Impaired threat prioritisation after selective bilateral amygdala lesions

Dominik R Bach,Rene Hurlemann,Raymond J Dolan

doi:10.1016/j.cortex.2014.08.017

Dominik R Bach, Rene Hurlemann + Show 1 more

Open Access

https://doi.org/10.1016/j.cortex.2014.08.017

Copy DOI

Abstract

The amygdala is proposed to process threat-related information in non-human animals. In humans, empirical evidence from lesion studies has provided the strongest evidence for a role in emotional face recognition and social judgement. Here we use a face-in-the-crowd (FITC) task which in healthy control individuals reveals prioritised threat processing, evident in faster serial search for angry compared to happy target faces. We investigate AM and BG, two individuals with bilateral amygdala lesions due to Urbach–Wiethe syndrome, and 16 control individuals. In lesion patients we show a reversal of a threat detection advantage indicating a profound impairment in prioritising threat information. This is the first direct demonstration that human amygdala lesions impair prioritisation of threatening faces, providing evidence that this structure has a causal role in responding to imminent danger.

Highlights

Extant theories implicate the amygdala in detection and prioritisation of threat-related information (LeDoux, 2000) and place it centre stage for disorders from the anxiety and fear spectrum
In this framework, probing detection of fearful faces does not address the question of threat detection
The detection of angry facial expression after human amygdala lesion has only been probed in social judgement tasks requiring explicit intensity rating (Adolphs et al, 1994), free verbal response (Becker et al, 2012), or explicit comparison of threat potential (Tsuchiya et al, 2009)

Summary

Introduction

Extant theories implicate the amygdala in detection and prioritisation of threat-related information (LeDoux, 2000) and place it centre stage for disorders from the anxiety and fear spectrum. Several human individuals with selective amygdala lesion (SM, AM, BG) are reported to be impaired in verbal recognition and intensity rating of fearful face expression when there are no time constraints (Adolphs, Tranel, Damasio, & Damasio, 1994; Becker et al, 2012), there is a spared ability in one of these individuals, SM, to detect fearful faces under time constraints, or when no explicit evaluation of the depicted emotion is required (Tsuchiya, Moradi, Felsen, Yamazaki, & Adolphs, 2009). The detection of angry facial expression after human amygdala lesion has only been probed in social judgement tasks requiring explicit intensity rating (Adolphs et al, 1994), free verbal response (Becker et al, 2012), or explicit comparison of threat potential (Tsuchiya et al, 2009). Given the amygdala damage in AM and BG, and the posited function of the amygdala in prioritising threat information, we hypothesised a reduced angry face advantage in the FITC task in AM and BG, compared to healthy individuals

Design

Participants

Analysis

Results

Discussion

Results within the control group