Attentional bias towards and away from fearful faces is modulated by developmental amygdala damage

Abstract

The amygdala is believed to play a major role in orienting attention towards threat-related stimuli. However, behavioral studies on amygdala-damaged patients have given inconsistent results—variously reporting decreased, persisted, and increased attention towards threat. Here we aimed to characterize the impact of developmental amygdala damage on emotion perception and the nature and time-course of spatial attentional bias towards fearful faces. We investigated SF, a 14-year-old with selective bilateral amygdala damage due to Urbach–Wiethe disease (UWD), and ten healthy controls. Participants completed a fear sensitivity questionnaire, facial expression classification task, and dot-probe task with fearful or neutral faces for spatial cueing. Three cue durations were used to assess the time-course of attentional bias. SF expressed significantly lower fear sensitivity, and showed a selective impairment in classifying fearful facial expressions. Despite this impairment in fear recognition, very brief (100 msec) fearful cues could orient SF's spatial attention. In healthy controls, the attentional bias emerged later and persisted longer. SF's attentional bias was due solely to facilitated engagement to fear, while controls showed the typical phenomenon of difficulty in disengaging from fear. Our study is the first to demonstrate the separable effects of amygdala damage on engagement and disengagement of spatial attention. The findings indicate that multiple mechanisms contribute in biasing attention towards fear, which vary in their timing and dependence on amygdala integrity. It seems that the amygdala is not essential for rapid attention to emotion, but probably has a role in assessment of biological relevance.

Bilateral amygdala damage linked to impaired ability to predict others' fear but preserved moral judgements about causing others fear

“…These responses are consistent with SM's own self-report; she has been held at gunpoint and physically assaulted in the past, and reports feeling calm, not afraid, during those experiences [6]. The observed deficits are consistent with prior evidence that the amygdala is recruited specifically when evaluating fear-eliciting statements [36,37], and closely mirrors social fear recognition deficits observed when individuals with amygdala lesions evaluate facial, vocal, postural and musical expressions of emotion [10,11,15,16,49,50]. Together, these findings support the amygdala's hypothesized role in coordinating internal representations of fear, which incorporate episodic, sensory and interoceptive information.…”

“…Acquired amygdala damage reliably impairs fear conditioning, and behavioural, physiological and (in humans and perhaps other species, subjective) responses to threats [6][7][8][9]. These impairments are typically paralleled by deficits in social recognition of others' fear (but typically not other emotions) across multiple cues and modalities, including facial expressions, vocal tones, body postures and musical compositions [10][11][12][13][14][15][16][17]. Various theories aimed at explaining these paired deficits in fear responding and social fear recognition do not capture some portion of the observed findings.…”

Social attention in children with epilepsy

“…27 Beyond evidence of age-related reductions in processing speed, delayed disengagement was also linked to increased epilepsy duration, pointing toward deleterious effects of continuing epileptiform activity on this cortical -subcortical functional integration. The amygdala is implicated in engagement and disengagement components of fear-related spatial orienting, 35 and it is important for future research to delineate amygdala hyperactivity versus weakened top-down control underlying this observed fear-related attentional bias in children with epilepsy.…”

The Role of Amygdala in Self-Conscious Emotions in a Patient With Acquired Bilateral Damage

“…Healthy control samples included 13 age- and education-matched healthy male individuals (age: 48.6 ± 9.3, education: 13.8 ± 3.2, MMSE: 29.5 ± 0.5) who were tested on all the experimental tasks, as well as on Positive and Negative Affect Schedule (PANAS) and TOSCA. The sample size of the healthy control group was chosen based on previous single-case studies in the field of emotion processing ( Pishnamazi et al, 2016 ; Bennetts et al, 2017 ; Bach et al, 2019 ).…”