Amygdala Responses to Fearful and Happy Facial Expressions under Conditions of Binocular Suppression

Abstract

The human amygdala plays a crucial role in processing affective information conveyed by sensory stimuli. Facial expressions of fear and anger, which both signal potential threat to an observer, result in significant increases in amygdala activity, even when the faces are unattended or presented briefly and masked. It has been suggested that afferent signals from the retina travel to the amygdala via separate cortical and subcortical pathways, with the subcortical pathway underlying unconscious processing. Here we exploited the phenomenon of binocular rivalry to induce complete suppression of affective face stimuli presented to one eye. Twelve participants viewed brief, rivalrous visual displays in which a fearful, happy, or neutral face was presented to one eye while a house was presented simultaneously to the other. We used functional magnetic resonance imaging to study activation in the amygdala and extrastriate visual areas for consciously perceived versus suppressed face and house stimuli. Activation within the fusiform and parahippocampal gyri increased significantly for perceived versus suppressed faces and houses, respectively. Amygdala activation increased bilaterally in response to fearful versus neutral faces, regardless of whether the face was perceived consciously or suppressed because of binocular rivalry. Amygdala activity also increased significantly for happy versus neutral faces, but only when the face was suppressed. This activation pattern suggests that the amygdala has a limited capacity to differentiate between specific facial expressions when it must rely on information received via a subcortical route. We suggest that this limited capacity reflects a tradeoff between specificity and speed of processing.

Cortico-subcortical visual, somatosensory, and motor activations for perceiving dynamic whole-body emotional expressions with and without striate cortex (V1)

“…Enhanced activity in this subcortical pathway has been repeatedly reported during nonconscious perception of static facial and whole-body expressions of fear and joy in blindsight patients (20,25,27) as well as in healthy subjects in whom nonconscious perception was induced by experimental manipulations such as visual masking (19,21,23), binocular rivalry (33,34), or flash suppression (35). Consistent with these data, recent anatomical studies revealed the existence of direct anatomical connections between the SC, Pulv, and Amg in nonhuman primates (36), and in vivo tractography found the same connections in healthy human subjects and in patient GY (37).…”

Fearful expressions gain preferential access to awareness during continuous flash suppression.

“…Other lesion studies have reported amygdala responsivity towards fearful or fear conditioned faces when presented in subjects' blind field (Morris et al, 2001) and during visual extinction (Vuilleumier et al, 2002). Neuroimaging studies have found similar results in amygdala activity using psychophysical techniques that manipulate subjects' awareness, including visual masking (Whalen, 1998;Whalen et al, 2004;Williams et al, 2006, but see Pessoa et al, 2006Phillips et al, 2004), and binocular rivalry (Pasley et al, 2004;Williams et al, 2004).…”

Perceptual Organization and Consciousness

“…Images of emotional faces rendered invisible through masking, can influence behavioural performance (Yang et al 2007;Faivre et al 2012;Almeida et al 2013) and produce brain activation in neuroimaging experiments linked to emotional processing, like enhanced amygdala responses to fearful faces (Williams et al 2004;de Gelder et al 2005). This suggests that the neural mechanisms required for detecting emotional expressions operate even when we are not aware of the stimulus.…”