Impaired emotional biases in visual attention after bilateral amygdala lesion

Abstract

It is debated whether the amygdala is critical for the emotional modulation of attention. While some studies show reduced attentional benefits for emotional stimuli in amygdala-damaged patients, others report preserved emotional effects. Various factors may account for these discrepant findings, including the temporal onset of the lesion, the completeness and severity of tissue damage, or the extent of neural plasticity and compensatory mechanisms, among others. Here, we investigated a rare patient with focal acute destruction of bilateral amygdala and adjacent hippocampal structures after late-onset herpetic encephalitis in adulthood. We compared her performance in two classic visual attention paradigms with that of healthy controls. First, we tested for any emotional advantage during an attentional blink task. Whereas controls showed better report of fearful and happy than neutral faces on trials with short lags between targets, the patient showed no emotional advantage, but also globally reduced report rates for all faces. Second, to ensure that memory disturbance due to hippocampal damage would not interfere with report performance, we also used a visual search task with either emotionally or visually salient face targets. Although the patient still exhibited efficient guided search for visually salient, non-emotional faces, her search slopes for emotional versus neutral faces showed no comparable benefit. In both tasks, however, changes in the patient predominated for happy more than fear stimuli, despite her normal explicit recognition of happy expressions. Our results provide new support for a causal role of the amygdala in emotional facilitation of visual attention, especially under conditions of increasing task-demands, and not limited to negative information. In addition, our data suggest that such deficits may not be amenable to plasticity and compensation, perhaps due to sudden and late-onset damage occurring in adulthood.