groups differed dramatically. The near absence of group differences forvalence correlates and the presence of strong group differences for arousal correlates suggest that indi-viduals with ASD are not atypical in all aspects of emotion-processing. Studying these similarities anddifferences may help us to understand the origins of divergent interpersonal emotional experience inpersons with ASD. Hum Brain Mapp 00:000000, 2015. VC 2015 Wiley Periodicals, Inc.

    Additional Supporting Information may be found in the onlineversion of this article.

    Contract grant sponsor: NIMH; Contract grant numbers: R01MH089582 (BSP), 2 T32 MH16434 (BSP)

    *Correspondence to: Bradley S. Peterson, M.D., 4650 Sunset Blvd.MS# 135, Los Angeles, CA 90027, E-mail: bpeterson@chla.usc.edu

    Received for publication 27 May 2015; Revised 21 September2015; Accepted 19 October 2015.

    DOI: 10.1002/hbm.23041Published online 00 Month 2015 in Wiley Online Library(wileyonlinelibrary.com).

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    VC 2015 Wiley Periodicals, Inc.

  • Key words: autism spectrum disorders; arousal; valence; facial emotion; fMRI

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    INTRODUCTION

    Autism spectrum disorders (ASD) are a set of complexneurodevelopmental disabilities that cause lifelong impair-ments in social ability, communication, and behavioralflexibility [American Psychiatric Association, 2000]. Indi-viduals with ASD often have difficulty recognizing andinterpreting facial expressions of emotions, which mayimpair their ability to understand the intentionality andminds of others, a capacity needed for successful socialcommunication [Golan et al., 2006; Grelotti et al., 2002].Despite having a general consensus that persons with ASDare atypical in their processing of human faces and emo-tional expressions [Harms et al., 2010; Sasson, 2006],researchers do not agree on the underlying brain andbehavioral mechanisms through which individuals withASD decode emotional faces. Some prior research suggests

    that individuals with ASD rely more on cognitive-perceptual systems involving explicit cognitive or verballymediated processes to interpret facial expressions of emo-tions, in contrast to neurotypical individuals who processemotions more automatically [Harms et al., 2010; Pelphreyet al., 2007].

    Although ASD is generally considered to involve deficitsin emotion recognition, prior studies have provided onlyinconsistent evidence for those deficits. For example, sev-eral studies have reported that adults and children withASD have more difficulty recognizing, responding to, andexpressing emotions than typically developing (TD) indi-viduals [Ashwin et al., 2006; Tantam et al., 1989; Uljarevicand Hamilton, 2013] and more than persons with otherneurodevelopmental disorders [Celani et al., 1999; Ribyet al., 2008]. However, other studies have reported typicallevels of facial emotion recognition in persons with ASD[Castelli, 2005; Harms et al., 2010; Ozonoff et al., 1990;Tseng et al., 2014].

    Disparities in findings for the recognition and under-standing of emotions in individuals with ASD may, tosome extent, be due to fundamental differences in theunderlying model of emotion implicitly assumed whendesigning those studies. That underlying model has mostoften been the theory of basic emotions [Ekman, 1992; Pan-ksepp, 1992], which posits that each member of a core setof discrete, or basic, emotions (e.g., anger, sadness, orhappiness) are subserved by its own distinct and inde-pendent neural system [Ekman, 1992; Panksepp, 1992].Earlier reviews have documented the limitations andinconsistencies of this theory, including the absence ofone-to-one mappings of individual emotions with specificfacial expressions, motor behaviors, and autonomicresponses, as well as the absence of evidence for a core setof emotions from which other emotions derive [Hamann,2012; Posner et al., 2005; Russell, 1980; Vytal and Hamann,2010]. Moreover, interpreting findings from neuroimagingstudies based on the theory of basic emotions is compli-cated by the subtraction method employed in most func-tional imaging designs, in which brain activity ismeasured by comparing two tasks or stimuli that areassumed to differ only in the cognitive process of interest.Most functional imaging studies based on the theory ofbasic emotions have contrasted neural responses to indi-vidual emotions with neural responses to stimuli intendedto be emotion-neutral. Unfortunately, the use of neutralfaces as control stimuli is an inherent confound in emotionresearch because of the difficulties involved in creatingtruly neutral stimuli [Killgore and Yurgelun-Todd, 2004;Klein et al., 2015; Posner et al., 2005; Thomas et al., 2001].

    Additionally, most imaging studies of the basic emo-tions theory have focused only on a small number of

    Abbreviation

    ACC anterior cingulate cortexAMYG amygdalaBOLD blood oxygen level dependentBroca Brocas areaCb cerebellumCN caudate nucleusCu cuneusDLPFC dorsolateral prefrontal cortexFG fusiform gyrusHIPP hippocampusILPFC inferolateral prefrontal cortexINS insulaIPC inferior parietal cortexIPS intraparietal sulcusM1 primary motor cortexMCC middle cingulate cortexMFG middle frontal gyrusMOG middle occipital gyrusMTG middle temporal gyrusOFC orbitofrontal cortexPC parietal cortexPCC posterior cingulate cortexPCu precuneusPreMC premotor cortexPrG precentral gyrusPUT putamenS1 primary somatosensory cortexS2 secondary somatosensory cortexSFG superior frontal gyrusSMA supplementary motor areaSPL superior parietal lobuleSTS superior temporal sulcusTHAL thalamusV1 primary visual cortex

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  • emotions, generally those of high arousal and negativevalence (e.g., fear and anger), low arousal and negativevalence (e.g., sadness), or moderate arousal and positivevalence (e.g., happy). Consequently, researchers have hadtrouble disentangling the differing contributions of arousaland valence to the neural correlates of emotions. Forexample, happy stimuli are often the only positivevalence emotions included in study designs. Comparingthem to stimuli that are putatively neutral or even nega-tively valenced confounds the positive arousal componentwith the positive valence of the happy stimulus. In effect,even when comparing happy with putatively neutral faces,both of these types of stimuli have not only a valence, butalso an arousal component that is never considered as con-tributing to the reported fMRI activation [Fusar-Poli et al.,2009; Harms et al., 2010; Murphy et al., 2003].

    An alternative theoretical framework to the theory ofbasic emotions is the Circumplex Model of Affect, whichholds that the subjective experience of all emotions arisesfrom the linear combination of two independent neuro-physiological systems, valence and arousal. Valence refersto hedonic tone, or the degree to which an emotion ispleasant or unpleasant, whereas arousal represents thedegree to which an emotion is associated with high or lowenergy. Under this model, a happy response to a stimu-lus arises from relatively intense activation of the neuralsystem associated with positive valence and moderate acti-vation of the neural system associated with positivearousal. Other emotional states thus arise from the sametwo underlying neurophysiological systems but differ indegree of activation of each. Because all emotions can berepresented as a linear combination of the dimensions ofarousal and valence, emotions sha