Consistent with the valence hypothesis, the findings suggest that the amygdala is involved in general valence evaluation of novel faces rather than in evaluation of faces on specific trait dimensions. The findings also suggest that the amygdala's engagement in general valence evaluation of novel faces is automatic, as the fMRI task did not demand explicit face evaluation. The extent to which the amygdala is engaged in tracking variations of faces on social dimensions is a function of the valence content of these dimensions. Therefore, it is not surprising that previous studies have found significant negative correlations between the amygdala's response and the perceived trustworthiness of emotionally neutral faces (Winston et al.
; Engell et al.
; Todorov et al.
) given the strong correlation between this trait and the valence component (0.95).
Though valence evaluation of faces encompasses evaluation on multiple social dimensions, it is best approximated by trustworthiness judgments (Oosterhof and Todorov, 2008
). Thus, trustworthiness judgments may be sufficient to model how the valence of faces is evaluated in the brain, as practically it would often be unfeasible to collect multiple judgments of faces to measure their valence evaluation. However, it would be misleading to describe this evaluation as trustworthiness evaluation per se
at the level of neural response, at least, in experimental contexts that do not provide information other than still images of faces. As shown here, this evaluation most likely reflects general valence evaluation of faces.
Our findings also showed that in addition to the amygdala, activation in a number of regions in occipital and temporal cortex varied as a function of the valence evaluation of faces. As in the case of the amygdala, the activation to faces in these regions was negatively correlated with all positive judgments of faces and positively correlated with all negative judgments. Moreover, after controlling for the valence content of these judgments, these correlations were no longer significant. These findings suggest that in addition to medial temporal lobe regions, regions in occipital and inferotemporal cortex were recruited during valence evaluation of faces.
Although the patterns of responses in the amygdala and the regions in the occipital and inferotemporal cortex were similar ( and ), the magnitude of correlations between the latter and face evaluation was weaker than the magnitude of correlations between the former and face evaluation. Further, the correlation between valence evaluation of faces and the activation in these regions was no longer significant after the analysis controlled for the amygdala's response to faces. In contrast, the correlation with the amygdala remained significant after controlling for the activation in these regions. These findings are consistent with the hypothesis that the activity in occipital and inferotemporal regions was modulated by the amygdala (Morris et al.
; Vuilleumier et al.
, 2004; Sabatinelli et al.
; Vuilleumier, 2005
). Anatomical evidence from tracing studies of the macaque brain shows that the projections from the amygdala to visual cortex are more extensive than those from visual cortex to the amygdala (Amaral et al.
). Whereas the amygdala receives visual input only from temporal visual areas (from area TE to the lateral nucleus of the amygdala), it projects to multiple areas in both temporal and occipital visual areas, including early visual areas (from the basal nucleus to these areas).
It is not possible to prove the causal influence of the amygdala on regions in occipital and inferotemporal cortex with correlational evidence such as the one presented here and from functional connectivity studies (Morris et al.
; Sabatinelli et al.
). However, Vuilleumier et al.
(2004) showed that whereas patients with hippocampal lesions show enhanced response in regions in occipital and inferotemporal cortex to emotionally salient but unattended stimuli, patients with amygdala lesions did not show this response. These regions included SOG, lateral occipital cortex and FG. Given these findings, one would expect that patients with amygdala lesions would not show enhanced responses to negatively evaluated faces in face-responsive regions in occipital and inferotemporal cortex.
As shown in C and D, the response of the amygdala to face valence was linear. Yet, there have been three recent studies reporting a U-shaped, nonlinear amygdala response to face trustworthiness (Todorov et al.
; Said et al.
, in press) and face attractiveness (Winston et al.
). Specifically, the activation was stronger to faces at the extremes of the dimensions than to faces at the middle of the dimensions. There are, at least, two hypotheses about the conditions under which the amygdala's response to face valence may be quadratic. According to the first hypothesis, the nature of the evaluation—implicit vs
explicit—may be critical. In contrast to the current study, participants in Said et al.
's study explicitly evaluated the faces on trustworthiness and this may have biased attention to extreme faces. In a recent study, Cunningham et al.
) observed similar quadratic responses in the amygdala in a valence evaluation task of famous people. When participants focused on the positivity of the evaluation, the response was enhanced to positive stimuli; when they focused on the negativity, the response was enhanced to negative stimuli.
However, this hypothesis cannot account for the all of the data. In Todorov et al.
), the task was the same as the task used in the current study. According to the second hypothesis, the range of face valence used in a particular study may determine the nature of the amygdala's response. For wider ranges of face valence, the response may be quadratic. For example, we compared the trustworthiness of the faces used in Todorov et al.
) and the faces used in Engell et al.
) in a computer model that can assign trustworthiness values to faces based on shape information (Oosterhof and Todorov, 2008
). The range of trustworthiness in the former study was from −3.26 to 2.64 in standard deviation units, whereas the range in the latter study was from –1.79 to 1.53. Studies on attractiveness also typically use extreme faces (O’Doherty et al.
; Winston et al.
) and given the high correlation between attractiveness and face valence (), this can lead to nonlinear responses in the amygdala as observed by Winston et al.
Although the current findings suggest that the amygdala is involved in valence evaluation of faces, they do not rule out the possibility that the amygdala is involved in arousal evaluation. For example, studies using olfactory (Anderson et al.
) and gustatory (Small et al.
) stimuli show that the amygdala responds to the intensity of stimuli rather than to their valence (pleasantness/unpleasantness). These findings are consistent with U-shaped responses in the amygdala to faces. There are, at least, two possibilities that can reconcile our findings with hypotheses that the amygdala is primarily involved in processing of arousing stimuli. First, for visual stimuli, arousal and valence are highly negatively correlated. Negative stimuli (e.g. an angry face) are more arousing than neutral and often positive stimuli (e.g. a smiling face), consistent with well-documented negativity biases in processing of social stimuli (Fiske, 1980
; Skowronski and Carlston, 1989
; Pratto and John, 1991
; Rozin and Royzman, 2001
). The stimuli in the current study were not sampled to represent different levels of arousal and, as noted above, were not highly positive. Thus, their valence was most likely correlated with their arousal value. Second, it is possible that the amygdala involvement in processing of stimuli depends on their sensory modality. Prior studies testing the arousal hypothesis used olfactory and gustatory stimuli because it is relatively easy to manipulate their pleasantness and intensity independently. Even for olfactory stimuli, the amygdala's response to arousing stimuli may depend on their valence. For example, Winston et al.
) showed that whereas the amygdala responded more strongly to high- than to low-arousal stimuli for both pleasant and unpleasant odors, it did not discriminate between high- and low-arousal stimuli for neutral odors.
Both linear and U-shaped responses in the amygdala are consistent with a common attentional mechanism according to which the amygdala biases attention toward stimuli that are of current motivational significance to the person (LaBar et al.
; Vuilleumier, 2005
; Cunningham et al.
). Interestingly, early studies in social cognition showed that allocation of attention to social stimuli exhibits nonlinear quadratic response to people as a function of their extremeness rather than their valence (Fiske, 1980
) and more recent studies show that evaluative processes are context dependent (Ferguson and Bargh, 2004
Yet, when no specific context is provided as in the current study, faces are automatically evaluated in terms of their valence. As argued by both Whalen (1998
) and Amaral (2002
), one of the primary functions of the amygdala may be to provide continuous vigilance by evaluating objects and agents prior to interacting with them. The valence evaluation of stimuli guides approach/avoidance behavior (Chen and Bargh, 1999
), and the valence evaluation of emotionally neutral faces is derived from similarity to emotional expressions signaling approach/avoidance behaviors (Oosterhof and Todorov, 2008
; Todorov, 2008
). Evaluation processes in the amygdala may not only enhance attention and processing of stimuli in perceptual areas (Anderson and Phelps, 2001
; Vuilleumier et al.
, 2004), but may also influence approach/avoidance decisions via interactions with orbital frontal cortex (Baxter et al.
). In fact, macaque monkeys with bilateral amygdala lesions exhibit uninhibited approach behaviors during social interactions (Emery et al.
). Together, these findings suggest that an important role of the primate amygdala is to influence the likelihood of social engagement with unfamiliar conspecifics.