Task-irrelevant fear enhances amygdala-FFG inhibition and decreases subsequent face processing

Abstract

Facial threat is associated with changes in limbic activity as well as modifications in the cortical face-related N170. It remains unclear if task-irrelevant threat modulates the response to a subsequent facial stimulus, and whether the amygdala's role in early threat perception is independent and direct, or modulatory. In 19 participants, crowds of emotional faces were followed by target faces and a rating task while simultaneous EEG-fMRI were recorded. In addition to conventional analyses, fMRI-informed EEG analyses and fMRI dynamic causal modeling (DCM) were performed. Fearful crowds reduced EEG N170 target face amplitudes and increased responses in a fMRI network comprising insula, amygdala and inferior frontal cortex. Multimodal analyses showed that amygdala response was present ∼60 ms before the right fusiform gyrus-derived N170. DCM indicated inhibitory connections from amygdala to fusiform gyrus, strengthened when fearful crowds preceded a target face. Results demonstrated the suppressing influence of task-irrelevant fearful crowds on subsequent face processing. The amygdala may be sensitive to task-irrelevant fearful crowds and subsequently strengthen its inhibitory influence on face-responsive fusiform N170 generators. This provides spatiotemporal evidence for a feedback mechanism of the amygdala by narrowing attention in order to focus on potential threats.

Neural activities during the Processing of unattended and unseen emotional faces: a voxel-wise Meta-analysis

“…Similar to certain sensory unawareness findings, attentional unawareness paradigms found stronger activations in frontal and temporal areas (e.g., Holtmann et al, 2013;Vuilleumier et al, 2001) and the amygdala (e.g., Schulte Holthausen et al, 2016;Pichon et al, 2012) for unattended emotional compared to neutral faces. Additional subcortical regions including the thalamus and the striatum showed stronger activity to unattended emotional compared to neutral faces (e.g., Holtmann et al, 2013).…”

Altered upright face recognition and presence of face inversion effect in temporal lobe epilepsy: An event‐related potential study

“…Anatomical connections between the amygdala and fusiform gyrus have been indicated by evaluating structural and functional connectivity in MRI studies . In a simultaneous EEG–fMRI study, task‐irrelevant fear enhanced amygdala‐fusiform gyrus inhibition and led to a reduced N170 amplitude . These prior studies support the explanation that patients with TLE exhibit functional abnormalities of the amygdala or fusiform gyrus, which result in face‐specific processing dysfunction, made evident by a reduced N170 amplitude.…”

Cumulative childhood interpersonal trauma is associated with reduced cortical differentiation between threat and non-threat faces in posttraumatic stress disorder adults

“…A possible explanation for attenuated N170 responses to emotion faces with greater CIT exposure is the inhibitory effect of amygdala activation over the fusiform gyrus (FFG), which has been demonstrated in healthy adults following fear priming (Schulte Holthausen et al, 2016). Reports of heightened amygdala activation to salient, non-threat stimuli in CIT-exposed youth and adults (Swartz et al, 2015; van Harmelen et al, 2013), and a dose–response relationship between left amygdala activation and cumulative CIT exposure (Maheu et al, 2010), suggest amygdala hyperactivation to emotion faces is likely in this sample of CIT-exposed PTSD adults.…”