Mapping neural activity patterns to contextualized fearful facial expressions onto callous-unemotional (CU) traits: intersubject representational similarity analysis reveals less variation among high-CU adolescents.

Shawn A Rhoads,John W Vanmeter,Katherine O’Connell,Abigail A Marsh,Elise M Cardinale,Amy L Palmer

doi:10.1017/pen.2020.13

Abstract

Callous-unemotional (CU) traits are early-emerging personality features characterized by deficits in empathy, concern for others, and remorse following social transgressions. One of the interpersonal deficits most consistently associated with CU traits is impaired behavioral and neurophysiological responsiveness to fearful facial expressions. However, the facial expression paradigms traditionally employed in neuroimaging are often ambiguous with respect to the nature of threat (i.e., is the perceiver the threat, or is something else in the environment?). In the present study, 30 adolescents with varying CU traits viewed fearful facial expressions cued to three different contexts ("afraid for you," "afraid of you," "afraid for self") while undergoing functional magnetic resonance imaging (fMRI). Univariate analyses found that mean right amygdala activity during the "afraid for self" context was negatively associated with CU traits. With the goal of disentangling idiosyncratic stimulus-driven neural responses, we employed intersubject representational similarity analysis to link intersubject similarities in multivoxel neural response patterns to contextualized fearful expressions with differential intersubject models of CU traits. Among low-CU adolescents, neural response patterns while viewing fearful faces were most consistently similar early in the visual processing stream and among regions implicated in affective responding, but were more idiosyncratic as emotional face information moved up the cortical processing hierarchy. By contrast, high-CU adolescents' neural response patterns consistently aligned along the entire cortical hierarchy (but diverged among low-CU youths). Observed patterns varied across contexts, suggesting that interpretations of fearful expressions depend to an extent on neural response patterns and are further shaped by levels of CU traits.

Highlights

Callous-unemotional (CU) traits are early-emerging personality features characterized by deficits in empathy, concern for others, and remorse following social transgressions (Frick & White, 2008)
Among the interpersonal deficits most consistently associated with CU traits are reduced behavioral and neurophysiological responsiveness to signs of others’ distress (Fanti et al, 2017; Jusyte, Mayer, Künzel, Hautzinger, & Schönenberg, 2015; Lozier et al, 2014; Marsh et al, 2008; Sebastian et al, 2014) as well as difficulty accurately interpreting these expressions (Dawel, O’Kearney, McKone, & Palermo, 2012; Marsh & Blair, 2008; Wilson, Juodis, & Porter, 2011)
Activation patterns in regions implicated in emotional face processing and perception (e.g., fusiform gyrus (FFG), STG, posterior superior temporal sulcus (pSTS)) and higher-level social cognition more often showed intersubject structure whereby high-CU adolescents were alike while others were more dissimilar

Summary

Introduction

Callous-unemotional (CU) traits are early-emerging personality features characterized by deficits in empathy, concern for others, and remorse following social transgressions (Frick & White, 2008). Functional coupling among face-selective regions shows evidence for hierarchical clustering roughly into three subnetworks likely corresponding to processing individual identity (e.g., inferior occipital gyri, FFG), retrieval of semantic knowledge (e.g., lPFC, inferior parietal sulci, supramarginal gyri), and representation of emotional information (e.g., mPFC, orbital frontal cortex, insula, superior temporal sulci, temporal pole) (Zhen, Fang, & Liu, 2013). These regions receive input from and send modulatory feedback to lower-level sensory areas, which may enable the derivation of socioaffective meaning from emotional face stimuli. This suggests the importance of understanding variation in neurophysiological responses to fearful expressions as a function of how these expressions are interpreted in high-CU youths

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Discussion

Conclusion