Amygdala and cortical gamma-band responses to emotional faces depend on the attended to valence

The amygdala is assumed to contribute to a bottom-up attentional bias during visual processing of emotional faces. Still, how its response to emotion interacts with top-down attention is not fully understood. It is also unclear if amygdala activity and scalp EEG respond to emotion and attention in a similar way. Therefore, we studied the interaction of emotion and attention during face processing in oscillatory gamma-band activity (GBA) in the amygdala and on the scalp. Amygdala signals were recorded via intracranial EEG (iEEG) in 9 patients with epilepsy. Scalp recordings were collected from 19 healthy participants. Three randomized blocks of angry, neutral, and happy faces were presented, and either negative, neutral, or positive expressions were denoted as targets. Both groups detected happy faces fastest and most accurately. In the amygdala, the earliest effect was observed around 170 ms in high GBA (105-117.5 Hz) when neutral faces served as targets. Here, GBA was higher for emotional than neutral faces. During attention to negative faces, low GBA (< 90 Hz) increased specifically for angry faces both in the amygdala and over posterior scalp regions, albeit earlier on the scalp (60 ms) than in the amygdala (210 ms). From 570 ms, amygdala high GBA (117.5-145 Hz) was also increased for both angry and neutral, compared to happy, faces. When positive faces were the targets, GBA did not differentiate between expressions. The present data reveal that attention-independent emotion detection in amygdala high GBA may only occur during a neutral focus of attention. Top-down threat vigilance coordinates widespread low GBA, biasing stimulus processing in favor of negative faces. These results are in line with a multi-pathway model of emotion processing and help specify the role of GBA in this process by revealing how attentional focus can tune timing and amplitude of emotional GBA responses.