Is the human amygdala critical for the subjective experience of emotion? Evidence of intact dispositional affect in patients with amygdala lesions

Abstract

It is thought that the human amygdala is a critical component of the neural substrates of emotional experience, involved particularly in the generation of fear, anxiety, and general negative affectivity. Although many neuroimaging studies demonstrate findings consistent this notion, little evidence of altered emotional experience following amygdala damage has been gathered in humans. In a preliminary test of the amygdala's role in phenomenal affective states, we assessed the extent of experienced positive and negative affective states in patients with amygdala damage and age-, sex-, and education-matched controls. To assess chronic changes in experienced affect, all groups were administered the Positive and Negative Affect Schedules (PANAS, Watson, Clark, & Tellegen, 1988). In the first study, we examined the effects of amygdala lesions on affective traits in 10 left and 10 right amygdala-damaged patients, 1 patient with bilateral amygdala damage (SP), and 20 control subjects. Subjects were asked to indicate the typicality of different experiential states of positive (e.g., inspired, excited) and negative (e.g., afraid, nervous) valence. In a second study, we examined more closely the effects of bilateral amygdala damage on the day-to-day generation of affective states by administering the PANAS daily for a 30-day period to patient SP and age-, sex-, and education-matched controls. In both experiments, no differences in the magnitude and frequency of self-reported positive or negative affect were found between control subjects and patients with amygdala damage. Moreover, principal components analyses of the covariation among different affects (across individuals in Study 1 and within individuals across days in Study 2) confirmed a two-factor (positive vs. negative) description of experienced affect in controls. A highly similar two-factor description of experienced affect was found in patients with amygdala lesions. This suggests that the underlying structure of affective states was intact following amygdala damage. It is concluded that the human amygdala may be recruited during phenomenal affective states in the intact brain, but is not necessary for the production of these states.