Mode of Functional Connectivity in Amygdala Pathways Dissociates Level of Awareness for Signals of Fear

Abstract

Many of the same regions of the human brain are activated during conscious attention to signals of fear and in the absence of awareness for these signals. The neural mechanisms that dissociate level of awareness from activation in these regions remain unknown. Using functional magnetic resonance imaging with connectivity analysis in healthy human subjects, we demonstrate that level of awareness for signals of fear depends on mode of functional connectivity in amygdala pathways rather than discrete patterns of activation in these pathways. Awareness for fear relied on negative connectivity within both cortical and subcortical pathways to the amygdala, suggesting that reentrant feedback may be necessary to afford such awareness. In contrast, responses to fear in the absence of awareness were supported by positive connections in a direct subcortical pathway to the amygdala, consistent with the view that excitatory feedforward connections along this pathway may be sufficient for automatic responses to "unseen" fear.

From affective blindsight to emotional consciousness

“…By contrast, the major cortical pathway relaying visual input to the amygdala does not show substantial activity and functional connectivity under the same conditions but does so during conscious perception of emotional stimuli (Pasley, Mayes, & Schultz, 2004;Williams et al, 2006). Not surprisingly, similar findings have been reported in patients with affective blindsight in response to unseen facial and bodily expressions and indicate that a functional subcortical pathway to the amygdala is engaged during nonconscious emotion perception (de Gelder et al, 2005;Morris et al, 2001;Pegna et al, 2005;Van den Stock et al, 2011.…”

“…Neuroimaging data on healthy subjects in whom nonconscious perception of emotions had been induced by experimental manipulations such as visual masking, flash suppression, or spatial filtering have revealed that the superior colliculus, pulvinar and amygdala constitute a functional network that shows increased, positive covariation of activity in response to nonconsciously perceived fearful facial expressions (Liddell et al, 2005;Morris et al, 1999;Vuilleumier et al, 2003;Whalen et al, 1998Whalen et al, , 2004Williams et al, 2006). By contrast, the major cortical pathway relaying visual input to the amygdala does not show substantial activity and functional connectivity under the same conditions but does so during conscious perception of emotional stimuli (Pasley, Mayes, & Schultz, 2004;Williams et al, 2006).…”

Faces, Bodies, Social Vision as Agent Vision, and Social Consciousness

“…The latter may have become impossible due to brain damage, as in the rare cases of selective striate cortex damage, or because awareness is prevented by experimental manipulation; most typically visual masking (Dimberg et al, 2000;Esteves, Dimberg, & Öhman, 1994;Jolij & Lamme, 2005;Killgore & Yurgelun-Todd, 2004;Liddell et al, 2005;Morris, Ohman et al, 1998;Murphy & Zajonc, 1993;Niedenthal, 1990;Pessoa, Japee, Sturman, & Ungerleider, 2006;Pessoa, Japee, & Ungerleider, 2005;Tamietto & de Gelder, 2008a;Whalen et al, 2004;Whalen et al, 1998b;Williams et al, 2006;Williams et al, 2004). This suggests that there might be a nonconscious perceptual subsystem for visually based affect experience and cognition.…”

“…Even though the presentation of affective stimuli to the blind fields of other patients also activated subcortical structures like the amygdala, the functional or anatomical connectivity of the different structures putatively implicated along this route have not been directly tested in patients different from GY. Interestingly, however, subliminal emotional expressions activate in healthy subjects the same subcortical pathway that is the most likely candidate in affective blindsight following striate cortex lesions (Liddell et al, 2005;Morris et al, 1999;Williams et al, 2006). Studies that will trace the pathways involved in noncortical processing are now under way using tractography methods like …”

Common regions of dorsal anterior cingulate and prefrontal–parietal cortices provide attentional control of distracters varying in emotionality and visibility

“…This issue has direct implications for the understanding of a variety of psychiatric disorders including anxiety disorders and posttraumatic stress disorder. Individuals with these disorders are characterized by increased susceptibility to emotional interference relative to healthy individuals (Armony et al, 2005;Phan et al, 2006;Williams et al, 2006) even when the emotional stimuli are subliminal (Armony et al, 2005;Bradley et al, 1995;Mineka & Ohman, 2002;Mogg et al, 1993). It is important to determine whether there are systems which specifically respond to emotional distracters (and which, when dysfunctional, might lead to this increased susceptibility in anxiety disorders) or whether responding to emotional distracters recruits general attentional systems (indicating more general attentional difficulties in anxiety disorders or that the increased susceptibility reflects increased emotional responding).…”