Cody Cushing

Differential hemispheric and visual stream contributions to ensemble coding of crowd emotion

In crowds, where scrutinizing individual facial expressions is inefficient, humans can make snap judgments about the prevailing mood by reading ‘crowd emotion’. We investigated how the brain accomplishes this feat in a set of behavioural and functional magnetic resonance imaging studies. Participants were asked to either avoid or approach one of two crowds of faces presented in the left and right visual hemifields. Perception of crowd emotion was improved when crowd stimuli contained goal-congruent cues and was highly lateralized to the right hemisphere. The dorsal visual stream was preferentially activated in crowd emotion processing, with activity in the intraparietal sulcus and superior frontal gyrus predicting perceptual accuracy for crowd emotion perception, whereas activity in the fusiform cortex in the ventral stream predicted better perception of individual facial expressions. Our findings thus reveal significant behavioural differences and differential involvement of the hemispheres and the major visual streams in reading crowd versus individual face expressions.Im et al. examine how people process crowd facial expressions as opposed to individual ones, finding significant behavioural and neural differences.

Sex-related differences in behavioral and amygdalar responses to compound facial threat cues

During face perception, we integrate facial expression and eye gaze to take advantage of their shared signals. For example, fear with averted gaze provides a congruent avoidance cue, signaling both threat presence and its location, whereas fear with direct gaze sends an incongruent cue, leaving threat location ambiguous. It has been proposed that the processing of different combinations of threat cues is mediated by dual processing routes: reflexive processing via magnocellular (M) pathway and reflective processing via parvocellular (P) pathway. Because growing evidence has identified a variety of sex differences in emotional perception, here we also investigated how M and P processing of fear and eye gaze might be modulated by observers sex, focusing on the amygdala, a structure important to threat perception and affective appraisal. We adjusted luminance and color of face stimuli to selectively engage M or P processing and asked observers to identify emotion of the face. Female observers showed more accurate behavioral responses to faces with averted gaze and greater left amygdala reactivity both to fearful and neutral faces. Conversely, males showed greater right amygdala activation only for M‐biased averted‐gaze fear faces. In addition to functional reactivity differences, females had proportionately greater bilateral amygdala volumes, which positively correlated with behavioral accuracy for M‐biased fear. Conversely, in males only the right amygdala volume was positively correlated with accuracy for M‐biased fear faces. Our findings suggest that M and P processing of facial threat cues is modulated by functional and structural differences in the amygdalae associated with observers sex.

Neurodynamics and connectivity during facial fear perception: The role of threat exposure and signal congruity

Fearful faces convey threat cues whose meaning is contextualized by eye gaze: While averted gaze is congruent with facial fear (both signal avoidance), direct gaze (an approach signal) is incongruent with it. We have previously shown using fMRI that the amygdala is engaged more strongly by fear with averted gaze during brief exposures. However, the amygdala also responds more to fear with direct gaze during longer exposures. Here we examined previously unexplored brain oscillatory responses to characterize the neurodynamics and connectivity during brief (~250 ms) and longer (~883 ms) exposures of fearful faces with direct or averted eye gaze. We performed two experiments: one replicating the exposure time by gaze direction interaction in fMRI (N = 23), and another where we confirmed greater early phase locking to averted-gaze fear (congruent threat signal) with MEG (N = 60) in a network of face processing regions, regardless of exposure duration. Phase locking to direct-gaze fear (incongruent threat signal) then increased significantly for brief exposures at ~350 ms, and at ~700 ms for longer exposures. Our results characterize the stages of congruent and incongruent facial threat signal processing and show that stimulus exposure strongly affects the onset and duration of these stages.

Differential hemispheric and visual stream involvement in ensemble coding of emotion in facial crowds

The visual system takes advantage of redundancies in the scene by extracting summary statistics from groups of similar items. Similary, in social situations, we routinely make snap judgments of crowds of people. Reading “crowd emotion” is critical for guiding us away from danger (e.g., mass panic or violent mobs) and towards help from friendly groups. Scrutinizing each individual’s expression would be too slow and inefficient. How the brain accomplishes this feat, however, remains unaddressed. Here we report a set of behavioral and fMRI studies in which participants made avoidance or approach decisions by choosing between two facial crowds presented in the left and right visual fields (LVF/RVF). Behaviorally, participants were most accurate for crowds containing task-relevant cues-avoiding angry crowds/approaching happy crowds. This effect was amplified by sex-linked facial cues (angry male/happy female crowds), and highly lateralized with greater recognition of task-congruent stimuli presented in LVF. In a related fMRI study, the processing of facial crowds evoked right-lateralized activations in the dorsal visual stream, whereas similar processing of single faces preferentially activated the ventral stream bilaterally. Our results shed new light on our understand of ensemble face coding, revealing qualitatively different mechanisms involved in reading crowd vs. individual emotion.

Anxiety Modulates Perception Of Facial Fear In A Pathway-Specific, Lateralized, Manner

Facial expression and eye gaze provide a shared signal about threats. While averted-gaze fear clearly points to the source of threat, direct-gaze fear renders the source of threat ambiguous. Dual processing routes have been proposed to mediate these processes: reflexive processing via magnocellular (M-) pathway and reflective processing via parvocellular (P-) pathway. We investigated how observers’ trait anxiety modulates Mand P-pathway processing of clear and ambiguous threat cues. We performed fMRI on a large cohort (N=108) widely ranging in trait anxiety while they viewed fearful or neutral faces with averted or directed gaze. We adjusted luminance and color of the stimuli to selectively engage M- or P-pathway processing. We found that higher anxiety facilitated processing of averted-gaze fear projected to M-pathway, but impaired perception of direct-gaze fear projected to P-pathway. Increased right amygdala reactivity was associated with higher anxiety, only for averted-gaze fear presented to M-pathway. Conversely, increased left amygdala reactivity was associated with higher anxiety for P-biased, direct-gaze fear. This lateralization was more pronounced with higher anxiety. Our findings suggest that trait anxiety has differential effects on perception of clear and ambiguous facial threat cues via selective engagement of M and P pathways and lateralization of amygdala reactivity.

Observer’s anxiety facilitates magnocellular processing of clear facial threat cues, but impairs parvocellular processing of ambiguous facial threat cues

Facial expression and eye gaze provide a shared signal about threats. While a fear expression with averted gaze clearly points to the source of threat, direct-gaze fear renders the source of threat ambiguous. Separable routes have been proposed to mediate these processes, with preferential attunement of the magnocellular (M) pathway to clear threat, and of the parvocellular (P) pathway to threat ambiguity. Here we investigated how observers’ trait anxiety modulates M- and P-pathway processing of clear and ambiguous threat cues. We scanned subjects (N = 108) widely ranging in trait anxiety while they viewed fearful or neutral faces with averted or directed gaze, with the luminance and color of face stimuli calibrated to selectively engage M- or P-pathways. Higher anxiety facilitated processing of clear threat projected to M-pathway, but impaired perception of ambiguous threat projected to P-pathway. Increased right amygdala reactivity was associated with higher anxiety for M-biased averted-gaze fear, while increased left amygdala reactivity was associated with higher anxiety for P-biased, direct-gaze fear. This lateralization was more pronounced with higher anxiety. Our findings suggest that trait anxiety differentially affects perception of clear (averted-gaze fear) and ambiguous (direct-gaze fear) facial threat cues via selective engagement of M and P pathways and lateralized amygdala reactivity.