Detecting emotional facial expressions is an initial and indispensable stage in conscious face-to-face emotional communication. Appropriate detection of others’ emotional expressions allows us to understand their emotional states, and thus regulates social behavior and promotes the creation and maintenance of social relationships.
Experimental psychology studies of healthy participants have demonstrated that the detection of emotional expressions is faster than that of emotionally neutral expressions using the visual search paradigm1–11. For instance, Williams et al.3 instructed participants to search for target faces in arrays of distractor faces and tested the effects of emotional expressions on search behavior. The reaction times (RTs) for the detection of emotional (e.g., angry and happy) expressions among neutral expressions were shorter than those for the detection of neutral expressions among emotional expressions. Some studies suggested that this efficient detection of emotional expressions is due to the emotional, but not visual, factors of the expressions5,6. For instance, Sato and Yoshikawa5 instructed participants to search for normal emotional (angry and happy) facial expressions and their anti-expressions among neutral expression distractors. The anti-expressions were artificial facial expressions that contained visual changes quantitatively comparable to normal expressions and were recognized as emotionally neutral12. The RTs for the detection of normal emotional expressions were shorter than those for the detection of anti-expressions. These data indicate that emotional facial expressions are efficiently detected because of their emotional significance.
A few previous neuropsychological studies have examined the neural substrates of this process, and found that a bilateral amygdala lesion impaired the detection of emotional facial expressions in visual search tasks13,14. Specifically, Bach et al.13 tested two patients with bilateral amygdala damage, and a group of normal controls, on a visual search task in which participants searched for an angry target among a crowd of happy expressions or a happy target among a crowd of angry expressions. Although controls detected angry expressions more rapidly than happy ones, the patients showed the opposite pattern, detecting happy expressions more rapidly. Domínguez-Borràs et al.14 tested a patient with bilateral amygdala damage, and a control group, on a visual search task in which participants searched for an emotional (fearful or happy) facial expression or a neutral facial expression among a crowd of neutral facial expressions. Whereas controls detected facial expressions of fear and happiness more rapidly than neutral expressions, the patient did not. Although the results are not completely consistent, collectively, these studies suggest that amygdala lesions impair the detection of emotional facial expressions.
However, some issues regarding the involvement of the amygdala in the detection of emotional facial expressions remain unresolved. First, one study15 has reported no effect of amygdala lesions on the detection of facial expressions in a visual search task. That study tested a bilateral amygdala-damaged patient and normal controls using a visual search task, in which participants detected a fear expression among a crowd with neutral expressions, or a neutral expression among a crowd with different neutral expressions. Both the patient and the controls detected fearful expressions more rapidly than neutral ones. These results suggest that amygdala lesions may not impair the detection of emotional facial expressions. One plausible explanation for the inconsistent findings is the small samples of the studies, which tested only one or two bilateral amygdala-damaged patients. Because such small samples do not provide reliable findings16, investigating this issue in a group of patients is warranted.
Furthermore, whether impaired detection of emotional expressions in amygdala-damaged patients is due to emotional or visual factors remains untested. Emotional and neutral facial expressions possess differences not only in emotional significance, but also in physical features (e.g., oblique eyebrows in angry expressions versus horizontal eyebrows in neutral expressions). Because some studies have demonstrated that several visual features, such as oblique lines and curves, were detected more efficiently than other features, such as horizontal lines17,18, it may be that the abnormal detection of emotional facial expressions in amygdala-damaged patients reported in previous studies reflected problems with visual processing. Regarding this issue, some functional neuroimaging studies have demonstrated that amygdala activity in response to emotional facial expressions reflected the emotional significance, but not the visual features, of the expressions19–21. Based on these data, we hypothesized that an amygdala lesion may impair the detection of emotional facial expressions, even after controlling for the visual elements of the expressions.
To investigate this hypothesis, we tested a group of patients with unilaterally resected temporal lobe structures, including the amygdala (Fig. 1), using a visual search paradigm. Normal facial expressions of anger and happiness, and their corresponding anti-expressions, were the target stimuli among a crowd with neutral expressions presented to the unilateral visual field (Fig. 2). Because the anti-expressions showed neutral emotions, but had visual feature changes equivalent to those between normal emotional and neutral expressions12, they allowed us to compare emotional and neutral facial expressions while controlling for the effects of basic visual processing. Because visual images presented in a unilateral visual field are primarily processed in the contralateral hemisphere22, we compared the RT required to detect normal and anti-expressions between normal and resected hemisphere stimulation conditions. This paradigm has been shown to effectively reveal the effects of amygdala lesions on psychological impairment23,24. To confirm the emotional impact of normal and anti-expressions, we also obtained subjective ratings of the stimuli from the patients, in terms of valence and arousal, and also investigated familiarity and naturalness as possible cognitive confounding factors.