Unseen fearful faces promote amygdala guidance of attention

Abstract

Little is known about the network of brain regions activated prior to explicit awareness of emotionally salient social stimuli. We investigated this in a functional magnetic resonance imaging study using a technique that combined elements of binocular rivalry and motion flash suppression in order to prevent awareness of fearful faces and houses. We found increased left amygdala and fusiform gyrus activation for fearful faces compared to houses, despite suppression from awareness. Psychophysiological interaction analyses showed that amygdala activation was associated with task-specific (fearful faces greater than houses) modulation of an attention network, including bilateral pulvinar, bilateral insula, left frontal eye fields, left intraparietal sulcus and early visual cortex. Furthermore, we report an unexpected main effect of increased left parietal cortex activation associated with suppressed fearful faces compared to suppressed houses. This parietal finding is the first report of increased dorsal stream activation for a social object despite suppression, which suggests that information can reach parietal cortex for a class of emotionally salient social objects, even in the absence of awareness.

Oxytocin Modulates Amygdala Reactivity to Masked Fearful Eyes

“…Under placebo conditions, we noted enhanced amygdala reactivity to fearful as compared with happy eye whites masked with a neutral face, thereby replicating previous studies' results (Straube et al, 2010;Whalen et al, 2004). In addition, we observed the same effect within the pulvinar that is known to be extensively interconnected with the amygdala both anatomically (Tamietto et al, 2012) and functionally (Morris et al, 1999;Troiani et al, 2014). These heightened neural responses occurred despite subjective unawareness of the presented stimuli.…”

Early Left Parietal Activity Elicited by Direct Gaze: A High-Density EEG Study

“…When testing hemianopic patients, the presentation of a visual stimulus associated at a prior stage with a threatening sound, in the blind field of the patients, induced an enhancement of left parietal cortex activation, in spite of a lack of stimulus awareness [88]. Furthermore, fearful faces presented without awareness activated the left posterior parietal region, too [89]. Thus, our results are consistent with a prominent role of the posterior parietal region encompassing the precuneus in the reflexive attention capture elicited by the highly biologically relevant and salient stimulus formed by direct gaze in humans [90].…”

“…An occipito-temporal visual pathway would be involved in the perceptual analysis of faces [112]. Another pathway, involving subcortical and cortical regions—including the amygdala, the pulvinar and the posterior parietal lobule—would subserve rapid, automatic (and potentially unconscious) orienting response to these stimuli [36, 89, 113–116]. This dual route view fits the two-process theory of face perception [117, 118], which was recently extended to eye contact detection [119].…”

Exposure to social-evaluative video clips: Neural, facial-muscular, and experiential responses and the role of social anxiety

“…It is a relatively robust finding in functional magnetic resonance imaging (fMRI) research, for instance, that the amygdala along with the fusiform gyrus, and temporal structures respond more to faces than objects (i.e., face selectivity, reviewed by Troiani, Price, & Schultz, 2014). The speed of this face selective system has been unraveled in electroencephalography (EEG) research where the N170, as the earliest component, has received much attention demonstrating increased negative amplitudes of faces compared to non-face objects (e.g., Blau, Maurer, Tottenham, & McCandliss, 2007;Wang, Miao, & Zhao, 2014).…”