Psychopathy is associated with fear-specific reductions in neural activity during affective perspective-taking

Abstract

Psychopathic individuals are notorious for their callous disregard for others' emotions. Prior research has linked psychopathy to deficits in affective mechanisms underlying empathy (e.g., affective sharing), yet research relating psychopathy to cognitive mechanisms underlying empathy (e.g., affective perspective-taking and Theory of Mind) requires further clarification. To elucidate the neurobiology of cognitive mechanisms of empathy in psychopathy, we administered an fMRI task and tested for global as well as emotion-specific deficits in affective perspective-taking. Adult male incarcerated offenders (N = 94) viewed images of two people interacting, with one individual's face obscured by a shape. Participants were cued to either identify the emotion of the obscured individual or identify the shape from one of two emotion or shape choices presented on each trial. Target emotions included anger, fear, happiness, sadness, and neutral. Contrary to predictions, psychopathy was unrelated to neural activity in the Affective Perspective-taking > Shape contrast. In line with predictions, psychopathy was negatively related to task accuracy during affective perspective-taking for fear, happiness, and sadness. Psychopathy was related to reduced hemodynamic activity exclusively during fear perspective-taking in several areas: left anterior insula extending into posterior orbitofrontal cortex, right precuneus, left superior parietal lobule, and left superior occipital cortex. Although much prior research has emphasized psychopathy-related abnormalities in affective mechanisms mediating empathy, current results add to growing evidence of psychopathy-related abnormalities in a cognitive mechanism related to empathy. These findings highlight brain regions that are hypoactive in psychopathy when explicitly processing another's fear.

Keywords: Emotion; Empathy; Fmri; Psychopathology; Psychopathy; Social cognition.

Fig. 1.

Temporal sequence of the affective perspective-taking task. Participants selected one of two emotional faces that best matched the emotion of the obscured face from the social scene. For the shape task, participants selected one of two shapes that matched the shape embedded within the social scene.

Fig. 2.

Areas of significant activation across the entire sample for A) the Affective Perspective-Taking > Shape contrast, and B) the emotion-specific contrasts within the affective perspective-taking task: Anger > Neutral, Fear > Neutral, Sadness > Neutral, and Happiness > Neutral (uncorrected p = .002, p_FWE < 0.05).

Fig. 3.

The significant association between PCL-R Total scores and Fear > Neutral activity in left anterior insula (AI) extending into posterior orbitofrontal cortex (pOFC) in the affective perspective-taking task (uncorrected p = .002, p_FWE < 0.05). The activation plot shows regression lines with error bands representing 1 SE above and below the point estimate of the model.

Fig. 4.

The significant association between PCL-R Total scores and Fear > Neutral activity in right precuneus in the affective perspective-taking task (uncorrected p = .002, p_FWE < 0.05). The activation plot shows regression lines with error bands representing 1 SE above and below the point estimate of the model.