The purpose of the present study was to: (a) examine the neural signature associated with viewing disapproving facial expressions, which have not been investigated with neuroimaging methods, and (b) to examine how neural responses to disapproving faces are moderated by rejection sensitivity. To accomplish these goals, participants completed a measure of rejection sensitivity and were scanned while viewing disapproval, anger, and disgust facial expressions.
As expected, all three facial expressions (disapproval, anger, disgust) resulted in significant bilateral amygdala activity compared to fixation. This extends prior work showing amygdala activity in response to viewing negative emotional expressions, such as anger, fear, or disgust (Fitzgerald et al., 2006
; Morris et al., 1996
; Phillips et al., 1997
; Whalen et al., 1998
), and indicates that a disapproving facial expression may be interpreted as an inherently threatening emotional expression as well. Interestingly, when comparing neural activity to disapproving facial expressions versus anger expressions, there was significantly greater left amygdala activation, suggesting that disapproving faces may represent a more potent threat at the neural level than some other previously studied negative expressions. In addition, the finding of greater insula activity in response to disgust expressions relative to disapproval expressions provides additional evidence that distinguishes disapproval faces from other threatening facial expressions, highlighting the notion that disapproval may not just be a variant of disgust (cf. Ekman & Friesen, 1986
Contrary to our predictions, however, individuals did not show greater dACC activity while viewing disapproving faces compared to fixation. In hindsight, this lack of a main effect for dACC may not be entirely surprising. The dACC is a region that has been shown to be involved in responding to personal threats to the self such as the distress associated with social exclusion (Eisenberger et al., 2003
, 2007) or the distressing or unpleasant experience associated with physical pain (Rainville, Duncan, Price, Carrier, & Bushnell, 1997
). In the present study, participants watched video clips of strangers demonstrating disapproving expressions, which may not have been experienced as personally threatening.
Nonetheless, as predicted, dACC activity was moderated by rejection sensitivity in response to viewing disapproving facial expressions. Specifically, individuals high in rejection sensitivity exhibited greater dACC activity in response to viewing the disapproving facial expressions than individuals low in rejection sensitivity. This was true even when disapproving facial expressions were compared directly with anger and disgust facial expressions. Thus, for individuals who are dispositionally sensitive to rejection, stimuli that signal social rejection (i.e., video clips of strangers demonstrating disapproving expressions) elicited activity in some of the same neural regions that are involved in the experience of social rejection. Because individuals high in rejection sensitivity are more likely to interpret ambiguous stimuli as rejecting (Downey & Feldman, 1996
), these individuals may have interpreted these disapproving facial expressions as more personally threatening. It is also possible that individuals high in rejection sensitivity were more likely to become distressed by these disapproving facial expressions, either because they are more sensitive to these types of rejecting expressions or because these rejecting expressions are more likely to trigger memories of past episodes of rejecting experiences. Because we did not assess distress levels in response to viewing the disapproving faces, we cannot determine whether the greater dACC activity observed in rejection-sensitive individuals is related to greater experiences of distress or to a more sensitive detection of cues that predict social rejection. Future studies will be needed to disentangle these two alternatives.
Of particular interest is that the positive relationship between rejection sensitivity and dACC activity was not seen in response to the anger or disgust faces, suggesting that individuals sensitive to rejection exhibited a greater dACC response specifically to facial expressions indicating possible rejection, but not to threatening facial expressions in general. Although previous researchers have suggested that disgust expressions may actually represent social rejection (Amir et al., 2005
; Rozin, Haidt, & McCauley, 1999
) the results here qualify this claim. The selective dACC response to disapproving facial expressions by high rejection sensitive individuals is also consistent with previous work showing that high-rejection-sensitive individuals showed heightened autonomic reactivity in response to rejection-themed cues, but not to other negative (but non-rejection-themed) stimuli (Downey, Mougios, Ayduk, London, & Shoda, 2004
Another interesting point is that rejection sensitivity correlated specifically with dACC activity to disapproving faces, but not with other limbic system activity (e.g., amygdala, insula), suggesting that dACC activity, rather than more general limbic system activity, is specifically responsive to these disapproving faces in high, relative to low, rejection-sensitive individuals. Again, this finding suggests that disapproving facial expressions may represent a distinct type of threat that has not been examined previously in fMRI studies and that the dACC may play a unique role in responding to this expression.
In light of these findings, disapproving face stimuli may be more appropriate to use than other face stimuli when assessing negative affective processes in clinical disorders that involve a heightened sensitivity to negative social experiences. For example, fear of rejection has been shown to be the primary cognition for individuals with social anxiety (Turner, Johnson, Beidel, Heiser, & Lydiard, 2003
), and hypersensitivity to social threat cues is a key feature of depressed states (Allen & Badcock, 2003
; Mathews, Ridgeway, & Williamson, 1996
). Thus, a socially threatening facial expression that specifically conveys potential social rejection may be more effective in engaging the maladaptive affective processes present in these populations.
In addition to its role in personal threats to the self, dACC has also been theorized to play a role in conflict monitoring, in which the dACC monitors for conflicting response tendencies (Botvinick, Cohen, & Carter, 2004
; Carter et al., 2000
; MacDonald, Cohen, Stenger, & Carter, 2000
). Indeed, some have suggested that the dACC activity observed in response to the Cyber-ball social exclusion paradigm (Eisenberger et al., 2003
) is due to the fact that the exclusion episode is unexpected and thus conflicts with prior expectations to be included (Somerville, Heatherton, & Kelley, 2006
). Based on these accounts of dACC function, it may be argued that the dACC activity seen in response to the disapproving facial expressions is the consequence of disapproving faces being more “unexpected” than anger or disgust faces. However, if this were the case, we would expect to see a main effect of greater dACC activity in response to the disapproving facial expressions compared to the anger or disgust faces. Instead, dACC activity in response to the disapproving facial expressions correlated with rejection sensitivity. Because rejection-sensitive individuals are presumably more likely to expect to see disapproving faces (Downey & Feldman, 1996
), it is unlikely that the enhanced dACC activity observed in rejection-sensitive individuals is due to expectancy violations (cf. Somerville et al., 2006
). Furthermore, rejection-sensitive individuals have previously been shown to have an emotional response to rejection-related stimuli (Downey et al., 2004
). In that study, high-rejection-sensitive individuals exhibited amplified startle responses in response to rejection-themed images. As the startle response is a measure of autonomic nervous system activity, this finding supports the idea that rejection sensitive individuals' responses to rejection cues have an affective component and are not strictly reducible to cognitive expectation effects. Thus, rejection sensitivity is associated with emotional responses to rejection-related cues. It follows that neural responses that differ by level of rejection sensitivity while viewing rejection-related cues may be involved in this emotional process.
Rejection sensitivity also correlated negatively with subACC/VMPFC activity in response to the disapproving facial expressions. The fact that rejection-sensitive individuals showed reduced subACC/VMPFC activity to disapproving facial expressions is consistent with previous work demonstrating a role for the subACC/VMPFC in the extinction of conditioned fear responses in both animals and humans (Morgan, Romanski, & LeDoux, 1993
; Phelps et al., 2004
; Quirk, Russo, Barron, & Lebron, 2000
). For example, conditioned fear responses, which normally decrease during extinction trials (when the conditioned stimulus is presented without the unconditioned stimulus), persist among rats with lesions to the VMPFC, suggesting that the VMPFC may be essential for inhibiting the conditioned response. Moreover, in humans, extinction of a conditioned fear response has been associated with reduced amygdala activation and increased subACC/VMPFC activation (Phelps et al., 2004
). Thus, it is possible that decreased subACC/VMPFC activity to disapproving faces in rejection-sensitive individuals may reflect a diminished ability to regulate the negative responses to these disapproving facial expressions.4
Consistent with this idea, in a functional connectivity analysis, we found dACC activity to be negatively correlated with subACC/VMPFC activity. This result is also similar to previous findings showing an inverse relationship between subACC/VMPFC and amygdala activity when assessing the valence of certain stimuli (Kim et al., 2003
). In that study, to the extent that surprised facial expressions were interpreted more negatively, participants showed reduced subACC/VMPFC activity and greater amygdala activity; conversely, to the extent that surprised facial expressions were interpreted more positively, participants showed greater subACC/VMPFC activity and reduced amygdala activity. Additionally, these two regions were negatively correlated with each other, suggesting that sub-ACC/VMPFC inputs to the amygdala may be involved in down-regulating the activity of the amygdala, leading to more positive interpretations of certain stimuli. In a similar manner, the present findings may suggest that individuals who interpret the disapproving facial expressions more negatively (i.e., those high in rejection sensitivity) show reduced subACC/VMPFC and greater dACC activity, whereas individuals who interpret the disapproving facial expressions less negatively (i.e., those low in rejection sensitivity) show greater subACC/VMPFC and reduced dACC activity. Consistent with these results, Somerville and colleagues (Somerville et al., 2006
) recently observed that the receipt of gestures of social acceptance were associated with increased activity in the subACC/VMPFC.
Thus, it is possible that the reduced subACC/VMPFC activity observed in rejection-sensitive individuals in the present study may be indicative of biased appraisal processes, such that rejection-sensitive individuals are less able to interpret these disapproving facial expressions in a non-threatening way. The diminished ability to reinterpret these disapproving facial expressions as non-threatening may then be related to the increased dACC activity that was evidenced among those high in rejection sensitivity.
One possible confound in our study may have been the level of realism present in each of the facial expressions. Like the classic Ekman-style photographs of emotions, the anger and disgust expressions may have seemed exaggerated and thus less ecologically valid than the disapproving facial expressions. Future studies should involve more realistic dynamic facial expressions of anger and disgust in addition to disapproval.
Additionally, future studies should include a direct comparison of disapproval faces with contempt faces, in order to determine whether or not there are meaningful differences in the responses to these expressions at the neural level. Darwin's original description of the contempt expression focused on its role in displaying hatred for another person, specifically when that person is considered insignificant (Darwin, 1872/1998
, p. 234). Accordingly, a contempt expression is dismissive, signaling a lack of interest in establishing or maintaining any sort of social relationship. In contrast, a disapproving face is more akin to the facial expression that a parent would direct at a child who is misbehaving, a signal, not of hatred, but of disappointment in the child's behavior. The disapproving facial expression acts as a signal or motivational cue to correct another's behavior and, perhaps, to improve the state of the social relationship. Thus, these facial expressions may trigger different types of neural activity that reflect being rejected with the inability to reconcile (contempt) versus the ability to make amends (disapproval).
In future studies, it would also be interesting to examine how neural responses to disapproving and other facial expressions would differ from the results presented here if participants were given more specific instructions for viewing the video clips, such as to “imagine the facial expressions are directed at you,” or “imagine what this person is thinking.” It is likely that participants in our study used a variety of cognitive processes while watching the video clips. Constraining what participants are thinking while viewing the video clips may provide stronger, more uniform neural responses to the expressions presented.
Finally, future studies should also include a “baseline” control condition other than a crosshair fixation to more tightly control for the viewing of facial stimuli. Future studies would also benefit by including a baseline condition other than “neutral” facial expressions, as these expressions have been shown to elicit amygdala activity (Fitzgerald et al., 2006
) and can be interpreted as threatening (Somerville, Kim, Johnstone, Alexander, & Whalen, 2004
In conclusion, the current study is the first to examine neural responses to disapproving facial expressions. In addition to finding significant bilateral amygdala activity to this threatening facial expression, we also found that individuals who scored higher in rejection sensitivity showed greater dACC and reduced subACC/VMPFC activity to these disapproving faces. Not only did individuals sensitive to rejection show a greater threat response to the facial expressions indicating possible rejection, but they also did so selectively, suggesting that different types of threatening facial expressions convey specific types of threats, with disapproving facial expressions primarily signifying a threat to social connection.
Over a hundred years ago, Darwin observed how different emotional facial expressions convey unique information, with each expression adapted for a specific purpose. Today, we are extending these observations to the neural level. Clearly, facial expressions other than those representing “basic emotions” can have a profound effect on our functioning and well-being. Further research in this area will enable us to better understand these effects. As Ovid observed centuries ago, “Often a silent face has voice and words” (Ars Amatoria, Bk. I, 574).