Maladaptive social information processing in childhood predicts young men's atypical amygdala reactivity to threat

Abstract

Background Maladaptive social information processing, such as hostile attributional bias and aggressive response generation, is associated with childhood maladjustment. Although social information processing problems are correlated with heightened physiological responses to social threat, few studies have examined their associations with neural threat circuitry, specifically amygdala activation to social threat. Methods A cohort of 310 boys participated in an ongoing longitudinal study and completed questionnaires and laboratory tasks assessing their social and cognitive characteristics between 10- and 12-years-old. At age 20, 178 of these young men underwent functional magnetic resonance imaging and a social threat task. At age 22, adult criminal arrest records and self-reports of impulsiveness were obtained. Results Path models indicated that maladaptive social information processing at ages 10 and 11 predicted increased left amygdala reactivity to fear faces, an ambiguous threat, at age 20 while accounting for childhood antisocial behavior, empathy, IQ, and socioeconomic status. Exploratory analyses indicated that aggressive response generation—the tendency to respond to threat with reactive aggression—predicted left amygdala reactivity to fear faces and was concurrently associated with empathy, antisocial behavior, and hostile attributional bias, whereas hostile attributional bias correlated with IQ. Although unrelated to social information processing problems, bilateral amygdala reactivity to anger faces at age 20 was unexpectedly predicted by low IQ at age 11. Amygdala activation did not mediate associations between social information processing and number of criminal arrests, but both impulsiveness at age 22 and arrests were correlated with right amygdala reactivity to anger facial expressions at age 20. Conclusions Childhood social information processing and IQ predicted young men’s amygdala response to threat a decade later, which suggests that childhood social-cognitive characteristics are associated with the development of neural threat processing and adult adjustment.

Neighborhood Deprivation during Early Childhood and Conduct Problems in Middle Childhood: Mediation by Aggressive Response Generation

“…Youth who were more likely to generate aggressive responses to ambiguous social conflict were rated by their parents and teachers as exhibiting higher levels of CPs. Choe et al (2015) demonstrated similar findings in an independent sample of urban, male, low-income youth, linking ARG in middle childhood to a greater number of criminal arrests in young adulthood. These findings also are consistent with the extensive body of literature indicating that SIP problems in childhood, particularly ARG, have long-standing consequences for adolescents’ CPs (e.g., Hyde et al 2010).…”

“…The present findings should also be considered in conjunction with evidence using neuroimaging indicating that regions of the limbic system (e.g., amygdala) and the prefrontal cortex (e.g., ventral prefrontal cortex) are activated as individuals process information in response to interpersonal conflict (Choe et al 2015; Meyer-Lindenberg et al 2006). For example, in an independent sample of 310 racially diverse and low-income men, Choe et al (2015) found that maladaptive SIP patterns at ages 10 and 11 predicted increased left amygdala reactivity to facial expressions of fear at age 20, suggesting hypervigilance to indications of social threat.…”

“…For example, in an independent sample of 310 racially diverse and low-income men, Choe et al (2015) found that maladaptive SIP patterns at ages 10 and 11 predicted increased left amygdala reactivity to facial expressions of fear at age 20, suggesting hypervigilance to indications of social threat. Thus, transgressions from normative information processing may have an underlying biological basis that involves an altered neural threat circuit.…”

The Neurobiology of Impulsive Aggression

“…Moreover, a recent study reported a positive association between propensity for impulsive aggression and amygdala responses to fearful expressions in a large sample of individuals (n = 310) (Choe et al 2015). However, none of these studies reported either increased responsiveness of the hypothalamus or the PAG.…”

“…Given the literature briefly reviewed previously, it can be predicted that such patients will show heightened responsiveness in regions implicated in impulsive aggression to emotional provocation (Blair 2001) ; that is, the amygdala, hypothalamus, and PAG (Panksepp 1998;Gregg and Siegel 2001;Nelson and Trainor 2007;Lin et al 2011). In line with this suggestion, patients with posttraumatic stress disorder (PTSD) (Shin et al 2006), intermittent explosive disorder (Coccaro et al 2007), severe mood dysregulation (Thomas et al 2013), and borderline personality disorder (Hazlett et al 2012), as well as impulsively aggressive spouse abusers (Lee et al 2008), all with an increased risk for reactive aggression, all show increased amygdala responsiveness to threatening stimuli relative to comparison FIG. 1.…”