- Email: [email protected]
Defiant-Conduct Disorder symptoms in school-aged youth
Accepted Manuscript Title: Valence, arousal or both? Shared emotional deficits associated with Attention Deficit and Hyperactivity Disorder and Oppositional/Defiant-Conduct Disorder symptoms in school-aged youth Authors: Andry V. Souroulla, Maria Panteli, Jason D. Robinson, Georgia Panayiotou PII: DOI: Reference:
S0301-0511(18)30383-1 https://doi.org/10.1016/j.biopsycho.2018.11.007 BIOPSY 7621
To appear in: Received date: Revised date: Accepted date:
10 May 2018 16 November 2018 19 November 2018
Please cite this article as: Souroulla AV, Panteli M, Robinson JD, Panayiotou G, Valence, arousal or both? Shared emotional deficits associated with Attention Deficit and Hyperactivity Disorder and Oppositional/Defiant-Conduct Disorder symptoms in school-aged youth, Biological Psychology (2018), https://doi.org/10.1016/j.biopsycho.2018.11.007 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Valence, arousal or both? Shared emotional deficits associated with Attention Deficit and Hyperactivity Disorder and Oppositional/Defiant-Conduct Disorder symptoms in school-
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aged youth
Running Head: VALENCE AND AROUSAL DEFICITS IN DISRUPTIVE PROBLEMS
Andry V. Souroulla¹, Maria Panteli¹, Jason D. Robinson² & Georgia Panayiotou¹
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¹University of Cyprus, Cyprus
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² The University of Texas M. D. Anderson Cancer Center, USA
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Contact: Georgia Panayiotou
Department of Psychology and Center for Applied Neuroscience
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University of Cyprus
P.O. Box 20537, 1678 Nicosia, Cyprus
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TEL: +35722892081
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Email: [email protected]
Highlights
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Valence and arousal deficits associated with ADHD and CD/ODD symptoms were studied Heart rate, skin conductance and facial EMG were assessed during emotional pictures Decreased baseline heart rate and reactivity to fear was associated with ADHD Valence systems measured with facial EMG were unassociated with any symptom type Deficits seem arousal based and may increase with comorbidity or severity
Abstract
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We examined emotional responses in Attention Deficit Hyperactivity and Oppositional Defiant/Conduct Disorder to affective pictures. Eighty seven children (42 female, Mage=11.2), with clinical or subclinical symptoms and controls viewed joy, fear, sadness
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or neutral pictures while heart rate, skin conductance, corrugator and zygomaticus responses were recorded. The moderating role of Callous-Unemotional and anxiety traits was evaluated. Lower resting heart rate and decreased skin conductance across picture
types was associated with ADHD symptoms. Decreased heart rate reactivity to fear and sad stimuli was associated with ADHD and ODD/CD. Corrugator and zygomaticus
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responses were not associated with ADHD or ODD/CD. Findings are mostly consistent
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with a fearlessness account of disruptive behavior, and seem to also pertain to ADHD,
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with intact valence systems. Findings are discussed in light of the significance of
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identifying common pathogenic mechanisms across traditional diagnostic categories,
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consistent with trans-diagnostic approaches to the study of psychopathology.
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Keywords: arousal, valence, psychophysiology, disruptive problems, children
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Valence, arousal or both? Shared emotional deficits associated with Attention Deficit and Hyperactivity Disorder and Oppositional/Defiant-Conduct Disorder
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symptoms in school-aged youth Attention Deficit Hyperactivity Disorder (ADHD), Conduct Disorder (CD) and
Oppositional Defiant Disorder (ODD) are typically diagnosed in childhood. ADHD manifests as inattention and/or hyperactivity-impulsivity that interfere with schoolwork
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and social functioning; combined and hyperactive types also involve disruptive behaviors. ODD is characterized by non-compliance, angry or irritable mood, argumentativeness or vindictiveness. CD involves violation of social norms or others’
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rights and can include bullying (Lazarou, 2013), physical fighting, cruelty to people and animals, destruction of property and other antisocial acts (DSM-5; American Psychiatric Association, 2013a). The three conditions share many phenotypic similarities, including
behavioral disinhibition, impulsivity, non-compliance, rule breaking and oppositionality. These were underscored in the 4th edition of the Diagnostic and Statistical Manual
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(DSM-IV-TR; American Psychiatric Association, 2000), which categorized them as
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“disruptive” disorders in the same taxonomy. DSM-5 classifies them separately. ODD
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and CD, due to behavioral dysregulation, are listed as Disruptive, Impulse Control and
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Conduct Disorders. ADHD is a Neurodevelopmental Disorder, based on its early onset and neuropsychological deficits (American Psychiatric Association, 2013a, 2013b).
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In spite of this change, their similarities and high comorbidity cannot be ignored:
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In 39.9% of cases, a diagnosis of ADHD co-exists with ODD and in 14.3% with CD
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(Jensen, 1999). ODD and CD were not typically diagnosed as comorbid in DSM-IV, (something allowed in DSM-5) because it was assumed that all ODD features are also
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present in CD (APA, 2013b, 2000). When symptoms of both were observed, CD was given precedence, as a more severe form of the same disorder, an assumption justified by
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CD and ODD’s shared phenotypic behavioral dysregulation, and psychosocial or hereditary risk factors (Burke, Loeber, Mutchka, & Lahey, 2002; Rowe, Maughan, Pickles, Costello, & Angold, 2002). In both DSM versions, ODD is considered a premorbid condition, which progresses to CD in some children (APA, 2013b, 2000). For
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these reasons CD and ODD are seen as more similar between them than with ADHD, justifying their continued inclusion in the same taxonomic category. ADHD is viewed as distinct because it does not typically involve vindictiveness and deliberate rule violation.
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In this paper we treat CD and ODD as representing a common psychopathology dimension, which we call ODD/CD, as done by others (e.g. Noordermeer, Luman, & Oosterlaan, 2016). However, because of phenotypic and probably endophenotypic
similarities, all three disorders are believed to share important elements, including a
common developmental pathway, with ADHD typically appearing earlier, followed by
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ODD and CD, such that earlier disorders increase the risk for later ones (Beauchaine,
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Hinshaw, & Pang, 2010; Biederman et al., 2006; Campbell, Shaw, & Gilliom, 2000;
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Harvey, Breaux, & Lugo-Candelas, 2016; Kronenberger & Meyer, 2001).
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The similarities between ODD/CD and ADHD have instigated a search for common mechanisms (Nigg, 2001; Scheres, Oosterlaan, & Sergeant, 2001). In this study,
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we focus on emotional mechanisms that may underlie the externalizing behaviors found
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in all three disorders, hoping to contribute to enlightening their etiologies. To this end, we
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adopt a dimensional framework, as described in the Research Domain Criteria (RDoC; Cuthbert & Insel, 2013; Etkin & Cuthbert, 2014), promoted by the NIMH. The RDoC, in
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contrast to the traditional categorical framework to psychopathology used by the DSM, relies on empirically documented neurobiological dimensions and systems of behavior
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instead of the conventional, syndromal focus on symptom clusters (Casey, Oliveri, & Insel, 2014). Consistent with the RDoC, we examine emotional mechanisms, which transcend diagnostic categories and levels of severity, in ODD/CD and ADHD.
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Specifically, we study the functioning of the arousal, the positive and negative valence systems in children with symptoms of ADHD, CD and ODD, across levels of severity, including clinical, subclinical and no symptoms, measuring physiology and self-
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report. Examining both valence and arousal allows for specification of emotional deficits, as these represent two basic dimensions of affective responses (Russell & Carroll, 1999; Russell & Mehrabian, 1977). Arousal describes response intensity and valence its motivational direction of approach/avoidance (Lang, Bradley & Cuthbert, 1990).
Although the link between specific physiological indices and the valence and
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arousal dimensions is complex rather than simple and direct, some measures are more
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strongly associated with each of these systems. Skin conductance (SC), primarily affected
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by the sympathetic system, typically measures arousal (Bradley, Codispoti, Cuthbert, &
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Lang, 2001; Dawson, Schell, & Filion, 2007; Witvliet & Vrana, 1995), although depending on the situation, it may be more strongly associated with arousing positive or
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negative emotions (Bernat, Patrick, Benning, & Tellegen, 2006; Driscoll, Tranel, &
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Anderson, 2009; Gomez, von Gunten, & Danuser, 2016). Heart rate (HR) is dually
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affected by both the sympathetic and parasympathetic system, and typically indexes arousal (Azarbarzin, Ostrowski, Hanly, & Younes, 2014; Driscoll et al., 2009) but is also
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affected by the activation required by the specific situation (Kreibig, 2010) and by valence (Cacioppo, Berntson, Larsen, Poehlmann, & Ito, 2000; Witvliet & Vrana, 1995),
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especially when examining phasic changes; for example, HR deceleration is greater during negative emotions (McManis, Bradley, Berg, Cuthbert, & Lang, 2001; Tan et al., 2016). Facial expressions measured with electromyography (EMG), at the corrugator and zygomaticus muscles, index negative and positive valence respectively (Dimberg, 1988,
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1990; Mauss & Robinson, 2009; Peasley-Miklus, Panayiotou, & Vrana, 2016), but may also be affected by stimulus intensity (Balconi, Vanutelli, & Finocchiaro, 2014). Emotional Dysfunctions Associated with Externalizing Behavior
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Most relevant theories implicate emotional dysfunctions in the etiology of CD and ODD. Although somewhat different paradigms have been used to study ADHD, this is
also known to entail emotional lability and dysregulation (Merwood et al., 2014; Rosen,
Walerius, Fogleman, & Factor, 2015; Sobanski et al., 2010; Villemonteix, Purper-Ouakil, & Romo, 2015). Based on these theories, externalizing symptoms may result from
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fearlessness, hypo-arousal or unregulated affect, or may have heterogeneous etiologies,
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involving anyone of these paths (Fowles & Dindo, 2006; Frick & Viding, 2009; Nigg,
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Goldsmith, & Sachek, 2004; Rosen et al., 2015). Although all implicate dysfunctions of
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the arousal or valence systems, each theory yields somewhat different predictions. A fearlessness account would predict decreased autonomic and defense system reactivity,
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specifically in threatening contexts. Hypo-arousal, would suggest decreased responses
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across negative affective, but also during positive situations. Emotion dysregulation
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accounts predict, instead, exaggerated responses to emotional challenges, due to response modulation problems and lability (Gomez, 2003; Newman & Lorenz, 2003).
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Based on the fearlessness hypothesis, behavioral problems entail temperamental lack of fearful inhibition and unresponsiveness to punishment (Frick, Lilienfeld, Ellis,
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Loney, & Silverthorn, 1999; Frick & Morris, 2004; Frick & Viding, 2009). Fearlessness is mainly attributed to the association between externalizing behaviors and CallousUnemotional Traits (CU) in youth and psychopathy in adults. Theories of moral socialization, suggest that fearlessness and punishment insensitivity inhibits the
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development of morality and conscience (Fowles & Kochanska, 2000), permitting antisocial behavior to occur. Evidence for a defense system dysfunction (i.e. fearlessness) has accrued for both adults with psychopathy (Armstrong, Keller, Franklin, &
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Macmillan, 2009; Hill, 2002; Patrick & Lang, 1999) and youth with CU traits (Fung et al., 2005; Kavish et al., 2017; Latvala, et al., 2015; Lorber, 2004; Portnoy et al., 2014). Findings include low tonic HR and SC and reduced startle reflex potentiation to
threatening stimuli, jointly indicating valence and arousal dysfunctions during defensive activation (Blair & Mitchell, 2009; Patrick & Lang, 1999; Portnoy & Farrington, 2015).
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The hypo-arousal theory suggests that externalizing behavior involves decreased
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tonic autonomic arousal and emotional reactivity, which is experienced as unpleasant.
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Attempts to achieve stimulation and avoid boredom result in sensation seeking and acting
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out, as in CD or ODD (Matthys, Vanderschuren, & Schutter, 2013). In line with this, recent findings indicate that lower resting HR in adolescence predicts risk for adult
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criminality (Latvala et al., 2015). In contrast, emotion dysregulation theories suggest that
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at least a subgroup of children with disruptive behaviors show increased, instead of
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decreased reactivity to provocation (Fowles & Dindo, 2006; Nigg et al., 2004), resulting from impulsivity and disinhibition, and valence or arousal dysfunctions.
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Notably, there are fewer theoretical accounts on the role of the positive valence system in disruptive behavior. Beauchaine (2012) posited that antisocial individuals have
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an under-responsive appetitive system due to low ventral striatum activation, requiring greater stimulation to initiate approach behaviors. A meta-analysis of fMRI data suggests ventral-striatal hypo-responsiveness also in ADHD (Plichta & Scheres, 2014) consistent with neuropsychological and physiological evidence of approach system deficits (Crone,
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Richard Jennings, & Van Der Molen, 2003; Scheres, Tontsch, Thoeny, & Kaczkurkin, 2010). Others, (Fowles & Dindo, 2009) suggest that the positive valence system in those with psychopathy and CU traits is normal or over- responsive, as, like controls, they
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show startle inhibition during pleasant stimuli (Fanti, Panayiotou, Lazarou, Michael, & Georgiou, 2016; Vaidyanathan, Hall, Patrick, & Bernat, 2011). We next review findings on arousal and valence system functioning specifically in CD, ODD and ADHD.
Dysfunction of the arousal system. There is consistent evidence of tonic
autonomic hypo-arousal in children with conduct problems, suggesting arousal system
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dysfunction. Two meta-analyses show that low resting HR is the best replicated
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biological correlate of youth antisocial behavior (Ortiz & Raine, 2004; Portnoy &
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Farrington, 2015). Lorber, (2004) showed that low resting HR is reliably associated with
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conduct problems in both children and adolescents; low resting SC was associated with conduct problems only in children but not adolescents.
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However, evidence linking low resting autonomic arousal to specific disorders is
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less consistent, and it is unclear how it pertains to ADHD, in light of its associated
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emotional lability (Rosen et al., 2015; Sobanski et al., 2010). In Van Bokhoven, Matthys, Van Goozen, & Van Engeland, (2005), lower resting SC, but not HR, predicted later
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externalizing problems in children with ODD or CD irrespective of comorbid ADHD. Van Goozen, et al., (2000) found both lower HR and SC across ODD, CD and ADHD.
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Beauchaine, Katkin, Strassberg, and Snarr, (2001) found low SC in adolescents with ADHD and those with comorbid CD, as did Crowell et al., (2006) in preschoolers. Jointly, findings suggest that resting hypo-arousal may be a common rather than a distinct mechanism of a specific disorder. Van Goozen et al., (2000) showed that children with
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disruptive disorders and comorbid ADHD had even lower SC than the other groups, signifying that comorbidity or severity may also modulate levels of resting arousal. Low autonomic reactivity has also been found, albeit inconsistently, in ODD/CD.
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Lorber, (2004) showed lower SC in response to non-aversive stimuli (tones or neutral slides) in children, but not adolescents with conduct problems, compared to controls.
Lower SC to negative stimuli was not systematically observed, in contrast to what is seen in adults with psychopathic traits (Blair & Mitchell, 2009; Patrick & Lang,
1999). Herpertz and colleagues (2005) found lower SC across positive, negative and
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neutral stimuli in children with ODD/CD and ADHD, but not those with ADHD only or
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controls. In other studies by the same group, boys with CD and ADHD had lower SC to
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orienting and aversive stimuli compared to those with ADHD only (Herpertz et al., 2003,
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2001). Recently, however, McQuade and Breaux, (2017) found that neither ODD or ADHD were related to SC reactivity to social and cognitive stressors. Thus, low SC
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reactivity is potentially linked more to ODD/CD than ADHD and may not be modulated
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by stimulus valence, but findings are not consistent across all relevant studies. Low HR
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reactivity in ODD/CD or ADHD has not been supported (de Wied, van Boxtel, Zaalberg, Goudena, & Matthys, 2006; Lorber, 2004), though de Wied, Boxtel, Posthumus,
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Goudena, and Matthys, (2009) noted less HR deceleration to sadness in ODD/CD (some cases with ADHD), which they explained as low empathy. Indirect support for
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hyporeactivity in children with ADHD comes from their relative insensitivity to punishment and reward (Crone et al., 2003; Iaboni, Douglas, & Ditto, 1997; Luman, Oosterlaan, & Sergeant, 2005; Masunami, Okazaki, & Maekawa, 2009; Meel, et al., 2011), but relevant physiological data are lacking.
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Dysfunction of positive and negative valence systems. Studies using facial EMG at the corrugator and zygomaticus muscles during emotional stimulation in children with ODD, CD or ADHD have yielded mixed results. Regarding the negative valence
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system, boys with ODD/CD showed smaller corrugator responses during sadness and anger films and angry faces than controls (de Wied et al., 2006, 2009). Contradictory evidence exists for 6-7 year-olds with ODD, CD and ADHD, who showed expected
corrugator response elevations to angry and sad faces (Deschamps, Munsters, Kenemans, Schutter, & Matthys, 2014). Regarding positive valence, the few existing studies found
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no significant zygomaticus response differences between children with ODD/CD or those
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with ADHD and controls during "happy" films or faces (de Wied et al., 2009, 2006;
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Deschamps, Coppes, Kenemans, Schutter, & Matthys, 2010; Deschamps et al., 2014).
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Together, extant physiological evidence reliably indicates resting state hypoarousal, especially in HR, in children with externalizing symptoms. It is less clear
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whether this is common across ADHD, CD and ODD. Lower SC emotional reactivity
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seems to be found, though inconsistently, in ODD and CD, but not ADHD, across
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valences. Findings indicate dysfunction of the arousal system, but additional research is needed to specify if it is common across disorders, its specificity to negative emotions,
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and to HR vs. SC, which may be theoretically relevant, because of their differential sympathetic and parasympathetic influences (Bradley et al., 2001; Hagemann, Waldstein,
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& Thayer, 2003). There is less support for a positive valence dysfunction in ODD/CD, though in ADHD there is a separate line of non-physiological evidence speaking for insensitivity of both reward and punishment systems and emotional lability.
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The moderating role of callous unemotional traits and anxiety. Although the emotional dysfunctions in ODD/CD and ADHD need to be better specified, there is some evidence that these may be driven by comorbid characteristics, such as Callous
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Unemotional (CU) Traits and anxiety (de Wied, van Boxtel, Matthys, & Meeus, 2012). Similar to the fearlessness hypothesis, Loney, Frick, Clements, Ellis, and Kerlin, (2003) argued that youth with disruptive symptoms characterized by high CU traits may show
low distress proneness. CU traits have been linked to decreased corrugator responses to negative films (Fanti, Kyranides, & Panayiotou, 2017) and less differentiation between
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positive and negative films in prefrontal cortex oxygenation compared to controls (Fanti,
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Panayiotou, Lombardo, & Kyranides, 2016). Also, children high in CU traits and CD had
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smaller fear potentiated startle responses to negative mental imagery (Fanti, Panayiotou,
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Lazarou, et al., 2016) and fear videos (Anastassiou-Hadjicharalambous & Warden, 2008) compared to children with CD low in CU and controls. Male adolescents with ODD or
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CD (most with comorbid ADHD), high in CU also showed less facial and HR reactivity
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during sadness than controls and those low in CU (de Wied et al., 2012). Male
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adolescents with disruptive behavior and low CU traits exhibited less zygomatic activity in response to joyful stimuli relative to controls, (de Wied et al., 2012), while participants
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with CD and high CU traits showed increased zygomaticus activity (interpreted as amusement) during anger films compared to those low in CU. Given that HR is affected
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by valence in addition to arousal (Cacioppo et al., 2000), such facial EMG and HR findings may suggest a valence deficit in CU. Musser, Galloway-Long, Frick, and Nigg, (2013) proposed that subtypes may exist in ADHD as well, based on the presence of CU
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traits, showing opposite patterns of autonomic responses. In sum, CU traits may moderate effects of ODD/CD and ADHD on physiological responses (Frick et al., 1999). Similarly, anxiety may represent another moderator. Youth with externalizing
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symptoms without CU traits but high anxiety may form a different subgroup, showing higher sensitivity to punishment and distress proneness, and normal or over-reactive
arousal and negative valence systems (Fanti, Kyranides, Lordos, Colins, & Andershed, 2018; Fanti et al., 2017; Loney et al., 2003; Nigg et al., 2004). de Wied et al., (2006),
showed that children with disruptive symptoms had higher HR during a relaxing film
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than controls, which they attributed to anxiety, given that these children were rated as
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more anxious than controls. Similarly, children with ODD or CD (some with comorbid
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ADHD) and anxiety had higher resting HR than controls (de Wied et al., 2009). Thus,
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comorbid anxiety may lead to patterns opposite to what fearlessness and hypo-arousal theories would predict. It appears, that examining the moderating role of CU traits and
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Current Study:
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anxiety can help specify any shared emotional dysfunctions across ODD/CD and ADHD.
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This study adopts a dimensional approach to describe how patterns of arousal and/or valence system responses are associated with ADHD and/or ODD/CD. The
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moderating role of CU and anxiety in these associations is also evaluated. To address these questions we assessed facial EMG, to index valence, and HR and SC, to index
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primarily arousal, during viewing of affective pictures (the latter two measures also at rest). The sample included children with clinical, subclinical or no symptoms of ADHD, and ODD/CD. Because of the mixed evidence as to whether emotional dysfunctions are similar across disruptive disorders and ADHD, we posed alternative hypotheses that
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dysfunctions would be associated with either one or both symptom types. We predicted that (1) lower resting SC and HR, and reactivity during negative stimuli, especially fear, would be associated with increased symptoms of ODD/CD and/or ADHD (Lorber, 2004;
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Ortiz & Raine, 2004; Portnoy & Farrington, 2015; Van Bokhoven et al., 2005; Van Goozen et al., 2000). Based also on the fearlessness hypothesis, (2) lower corrugator responses to unpleasant stimuli would be associated with ODD/CD and/or ADHD
symptoms. (3) for zygomaticus, as past literature has not reliably observed dysfunctions of the positive valence system using this measure (de Wied et al., 2009, 2006), despite
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suggestions for a hyper- vs hypo-reactive positive valence system (de Wied et al., 2012),
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we did not posit specific hypotheses. Based on evidence that CU and other psychopathic
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traits, are associated with fearlessness and hypo-arousal, (4) we expected CU to moderate
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the effects pertaining to hypotheses 1 and 2, so that decreased tonic arousal, autonomic and corrugator reactivity would mostly be associated with ODD/CD symptoms and/or
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ADHD at high but not at low levels of CU traits (Anastassiou-Hadjicharalambous &
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Warden, 2008; de Wied et al., 2012; Loney et al., 2003). Similarly, in line with the
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fearlessness hypothesis, anxiety would moderate effects, so that ODD/CD and ADHD would be associated with typical, or hyper HR, SC and corrugator reactivity (i.e. emotion
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dysregulation) at high but not low anxiety levels (de Wied et al., 2009, 2006). Method
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Participants Participants were 87 Greek-Cypriot children (42 female, Mage=11.2 years,
range=10.1-12.8), from elementary schools located in urban and suburban areas of the Nicosia district in Cyprus. Schools (N=18) were randomly selected from 125 elementary
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schools in the district, using Ministry of Education and Culture’s records; 17 schools agreed to participate (one did not for scheduling reasons). Parents or guardians (N=1565 families) of all children in grades 5 and 6 were sent a consent form, the study description
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and the Child Behavior Checklist (CBCL; Roussos et al., 1999), to complete at home. Children whose parents gave informed consent (N=87) and themselves provided assent were invited to participate. All families were Caucasian of Greek-Cypriot ethnicity. Of parents who responded (74.4% mothers), 34.5% had high school education or lower,
44.4%, university or college, 11.1% graduate degree. Most, 78.8%, rated their financial
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status as “good,” 13.8% as “very good”, and 7.5 % as “bad” or “very bad”.
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The Wechsler Abbreviated Scale of Intelligence (WASI; Wechsler, 1999) was
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administered to rule out mental retardation. The Mini International Neuropsychiatric
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Interview for Children and Adolescents (MINI-KID; Sheehan et al., 2010) assessed for ODD/CD, ADHD and other mental health problems. Raw intelligence scores on the
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WASI were in the normal range of 2 SD below or above the mean of children of the same
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age based on local normative data. The CBCL, completed by a parent/guardian and a
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brief teacher checklist, provided corroborative evidence for externalizing and anxiety symptoms. All 87 children were included as no-one had any sensory, psychotic or
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pervasive developmental problems, and none were taking psychotropic medications. Although we follow a dimensional approach in this study by using continuous
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CBCL measures of ADHD and ODD/CD symptoms as our dependent variables, to ensure that all levels of severity were included in the sample, children underwent a clinical diagnostic procedure to assess presence of one or more of these disorders. Diagnosis was based on both child reports on the MINI-KID and parent reports on the CBCL. Twenty
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four children (5 female) met criteria for comorbid ADHD-ODD/CD - no children were identified with ADHD diagnosis only. Fifteen (5 female), met criteria for ODD/CD and 48 (32 female) met no diagnosis and were included as Controls. In eight cases of
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disagreement between parent and child reports, where children reported subclinical or no symptoms on the MINI-KID, diagnosis was aided by the teacher’s checklist, on which reported behavioral problems at school corroborated the parent’s report on the CBCL.
Control children had CBCL symptoms between zero and just below the clinical cutoffs, to ensure a continuum of severity. Of 87 invited children, 81 participated in the
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experiment mostly due to scheduling difficulties. All blocks of the experiment were
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completed by 75 children, with the rest quitting due to boredom or other scheduled
Experimental Procedures
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zygomaticus analyses 62 participants.
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activities. Due to technical problems or noise, SC analyses included 69, corrugator 59 and
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The study was approved by the Ministry of Education and Culture and the
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National Bioethics Committee. Diagnostic assessment took place at school. The
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experiment took place at the university labs and included the present task and additional ones not relevant to this study. Participants took part in a passive picture viewing
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paradigm involving four presentations of each type of emotional picture, based on similar studies with undergraduates and children (Bernat et al., 2006; Sharp, Goozen, &
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Goodyer, 2006). Upon arrival to the lab, children were seated in a reclining chair in a sound-attenuated room and standard surface electrodes were attached. Following seven minutes of relaxation and a series of cognitive tasks irrelevant to this study, instructions were given for the experiment. Children were instructed to look at a series of pictures
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presented on a 45-inch TV monitor for six sec each, in one of three pseudorandom orders, with inter-trial intervals (ITIs) of 7, 12 or 18 sec. After the viewing task, sensors were detached and children viewed the pictures again to rate their subjective responses on
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valence and arousal, using 1-5 scales in a paper-and-pencil modification of the SelfAssessment Manikin (SAM; Lang, Bradley, & Cuthbert, 2005). After the experiment, (about 30 minutes), children were debriefed and received a toy and 15 euros. Materials
Pictures from the International Affective Picture System (IAPS; Lang et al., 2005)
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were selected, four of each, neutral (e.g., household objects), joy (e.g., birthday cake),
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fear (e.g., shark) and sad (e.g., crying boys)1, based on local normative valence and
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arousal ratings by a separate sample of 101 children and adolescents randomly selected
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from grades five to eight. Joy pictures were positive in valence (M=7.18) and high in arousal (M=5.26), sad pictures low in positive valence (M=1.89) and low in arousal
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(M=3.15), fear pictures low in positive valence (M=3.46) and high in arousal (M=6.65).
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Neutral pictures were medium in valence (M=5.42) and low in arousal (M=3.17).
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Apparatus and Response Measurement We obtained mean resting HR and SC from the last five minutes of initial
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relaxation. HR, SC, zygomaticus and corrugator reactivity was averaged for each picture duration and over same type pictures. One percent of observations on both ends for all
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physiological measures were removed as outlier values. Physiological data, sampled at 1000Hz, were recorded with BIOPAC MP150 for Windows and Acknowledge 3.9.0 software (BIOPAC Systems, Inc., Goleta, CA, USA). Stimulus presentation was achieved
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IAPS pictures used (Lang et al., 2005): 1302, 1427, 1930, 2312, 2345, 2703, 2900.1, 3300, 5480, 6821, 7004, 7009, 7010, 7020, 7250 and 7330.
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using E-prime 1.0 (Schneider, Eschman, & Zuccolotto, 2002). Electrodermal activity was recorded continuously on the forefinger of the participant’s non-dominant hand using a BIOPAC GSR100C amplifier and transducer (TSD203) in microsiemens (μS), with a
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high-pass filter set at 0.05 μS. Lead I EKG was recorded in beats per minute (BPM) using two Ag/AgC1 disposable electrodes placed on each forearm, filtered by a BIOPAC ECG100C bioamplifier. For facial EMG, 4-mm electrodes were placed at the right
zygomaticus and corrugator (Fridlund & Cacioppo, 1986). The signal was amplified, filtered (band pass, 20Hz high frequency, 500Hz low frequency) and rectified.
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Measures
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Intelligence. The Wechsler Abbreviated Scale of Intelligence (WASI; Wechsler,
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1999) was used to assess the children's verbal, non-verbal and general cognitive ability. It
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consists of four subtests, Vocabulary and Similarities, which form the Verbal Scale, and Block Design and Matrix Reasoning, which form the Performance Scale. For this study,
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only Vocabulary and Block Design of the Greek-Cypriot WASI (Spanoudis & Tourva,
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2012) were administered to estimate verbal and non-verbal ability, respectively.
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Psychopathology. Parents completed the 113 item Child Behavior Checklist, rated on a 3-point scale, (0=not true, 1=somewhat true, 2=very true/very often true), to
CC
assess their child’s symptoms. The original and Greek version have well-established psychometric properties (Achenbach & Rescorla, 2001; Roussou, 2003). DSM-adjusted
A
scales for ADHD, ODD, CD and Anxiety had reliabilities of .84, .83, .87 and .68. The Greek MINI-KID (Sheehan et al., 2010), a short, structured diagnostic
interview for DSM-IV and ICD-10 psychiatric disorders of children and adolescents was
17
administered to participants by trained psychology graduate students. It assesses for 30 disorders and generates valid and reliable diagnoses (Sheehan et al., 2010). Teachers completed a short checklist on behavior problems at school, for each
SC RI PT
participating child in their class (Cronbach’s α=.74). They reported with a yes or no the presence of any of these four types of problems: 1) inattention/hyperactivity/impulsivity, 2) oppositionality/arguing/refusal to comply with rules, 3) threatening/ bullying/physical violence, or 4) anxiety problems. The checklist was used as auxiliary information to
resolve diagnostic discrepancies between parent (CBCL) and child (MINI- KID) reports.
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Traits. The 24-item Inventory of Callous-Unemotional traits (ICU) was
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completed by children. It consists of 12 positively and 12 negatively worded items,
A
measuring CU traits in youth (Frick, 2004), rated on a 4-point Likert scale from 0 (not at
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all true) to 4 (definitely true). The test measures one general dimension of CU traits and three sub-dimensions, callousness (lack of empathy, guilt and remorse), uncaring (lack of
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caring about one’s performance and the feelings of others) and unemotional (absence of
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emotional expressions; Essau, Sasagawa, & Frick, 2006; Kimonis et al., 2008; Lazarou,
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2013). For this study, a reliability analysis showed that items 1 and 10 had low corrected item-total correlations. After removing these items, full scale reliability was α=.75.
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Data Reduction and Analysis Hypotheses were tested using mixed model analyses (SAS Proc Mixed v9.4; SAS
A
Institute Inc., Cary, NC, USA) for repeated measures (i.e., multiple trials) of the dependent variables (HR and SC during rest, HR, SC, corrugator and zygomatic reactivity, and ratings). All models included subject as a random effect. Predictors in all cases were ADHD, or ODD/CD CBCL symptoms. These models were then each repeated
18
two more times, to test separately the effects of potential moderators (CU traits and anxiety). Either anxiety or CU-traits (one at a time) were added to the model, both as main effects and in interaction with ADHD, or CD/ODD symptoms. Models were
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additionally repeated while controlling for the other symptom group (i.e. covarying ADHD when analyzing for ODD/CD and ODD/CD when analyzing for ADHD), to
account for the high comorbidity and examine unique effects of each symptom type. To rule out effects of gender, this dichotomous variable was included in additional
exploratory models. Post hoc differences between means following a significant mixed
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model effect were the result of contrast comparisons of least-square means (LSM) and
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standard errors (SE) of fixed effects using tests of simple effects. The family-wise α
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levels of post hoc contrasts were adjusted using the Holm-Bonferroni correction (Holm,
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1979) for the effects of multiple comparisons on type I error rate. For interactions between continuous and categorical variables, slopes were calculated for average change
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over the continuous variable, and reported as point estimates (PE) and standard errors
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(SE). Point estimates are analogous to a regression beta statistic in that the slopes indicate
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change on a dependent measure for every 1-unit increase in the predictor. All continuous predictors (ADHD, ODD/CD and anxiety CBCL scores, CU-traits) were mean centered.
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Effect sizes are reported as Cohen’ d (.2 small, .5 medium, >.8 large effect size). Linear mixed model analysis allows for estimates of the correlation structure of the residuals and
A
efficiently handles unbalanced designs and missing data, without excluding participants or imputing values (Bagiella et al. 2000). Results Correlations Between Indices of Symptomatology
19
Correlations were computed among the scales of interest on the CBCL, teachers’ checklist and scores on the ICU. Pearson correlations among CBCL scales were: anxiety with ADHD, ODD and CD, r=.53, .58, and .56 respectively. ADHD with ODD, r=.70,
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and CD, r=.68; ODD with CD, r=.74, all significant at p<0.01. Pearson correlations between CU traits and ADHD, ODD and CD symptoms, on the CBCL, were all
significant at p< 0.01; r=.35, .51, and .43 respectively. Point biserial correlations between CU traits and teacher ratings of ADHD, ODD, and CD (present/absent) on the teachers’ checklist, were also all significant, rpb= .47, .49, and .52 respectively. The correlations
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between CU traits and anxiety were not significant, either for the CBCL r=.20, p=.68 or
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teachers’ checklist rpb=.05, p=.67. Using Fisher’s exact ratio (Field, 2013) significant
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associations were found between teachers’ ratings for ADHD, ODD and CD
M
(presence/absence) and parents’ ratings for ADHD, ODD and CD symptoms on the CBCL (categorized as normal, borderline or clinical range), p=.009, p=.004, and
D
p=.001 respectively. However, teachers’ ratings of anxiety problems were not
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significantly associated with parents’ reports of anxiety on the CBCL, p=.57.
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Post-trial Picture Ratings
There was a main effect of picture type on valence ratings, F(3, 281)=301.95,
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p<.0001, with post hoc pairwise comparisons indicating that sad (LSM=0.53, SE=.08), fear (LSM=1.69, SE=.08), neutral (LSM=2.52, SE=.08), and joy (LSM=3.72, SE=.08)
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pictures all differed from one another. There was also a main effect of picture type on arousal ratings, F(3, 281)=29.67, p<.0001, with post hoc comparisons showing that joy (LSM=2.77 SE=.13), fear (LSM=2.39, SE=.13), sad (LSM=1.75, SE=.13) and neutral (LSM=1.09, SE=.13) pictures all differed from one another. Results indicate that emotion
20
was effectively induced. There were no significant effects of ADHD (p=.92) or interactions with CU or anxiety on valence (p=.39, p=.30 respectively) and arousal (p=.07, p=.65 respectively), and no significant effects of ODD/CD (p=.34) or interactions
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with CU or anxiety on valence (p=.61, p=.28 respectively) and arousal (p=.28, p=.20). Association Between ADHD and ODD/CD Symptoms and Resting HR and SC
ADHD symptoms were negatively associated (PE=-1.15, SE=0.50) with resting HR, F(1, 68)=5.41, p=0.023, Cohen’s d=0.40. Interactions with CU traits and anxiety
were non-significant (p=.44 and .50), showing no moderation by either trait. When the
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analysis was repeated with ODD/CD symptoms as covariate, the main effect of ADHD
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on resting HR dropped in significance to marginal, p=.07782. In the main analysis, main
A
effects of ODD/CD and interactions with CU and anxiety (p=.16, .55 and .56
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respectively) were not significant. ADHD had no significant main effect or interaction with CU traits and anxiety on resting SC (p=.14, .62 and .39). Main and interactive
D
effects of ODD/CD with CU traits and anxiety were also non-significant (p=.51, .80, .32
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respectively). The main effect of gender on HR reactivity was significant, (PE=-6.18,
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SE=2.94) F(1, 67)=4.42, p=0.039, Cohen’s d=0.36). with boys with ODD/CD having lower HR across picture types than girls3.
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Association Between ADHD and ODD/CD and HR Reactivity to Pictures There was no effect of picture type (p=.15) on HR reactivity to pictures (Table 1).
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The main effect of ADHD also did not reach significance (PE=-0.89, SE=0.50, F(1, 68)=3.18, p=.08), but this trend, irrespective of picture content, showed that HR tended to decrease as ADHD symptoms increased. There was a significant ADHD x Picture Type 2
Effects of the alternative symptom category entered as covariate did not change for all other dependent measures. These non-significant findings are not reported for the sake of brevity but are presented in Supplementary Table 1. 3 The effects of gender were non-significant in all other models and are not reported for the sake of brevity.
21
interaction, F(3, 1018)=4.56, p=0.0035 (Figure 1), which showed that, although at low and medium levels of ADHD HR reactivity did not differ significantly between picture types, at high levels of ADHD (+1SD), there was significantly lower reactivity for fear
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compared to joy (PE=-2.20, SE=0.58, t[212]=-3.82, p=.0002, Cohen’s d=0.37), and compared to neutral (PE=-1.30, SE=0.58, t[212]=-2.25, p=.025, Cohen’s d=0.22), but not compared to sadness (p=.18). Also at high levels of ADHD, HR reactivity for sadness
was lower compared to joy (PE=-1.43, SE=0.57, t[212]=-2.50, p=.013, Cohen’s d=0.24). There was no significant effect of ODD/CD (p=.32) on HR reactivity during
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picture viewing (Table 2). There was again a significant ODD/CD x Picture Type effect
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on HR reactivity, F(3, 1018)=3.33, p=0.0189 (Figure 2), indicating that, when ODD/CD
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was high, there was more decreased HR to fear compared to joy (PE=-1.38, SE=0.46,
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t[212]=-2.98, p=.0032, Cohen’s d=0.29), but not compared to sad (p=.47) or neutral pictures (p=.06). Also, at high levels of ODD/CD, HR reactivity to sadness was lower
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compared to joy (PE=-1.04, SE=0.46, t[212]=-2.26, p=.024, Cohen’s d=0.22). Neither
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ADHD nor ODD/CD effects on HR were moderated by CU traits (p=.67 and p=.49
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respectively) or anxiety (p=.56 and p=.74), as none of the interactions were significant. Association Between ADHD and ODD/CD and SC Reactivity to Pictures
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There were no significant effects of picture type (p=.70), ODD/CD (p=.26) or their interactions with CU traits (p=.98) or anxiety (p=.80). ADHD was associated with
A
lower SC (PE=-0.59, SE=0.22) response to pictures, F(1, 68)=7.35, p=0.0085, Cohen’s d=0.46. This association was not moderated by anxiety (p=.79) or CU traits (p=.71). Association Between ADHD and ODD/CD and Corrugator Reactivity to Pictures
22
There was a main effect of picture type on corrugator reactivity, F(3, 183)=5.30, p=0.0016 with post hoc comparisons indicating that joy pictures had smaller corrugator responses compared to fear (PE=0.67, SE=0.28, t[183]=2.37, p=0.019, Cohen´s d=0.25),
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sad (PE=1.07, SE=0.28, t[183]=3.83, p=0.0002, Cohen´s d=0.40), and neutral pictures (PE=0.80, SE=0.28, t[183]=2.85, p=0.005, Cohen´s d=0.30). There were no main effects of ADHD or ODD/CD (p=.22; p=.20) or interactions with CU and anxiety (p=.17, p=.37 respectively for ADHD and p=.24, p=.26 for ODD/CD).
Association Between ADHD and ODD/CD and Zygomaticus Reactivity to Pictures
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There were non-significant effects of picture type, p=.20 on zygomaticus
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reactivity, but marginal effects of ADHD and ODD/CD symptoms (PE=0.37, SE=0.2,
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F(1, 61)=3.37, p=.07 and PE=0.27, SE=0.14, F(1, 61)= 3.56, p=.06 respectively),
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showing a trend for higher zygomaticus reactivity across picture types as symptoms increased. There was no moderation by anxiety or CU traits (p=.14, p=.42 respectively
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Discussion
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for ADHD; p=.15, p=.23 for ODD/CD).
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In accordance with the RDoC, we examined the arousal and positive and negative valence system responses associated with ADHD and ODD/CD symptoms, searching for
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emotional mechanisms across these diagnostic categories that may explain their comorbidity, phenotypic similarities and shared developmental pathway (Casey et al.,
A
2014; Kronenberger & Meyer, 2001; Nigg, 2001). Decreased resting HR was associated with ADHD, while decreased HR reactivity to fearful and sad stimuli was associated with both ADHD and ODD/CD. Lower SC reactivity, irrespective of picture type viewed was associated with ADHD but not ODD/CD, indicative of a tonic than a reactivity effect. No
23
apparent valence deficits were found, as measured by EMG (though the decreased autonomic reactivity to fear and sad, but not joy pictures suggests that arousal deficits are specific to negative emotions), and no association between any of the symptoms and self-
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reported emotion. Findings are collectively consistent with the fearlessness theory of disruptive behavior (with effect sizes being somewhat larger for decreased fear than
decreased sadness in association with both ADHD and ODD/CD), an interpretation that
seems to apply across symptom types. The study contributes to understanding emotional
mechanisms in the disruptive disorders and ADHD, examining symptoms on a continuum
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of severity, with a balanced design of high/low arousal and positive/negative stimuli and
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multi-method assessment of arousal and valence using both physiology and self-report.
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ADHD symptoms were negatively associated with resting HR, consistent with
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similar findings for children with disruptive disorders. Contrary to some of this evidence (Hill, 2002; Ortiz & Raine, 2004; Portnoy & Farrington, 2015; Van Bokhoven et al.,
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2005; Van Goozen et al., 2000), this finding occurred for ADHD and not for ODD/CD
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only, and was not moderated by CU traits (de Wied et al., 2012; Musser et al., 2013).
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However, when ODD/CD was covaried, the effect of ADHD dropped in significance suggesting that disruptive disorder symptoms also contribute some variance. Given this
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finding, the fact that our sample with ADHD also had comorbid ODD/CD, and the fact that we had a significant number of cases who met formal diagnostic criteria, our findings
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may suggest that resting hypo-arousal may be moderated by comorbidity or severity; findings parallel those of others who found hypo-arousal in children with comorbid ADHD and CD or ODD (Herpertz et al., 2005; Van Goozen et al., 2000). It is possible that in samples with conduct problems not meeting diagnosis, CU traits carry the effect of
24
hyporeactivity by indexing more extreme antisocial traits. In samples with clinical levels of symptoms (in this case ADHD with comorbid ODD/CD), CU traits may not contribute significant additional variance, a tentative hypothesis for future empirical testing.
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No significant associations were found between ADHD or ODD/CD symptoms and baseline SC, indicating that resting hypoarousal may be more apparent in HR (as shown by past reviews, e.g. Ortiz & Raine, 2004). In accord with the fearlessness hypothesis, children with ADHD, especially those with high comorbid disruptive
symptoms, may maintain high parasympathetic control of their arousal, seen as decreased
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tonic HR (Ortiz & Raine, 2004; Portnoy & Farrington, 2015), when in the mildly
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stressful conditions of the lab. Precisely because HR is sensitive to valence in addition to
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arousal (Cacioppo et al., 2000), this measure may have captured better a lack of distress
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by children with these characteristics during the initial period upon arrival to the unfamiliar environment of the lab, and throughout the experiment (seen in tonically lower
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SC), consistent with a fearlessness account. The absence of effects in support of positive
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valence system deficits, indicates more circumscribed hypoarousal, consistent with lack
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of distress (i.e. fearlessness) rather than broad hypoarousal, irrespective of context. With regards to reactivity, higher ODD/CD and ADHD symptoms were both
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linked to lower HR during fear compared to joy, the most appropriate contrast, since joy is also a high arousal emotion but of positive valence. Hyporeactivity to fear, rather than
A
across high arousal (i.e. joy) emotions, and with larger effect sizes for fear than sadness, is more consistent with fearlessness and a defensive system deficit, as proposed before (Anastassiou-Hadjicharalambous & Warden, 2008; Frick et al., 1999; Loney et al., 2003). HR hyporeactivity to fear was associated in separate models with both ODD/CD and
25
ADHD indicating that fearlessness is a common mechanism. As reactivity was also lower to sad compared to joy pictures as either symptom type increased, a narrow fearlessness account may need to be modified: Children with symptoms across ODD/CD and ADHD
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may have a broader deficit in experiencing distress rather than fear only. Our findings do not support a specific empathy impairment, considered as a risk factor for antisocial behavior (de Wied et al., 2009). Although HR was lower as both symptom types increased in sadness compared to joy (an expected effect given our
selection of joy and sad stimuli to differ in arousal), a stronger effect was found for the
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fear-joy contrast. Differences in findings from de Wied et al. (2009) may be a function of
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the specific stimuli used. Pictures in the current study may have been emotionally
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provoking for all participants as they depicted children of their age feeling pain or crying.
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More importantly, sadness stimuli were selected to be low in arousal and high in negative valence. The sad films in de Wied et al. (2009), may have been highly arousing, tapping
D
into the hyporeactivity to distressing stimuli we observed. Collectively, our physiological
TE
findings indicate tonic autonomic hypoarousal related to ADHD and hyporeactivity for
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both types of symptoms to distressing situations. Given that our ADHD sample was more comorbid, it may be that circumscribed fearlessness in disruptive disorders generalizes,
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even to mildly distressing contexts (the experiment) as comorbidity increases. Importantly, physiological reactivity effects of ADHD and ODD/CD were not
A
paralleled by decreased subjective ratings of arousal or negative valence, although we had found such effects in prior studies of externalizing symptoms (Panayiotou, Fanti, & Lazarou, 2015; Panayiotou et al., 2015). It is unclear what led to this difference from our own past studies (although it should also be noted that in the previous studies it was
26
primarily CU traits that accounted for self-report effects), which mostly differed in the somewhat younger age of the present sample. One possibility is that children at this age have not yet learned to accurately report on their experiences, which eliminated any
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influence of externalizing symptoms due to floor effects. It is also possible that learning to accurately report on experiences depends on interoceptive feedback (Herbert, Herbert, & Pollatos, 2011), so that over development children with ADHD and/or ODD/CD
progressively fall behind their typical cohorts’ ability to verbally express emotions, due to lack of intense physiological reactions, and indications of lower verbal ability (e.g.
U
Frazier, Demaree, & Youngstrom, 2004; Hill, 2002) in these disorders. An alternative
N
hypothesis, which though fails to explain the past discrepant results, is that the emotional
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difficulties of these children are specific to physiology, because contextual cues (e.g.
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questions, rating scales) can guide their self-report. These tentative hypotheses can only be addressed by more and longitudinal research, but they are consistent with evidence
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that children with CD have good theory of mind abilities (Gillespie, Kongerslev, Sharp,
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& Abu-Akel, 2018), which may aid them in socially appropriate self-report.
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ADHD and ODD/CD symptoms were unrelated to corrugator reactivity. This suggest that children with various levels of these symptoms show typical negative
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valence system function (Deschamps et al., 2014; McManis et al., 2001), in contrast to some past studies which had implicated a valence deficit in disruptive disorders or
A
ADHD (de Wied et al., 2009, 2006). Divergence from past findings may pertain to the balanced stimuli and measures that disentangle valence from arousal effects in our study. With regards to positive valence, our findings are consistent with a normally functioning system (de Wied et al., 2006; Deschamps et al., 2014), strengthening the
27
argument that valence systems are not generally implicated in ADHD and ODD/CD dysfunctions. In the present study ADHD and ODD/CD were not significantly associated with abnormal zygomaticus reactivity to joy. However, we did observe an increase in
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zygomaticus reactivity, approaching significance, across valences associated with both ADHD and ODD/CD. In the unfamiliar environment of a psychophysiological
experiment, the expected affective response might have been of mild displeasure rather
than of positive affect. The fact that both types of symptoms were associated with higher zygomaticus activity across the experiment may be consistent with a general lack of
U
distress (including decreased anxiety and stress; e.g. Fanti & Kimonis, 2017), rather than
N
augmented positive valence, associated with ADHD and ODD/CD. These interpretations
A
are tentative, and should be seen with caution, due to the marginal nature of these effects.
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A novel aspect of this study was our attempt to examine if arousal or valence deficits are moderated by CU and anxiety traits. Previous studies had found patterns of
D
hyporeactivity and fearlessness associated with CU (Anastassiou-Hadjicharalambous &
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Warden, 2008; de Wied et al., 2012; Loney et al., 2003), and high emotional reactivity
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associated with anxiety, suggesting that these traits may contribute to heterogeneity in both disruptive disorders (Fanti & Kimonis, 2017) and ADHD (Musser et al., 2013).
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However, our findings do not support such moderation. Instead they suggest that underarousal in distressing contexts is a function of primary characteristics of these symptoms
A
and not accounted for by comorbid traits. Potentially, divergence from previous findings may have to do with the inclusion of formally diagnosed children, many with comorbid ADHD, ODD/CD in the current study. Alternatively, as we based assessment of socially
28
undesirable CU traits, on children’s self-reports, they may have under-reported them given the good theory of mind suggested to characterize CD (Gillespie et al., 2018). Some limitations of this study could influence the interpretation of findings. First,
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we had a small sample size because, even though a large number of students and parents were informed about the study, only a few families agreed to participate. This can be
partly attributed to the time commitment and paperwork (complicated consent forms)
required for both phases of the study and concern that children might be stigmatized for having externalizing disorders. However, taking into consideration the prevalence of
U
these disorders in the population and the statistical power of similar studies, the number
N
of participants may be less of a concern (e.g. de Wied et al., 2006; McQuade & Breaux,
A
2017), though it is strongly desirable to replicate our findings with larger samples to
M
ensure adequate power to detect small effects. A second limitation has to do with the fact that children meeting ADHD only criteria appeared negligible in our 10-12 aged sample,
D
whereas a substantial number of children had comorbid ADHD and ODD/CD. Although,
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disruptive symptoms were treated as continuous, the absence of children with only
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ADHD makes the interpretation of results more difficult. Future research could select for larger numbers of participants with “pure” category symptoms, perhaps by targeting
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younger ages where comorbidity is expectedly lower (given the developmental progression of these disorders), in order to reach safer conclusions. Ideally, gender should
A
also be balanced between the clinical and control participants, something we aimed for but were unable to do based on the sample who consented to participate. This aim presents a challenge given the much higher prevalence of externalizing disorders in males (APA, 2013a). Examination of the effect of gender in our study revealed only one
29
significant effect; ODD/CD boys had lower HR reactivity than girls, suggesting that using a gender balanced design in the future may reveal interpretable effects on some measures. Also, the experimental stimuli could have included more pictures for each
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valence/arousal category, to strengthen obtained effects. However, our number of pictures was similar to others (e.g. Bernat et al., 2006; Sharp et al., 2006), and several of our effects were strong, suggesting that the presented stimuli adequately induced
emotion. Finally, future studies could benefit from the inclusion of more specific
measures of sympathetic and parasympathetic influences, in order to specify these
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deficits further, such as respiratory sinus arrhythmia (RSA) and cardiac pre-ejection
N
period (PEP; Beauchaine et al., 2013; Karalunas et al., 2018; Musser et al., 2013).
A
In sum, our findings suggest that the dysfunctions associated with disruptive
M
symptoms of ADHD and ODD/CD are mostly common rather than distinct and are consistent with fearlessness and decreased distress at both resting baseline and during
D
fearful and sad contexts. This pattern may be more profound and widespread (apparent in
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both SC and HR) in children with greater comorbidity and severity of symptoms rather
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than pertaining to a specific symptoms category, and rather than being a function of the level of co-existing traits like CU and anxiety. Our findings are consistent with a trans-
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diagnostic approach to treating disruptive behaviors, taking into consideration the potential fearlessness of these children that may impair the effectiveness of using
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negative consequences, and their under-arousal that may motivate behaviors aimed at increasing stimulation. Parents, teachers and specialists should perhaps invest in positive reinforcement, taking into account their normally functioning positive valence system,
30
and in creating a positive environment rich in learning stimuli that captures these
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children’s needs for sensation seeking and emotional stimulation.
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Figure 1
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Figure 1. ADHD symptom x Picture Type interaction on HR reactivity
Note. NEU = neutral stimuli, Fear = fear stimuli, Joy = joy stimuli, Sad = sadness stimuli
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HR = Heart rate, BPM = Beats per minutes, ADHD = Attention Deficit Hyperactivity
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Disorder
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Figure 2
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Figure 2. ODD/CD symptom x Picture Type interaction on HR reactivity
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Note. NEU = neutral stimuli, Fear = fear stimuli, Joy = joy stimuli, Sad = sadness stimuli
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HR = Heart rate, BPM = Beats per minutes, ODD/CD = Oppositional Defiant
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Disorder/Conduct Disorder
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Table 1 Least Squares Means (LSM) and Standard Error (SE) of HR, SC, Corrugator and Zygomaticus responses of ADHD children during Neutral, Fear, Joy and Sadness Stimuli.
SC
Corrugator
10.01 (0.60) 10.09 (0.60) 10.02 (0.60) 10.06 (0.60)
8.06 (0.52) 7.93 (0.52) 7.26 (0.52) 8.33 (0.52)
Zygomaticus
7.61 (0.58) 7.68 (0.58) 7.68 (0.58) 7.22 (0.58)
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77.54 (1.40) Neutral 77.14 (1.40) Fear 77.83 (1.40) Joy 76.98 Sadness (1.40)
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HR
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Note. Means indicate the average of the four pictures per emotion. HR = Heart rate, SC = Skin conductance. HR reactivity is measured in beats per minutes. SC is measured in microsiemens. Corrugator and Zygomaticus reactivity are measured in microvolts.
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Table 2
HR Neutral
77.50 (1.42) 77.10 (1.42) Joy 77.79 (1.42) Sadness 76.94 (1.42) Fear
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Least Squares Means (LSM) and Standard Error (SE) of HR, SC, Corrugator and Zygomaticus responses of ODD/CD children during Neutral, Fear, Joy and Sadness Stimuli.
SC
Corrugator
Zygomaticus
10.00 (0.63) 10.09 (0.63) 10.01 (0.63) 10.05 (0.63)
8.06 (0.52) 7.92 (0.52) 7.26 (0.51) 8.33 (0.51)
7.60 (0.58) 7.67 (0.58) 7.67 (0.58) 7.21 (0.58)
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Note. Means indicate the average of the four pictures per emotion. HR = Heart rate, SC = Skin conductance. HR reactivity is measured in beats per minutes. SC is measured in microsiemens. Corrugator and Zygomaticus reactivity are measured in microvolts.
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S0301-0511(18)30383-1 https://doi.org/10.1016/j.biopsycho.2018.11.007 BIOPSY 7621
To appear in: Received date: Revised date: Accepted date:
10 May 2018 16 November 2018 19 November 2018
Please cite this article as: Souroulla AV, Panteli M, Robinson JD, Panayiotou G, Valence, arousal or both? Shared emotional deficits associated with Attention Deficit and Hyperactivity Disorder and Oppositional/Defiant-Conduct Disorder symptoms in school-aged youth, Biological Psychology (2018), https://doi.org/10.1016/j.biopsycho.2018.11.007 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Valence, arousal or both? Shared emotional deficits associated with Attention Deficit and Hyperactivity Disorder and Oppositional/Defiant-Conduct Disorder symptoms in school-
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aged youth
Running Head: VALENCE AND AROUSAL DEFICITS IN DISRUPTIVE PROBLEMS
Andry V. Souroulla¹, Maria Panteli¹, Jason D. Robinson² & Georgia Panayiotou¹
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¹University of Cyprus, Cyprus
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² The University of Texas M. D. Anderson Cancer Center, USA
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Contact: Georgia Panayiotou
Department of Psychology and Center for Applied Neuroscience
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University of Cyprus
P.O. Box 20537, 1678 Nicosia, Cyprus
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TEL: +35722892081
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Email: [email protected]
Highlights
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Valence and arousal deficits associated with ADHD and CD/ODD symptoms were studied Heart rate, skin conductance and facial EMG were assessed during emotional pictures Decreased baseline heart rate and reactivity to fear was associated with ADHD Valence systems measured with facial EMG were unassociated with any symptom type Deficits seem arousal based and may increase with comorbidity or severity
Abstract
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We examined emotional responses in Attention Deficit Hyperactivity and Oppositional Defiant/Conduct Disorder to affective pictures. Eighty seven children (42 female, Mage=11.2), with clinical or subclinical symptoms and controls viewed joy, fear, sadness
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or neutral pictures while heart rate, skin conductance, corrugator and zygomaticus responses were recorded. The moderating role of Callous-Unemotional and anxiety traits was evaluated. Lower resting heart rate and decreased skin conductance across picture
types was associated with ADHD symptoms. Decreased heart rate reactivity to fear and sad stimuli was associated with ADHD and ODD/CD. Corrugator and zygomaticus
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responses were not associated with ADHD or ODD/CD. Findings are mostly consistent
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with a fearlessness account of disruptive behavior, and seem to also pertain to ADHD,
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with intact valence systems. Findings are discussed in light of the significance of
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identifying common pathogenic mechanisms across traditional diagnostic categories,
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consistent with trans-diagnostic approaches to the study of psychopathology.
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Keywords: arousal, valence, psychophysiology, disruptive problems, children
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Valence, arousal or both? Shared emotional deficits associated with Attention Deficit and Hyperactivity Disorder and Oppositional/Defiant-Conduct Disorder
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symptoms in school-aged youth Attention Deficit Hyperactivity Disorder (ADHD), Conduct Disorder (CD) and
Oppositional Defiant Disorder (ODD) are typically diagnosed in childhood. ADHD manifests as inattention and/or hyperactivity-impulsivity that interfere with schoolwork
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and social functioning; combined and hyperactive types also involve disruptive behaviors. ODD is characterized by non-compliance, angry or irritable mood, argumentativeness or vindictiveness. CD involves violation of social norms or others’
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rights and can include bullying (Lazarou, 2013), physical fighting, cruelty to people and animals, destruction of property and other antisocial acts (DSM-5; American Psychiatric Association, 2013a). The three conditions share many phenotypic similarities, including
behavioral disinhibition, impulsivity, non-compliance, rule breaking and oppositionality. These were underscored in the 4th edition of the Diagnostic and Statistical Manual
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(DSM-IV-TR; American Psychiatric Association, 2000), which categorized them as
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“disruptive” disorders in the same taxonomy. DSM-5 classifies them separately. ODD
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and CD, due to behavioral dysregulation, are listed as Disruptive, Impulse Control and
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Conduct Disorders. ADHD is a Neurodevelopmental Disorder, based on its early onset and neuropsychological deficits (American Psychiatric Association, 2013a, 2013b).
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In spite of this change, their similarities and high comorbidity cannot be ignored:
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In 39.9% of cases, a diagnosis of ADHD co-exists with ODD and in 14.3% with CD
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(Jensen, 1999). ODD and CD were not typically diagnosed as comorbid in DSM-IV, (something allowed in DSM-5) because it was assumed that all ODD features are also
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present in CD (APA, 2013b, 2000). When symptoms of both were observed, CD was given precedence, as a more severe form of the same disorder, an assumption justified by
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CD and ODD’s shared phenotypic behavioral dysregulation, and psychosocial or hereditary risk factors (Burke, Loeber, Mutchka, & Lahey, 2002; Rowe, Maughan, Pickles, Costello, & Angold, 2002). In both DSM versions, ODD is considered a premorbid condition, which progresses to CD in some children (APA, 2013b, 2000). For
3
these reasons CD and ODD are seen as more similar between them than with ADHD, justifying their continued inclusion in the same taxonomic category. ADHD is viewed as distinct because it does not typically involve vindictiveness and deliberate rule violation.
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In this paper we treat CD and ODD as representing a common psychopathology dimension, which we call ODD/CD, as done by others (e.g. Noordermeer, Luman, & Oosterlaan, 2016). However, because of phenotypic and probably endophenotypic
similarities, all three disorders are believed to share important elements, including a
common developmental pathway, with ADHD typically appearing earlier, followed by
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ODD and CD, such that earlier disorders increase the risk for later ones (Beauchaine,
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Hinshaw, & Pang, 2010; Biederman et al., 2006; Campbell, Shaw, & Gilliom, 2000;
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Harvey, Breaux, & Lugo-Candelas, 2016; Kronenberger & Meyer, 2001).
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The similarities between ODD/CD and ADHD have instigated a search for common mechanisms (Nigg, 2001; Scheres, Oosterlaan, & Sergeant, 2001). In this study,
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we focus on emotional mechanisms that may underlie the externalizing behaviors found
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in all three disorders, hoping to contribute to enlightening their etiologies. To this end, we
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adopt a dimensional framework, as described in the Research Domain Criteria (RDoC; Cuthbert & Insel, 2013; Etkin & Cuthbert, 2014), promoted by the NIMH. The RDoC, in
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contrast to the traditional categorical framework to psychopathology used by the DSM, relies on empirically documented neurobiological dimensions and systems of behavior
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instead of the conventional, syndromal focus on symptom clusters (Casey, Oliveri, & Insel, 2014). Consistent with the RDoC, we examine emotional mechanisms, which transcend diagnostic categories and levels of severity, in ODD/CD and ADHD.
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Specifically, we study the functioning of the arousal, the positive and negative valence systems in children with symptoms of ADHD, CD and ODD, across levels of severity, including clinical, subclinical and no symptoms, measuring physiology and self-
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report. Examining both valence and arousal allows for specification of emotional deficits, as these represent two basic dimensions of affective responses (Russell & Carroll, 1999; Russell & Mehrabian, 1977). Arousal describes response intensity and valence its motivational direction of approach/avoidance (Lang, Bradley & Cuthbert, 1990).
Although the link between specific physiological indices and the valence and
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arousal dimensions is complex rather than simple and direct, some measures are more
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strongly associated with each of these systems. Skin conductance (SC), primarily affected
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by the sympathetic system, typically measures arousal (Bradley, Codispoti, Cuthbert, &
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Lang, 2001; Dawson, Schell, & Filion, 2007; Witvliet & Vrana, 1995), although depending on the situation, it may be more strongly associated with arousing positive or
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negative emotions (Bernat, Patrick, Benning, & Tellegen, 2006; Driscoll, Tranel, &
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Anderson, 2009; Gomez, von Gunten, & Danuser, 2016). Heart rate (HR) is dually
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affected by both the sympathetic and parasympathetic system, and typically indexes arousal (Azarbarzin, Ostrowski, Hanly, & Younes, 2014; Driscoll et al., 2009) but is also
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affected by the activation required by the specific situation (Kreibig, 2010) and by valence (Cacioppo, Berntson, Larsen, Poehlmann, & Ito, 2000; Witvliet & Vrana, 1995),
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especially when examining phasic changes; for example, HR deceleration is greater during negative emotions (McManis, Bradley, Berg, Cuthbert, & Lang, 2001; Tan et al., 2016). Facial expressions measured with electromyography (EMG), at the corrugator and zygomaticus muscles, index negative and positive valence respectively (Dimberg, 1988,
5
1990; Mauss & Robinson, 2009; Peasley-Miklus, Panayiotou, & Vrana, 2016), but may also be affected by stimulus intensity (Balconi, Vanutelli, & Finocchiaro, 2014). Emotional Dysfunctions Associated with Externalizing Behavior
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Most relevant theories implicate emotional dysfunctions in the etiology of CD and ODD. Although somewhat different paradigms have been used to study ADHD, this is
also known to entail emotional lability and dysregulation (Merwood et al., 2014; Rosen,
Walerius, Fogleman, & Factor, 2015; Sobanski et al., 2010; Villemonteix, Purper-Ouakil, & Romo, 2015). Based on these theories, externalizing symptoms may result from
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fearlessness, hypo-arousal or unregulated affect, or may have heterogeneous etiologies,
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involving anyone of these paths (Fowles & Dindo, 2006; Frick & Viding, 2009; Nigg,
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Goldsmith, & Sachek, 2004; Rosen et al., 2015). Although all implicate dysfunctions of
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the arousal or valence systems, each theory yields somewhat different predictions. A fearlessness account would predict decreased autonomic and defense system reactivity,
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specifically in threatening contexts. Hypo-arousal, would suggest decreased responses
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across negative affective, but also during positive situations. Emotion dysregulation
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accounts predict, instead, exaggerated responses to emotional challenges, due to response modulation problems and lability (Gomez, 2003; Newman & Lorenz, 2003).
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Based on the fearlessness hypothesis, behavioral problems entail temperamental lack of fearful inhibition and unresponsiveness to punishment (Frick, Lilienfeld, Ellis,
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Loney, & Silverthorn, 1999; Frick & Morris, 2004; Frick & Viding, 2009). Fearlessness is mainly attributed to the association between externalizing behaviors and CallousUnemotional Traits (CU) in youth and psychopathy in adults. Theories of moral socialization, suggest that fearlessness and punishment insensitivity inhibits the
6
development of morality and conscience (Fowles & Kochanska, 2000), permitting antisocial behavior to occur. Evidence for a defense system dysfunction (i.e. fearlessness) has accrued for both adults with psychopathy (Armstrong, Keller, Franklin, &
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Macmillan, 2009; Hill, 2002; Patrick & Lang, 1999) and youth with CU traits (Fung et al., 2005; Kavish et al., 2017; Latvala, et al., 2015; Lorber, 2004; Portnoy et al., 2014). Findings include low tonic HR and SC and reduced startle reflex potentiation to
threatening stimuli, jointly indicating valence and arousal dysfunctions during defensive activation (Blair & Mitchell, 2009; Patrick & Lang, 1999; Portnoy & Farrington, 2015).
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The hypo-arousal theory suggests that externalizing behavior involves decreased
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tonic autonomic arousal and emotional reactivity, which is experienced as unpleasant.
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Attempts to achieve stimulation and avoid boredom result in sensation seeking and acting
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out, as in CD or ODD (Matthys, Vanderschuren, & Schutter, 2013). In line with this, recent findings indicate that lower resting HR in adolescence predicts risk for adult
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criminality (Latvala et al., 2015). In contrast, emotion dysregulation theories suggest that
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at least a subgroup of children with disruptive behaviors show increased, instead of
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decreased reactivity to provocation (Fowles & Dindo, 2006; Nigg et al., 2004), resulting from impulsivity and disinhibition, and valence or arousal dysfunctions.
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Notably, there are fewer theoretical accounts on the role of the positive valence system in disruptive behavior. Beauchaine (2012) posited that antisocial individuals have
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an under-responsive appetitive system due to low ventral striatum activation, requiring greater stimulation to initiate approach behaviors. A meta-analysis of fMRI data suggests ventral-striatal hypo-responsiveness also in ADHD (Plichta & Scheres, 2014) consistent with neuropsychological and physiological evidence of approach system deficits (Crone,
7
Richard Jennings, & Van Der Molen, 2003; Scheres, Tontsch, Thoeny, & Kaczkurkin, 2010). Others, (Fowles & Dindo, 2009) suggest that the positive valence system in those with psychopathy and CU traits is normal or over- responsive, as, like controls, they
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show startle inhibition during pleasant stimuli (Fanti, Panayiotou, Lazarou, Michael, & Georgiou, 2016; Vaidyanathan, Hall, Patrick, & Bernat, 2011). We next review findings on arousal and valence system functioning specifically in CD, ODD and ADHD.
Dysfunction of the arousal system. There is consistent evidence of tonic
autonomic hypo-arousal in children with conduct problems, suggesting arousal system
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dysfunction. Two meta-analyses show that low resting HR is the best replicated
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biological correlate of youth antisocial behavior (Ortiz & Raine, 2004; Portnoy &
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Farrington, 2015). Lorber, (2004) showed that low resting HR is reliably associated with
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conduct problems in both children and adolescents; low resting SC was associated with conduct problems only in children but not adolescents.
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However, evidence linking low resting autonomic arousal to specific disorders is
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less consistent, and it is unclear how it pertains to ADHD, in light of its associated
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emotional lability (Rosen et al., 2015; Sobanski et al., 2010). In Van Bokhoven, Matthys, Van Goozen, & Van Engeland, (2005), lower resting SC, but not HR, predicted later
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externalizing problems in children with ODD or CD irrespective of comorbid ADHD. Van Goozen, et al., (2000) found both lower HR and SC across ODD, CD and ADHD.
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Beauchaine, Katkin, Strassberg, and Snarr, (2001) found low SC in adolescents with ADHD and those with comorbid CD, as did Crowell et al., (2006) in preschoolers. Jointly, findings suggest that resting hypo-arousal may be a common rather than a distinct mechanism of a specific disorder. Van Goozen et al., (2000) showed that children with
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disruptive disorders and comorbid ADHD had even lower SC than the other groups, signifying that comorbidity or severity may also modulate levels of resting arousal. Low autonomic reactivity has also been found, albeit inconsistently, in ODD/CD.
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Lorber, (2004) showed lower SC in response to non-aversive stimuli (tones or neutral slides) in children, but not adolescents with conduct problems, compared to controls.
Lower SC to negative stimuli was not systematically observed, in contrast to what is seen in adults with psychopathic traits (Blair & Mitchell, 2009; Patrick & Lang,
1999). Herpertz and colleagues (2005) found lower SC across positive, negative and
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neutral stimuli in children with ODD/CD and ADHD, but not those with ADHD only or
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controls. In other studies by the same group, boys with CD and ADHD had lower SC to
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orienting and aversive stimuli compared to those with ADHD only (Herpertz et al., 2003,
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2001). Recently, however, McQuade and Breaux, (2017) found that neither ODD or ADHD were related to SC reactivity to social and cognitive stressors. Thus, low SC
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reactivity is potentially linked more to ODD/CD than ADHD and may not be modulated
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by stimulus valence, but findings are not consistent across all relevant studies. Low HR
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reactivity in ODD/CD or ADHD has not been supported (de Wied, van Boxtel, Zaalberg, Goudena, & Matthys, 2006; Lorber, 2004), though de Wied, Boxtel, Posthumus,
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Goudena, and Matthys, (2009) noted less HR deceleration to sadness in ODD/CD (some cases with ADHD), which they explained as low empathy. Indirect support for
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hyporeactivity in children with ADHD comes from their relative insensitivity to punishment and reward (Crone et al., 2003; Iaboni, Douglas, & Ditto, 1997; Luman, Oosterlaan, & Sergeant, 2005; Masunami, Okazaki, & Maekawa, 2009; Meel, et al., 2011), but relevant physiological data are lacking.
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Dysfunction of positive and negative valence systems. Studies using facial EMG at the corrugator and zygomaticus muscles during emotional stimulation in children with ODD, CD or ADHD have yielded mixed results. Regarding the negative valence
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system, boys with ODD/CD showed smaller corrugator responses during sadness and anger films and angry faces than controls (de Wied et al., 2006, 2009). Contradictory evidence exists for 6-7 year-olds with ODD, CD and ADHD, who showed expected
corrugator response elevations to angry and sad faces (Deschamps, Munsters, Kenemans, Schutter, & Matthys, 2014). Regarding positive valence, the few existing studies found
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no significant zygomaticus response differences between children with ODD/CD or those
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with ADHD and controls during "happy" films or faces (de Wied et al., 2009, 2006;
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Deschamps, Coppes, Kenemans, Schutter, & Matthys, 2010; Deschamps et al., 2014).
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Together, extant physiological evidence reliably indicates resting state hypoarousal, especially in HR, in children with externalizing symptoms. It is less clear
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whether this is common across ADHD, CD and ODD. Lower SC emotional reactivity
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seems to be found, though inconsistently, in ODD and CD, but not ADHD, across
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valences. Findings indicate dysfunction of the arousal system, but additional research is needed to specify if it is common across disorders, its specificity to negative emotions,
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and to HR vs. SC, which may be theoretically relevant, because of their differential sympathetic and parasympathetic influences (Bradley et al., 2001; Hagemann, Waldstein,
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& Thayer, 2003). There is less support for a positive valence dysfunction in ODD/CD, though in ADHD there is a separate line of non-physiological evidence speaking for insensitivity of both reward and punishment systems and emotional lability.
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The moderating role of callous unemotional traits and anxiety. Although the emotional dysfunctions in ODD/CD and ADHD need to be better specified, there is some evidence that these may be driven by comorbid characteristics, such as Callous
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Unemotional (CU) Traits and anxiety (de Wied, van Boxtel, Matthys, & Meeus, 2012). Similar to the fearlessness hypothesis, Loney, Frick, Clements, Ellis, and Kerlin, (2003) argued that youth with disruptive symptoms characterized by high CU traits may show
low distress proneness. CU traits have been linked to decreased corrugator responses to negative films (Fanti, Kyranides, & Panayiotou, 2017) and less differentiation between
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positive and negative films in prefrontal cortex oxygenation compared to controls (Fanti,
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Panayiotou, Lombardo, & Kyranides, 2016). Also, children high in CU traits and CD had
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smaller fear potentiated startle responses to negative mental imagery (Fanti, Panayiotou,
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Lazarou, et al., 2016) and fear videos (Anastassiou-Hadjicharalambous & Warden, 2008) compared to children with CD low in CU and controls. Male adolescents with ODD or
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CD (most with comorbid ADHD), high in CU also showed less facial and HR reactivity
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during sadness than controls and those low in CU (de Wied et al., 2012). Male
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adolescents with disruptive behavior and low CU traits exhibited less zygomatic activity in response to joyful stimuli relative to controls, (de Wied et al., 2012), while participants
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with CD and high CU traits showed increased zygomaticus activity (interpreted as amusement) during anger films compared to those low in CU. Given that HR is affected
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by valence in addition to arousal (Cacioppo et al., 2000), such facial EMG and HR findings may suggest a valence deficit in CU. Musser, Galloway-Long, Frick, and Nigg, (2013) proposed that subtypes may exist in ADHD as well, based on the presence of CU
11
traits, showing opposite patterns of autonomic responses. In sum, CU traits may moderate effects of ODD/CD and ADHD on physiological responses (Frick et al., 1999). Similarly, anxiety may represent another moderator. Youth with externalizing
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symptoms without CU traits but high anxiety may form a different subgroup, showing higher sensitivity to punishment and distress proneness, and normal or over-reactive
arousal and negative valence systems (Fanti, Kyranides, Lordos, Colins, & Andershed, 2018; Fanti et al., 2017; Loney et al., 2003; Nigg et al., 2004). de Wied et al., (2006),
showed that children with disruptive symptoms had higher HR during a relaxing film
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than controls, which they attributed to anxiety, given that these children were rated as
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more anxious than controls. Similarly, children with ODD or CD (some with comorbid
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ADHD) and anxiety had higher resting HR than controls (de Wied et al., 2009). Thus,
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comorbid anxiety may lead to patterns opposite to what fearlessness and hypo-arousal theories would predict. It appears, that examining the moderating role of CU traits and
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Current Study:
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anxiety can help specify any shared emotional dysfunctions across ODD/CD and ADHD.
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This study adopts a dimensional approach to describe how patterns of arousal and/or valence system responses are associated with ADHD and/or ODD/CD. The
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moderating role of CU and anxiety in these associations is also evaluated. To address these questions we assessed facial EMG, to index valence, and HR and SC, to index
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primarily arousal, during viewing of affective pictures (the latter two measures also at rest). The sample included children with clinical, subclinical or no symptoms of ADHD, and ODD/CD. Because of the mixed evidence as to whether emotional dysfunctions are similar across disruptive disorders and ADHD, we posed alternative hypotheses that
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dysfunctions would be associated with either one or both symptom types. We predicted that (1) lower resting SC and HR, and reactivity during negative stimuli, especially fear, would be associated with increased symptoms of ODD/CD and/or ADHD (Lorber, 2004;
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Ortiz & Raine, 2004; Portnoy & Farrington, 2015; Van Bokhoven et al., 2005; Van Goozen et al., 2000). Based also on the fearlessness hypothesis, (2) lower corrugator responses to unpleasant stimuli would be associated with ODD/CD and/or ADHD
symptoms. (3) for zygomaticus, as past literature has not reliably observed dysfunctions of the positive valence system using this measure (de Wied et al., 2009, 2006), despite
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suggestions for a hyper- vs hypo-reactive positive valence system (de Wied et al., 2012),
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we did not posit specific hypotheses. Based on evidence that CU and other psychopathic
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traits, are associated with fearlessness and hypo-arousal, (4) we expected CU to moderate
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the effects pertaining to hypotheses 1 and 2, so that decreased tonic arousal, autonomic and corrugator reactivity would mostly be associated with ODD/CD symptoms and/or
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ADHD at high but not at low levels of CU traits (Anastassiou-Hadjicharalambous &
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Warden, 2008; de Wied et al., 2012; Loney et al., 2003). Similarly, in line with the
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fearlessness hypothesis, anxiety would moderate effects, so that ODD/CD and ADHD would be associated with typical, or hyper HR, SC and corrugator reactivity (i.e. emotion
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dysregulation) at high but not low anxiety levels (de Wied et al., 2009, 2006). Method
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Participants Participants were 87 Greek-Cypriot children (42 female, Mage=11.2 years,
range=10.1-12.8), from elementary schools located in urban and suburban areas of the Nicosia district in Cyprus. Schools (N=18) were randomly selected from 125 elementary
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schools in the district, using Ministry of Education and Culture’s records; 17 schools agreed to participate (one did not for scheduling reasons). Parents or guardians (N=1565 families) of all children in grades 5 and 6 were sent a consent form, the study description
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and the Child Behavior Checklist (CBCL; Roussos et al., 1999), to complete at home. Children whose parents gave informed consent (N=87) and themselves provided assent were invited to participate. All families were Caucasian of Greek-Cypriot ethnicity. Of parents who responded (74.4% mothers), 34.5% had high school education or lower,
44.4%, university or college, 11.1% graduate degree. Most, 78.8%, rated their financial
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status as “good,” 13.8% as “very good”, and 7.5 % as “bad” or “very bad”.
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The Wechsler Abbreviated Scale of Intelligence (WASI; Wechsler, 1999) was
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administered to rule out mental retardation. The Mini International Neuropsychiatric
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Interview for Children and Adolescents (MINI-KID; Sheehan et al., 2010) assessed for ODD/CD, ADHD and other mental health problems. Raw intelligence scores on the
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WASI were in the normal range of 2 SD below or above the mean of children of the same
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age based on local normative data. The CBCL, completed by a parent/guardian and a
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brief teacher checklist, provided corroborative evidence for externalizing and anxiety symptoms. All 87 children were included as no-one had any sensory, psychotic or
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pervasive developmental problems, and none were taking psychotropic medications. Although we follow a dimensional approach in this study by using continuous
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CBCL measures of ADHD and ODD/CD symptoms as our dependent variables, to ensure that all levels of severity were included in the sample, children underwent a clinical diagnostic procedure to assess presence of one or more of these disorders. Diagnosis was based on both child reports on the MINI-KID and parent reports on the CBCL. Twenty
14
four children (5 female) met criteria for comorbid ADHD-ODD/CD - no children were identified with ADHD diagnosis only. Fifteen (5 female), met criteria for ODD/CD and 48 (32 female) met no diagnosis and were included as Controls. In eight cases of
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disagreement between parent and child reports, where children reported subclinical or no symptoms on the MINI-KID, diagnosis was aided by the teacher’s checklist, on which reported behavioral problems at school corroborated the parent’s report on the CBCL.
Control children had CBCL symptoms between zero and just below the clinical cutoffs, to ensure a continuum of severity. Of 87 invited children, 81 participated in the
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experiment mostly due to scheduling difficulties. All blocks of the experiment were
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completed by 75 children, with the rest quitting due to boredom or other scheduled
Experimental Procedures
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zygomaticus analyses 62 participants.
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activities. Due to technical problems or noise, SC analyses included 69, corrugator 59 and
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The study was approved by the Ministry of Education and Culture and the
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National Bioethics Committee. Diagnostic assessment took place at school. The
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experiment took place at the university labs and included the present task and additional ones not relevant to this study. Participants took part in a passive picture viewing
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paradigm involving four presentations of each type of emotional picture, based on similar studies with undergraduates and children (Bernat et al., 2006; Sharp, Goozen, &
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Goodyer, 2006). Upon arrival to the lab, children were seated in a reclining chair in a sound-attenuated room and standard surface electrodes were attached. Following seven minutes of relaxation and a series of cognitive tasks irrelevant to this study, instructions were given for the experiment. Children were instructed to look at a series of pictures
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presented on a 45-inch TV monitor for six sec each, in one of three pseudorandom orders, with inter-trial intervals (ITIs) of 7, 12 or 18 sec. After the viewing task, sensors were detached and children viewed the pictures again to rate their subjective responses on
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valence and arousal, using 1-5 scales in a paper-and-pencil modification of the SelfAssessment Manikin (SAM; Lang, Bradley, & Cuthbert, 2005). After the experiment, (about 30 minutes), children were debriefed and received a toy and 15 euros. Materials
Pictures from the International Affective Picture System (IAPS; Lang et al., 2005)
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were selected, four of each, neutral (e.g., household objects), joy (e.g., birthday cake),
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fear (e.g., shark) and sad (e.g., crying boys)1, based on local normative valence and
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arousal ratings by a separate sample of 101 children and adolescents randomly selected
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from grades five to eight. Joy pictures were positive in valence (M=7.18) and high in arousal (M=5.26), sad pictures low in positive valence (M=1.89) and low in arousal
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(M=3.15), fear pictures low in positive valence (M=3.46) and high in arousal (M=6.65).
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Neutral pictures were medium in valence (M=5.42) and low in arousal (M=3.17).
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Apparatus and Response Measurement We obtained mean resting HR and SC from the last five minutes of initial
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relaxation. HR, SC, zygomaticus and corrugator reactivity was averaged for each picture duration and over same type pictures. One percent of observations on both ends for all
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physiological measures were removed as outlier values. Physiological data, sampled at 1000Hz, were recorded with BIOPAC MP150 for Windows and Acknowledge 3.9.0 software (BIOPAC Systems, Inc., Goleta, CA, USA). Stimulus presentation was achieved
1
IAPS pictures used (Lang et al., 2005): 1302, 1427, 1930, 2312, 2345, 2703, 2900.1, 3300, 5480, 6821, 7004, 7009, 7010, 7020, 7250 and 7330.
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using E-prime 1.0 (Schneider, Eschman, & Zuccolotto, 2002). Electrodermal activity was recorded continuously on the forefinger of the participant’s non-dominant hand using a BIOPAC GSR100C amplifier and transducer (TSD203) in microsiemens (μS), with a
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high-pass filter set at 0.05 μS. Lead I EKG was recorded in beats per minute (BPM) using two Ag/AgC1 disposable electrodes placed on each forearm, filtered by a BIOPAC ECG100C bioamplifier. For facial EMG, 4-mm electrodes were placed at the right
zygomaticus and corrugator (Fridlund & Cacioppo, 1986). The signal was amplified, filtered (band pass, 20Hz high frequency, 500Hz low frequency) and rectified.
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Measures
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Intelligence. The Wechsler Abbreviated Scale of Intelligence (WASI; Wechsler,
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1999) was used to assess the children's verbal, non-verbal and general cognitive ability. It
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consists of four subtests, Vocabulary and Similarities, which form the Verbal Scale, and Block Design and Matrix Reasoning, which form the Performance Scale. For this study,
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only Vocabulary and Block Design of the Greek-Cypriot WASI (Spanoudis & Tourva,
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2012) were administered to estimate verbal and non-verbal ability, respectively.
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Psychopathology. Parents completed the 113 item Child Behavior Checklist, rated on a 3-point scale, (0=not true, 1=somewhat true, 2=very true/very often true), to
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assess their child’s symptoms. The original and Greek version have well-established psychometric properties (Achenbach & Rescorla, 2001; Roussou, 2003). DSM-adjusted
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scales for ADHD, ODD, CD and Anxiety had reliabilities of .84, .83, .87 and .68. The Greek MINI-KID (Sheehan et al., 2010), a short, structured diagnostic
interview for DSM-IV and ICD-10 psychiatric disorders of children and adolescents was
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administered to participants by trained psychology graduate students. It assesses for 30 disorders and generates valid and reliable diagnoses (Sheehan et al., 2010). Teachers completed a short checklist on behavior problems at school, for each
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participating child in their class (Cronbach’s α=.74). They reported with a yes or no the presence of any of these four types of problems: 1) inattention/hyperactivity/impulsivity, 2) oppositionality/arguing/refusal to comply with rules, 3) threatening/ bullying/physical violence, or 4) anxiety problems. The checklist was used as auxiliary information to
resolve diagnostic discrepancies between parent (CBCL) and child (MINI- KID) reports.
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Traits. The 24-item Inventory of Callous-Unemotional traits (ICU) was
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completed by children. It consists of 12 positively and 12 negatively worded items,
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measuring CU traits in youth (Frick, 2004), rated on a 4-point Likert scale from 0 (not at
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all true) to 4 (definitely true). The test measures one general dimension of CU traits and three sub-dimensions, callousness (lack of empathy, guilt and remorse), uncaring (lack of
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caring about one’s performance and the feelings of others) and unemotional (absence of
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emotional expressions; Essau, Sasagawa, & Frick, 2006; Kimonis et al., 2008; Lazarou,
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2013). For this study, a reliability analysis showed that items 1 and 10 had low corrected item-total correlations. After removing these items, full scale reliability was α=.75.
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Data Reduction and Analysis Hypotheses were tested using mixed model analyses (SAS Proc Mixed v9.4; SAS
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Institute Inc., Cary, NC, USA) for repeated measures (i.e., multiple trials) of the dependent variables (HR and SC during rest, HR, SC, corrugator and zygomatic reactivity, and ratings). All models included subject as a random effect. Predictors in all cases were ADHD, or ODD/CD CBCL symptoms. These models were then each repeated
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two more times, to test separately the effects of potential moderators (CU traits and anxiety). Either anxiety or CU-traits (one at a time) were added to the model, both as main effects and in interaction with ADHD, or CD/ODD symptoms. Models were
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additionally repeated while controlling for the other symptom group (i.e. covarying ADHD when analyzing for ODD/CD and ODD/CD when analyzing for ADHD), to
account for the high comorbidity and examine unique effects of each symptom type. To rule out effects of gender, this dichotomous variable was included in additional
exploratory models. Post hoc differences between means following a significant mixed
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model effect were the result of contrast comparisons of least-square means (LSM) and
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standard errors (SE) of fixed effects using tests of simple effects. The family-wise α
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levels of post hoc contrasts were adjusted using the Holm-Bonferroni correction (Holm,
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1979) for the effects of multiple comparisons on type I error rate. For interactions between continuous and categorical variables, slopes were calculated for average change
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over the continuous variable, and reported as point estimates (PE) and standard errors
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(SE). Point estimates are analogous to a regression beta statistic in that the slopes indicate
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change on a dependent measure for every 1-unit increase in the predictor. All continuous predictors (ADHD, ODD/CD and anxiety CBCL scores, CU-traits) were mean centered.
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Effect sizes are reported as Cohen’ d (.2 small, .5 medium, >.8 large effect size). Linear mixed model analysis allows for estimates of the correlation structure of the residuals and
A
efficiently handles unbalanced designs and missing data, without excluding participants or imputing values (Bagiella et al. 2000). Results Correlations Between Indices of Symptomatology
19
Correlations were computed among the scales of interest on the CBCL, teachers’ checklist and scores on the ICU. Pearson correlations among CBCL scales were: anxiety with ADHD, ODD and CD, r=.53, .58, and .56 respectively. ADHD with ODD, r=.70,
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and CD, r=.68; ODD with CD, r=.74, all significant at p<0.01. Pearson correlations between CU traits and ADHD, ODD and CD symptoms, on the CBCL, were all
significant at p< 0.01; r=.35, .51, and .43 respectively. Point biserial correlations between CU traits and teacher ratings of ADHD, ODD, and CD (present/absent) on the teachers’ checklist, were also all significant, rpb= .47, .49, and .52 respectively. The correlations
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between CU traits and anxiety were not significant, either for the CBCL r=.20, p=.68 or
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teachers’ checklist rpb=.05, p=.67. Using Fisher’s exact ratio (Field, 2013) significant
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associations were found between teachers’ ratings for ADHD, ODD and CD
M
(presence/absence) and parents’ ratings for ADHD, ODD and CD symptoms on the CBCL (categorized as normal, borderline or clinical range), p=.009, p=.004, and
D
p=.001 respectively. However, teachers’ ratings of anxiety problems were not
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significantly associated with parents’ reports of anxiety on the CBCL, p=.57.
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Post-trial Picture Ratings
There was a main effect of picture type on valence ratings, F(3, 281)=301.95,
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p<.0001, with post hoc pairwise comparisons indicating that sad (LSM=0.53, SE=.08), fear (LSM=1.69, SE=.08), neutral (LSM=2.52, SE=.08), and joy (LSM=3.72, SE=.08)
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pictures all differed from one another. There was also a main effect of picture type on arousal ratings, F(3, 281)=29.67, p<.0001, with post hoc comparisons showing that joy (LSM=2.77 SE=.13), fear (LSM=2.39, SE=.13), sad (LSM=1.75, SE=.13) and neutral (LSM=1.09, SE=.13) pictures all differed from one another. Results indicate that emotion
20
was effectively induced. There were no significant effects of ADHD (p=.92) or interactions with CU or anxiety on valence (p=.39, p=.30 respectively) and arousal (p=.07, p=.65 respectively), and no significant effects of ODD/CD (p=.34) or interactions
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with CU or anxiety on valence (p=.61, p=.28 respectively) and arousal (p=.28, p=.20). Association Between ADHD and ODD/CD Symptoms and Resting HR and SC
ADHD symptoms were negatively associated (PE=-1.15, SE=0.50) with resting HR, F(1, 68)=5.41, p=0.023, Cohen’s d=0.40. Interactions with CU traits and anxiety
were non-significant (p=.44 and .50), showing no moderation by either trait. When the
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analysis was repeated with ODD/CD symptoms as covariate, the main effect of ADHD
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on resting HR dropped in significance to marginal, p=.07782. In the main analysis, main
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effects of ODD/CD and interactions with CU and anxiety (p=.16, .55 and .56
M
respectively) were not significant. ADHD had no significant main effect or interaction with CU traits and anxiety on resting SC (p=.14, .62 and .39). Main and interactive
D
effects of ODD/CD with CU traits and anxiety were also non-significant (p=.51, .80, .32
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respectively). The main effect of gender on HR reactivity was significant, (PE=-6.18,
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SE=2.94) F(1, 67)=4.42, p=0.039, Cohen’s d=0.36). with boys with ODD/CD having lower HR across picture types than girls3.
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Association Between ADHD and ODD/CD and HR Reactivity to Pictures There was no effect of picture type (p=.15) on HR reactivity to pictures (Table 1).
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The main effect of ADHD also did not reach significance (PE=-0.89, SE=0.50, F(1, 68)=3.18, p=.08), but this trend, irrespective of picture content, showed that HR tended to decrease as ADHD symptoms increased. There was a significant ADHD x Picture Type 2
Effects of the alternative symptom category entered as covariate did not change for all other dependent measures. These non-significant findings are not reported for the sake of brevity but are presented in Supplementary Table 1. 3 The effects of gender were non-significant in all other models and are not reported for the sake of brevity.
21
interaction, F(3, 1018)=4.56, p=0.0035 (Figure 1), which showed that, although at low and medium levels of ADHD HR reactivity did not differ significantly between picture types, at high levels of ADHD (+1SD), there was significantly lower reactivity for fear
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compared to joy (PE=-2.20, SE=0.58, t[212]=-3.82, p=.0002, Cohen’s d=0.37), and compared to neutral (PE=-1.30, SE=0.58, t[212]=-2.25, p=.025, Cohen’s d=0.22), but not compared to sadness (p=.18). Also at high levels of ADHD, HR reactivity for sadness
was lower compared to joy (PE=-1.43, SE=0.57, t[212]=-2.50, p=.013, Cohen’s d=0.24). There was no significant effect of ODD/CD (p=.32) on HR reactivity during
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picture viewing (Table 2). There was again a significant ODD/CD x Picture Type effect
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on HR reactivity, F(3, 1018)=3.33, p=0.0189 (Figure 2), indicating that, when ODD/CD
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was high, there was more decreased HR to fear compared to joy (PE=-1.38, SE=0.46,
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t[212]=-2.98, p=.0032, Cohen’s d=0.29), but not compared to sad (p=.47) or neutral pictures (p=.06). Also, at high levels of ODD/CD, HR reactivity to sadness was lower
D
compared to joy (PE=-1.04, SE=0.46, t[212]=-2.26, p=.024, Cohen’s d=0.22). Neither
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ADHD nor ODD/CD effects on HR were moderated by CU traits (p=.67 and p=.49
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respectively) or anxiety (p=.56 and p=.74), as none of the interactions were significant. Association Between ADHD and ODD/CD and SC Reactivity to Pictures
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There were no significant effects of picture type (p=.70), ODD/CD (p=.26) or their interactions with CU traits (p=.98) or anxiety (p=.80). ADHD was associated with
A
lower SC (PE=-0.59, SE=0.22) response to pictures, F(1, 68)=7.35, p=0.0085, Cohen’s d=0.46. This association was not moderated by anxiety (p=.79) or CU traits (p=.71). Association Between ADHD and ODD/CD and Corrugator Reactivity to Pictures
22
There was a main effect of picture type on corrugator reactivity, F(3, 183)=5.30, p=0.0016 with post hoc comparisons indicating that joy pictures had smaller corrugator responses compared to fear (PE=0.67, SE=0.28, t[183]=2.37, p=0.019, Cohen´s d=0.25),
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sad (PE=1.07, SE=0.28, t[183]=3.83, p=0.0002, Cohen´s d=0.40), and neutral pictures (PE=0.80, SE=0.28, t[183]=2.85, p=0.005, Cohen´s d=0.30). There were no main effects of ADHD or ODD/CD (p=.22; p=.20) or interactions with CU and anxiety (p=.17, p=.37 respectively for ADHD and p=.24, p=.26 for ODD/CD).
Association Between ADHD and ODD/CD and Zygomaticus Reactivity to Pictures
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There were non-significant effects of picture type, p=.20 on zygomaticus
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reactivity, but marginal effects of ADHD and ODD/CD symptoms (PE=0.37, SE=0.2,
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F(1, 61)=3.37, p=.07 and PE=0.27, SE=0.14, F(1, 61)= 3.56, p=.06 respectively),
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showing a trend for higher zygomaticus reactivity across picture types as symptoms increased. There was no moderation by anxiety or CU traits (p=.14, p=.42 respectively
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Discussion
D
for ADHD; p=.15, p=.23 for ODD/CD).
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In accordance with the RDoC, we examined the arousal and positive and negative valence system responses associated with ADHD and ODD/CD symptoms, searching for
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emotional mechanisms across these diagnostic categories that may explain their comorbidity, phenotypic similarities and shared developmental pathway (Casey et al.,
A
2014; Kronenberger & Meyer, 2001; Nigg, 2001). Decreased resting HR was associated with ADHD, while decreased HR reactivity to fearful and sad stimuli was associated with both ADHD and ODD/CD. Lower SC reactivity, irrespective of picture type viewed was associated with ADHD but not ODD/CD, indicative of a tonic than a reactivity effect. No
23
apparent valence deficits were found, as measured by EMG (though the decreased autonomic reactivity to fear and sad, but not joy pictures suggests that arousal deficits are specific to negative emotions), and no association between any of the symptoms and self-
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reported emotion. Findings are collectively consistent with the fearlessness theory of disruptive behavior (with effect sizes being somewhat larger for decreased fear than
decreased sadness in association with both ADHD and ODD/CD), an interpretation that
seems to apply across symptom types. The study contributes to understanding emotional
mechanisms in the disruptive disorders and ADHD, examining symptoms on a continuum
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of severity, with a balanced design of high/low arousal and positive/negative stimuli and
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multi-method assessment of arousal and valence using both physiology and self-report.
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ADHD symptoms were negatively associated with resting HR, consistent with
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similar findings for children with disruptive disorders. Contrary to some of this evidence (Hill, 2002; Ortiz & Raine, 2004; Portnoy & Farrington, 2015; Van Bokhoven et al.,
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2005; Van Goozen et al., 2000), this finding occurred for ADHD and not for ODD/CD
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only, and was not moderated by CU traits (de Wied et al., 2012; Musser et al., 2013).
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However, when ODD/CD was covaried, the effect of ADHD dropped in significance suggesting that disruptive disorder symptoms also contribute some variance. Given this
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finding, the fact that our sample with ADHD also had comorbid ODD/CD, and the fact that we had a significant number of cases who met formal diagnostic criteria, our findings
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may suggest that resting hypo-arousal may be moderated by comorbidity or severity; findings parallel those of others who found hypo-arousal in children with comorbid ADHD and CD or ODD (Herpertz et al., 2005; Van Goozen et al., 2000). It is possible that in samples with conduct problems not meeting diagnosis, CU traits carry the effect of
24
hyporeactivity by indexing more extreme antisocial traits. In samples with clinical levels of symptoms (in this case ADHD with comorbid ODD/CD), CU traits may not contribute significant additional variance, a tentative hypothesis for future empirical testing.
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No significant associations were found between ADHD or ODD/CD symptoms and baseline SC, indicating that resting hypoarousal may be more apparent in HR (as shown by past reviews, e.g. Ortiz & Raine, 2004). In accord with the fearlessness hypothesis, children with ADHD, especially those with high comorbid disruptive
symptoms, may maintain high parasympathetic control of their arousal, seen as decreased
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tonic HR (Ortiz & Raine, 2004; Portnoy & Farrington, 2015), when in the mildly
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stressful conditions of the lab. Precisely because HR is sensitive to valence in addition to
A
arousal (Cacioppo et al., 2000), this measure may have captured better a lack of distress
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by children with these characteristics during the initial period upon arrival to the unfamiliar environment of the lab, and throughout the experiment (seen in tonically lower
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SC), consistent with a fearlessness account. The absence of effects in support of positive
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valence system deficits, indicates more circumscribed hypoarousal, consistent with lack
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of distress (i.e. fearlessness) rather than broad hypoarousal, irrespective of context. With regards to reactivity, higher ODD/CD and ADHD symptoms were both
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linked to lower HR during fear compared to joy, the most appropriate contrast, since joy is also a high arousal emotion but of positive valence. Hyporeactivity to fear, rather than
A
across high arousal (i.e. joy) emotions, and with larger effect sizes for fear than sadness, is more consistent with fearlessness and a defensive system deficit, as proposed before (Anastassiou-Hadjicharalambous & Warden, 2008; Frick et al., 1999; Loney et al., 2003). HR hyporeactivity to fear was associated in separate models with both ODD/CD and
25
ADHD indicating that fearlessness is a common mechanism. As reactivity was also lower to sad compared to joy pictures as either symptom type increased, a narrow fearlessness account may need to be modified: Children with symptoms across ODD/CD and ADHD
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may have a broader deficit in experiencing distress rather than fear only. Our findings do not support a specific empathy impairment, considered as a risk factor for antisocial behavior (de Wied et al., 2009). Although HR was lower as both symptom types increased in sadness compared to joy (an expected effect given our
selection of joy and sad stimuli to differ in arousal), a stronger effect was found for the
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fear-joy contrast. Differences in findings from de Wied et al. (2009) may be a function of
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the specific stimuli used. Pictures in the current study may have been emotionally
A
provoking for all participants as they depicted children of their age feeling pain or crying.
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More importantly, sadness stimuli were selected to be low in arousal and high in negative valence. The sad films in de Wied et al. (2009), may have been highly arousing, tapping
D
into the hyporeactivity to distressing stimuli we observed. Collectively, our physiological
TE
findings indicate tonic autonomic hypoarousal related to ADHD and hyporeactivity for
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both types of symptoms to distressing situations. Given that our ADHD sample was more comorbid, it may be that circumscribed fearlessness in disruptive disorders generalizes,
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even to mildly distressing contexts (the experiment) as comorbidity increases. Importantly, physiological reactivity effects of ADHD and ODD/CD were not
A
paralleled by decreased subjective ratings of arousal or negative valence, although we had found such effects in prior studies of externalizing symptoms (Panayiotou, Fanti, & Lazarou, 2015; Panayiotou et al., 2015). It is unclear what led to this difference from our own past studies (although it should also be noted that in the previous studies it was
26
primarily CU traits that accounted for self-report effects), which mostly differed in the somewhat younger age of the present sample. One possibility is that children at this age have not yet learned to accurately report on their experiences, which eliminated any
SC RI PT
influence of externalizing symptoms due to floor effects. It is also possible that learning to accurately report on experiences depends on interoceptive feedback (Herbert, Herbert, & Pollatos, 2011), so that over development children with ADHD and/or ODD/CD
progressively fall behind their typical cohorts’ ability to verbally express emotions, due to lack of intense physiological reactions, and indications of lower verbal ability (e.g.
U
Frazier, Demaree, & Youngstrom, 2004; Hill, 2002) in these disorders. An alternative
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hypothesis, which though fails to explain the past discrepant results, is that the emotional
A
difficulties of these children are specific to physiology, because contextual cues (e.g.
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questions, rating scales) can guide their self-report. These tentative hypotheses can only be addressed by more and longitudinal research, but they are consistent with evidence
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that children with CD have good theory of mind abilities (Gillespie, Kongerslev, Sharp,
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& Abu-Akel, 2018), which may aid them in socially appropriate self-report.
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ADHD and ODD/CD symptoms were unrelated to corrugator reactivity. This suggest that children with various levels of these symptoms show typical negative
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valence system function (Deschamps et al., 2014; McManis et al., 2001), in contrast to some past studies which had implicated a valence deficit in disruptive disorders or
A
ADHD (de Wied et al., 2009, 2006). Divergence from past findings may pertain to the balanced stimuli and measures that disentangle valence from arousal effects in our study. With regards to positive valence, our findings are consistent with a normally functioning system (de Wied et al., 2006; Deschamps et al., 2014), strengthening the
27
argument that valence systems are not generally implicated in ADHD and ODD/CD dysfunctions. In the present study ADHD and ODD/CD were not significantly associated with abnormal zygomaticus reactivity to joy. However, we did observe an increase in
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zygomaticus reactivity, approaching significance, across valences associated with both ADHD and ODD/CD. In the unfamiliar environment of a psychophysiological
experiment, the expected affective response might have been of mild displeasure rather
than of positive affect. The fact that both types of symptoms were associated with higher zygomaticus activity across the experiment may be consistent with a general lack of
U
distress (including decreased anxiety and stress; e.g. Fanti & Kimonis, 2017), rather than
N
augmented positive valence, associated with ADHD and ODD/CD. These interpretations
A
are tentative, and should be seen with caution, due to the marginal nature of these effects.
M
A novel aspect of this study was our attempt to examine if arousal or valence deficits are moderated by CU and anxiety traits. Previous studies had found patterns of
D
hyporeactivity and fearlessness associated with CU (Anastassiou-Hadjicharalambous &
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Warden, 2008; de Wied et al., 2012; Loney et al., 2003), and high emotional reactivity
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associated with anxiety, suggesting that these traits may contribute to heterogeneity in both disruptive disorders (Fanti & Kimonis, 2017) and ADHD (Musser et al., 2013).
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However, our findings do not support such moderation. Instead they suggest that underarousal in distressing contexts is a function of primary characteristics of these symptoms
A
and not accounted for by comorbid traits. Potentially, divergence from previous findings may have to do with the inclusion of formally diagnosed children, many with comorbid ADHD, ODD/CD in the current study. Alternatively, as we based assessment of socially
28
undesirable CU traits, on children’s self-reports, they may have under-reported them given the good theory of mind suggested to characterize CD (Gillespie et al., 2018). Some limitations of this study could influence the interpretation of findings. First,
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we had a small sample size because, even though a large number of students and parents were informed about the study, only a few families agreed to participate. This can be
partly attributed to the time commitment and paperwork (complicated consent forms)
required for both phases of the study and concern that children might be stigmatized for having externalizing disorders. However, taking into consideration the prevalence of
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these disorders in the population and the statistical power of similar studies, the number
N
of participants may be less of a concern (e.g. de Wied et al., 2006; McQuade & Breaux,
A
2017), though it is strongly desirable to replicate our findings with larger samples to
M
ensure adequate power to detect small effects. A second limitation has to do with the fact that children meeting ADHD only criteria appeared negligible in our 10-12 aged sample,
D
whereas a substantial number of children had comorbid ADHD and ODD/CD. Although,
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disruptive symptoms were treated as continuous, the absence of children with only
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ADHD makes the interpretation of results more difficult. Future research could select for larger numbers of participants with “pure” category symptoms, perhaps by targeting
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younger ages where comorbidity is expectedly lower (given the developmental progression of these disorders), in order to reach safer conclusions. Ideally, gender should
A
also be balanced between the clinical and control participants, something we aimed for but were unable to do based on the sample who consented to participate. This aim presents a challenge given the much higher prevalence of externalizing disorders in males (APA, 2013a). Examination of the effect of gender in our study revealed only one
29
significant effect; ODD/CD boys had lower HR reactivity than girls, suggesting that using a gender balanced design in the future may reveal interpretable effects on some measures. Also, the experimental stimuli could have included more pictures for each
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valence/arousal category, to strengthen obtained effects. However, our number of pictures was similar to others (e.g. Bernat et al., 2006; Sharp et al., 2006), and several of our effects were strong, suggesting that the presented stimuli adequately induced
emotion. Finally, future studies could benefit from the inclusion of more specific
measures of sympathetic and parasympathetic influences, in order to specify these
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deficits further, such as respiratory sinus arrhythmia (RSA) and cardiac pre-ejection
N
period (PEP; Beauchaine et al., 2013; Karalunas et al., 2018; Musser et al., 2013).
A
In sum, our findings suggest that the dysfunctions associated with disruptive
M
symptoms of ADHD and ODD/CD are mostly common rather than distinct and are consistent with fearlessness and decreased distress at both resting baseline and during
D
fearful and sad contexts. This pattern may be more profound and widespread (apparent in
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both SC and HR) in children with greater comorbidity and severity of symptoms rather
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than pertaining to a specific symptoms category, and rather than being a function of the level of co-existing traits like CU and anxiety. Our findings are consistent with a trans-
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diagnostic approach to treating disruptive behaviors, taking into consideration the potential fearlessness of these children that may impair the effectiveness of using
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negative consequences, and their under-arousal that may motivate behaviors aimed at increasing stimulation. Parents, teachers and specialists should perhaps invest in positive reinforcement, taking into account their normally functioning positive valence system,
30
and in creating a positive environment rich in learning stimuli that captures these
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children’s needs for sensation seeking and emotional stimulation.
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Figure 1
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Figure 1. ADHD symptom x Picture Type interaction on HR reactivity
Note. NEU = neutral stimuli, Fear = fear stimuli, Joy = joy stimuli, Sad = sadness stimuli
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HR = Heart rate, BPM = Beats per minutes, ADHD = Attention Deficit Hyperactivity
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Disorder
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Figure 2
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Figure 2. ODD/CD symptom x Picture Type interaction on HR reactivity
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Note. NEU = neutral stimuli, Fear = fear stimuli, Joy = joy stimuli, Sad = sadness stimuli
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HR = Heart rate, BPM = Beats per minutes, ODD/CD = Oppositional Defiant
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Disorder/Conduct Disorder
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Table 1 Least Squares Means (LSM) and Standard Error (SE) of HR, SC, Corrugator and Zygomaticus responses of ADHD children during Neutral, Fear, Joy and Sadness Stimuli.
SC
Corrugator
10.01 (0.60) 10.09 (0.60) 10.02 (0.60) 10.06 (0.60)
8.06 (0.52) 7.93 (0.52) 7.26 (0.52) 8.33 (0.52)
Zygomaticus
7.61 (0.58) 7.68 (0.58) 7.68 (0.58) 7.22 (0.58)
U
77.54 (1.40) Neutral 77.14 (1.40) Fear 77.83 (1.40) Joy 76.98 Sadness (1.40)
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HR
A
CC
EP
TE
D
M
A
N
Note. Means indicate the average of the four pictures per emotion. HR = Heart rate, SC = Skin conductance. HR reactivity is measured in beats per minutes. SC is measured in microsiemens. Corrugator and Zygomaticus reactivity are measured in microvolts.
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Table 2
HR Neutral
77.50 (1.42) 77.10 (1.42) Joy 77.79 (1.42) Sadness 76.94 (1.42) Fear
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Least Squares Means (LSM) and Standard Error (SE) of HR, SC, Corrugator and Zygomaticus responses of ODD/CD children during Neutral, Fear, Joy and Sadness Stimuli.
SC
Corrugator
Zygomaticus
10.00 (0.63) 10.09 (0.63) 10.01 (0.63) 10.05 (0.63)
8.06 (0.52) 7.92 (0.52) 7.26 (0.51) 8.33 (0.51)
7.60 (0.58) 7.67 (0.58) 7.67 (0.58) 7.21 (0.58)
A
CC
EP
TE
D
M
A
N
U
Note. Means indicate the average of the four pictures per emotion. HR = Heart rate, SC = Skin conductance. HR reactivity is measured in beats per minutes. SC is measured in microsiemens. Corrugator and Zygomaticus reactivity are measured in microvolts.
50