The current study revealed the predicted interaction between culture of participant and culture of stimulus in a number of regions involving face, gaze and emotion processing, including the bilateral fusiform gyri, left posterior cingulate, bilateral thalamus, left insula, right caudate, left inferior frontal gyrus, and left ventro- and dorsolateral prefrontal cortices. Helping explain the interaction effects within these regions was the relative increase in activation to direct- versus averted-gaze fear expressions in both Japanese and US Caucasian participants when viewing other-culture faces, and the relative increase in activation to averted- versus direct-gaze fear expressions in both cultural groups when viewing same-culture faces. This general pattern was also apparent when we examined activation within the anatomically defined region of bilateral amygdalae. Thus, this analysis replicates Hadjikhani et al.
) finding for greater averted- versus direct-gaze fear activation in US Caucasian participants viewing same-culture fear faces. For Japanese participants, however, no differences were found in processing averted- and direct-gaze same-culture fear faces in the amygdala. Given evidence for differences in neural activation that favor direct- versus averted-gaze in Japanese participants and stimuli, it may be that the differences found here were attenuated for Japanese participants due to the cultural meaning applied to direct gaze in Japanese culture. Direct eye gaze could have been construed as a threatening social cue when viewed in the context of a fear expression. Notably, both Japanese and US Caucasian participants showed similar amygdala responses to other-culture faces, with greater responsivity to direct- relative to averted-gaze fear faces. This latter effect is consistent with evidence for more amygdala activation in response to direct- relative to averted-gaze displays when viewing other-race faces (Richeson et al.
There were also a number of regions related to face and eye gaze processing activated by the main effect of stimulus culture, including bilateral fusiform gyri, bilateral inferior temporal gyri, and bilateral angular gyri. Physiognomic differences in prototypical race appearance, such as eye size (see Zebrowitz, 1997
) and brow height (Keating, Mazur, and Segall, 1977
), could arguably be a source of such variation; however, our dependent variable of interest was computed as the direct comparison of direct and averted eye gaze on otherwise identical faces and expressions, thereby ruling out such explanations. The differences in activation necessarily reflect different processing of gaze behavior in the context of fear faces across the two cultures. Specifically, all participants showed greater activation to direct- relative to averted-gaze when displayed on Japanese faces, whereas the opposite was true for US Caucasian faces. This finding suggests that both Japanese and US Caucasian participants appear to share a common understanding of the distinct cultural meanings associated with gaze behavior and thereby process gaze in a similar manner. In this case, participants from both cultural groups showed more activation to incongruous eye gaze behaviors, based on what is generally considered most culturally appropriate. This is a unique finding suggesting that social cues related to culture may be transmitted and processed consistently across observers from different cultures.
The current investigation showed only one significant effect of gaze direction on the processing of fear expressions as a function of culture of participant, in the left angular gyrus. Given the known role of the angular gyrus/intraparietal sulcus in spatial orienting and gaze perception (Hoffman and Haxby, 2000; Sato et al., 2008), this finding may represent a fundamental difference in gaze perception for Japanese and US Caucasian individuals—particularly in the context of processing fear. Inspection of the means revealed that this effect was largely driven by greater responses to direct- relative to averted-gaze in Japanese participants and to averted- relative to direct-gaze in US Caucasian participants. Given the cultural differences in display rules associated with gaze behavior, this finding may reflect a different role for direct versus averted gaze in these cultural groups. Given that this was not an a priori region of interest, however and that the whole-brain analysis yielded just this one relatively small cluster of activation showing this pattern, this finding must be taken with caution and warrants future corroboration.
The activations reported here show considerable overlap and consistency with regions previously reported (). The current work extends previous findings by demonstrating a robust intracultural effect within these regions for the role of gaze in fear perception. Of particular interest was the finding that amygdala responses to threat-gaze pairings varied as a function of whether participants viewed same- versus other-culture faces. This finding may help inform current inconsistencies reported across studies for role of gaze on fear processing at the neural level, with some work showing greater amygdala responses to ambiguous threat-gaze pairs (i.e. Whalen et al.
; Adams et al.
) and other work showing greater amygdala responses to clear threat-gaze pairs (Sato et al.
; Hadjikhani et al.
). In the current study the pattern of these responses cannot be attributed simply to a particular task or stimulus feature, and thus although the current work does not resolve this issue, the findings reported here are uniquely informative to ongoing research efforts examining this issue.
These findings also contribute to basic emotion theory. Recall that the specific affect program
(Elfenbein and Ambady, 2003
) highlights subtle culturally driven variation in expressive output as well as perceptual attunements to such variation. The current work suggests that culture heightens attunement to subtle, universally relevant aspects of expressions as well, in this case the mere millimeter shifts of irises and pupils that constitute changes in gaze direction. Recent work examining the integration of gaze in threat perception by women at different points along the menstrual cycle offers similar insight (see Conway et al.
). This work found that women high in progesterone perceived fear and disgust expressions as more intense when coupled with averted relative to direct gaze, whereas those low in progesterone showed the opposite pattern. Given that both fear and disgust signal the presence of an external contagion or threat in the environment, gaze is ecologically relevant to detecting its source. Thus, they argued that because pregnancy is also marked by high progesterone, the greater integration of averted gaze in the perception of fear and disgust in this study was likely due to an enhanced attunement triggered by increased threat vigilance. Continued inquiry into intrapersonal influences such as those found by Conway et al.
, and cross-cultural influences such as those revealed by the present work, on compound threat cue processing is likely to yield important new insights into the perception of what are otherwise often regarded as obligatory responses to threat displays.
In sum, the dependent variable of interest employed in this examination represented a contrast between direct- and averted-gaze on otherwise identical faces posing identical expressions. Thus, every face and corresponding expression served as its own control. The neural differences we found were due to responses to the few millimeter shifts in pupils and irises that represent changes in gaze direction. Demonstrating any differences with such a small manipulation underscores just how powerful a social cue gaze is, despite being physically subtle. Gaze also holds different meanings cross-culturally and holds different meanings when conveyed by same- versus other-culture group members. That we found pronounced cultural variation in the influence of gaze on the neural processing of fear expressions highlights the extent to which both culture and gaze meaningfully influence what are often assumed to be obligatory neural responses to threat (see also Chiao et al.
). Taken together, these findings suggest that we must consider how various social cues are processed in combination with one another for our understanding of the processing of each type of cue to be fully realized. Moreover, these findings underscore how cross-cultural examination is likely to advance a basic understanding of the mental and neural operations underlying social and emotional perception.