Neural Response To Reward And Punishment For The Primary And Secondary Variants Of Callous-unemotional Traits Across Early Adolescence In The ABCD Study - Info and Reading Options

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Childhood conduct disorder (CD) is defined by repetitive and pervasive antisocial behavior, including rule-breaking and aggression. A prominent approach to characterizing risk for CD is based on the presence or absence of callous-unemotional (CU) traits (Frick et al., 2014a). CU traits are characterized by a lack of empathy and guilt, representing a downward extension of the affective features of adult psychopathy (Frick, 2009; Hare, 1991). Children with CU traits are at very high risk for exhibiting future violent behavior and substance use (Baskin-Sommers et al., 2015). Explanations on the etiology of CD have centered on increased sensitivity to cues of reward and decreased sensitivity to punishment cues (Byrd et al., 2014; Blair et al., 2018; Frick et al., 2014a, 2014b; Raine, 2018). These difficulties are thought to be particularly pronounced among children with CU traits (Byrd et al., 2014, 2018; Budhani & Blair, 2005; Frick et al., 2014b). A focus on reward and punishment sensitivity is important since these processes are also central to behavioral interventions designed to reduce CD symptoms (Hawes & Dadds (2005), including when children have high CU traits. However, interventions appear less effective or bring about less change in CD symptoms among children with high CU traits, which may be the result of differences in responding to punishment and reward cues. To better understand differential patterns of reward and punishment sensitivity associated with CD and CU traits, studies have investigated neural activation during functional imaging tasks whereby different cues of punishment and reward are presented. Findings have been mixed in terms of directionality (Byrd et al., 2014; Hyde et al., 2013). For example, decreased activation of the orbitofrontal cortex (OFC; Finger et al., 2011; Rubia et al., 2009), ventromedial prefrontal cortex (vmPFC; Zhang et al., 2019), striatum (Cohn et al., 2015; White et al., 2013; Zhang et al., 2019), and amygdala (Cohn et al., 2015) has been linked to CD and CU traits in children and adolescents during reward receipt. However, increased activation of the striatum, anterior cingulate cortex (ACC), OFC and amygdala (Bjork 2010; Hawes et al., 2021) has also been linked to CD and CU traits during reward receipt, with differences emerging on the basis of task used, as well as whether important covariates such as comorbid attention-deficit/hyperactivity (ADHD) or head motion were included in models. Moreover, during reward anticipation, CU traits were associated with decreased activation in mPFC (Veroude et al., 2016), and dorsal ACC (Hawes et al., 2021) and increased activation in striatum, insula and superior frontal gyrus (Hawes et al., 2021; Huang et al., 2019). Likewise, increased activation in caudate (Finger et al., 2008; White et al., 2013), vmPFC and amygdala (Finger et al., 2008; Cohn et al., 2015) during loss and punishment receipt has been related to CD and CU traits. However, the amygdala was also reported to show reduced activation (Byrd et al., 2018; Huang et al., 2019), or no difference in brain activity in any region when comparing children with low versus high CU traits (Byrd et al., 2021), with some differences based on whether studies accounted for comorbid externalizing symptoms (Huang et al., 2019), ADHD and internalizing symptoms (Byrd et al., 2018, 2021), or used longitudinal data (Cohn et al., 2015). One explanation for these discrepant findings is that children with CD and high CU traits are not a homogeneous group. In the last decade, research has further differentiated between CD with CU traits inspired by work by Karpman (1941), which categorized adults high on psychopathic traits into a “primary” subtype (characterized by low anxiety and low emotional reactivity) and a “secondary” subtype (characterized by high anxiety and high emotional reactivity). Among children with CU traits, studies have provided support for the existence of similar variants, with the secondary variant evidencing higher impulsivity, hostility, and hypervigilance to cues of threat and distress (Craig et al., 2021; Dean et al., 2013; Kimonis et al., 2012a), higher aggression (Ezpeleta et al., 2017; Kahn et al., 2013; Kimonis et al., 2011; Sheti et al., 2018), greater experience of maltreatment (Kimmonis et al., 2012a), physical and sexual abuse (Kahn et al., 2013; Sheti et al., 2018) as well as lower socioeconomic status and inconsistent parenting (Ezpeleta et al., 2017). There is mixed evidence with regards to whether secondary CU traits variant shows higher levels of substance use compared to primary group (Kimonis et al., 2012b) or no differences between groups (Sheti et al., 2018; Waller & Hicks, 2019). Importantly, based on prominent theory, the two variants might be expected to differ in sensitivity to reward and punishment (Lykken, 1995; Gray, 1987). In adults, primary psychopathy is thought to be underpinned by an underactive behavioral inhibition system (BIS) when facing punishment (i.e., fearless temperament) and secondary psychopathy by an overactive behavioral activation system (BAS; greater reward responsiveness). Consistent with Lykken’s hypothesis, some studies of youth that have used self-report measures of BIS and BAS have found a primary psychopathy variant is related to lower BIS scores and a secondary psychopathy variant to higher BAS scores (Bjornebekk & Gjesme, 2009; Gill & Stickle, 2015; Kahn et al., 2015; Krimbel et al., 2007; Ross et al., 2011), similar to findings in adults (Newman et al., 2005). However, in other studies, a secondary variant has also been reported to show high BIS scores (Gill & Stickle, 2015) and higher BAS scores to predict primary variant membership (Bjornebekk & Gjesme, 2009; Krimbel et al., 2007; Ross et al., 2011). When variants are directly compared, a secondary variant showed higher BAS and lower BIS than a primary variant in adolescents (Kahn et al. 2013) and greater sensitivity to both reward and punishment in childhood (Ezpezeleta et al. 2017). Neuroimaging can provide additional insight into differences between primary and secondary variants, including characterizing differences in sensitivity reward and punishment. A recent review concluded, based on endocrine and biological indicators that the secondary variant shows hyperarousal and dysregulation of the stress response in the amygdala and HPA axis, linked to greater experiences of trauma (see Craig et al., 2021 for details). However, only a handful of studies have investigated neural correlates of primary versus secondary variants, with a focus on punishment learning paradigms. In adults, a primary psychopathy variant showed heightened activation to punished stimuli in the middle frontal gyrus and dorsal ACC, suggesting normal learning and fear responding, while a secondary variant showed greater activation in subgenual ACC, previously related with fear inhibition (Schultz et al., 2016). In youth, the primary variant was associated with lower right amygdala activation while in response to unconditioned stimuli (neutral faces). In contrast, the secondary variant showed no difference in amygdala response comparing conditioned with aversive electric stimuli and unconditioned stimuli during extinction (Fanti et al., 2020). To date, however, no prior studies have explored whether primary and secondary CU traits variants differ in neural processing in response to reward and punishment anticipation and receipt, which could provide additional insight into the etiology of these different variants, with implications for intervention and treatment strategies. To address this gap, the current study aims to extend previous research by focusing on differences in reward and punishment processing and exploring factors that contribute to the belongingness of youth with primary versus secondary CU traits variants. Specifically, reward and punishment processing will be examined including the basis of BIS and BAS scores, and neural activation in regions linked to the processing of reward and punishment.

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