Amygdala and cortical gamma-band responses to emotional faces are modulated by attention to valence.

The amygdala might support an attentional bias for emotional faces. However, whether and how selective attention toward a specific valence modulates this bias is not fully understood. Likewise, it is unclear whether amygdala and cortical signals respond to emotion and attention in a similar way. We recorded gamma-band activity (GBA, > 30 Hz) intracranially in the amygdalae of 11 patients with epilepsy and collected scalp recordings from 19 healthy participants. We presented angry, neutral, and happy faces randomly, and we denoted one valence as the target. Participants detected happy targets most quickly and accurately. In the amygdala, during attention to negative faces, low gamma-band activity (LGBA, < 90 Hz) increased for angry compared with happy faces from 160 ms. From 220 ms onward, amygdala high gamma-band activity (HGBA, > 90 Hz) was higher for angry and neutral faces than for happy ones. Monitoring neutral faces increased amygdala HGBA for emotions compared with neutral faces from 40 ms. Expressions were not differentiated in GBA while monitoring positive faces. On the scalp, only threat monitoring resulted in expression differentiation. Here, posterior LGBA was increased selectively for angry targets from 60 ms. The data show that GBA differentiation of emotional expressions is modulated by attention to valence: Top-down-controlled threat vigilance coordinates widespread GBA in favor of angry faces. Stimulus-driven emotion differentiation in amygdala GBA occurs during a neutral attentional focus. These findings align with a multi-pathway model of emotion processing and specify the role of GBA in this process.

Emotion and attention in face processing: Complementary evidence from surface event-related potentials and intracranial amygdala recordings.

Face processing is biased by emotional and voluntarily directed attention, both of which modulate processing in distributed cortical areas. The amygdala is assumed to contribute to an attentional bias for emotional faces, although its interaction with directed attention awaits further clarification. Here, we studied the interaction of emotion and attention during face processing via scalp EEG potentials of healthy participants and intracranial EEG (iEEG) recordings of the right amygdala in one patient. Three randomized blocks consisting of angry, neutral, and happy facial expressions were presented, and one expression was denoted as the target category in each block. Happy targets were detected fastest and most accurately both in the group study and by the iEEG patient. Occipital scalp potentials revealed emotion differentiation for happy faces in the early posterior negativity (EPN) around 300 ms after stimulus onset regardless of the target condition. A similar response to happy faces occurred in the amygdala only for happy targets. On the scalp, a late positive potential (LPP, around 600 ms) enhancement for targets occurred for all target conditions alike. A simultaneous late signal in the amygdala was largest for emotional targets. No late signal enhancements were found for neutral targets in the amygdala. Cortical modulations, by contrast, showed both attention-independent effects of emotion and emotion-independent effects of attention. These results demonstrate an attention-dependence of amygdala activity during the processing of facial expressions and partly independent cortical mechanisms.