Looming Threats and Animacy: Reduced Responsiveness in Youth with Disrupted Behavior Disorders

Abstract

Theoretical models have implicated amygdala dysfunction in the development of Disruptive Behavior Disorders (DBDs; Conduct Disorder/Oppositional Defiant Disorder). Amygdala dysfunction impacts valence evaluation/response selection and emotion attention in youth with DBDs, particularly in those with elevated callous-unemotional (CU) traits. However, amygdala responsiveness during social cognition and the responsiveness of the acute threat circuitry (amygdala/periaqueductal gray) in youth with DBDs have been less well-examined, particularly with reference to CU traits. 31 youth with DBDs and 27 typically developing youth (IQ, age and gender-matched) completed a threat paradigm during fMRI where animate and inanimate, threatening and neutral stimuli appeared to loom towards or recede from participants. Reduced responsiveness to threat variables, including visual threats and encroaching stimuli, was observed within acute threat circuitry and temporal, lateral frontal and parietal cortices in youth with DBDs. This reduced responsiveness, at least with respect to the looming variable, was modulated by CU traits. Reduced responsiveness to animacy information was also observed within temporal, lateral frontal and parietal cortices, but not within amygdala. Reduced responsiveness to animacy information as a function of CU traits was observed in PCC, though not within the amygdala. Reduced threat responsiveness may contribute to risk taking and impulsivity in youth with DBDs, particularly those with high levels of CU traits. Future work will need to examine the degree to which this reduced response to animacy is independent of amygdala dysfunction in youth with DBDs and what role PCC might play in the dysfunctional social cognition observed in youth with high levels of CU traits.

Trial registration: ClinicalTrials.gov NCT00104039.

Keywords: Amygdala; Animacy; Conduct disorder; Disruptive behavior disorders; Oppositional defiant disorder; Threat.

Conflict of interest statement

Conflict of Interest No authors have any conflicts of interest to disclose.

Figures

Fig. 1

The Looming Task. Each trial consisted of a serial presentation of images that either increased in visual angle (looming trial, depicted in the figure) or decreased in visual angle (receding trial). Images were looming and animate, looming and inanimate, receding and animate or receding and inanimate. Participants pressed a button as soon as they saw the image

Fig. 2

Regions of Interest Showing a Significant Diagnosis-by-Direction-by-Emotion Interaction. A Significant activations within the right amygdala region of interest where increased BOLD responses to [looming threat − receding neutral], [looming neutral −receding neutral] and [receding threat − receding neutral] were observed in typically developing youth (TD; N = 27) compared to youth with disruptive behavior disorders (DBDs; N = 31); B Significant activations within the periaqueductal gray region of interest where increased BOLD responses to [receding threat – receding neutral] were observed in TD youth compared to youth with DBDs

Fig. 3

Regions Showing a Significant Callous-Unemotional Traits-by-Emotion Interaction within the 31 youth with disruptive behavior disorders. In left middle frontal gyrus (A) and left inferior parietal cortex (B), CU traits showed a significantly larger inverse association with BOLD responses in looming trials relative to receding trails