Intersubject variability in fearful face processing: the linkbetween behavior and neural activation

Abstract

Stimuli that signal threat show considerable variability in the extent to which they enhance behavior, even among healthy individuals. However, the neural underpinning of this behavioral variability is not well understood. By manipulating expectation of threat in an fMRI study of fearful vs. neutral face categorization, we uncovered a network of areas underlying variability in threat processing in healthy adults. We explicitly altered expectation by presenting face images at three different expectation levels: 80%, 50%, and 20%. Subjects were instructed to report as fast and as accurately as possible whether the face was fearful (signaled threat) or not. An uninformative cue preceded each face by 4 seconds (s). By taking the difference between response times (RT) to fearful compared to neutral faces, we quantified an overall fear RT bias (i.e. faster to fearful than neutral faces) for each subject. This bias correlated positively with late trial fMRI activation (8 s after the face) during unexpected fearful face trials in bilateral ventromedial prefrontal cortex, the left subgenual cingulate cortex, and the right caudate nucleus and correlated negatively with early trial fMRI activation (4 s after the cue) during expected neutral face trials in bilateral dorsal striatum and the right ventral striatum. These results demonstrate that the variability in threat processing among healthy adults is reflected not only in behavior but also in the magnitude of activation in medial prefrontal and striatal regions that appear to encode affective value.

Nasal Respiration Entrains Human Limbic Oscillations and Modulates Cognitive Function

“…That rhythmic breathing paces electrical activity in the human brain to modulate behavior raises the intriguing possibility that other physiological and autonomic rhythms, and even periodic sampling in other sensory domains (Kepecs et al, 2006;Moore et al, 2013;Ito et al, 2014), might also shape neuronal oscillations to optimize human perception, emotion, and cognition. We would note that, while the effect sizes of our behavioral results are relatively modest (e.g., a 28 ms difference between fear inhalation and fear exhalation for the nasal route; a 60 ms difference between fear inhalation/exhalation for the nasal vs oral route), the magnitude of the changes is on par with those found in many other cognitive studies examining the effects of facial emotion on perceptual discrimination, with differences typically in the range of 20 -100 ms (Doty et al, 2014;Li et al, 2014;Ye et al, 2014).…”

Toward a Social Psychophysics of Face Communication

“…In the field of social face perception, researchers tend to use specific sets of standardized stimuli (e.g., Beaupré et al 2000, Langner et al 2010, Lundqvist et al 1998, Matsumoto & Ekman 1988 to probe different social perceptions and their associated brain activities (Doty et al 2014). However, classic use of these stimuli cannot identify the information ontology of a social perceptioni.e., what stimulus information is driving behavior (or brain activity).…”

The neuroimaging and genetics of emotion perception in schizophrenia

“…We investigated the functional connectivity of the vmPFC, rAMY and rTPJ, with strong evidence for involvement of these brain regions in emotion perception influenced by prior expectations (Barbalat et al, 2013;Doty et al, 2014;Dzafic et al, 2016). In line with our hypotheses, our findings show that facilitation of response to threat congruent with prior expectations was associated with a subcortical network functionally connected to rAMY.…”

“…Functional networks were mapped for the three seed regions identified in Chapter1, the vmPFC, rAMY and rTPJ . Previous literature has implicated these regions in threat processing (Doty et al, 2014;Marstaller et al, 2016) and rapid re-orienting of attention to relevant stimuli (Corbetta et al, 2008). I found that faster recognition of congruent threat was associated with a subcortical network functionally connected to rAMY, implicated in fear conditioning and rapid processing of coarse emotional cues.…”

“…For instance, a functional connectivity study found that threatening emotions congruent with prior expectations engage a vmPFC network (Barbalat et al, 2013), but a brain-behaviour study found that faster detection of threatening emotions incongruent with prior expectations was related to vmPFC activity (Doty et al, 2014).…”