Amygdala, pulvinar, and inferior parietal cortex contribute to early processing of faces without awareness

Abstract

The goals of the present study were 2-fold. First, we wished to investigate the neural correlates of stimulus-driven processing of stimuli strongly suppressed from awareness and in the absence of top-down influences. We accomplished this using a novel approach in which participants performed an orthogonal task atop a flash suppression noise image to prevent top-down search. Second, we wished to investigate the extent to which amygdala responses differentiate between suppressed stimuli (fearful faces and houses) based on their motivational relevance. Using continuous flash suppression (CFS) in conjunction with fMRI, we presented fearful faces, houses, and a no stimulus control to one eye while participants performed an orthogonal task that appeared atop the flashing Mondrian image presented to the opposite eye. In 29 adolescents, we show activation in subcortical regions, including the superior colliculus, amygdala, thalamus, and hippocampus for suppressed objects (fearful faces and houses) compared to a no stimulus control. Suppressed stimuli showed less activation compared to a no stimulus control in early visual cortex (EVC), indicating that object information was being suppressed from this region. Additionally, we find no activation in regions associated with conscious processing of these percepts (fusiform gyrus and/or parahippocampal cortex) as assessed by mean activations and multi-voxel patterns. A psychophysiological interaction analysis (PPI) that seeded the amygdala showed task-specific (fearful faces greater than houses) modulation of right pulvinar and left inferior parietal cortex. Taken together, our results support a role for the amygdala in stimulus-driven attentional guidance toward objects of relevance and a potential mechanism for successful suppression of rivalrous stimuli.

Preferential awareness of protofacial stimuli in autism

“…This suggests that the primary sensitivity to protofaces, possibly supported by the subcortical face detection pathway Mondloch et al, 1999;, is intact in individuals with ASD. As the pattern of neural activity under CFS resembles brain function in newborns, with visual cortex activity being significantly suppressed during CFS (Hesselmann et al, 2011;Yuval-Greenberg & Heeger, 2013) while subcortical regions continue to respond to facial stimuli despite CFS (Jiang & He, 2006;Troiani & Schultz, 2013), this result could suggest that sensitivity to protofacial stimuli is intact in individuals with ASD from their early infancy, although the present study did not test infants.…”

“…rendered invisible) for several seconds, enabling researchers to study the processes that precede and lead to stimulus awareness for complex stimuli such as faces (Axelrod, Bar, & Rees, 2015) over extended periods of time. During CFS, visual cortex responses to the target are strongly suppressed (Hesselmann, Hebart, & Malach, 2011;Yuval-Greenberg & Heeger, 2013), while subcortical regions exhibit comparably robust responses to facial stimuli (Jiang & He, 2006;Troiani & Schultz, 2013). This pattern of activation bears a striking similarity to the structure of the newborn brain, in which subcortical regions are already well developed but cortical regions are anatomically (Barkovich, Kjos, Jackson, & Norman, 1988;Paus et al, 2001) and functionally immature (Muir, Clifton, & Clarkson, 1989).…”

“…Indeed, for TD adults in the breaking CFS task (Jiang, Costello, & He, 2007), upright protofaces overcome CFS and emerge into awareness more quickly than inverted protofaces (Stein, Peelen, & Sterzer, 2011). This preferential processing of protofacial stimuli under CFS in adults is similar to newborns' looking preferences, suggesting that preferential responses in both adults and newborns are based on the same inborn face detection system involving subcortical regions such as the amygdala and pulvinar (Jiang & He, 2006;Johnson, 2005;Troiani & Schultz, 2013). Moreover, research using CFS to study access to awareness of protoface stimuli in individuals with ASD will provide new insight into the basic perceptual mechanisms of face processing in ASD that goes beyond previous studies on attentional orienting to protofaces (Shah et al, 2013), as attention and conscious awareness are thought to be related but distinct processes (Koch & Tsuchiya, 2007;Lamme, 2003).…”

Dichoptic Viewing Methods for Binocular Rivalry Research: Prospects for Large-Scale Clinical and Genetic Studies

“…Crosstalk is therefore an important criterion when evaluating dichoptic viewing methods to present binocular illusions for the purpose of examining non-conscious processing. To date, the level of crosstalk across different display methods and its effect on CFS and BSS suppression dynamics has not yet been investigated (see Troiani & Schultz, 2013). Crosstalk is also a particular concern in studies that record highly sensitive measures (e.g., galvanic skin response) and where there is no established testing protocol to verify image suppression during each viewing trial.…”

“…For CFS and related phenomena, fMRI studies have used anaglyphs (Bahrami et al, 2007;Jiang & He, 2006;Tse et al, 2005;Vizueta et al, 2012;Watanabe et al, 2011;Williams et al, 2004), the mirror stereoscope , prism stereoscopes (Schurger et al, 2010;Yuval-Greenberg & Heeger, 2013) and HMDs (Troiani & Schultz, 2013).…”