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

Abstract

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 observer's 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 observer's sex.

Fast saccadic and manual responses to faces presented to the koniocellular visual pathway

“…The P pathway, formed from the midget retinal ganglion cells that combine the inputs of L and M cones in color-opponent fashion (i.e., L-M), is sensitive to color in the green-to-red range, and can resolve higher spatial and low temporal frequencies. We found it to be more attuned to incongruent threat cue combinations of facial expression and eye gaze (Cushing et al, in press;Im et al, 2017;Im et al, 2018). The third, K pathway, formed from the tiny, speck-like retinal ganglion cells that combine the inputs of short-wavelength sensitive (S) cones with the combined inputs of long and medium wavelength cones (i.e., S - [L+M]), has received less attention than the M and P pathways until relatively recently (Casagrande, 1994;Hendry & Reid, 2000).…”

“…It can resolve low and middle spatial frequencies and high temporal frequencies. We have found the M pathway to be more engaged by clear threat cues conveyed by congruent facial expression and eye gaze (Cushing et al, 2019;Im et al, 2017;Im et al, 2018) and clear threat in visual scenes (Kveraga, 2014). The P pathway, formed from the midget retinal ganglion cells that combine the inputs of L and M cones in color-opponent fashion (i.e., L-M), is sensitive to color in the green-to-red range, and can resolve higher spatial and low temporal frequencies.…”

“…Recently, we have demonstrated that two of the major visual pathways, the M and P pathways, are attuned to somewhat different aspects of face perception (Adams et al, 2019;Cushing et al, 2019;Im et al, 2018;Im et al, 2017). The M pathway, which is formed from the large retinal ganglion cells that combine the inputs of long (L) and medium (M) wavelength cones (i.e., L + M) and some rod contributions, is largely insensitive to color but has high gain and sensitivity to small Citation: Kveraga, K., Im, H. Y., Ward, N., & Adams, R. B.…”

“…Given its putative role in threat detection (Isbell, 2006;Van Le et al, 2013), we predicted that stimuli presented to the K pathway would evoke faster saccadic and manual responses, compared to stimuli presented to the M or P pathways. The threat cues present in faces can be dynamic and fleeting, such as anger or fear expressions that respectively signal danger to the observer and the expresser, with the threat locus indicated by overt attention cues such as eye gaze direction Adams et al, 2012;Cushing et al, 2018;Cushing et al, 2019;Im et al, 2017;Im et al, 2018). Facial threat cues also can be more stable or static, inherent in the facial configuration and texture associated with higher masculinity, such as a low, pronounced brow ridge, small eyes, a prominent jaw, facial hair, and a high facial width-to-height ratio (Zebrowitz & Collins, 1997;Zebrowitz & Montepare, 2008).…”

“…To test these hypotheses, we designed a task in which human observers viewed neutral or angry faces that were male or female and varied in masculinity across the stimulus set. The face stimuli were individually calibrated (see Methods) for each observer so as to bias processing towards the M, P, or K pathways, using procedures previously used in (Anstis & Cavanagh, 1983;Cushing et al, 2019;Im et al, 2017;Im et al, 2018;Kveraga, 2014;Kveraga et al, 2007;Thomas et al 2012) and were briefly presented to the left or right of the central fixation cross. We instructed observers to fixate in the center at the start of a trial, and then to categorize the face as angry or neutral, reporting their decision with a key press as quickly and accurately as possible.…”