Intact rapid detection of fearful faces in the absence of the amygdala

Abstract

The amygdala is thought to process fear-related stimuli rapidly and nonconsciously. We found that an individual with complete bilateral amygdala lesions, who cannot recognize fear from faces, nonetheless showed normal rapid detection and nonconscious processing of those same fearful faces. We conclude that the amygdala is not essential for early stages of fear processing but, instead, modulates recognition and social judgment.

Figure 1

Intact rapid, automatic and nonconscious detection of fearful faces in the absence of the amygdala. (a) Rapid detection of fear- and threat-related images. Viewers were shown two images side by side for 40 ms (unmasked), one neutral and the other showing fear, anger or threat. We carried out three experiments, one with fearful versus neutral faces, the second with angry versus neutral faces and the third with threat-related images versus neutral images. Subjects were asked to push a button as quickly as possible to indicate if the target image that showed more fear/anger or was more threatening was on the left or the right. Speed and accuracy tradeoffs in discriminating fear were normal in two sessions for SM (red) compared with 12 controls (solid black line indicates the mean and the dotted lines indicate the 95% confidence interval). Accuracy was quantified by d′, the difference between the z-transformed hit and the false alarm rate. (b) Visual search for fear. Subjects detected an oddball target among distractors; both were perceived as belonging either to the same category (for example, mild and extreme fear) or to different categories (for example, neutral and mild fear), even though they differed geometrically by the same degree. SM showed normal category boundary effects in reaction time. The black bars indicate the average across three age-matched controls and the white bars indicate SM's performance. (c) Breaking into consciousness probed by continuous flash suppression. Fearful faces broke interocular suppression faster than happy faces in SM (white) to the same degree as in controls (black). Subjects clicked a mouse as soon as any part of the face became visible. The dot and error bar indicate the mean and the s.d. for seven control subjects. All subjects gave written informed consent as approved by the institutional review board of the California Institute of Technology.