Neural Correlates of the Propensity for Retaliatory Behavior in Youths With Disruptive Behavior Disorders

Abstract

Objective Youth with Disruptive Behavior Disorders (DBD: Conduct Disorder/Oppositional Defiant Disorder) are at increased risk for maladaptive reactive aggression. Theory suggests this is due to increased sensitivity of basic threat circuitry implicated in retaliation (amygdala/periaqueductal gray) in youth with DBD and low levels of Callous-Unemotional Traits and dysfunctional regulatory activity within ventromedial prefrontal cortex (vmPFC) in youth with DBD irrespective of callous-unemotional traits. Methods Fifty-six youths participated (23 female) aged 10–18 (26 healthy and 30 with DBD [15 with high and 15 with low callous-unemotional traits]) who completed an Ultimatum Game during functional MRI. Results Youth with DBD and low callous-unemotional traits showed greater increases in activation of basic threat circuitry when punishing others relative to comparison groups and dysfunctional down regulation of vmPFC during retaliation. All youth with DBD showed reduced amygdala-vmPFC connectivity during high provocation relative to healthy youth. VmPFC responsiveness and vmPFC-amygdala connectivity were related to patients’ retaliatory propensity (behavioral responses during task) and parent reported reactive aggression. Conclusions These data suggest differences in the underlying neurobiology of maladaptive reactive aggression in youth with DBD and low relative to high levels of callous-unemotional traits. Youth with DBD and low callous-unemotional traits alone show significantly greater threat responses during retaliation relative to comparison individuals. Moreover, these data suggest that vmPFC-amygdala connectivity is critical for regulating retaliation/reactive aggression and when dysfunctional, contributes to reactive aggression, independent of level of callous-unemotional traits.

Emotion-based learning systems and the development of morality

“…An example of how dysfunction in the representation of expected value might result in increased “immoral” (antisocial) behavior is provided by recent work with a modified version of the Ultimatum game (White, Brislin, Meffert, Sinclair, & Blair, 2013; White, Brislin, Sinclair, & Blair, 2014; White et al, 2016). In this task, the participant plays against named opponents (in reality a computer).…”

“…Unsurprisingly, healthy individuals increase their retaliation the more unfair the offer (White, Brislin, et al, 2013; White, Brislin, et al, 2014). But this effect of provocation is significantly greater on individuals with CD; individuals with CD punish more than healthy youth (White et al, 2016). Interestingly, retaliatory activity on this task is positively associated with reported reactive aggression in youth with CD.…”

“…Interestingly, retaliatory activity on this task is positively associated with reported reactive aggression in youth with CD. More interesting still, the impairment in youth with CD relates to reduced representing of the costs of retaliation within vmPFC (and reduced integrated activity of this region with the amygdala) (White et al, 2016). Indeed, this neuro-computational impairment underpins the association between retaliation on task and reported reactive aggression.…”

“…Unfair resource allocations can be seen as disrespectful and, as such, may trigger retaliation (White, Brislin, et al, 2013). Interestingly, in healthy individuals magnitude of costly retaliatory behavior is inversely related to vmPFC activity, potentially reflecting representation of the costs of retaliation (White, Brislin, et al, 2013; White, Brislin, et al, 2014; White et al, 2016). As noted above, youth with CD (irrespective of level of psychopathy/callous-unemotional traits) show impaired representation of value within vmPFC (Crowley et al, 2010; Finger et al, 2011; Finger et al, 2008b; White, Pope, et al, 2013).…”

Envolvimento do núcleo accumbens e da amígdala na neurobiologia dos transtornos do comportamento disruptivo e do transtorno de déficit de atenção/hiperatividade: um estudo de conectividade funcional de repouso em crianças

“…TDAH: ↓CC entre amígdala E e COF E; ↑CC entre amígdala E e giro pré-central D Correlação negativa entre CC amígdala-giro pré-central e sintomas de desatenção ROI = região de interesse; RMcf-r = ressonância magnética de conectividade funcional de repouso; RMf = ressonância magnética funcional; E = esquerdo(a); D = direito(a); TDAH = transtorno de déficit de atenção/hiperatividade; ↑LE = alta pontuação de labilidade emocional; ↓LE = baixa pontuação de labilidade emocional; TDC = transtorno do desenvolvimento da coordenação; DT = desenvolvimento típico; CC = conectividade; CPFm = córtex pré-frontal medial; GTS = giro temporal superior; GOM = giro occipital médio; CPF = córtex pré-frontal; COF = córtex orbitofrontal TCD/↓TEPSL: ↓CC da amígdala com giro frontal inferior E, CCP E, caudado E e ínsula E, em resposta a estímulo emocional TCD/↑TEPSL: ↑CC da amígdala com o caudado em resposta a estímulo positivo ROI = região de interesse; RMcf-r = ressonância magnética de conectividade funcional de repouso; RMf = ressonância funcional; E = esquerdo(a); D = direito(a); TC = transtorno de conduta; TOD = transtorno de oposição desafiante; TP = traços psicopáticos; DT = desenvolvimento típico; TCD = transtornos do comportamento disruptivo; TEPSL = traços de emoção prossocial limitada; TDAH = transtorno de déficit de atenção/hiperatividade; DE = desregulação emocional; CC = conectividade; CPF = córtex préfrontal; GTS = giro temporal superior; CPFvm = córtex pré-frontal ventromedial; CCP = córtex cigulado porterior Considerando os TCD, estudos avaliaram a conectividade funcional da amígdala usando RMf de repouso (60,64) ou RMf tradicional (com tarefas) (44,(61)(62)(63). Os estudos encontraram redução da conectividade entre amígdala e: CPFvm/COF, córtex temporal superior, córtex parietal inferior, córtex cingulado posterior e insula (44,(60)(61)(62)(63) O recrutamento na comunidade permitiu a inclusão de uma amostra com maior representatividade da população afetada pelos transtornos e menos sujeita à influência de multi-morbidade, gravidade dos transtornos e uso de medicação, comuns em amostras clínicas. A inclusão de crianças com TDAH e com TCD no mesmo estudo permitiu comparar os transtornos e avaliar alterações da conectividade funcional do NAcc e da amígdala potencialmente específicas de cada transtorno.…”