Individual differences in structural and functional connectivity predict speed of emotion discrimination

Abstract

In social interactions, individuals who are slower at differentiating between facial expressions signalling direct and indirect threat might be at a serious disadvantage.However, the neurobiological underpinnings of individual differences in face processing are not yet fully understood. The aim of this study was to use multimodal neuroimaging to investigate how the speed of emotion recognition is related to the structural and functional connectivity underlying the differentiation of direct and indirect threat displays. Our results demonstrate that individuals, who are faster at discriminating angry faces, engaged areas of the extended emotional system more strongly than individuals with slower reaction times, showed higher white matter integrity in the inferior longitudinal fasciculus, as well as stronger functional connectivity with the right amygdala. In contrast, individuals, who were faster at discriminating fearful faces, engaged visual-attentional regions outside of the face processing network more strongly than individuals with slower reaction times, showed higher white matter integrity in the inferior longitudinal fasciculus, as well as reduced functional connectivity with the right amygdala. Our findings suggest that the high survival value of rapid and appropriate responses to threat has defined but separate neurobiological correlates for angry and fearful facial expressions.

The neuroimaging and genetics of emotion perception in schizophrenia

“…For this purpose, we used a previously validated Dynamic Emotion Perception task, in which instruction cues were used to elicit prior expectations during viewing of angry, audio-visual videos . Based on the results of previous studies we predicted that faster recognition of threat congruent with prior expectations would involve the recruitment of rAMY functionally connecting to thalamus, as these are known to be involved in efficient threat processing (Bishop, 2008;Dolan and Vuilleumier, 2003;Marstaller et al, 2016;Vuilleumier and Pourtois, 2007). Conversely, faster recognition of threat incongruent with prior expectations would involve the recruitment of rTPJ (a core region of the ventral attention network (Corbetta et al, 2008)) functionally connecting to inferior frontal regions, such as vmPFC, previously implicated in rapid processing of unexpected threat (Corbetta et al, 2008;Decety and Lamm, 2007).…”

“…In our study, the selection of the seed voxels was both data-driven (please see Dzafic et al, 2016), and literature driven (Bishop, 2008;Vuilleumier & Pourtois, 2007;Marstaller et al, 2016;Corbetta, Patel, analyses, we correlated activity in the vmPFC, rAMY, and rTPJ with activity in the rest of the brain and with accurate RTs of the participants in the congruent and incongruent conditions. One participant was removed from the final analysis due to being an outlier (z-score < 3.25).…”

“…Connectivity between the amygdala and hippocampus has been strongly associated with contextual fear conditioning, in which participants are exposed to a particular context paired with a threatening stimulus, such as a shock, resulting in an automatic fear response during that specific context (Alvarez et al, 2008;Marstaller et al 2016). …”

“…The rAMY is argued to be involved in allocating processing resources to prioritize cues relevant in a given situation (Pessoa & Adolphs, 2010), and as such would facilitate rapid detection of threat, relevant for survival (Bishop, 2008;Marstaller et al, 2016;Vuilleumier and Pourtois, 2007).…”

“…Previous studies have consistently used static displays of anger to display threatening emotion (Marstaller et al, 2016;Ohman et al, 2001); and converging results implicate an amygdala and thalamus functional network as core circuitry in rapid threat processing, by means of selective processing of threatening cues Vuilleumier et al, 2001Vuilleumier et al, , 2003. In a recent multimodal neuroimaging, brain-behaviour study, Marstaller et al (2016) have shown that individuals who are faster at detecting 'direct' threat (i.e., anger), have greater engagement of a right amygdala functional network. Furthermore, Marstaller and colleagues identified that these individuals also have greater integrity in the inferior longitudinal fasciculus, a white matter pathway connecting the amygdala to visual regions.…”