The role of human basolateral amygdala in ambiguous social threat perception

Abstract

Previous studies have shown that the amygdala (AMG) plays a role in how affective signals are processed. Animal research has allowed this role to be better understood and has assigned to the basolateral amygdala (BLA) an important role in threat perception. Here we show that, when passively exposed to bodily threat signals during a facial expressions recognition task, humans with bilateral BLA damage but with a functional central-medial amygdala (CMA) have a profound deficit in ignoring task-irrelevant bodily threat signals.

Introduction

It is a common experience that an angry face feels more menacing when accompanied by a pair of fists, but it is rather unsettling when the fists come with a smile. In that case we experience the overall signal as profoundly ambiguous. When instructed to attend to only the facial expression, the brain notices the conflict between the facial expression and the accompanying bodily expression in a matter of milliseconds (Meeren, van Heijnsbergen, & de Gelder, 2005).

A variety of functions related to affective processes have been attributed to the amygdala (AMG) including immediate perception of affective stimuli, learning and conditioning, as well as emotional memory (Phelps & LeDoux, 2005). The AMG is also involved in modulating behavioral responses and has multiple connections to brain areas directly involved in behavioral output (Mosher, Zimmerman, & Gothard, 2010). There is also overwhelming evidence that the AMG plays an important role in regulating emotion perception and preparing adapted motor behavior (Phelps & LeDoux, 2005).

Previous research has shown that the AMG plays an important role in face (Costafreda, Brammer, David, & Fu, 2008) and body (de Gelder, Snyder, Greve, Gerard, & Hadjikhani, 2004) expression recognition and is also highly sensitive to ambiguous signals (Kim et al., 2004, Whalen, 1998). But further progress in understanding the AMG will require understanding the specific contribution of the multiple nuclei of the AMG. Functions or loss of functions ascribed to the AMG as a whole may in fact result from activation of AMG nuclei or inter- and intra-amygdala connectivity. For example, facial expression recognition has been attributed to the AMG as a whole (Rutishauser et al., 2011) and consequently it was assumed that AMG damage abolishes this (Adolphs, Tranel, Damasio, & Damasio, 1994, but see Tsuchiya, Moradi, Felsen, Yamazaki, & Adolphs, 2009). But more recently it was shown that an impairment of one of the AMG nuclei, the basolateral amygdala (BLA), leads to hypersensitivity for facial fear expressions (Terburg et al., 2012).

Similarly, the same complete AMG impairment does not seems to abolish body expression recognition (Atkinson, Heberlein, & Adolphs, 2007). This finding does not rule out that an impairment of a specific nucleus of the AMG does nevertheless have consequences for normal processing of body expressions. In the case of a complex structure like the AMG a functional role attributed to the AMG as a whole cannot be attributed automatically to each of its subnuclei.

We addressed the issue of the functional role of the BLA in ambiguous social threat perception using subjects with Urbach–Wiethe disease (UWD), a rare genetic disorder that in our sample has resulted in bilateral focal calcification of the BLA. We tested three subjects from the South African UWD cohort (Thornton et al., 2008) selected for this specific BLA damage (Morgan, Terburg, Thornton, Stein, & van Honk, 2012) and a group of matched controls on a series of face and body expression recognition tasks. Our goal was first, to investigate the specific role of the BLA in implicit bodily expression recognition and second, the role of the BLA in ambiguity perception. We used angry and fearful Face Body Compounds created by combining a facial expression with either a congruent or incongruent bodily expression. Using convergent evidence from behavior and eye tracking measures, we investigated how BLA damage affects the processing of affective information from body expressions of anger and fear that are, unattended, not task relevant, and presented in the periphery. We conjectured that under these conditions of implicit perception participants with BLA damage would still process the threatening body signals and these signals would be more salient than in normal controls. Therefore we expect an increased effect from threatening bodily expressions on facial expression perception in the UWD group.