Psychopaths Show Enhanced Amygdala Activation during Fear Conditioning

Abstract

Psychopathy is a personality disorder characterized by emotional deficits and a failure to inhibit impulsive behavior and is often subdivided into "primary" and "secondary" psychopathic subtypes. The maladaptive behavior related to primary psychopathy is thought to reflect constitutional "fearlessness," while the problematic behavior related to secondary psychopathy is motivated by other factors. The fearlessness observed in psychopathy has often been interpreted as reflecting a fundamental deficit in amygdala function, and previous studies have provided support for a low-fear model of psychopathy. However, many of these studies fail to use appropriate screening procedures, use liberal inclusion criteria, or have used unconventional approaches to assay amygdala function. We measured brain activity with BOLD imaging in primary and secondary psychopaths and non-psychopathic control subjects during Pavlovian fear conditioning. In contrast to the low-fear model, we observed normal fear expression in primary psychopaths. Psychopaths also displayed greater differential BOLD activity in the amygdala relative to matched controls. Inverse patterns of activity were observed in the anterior cingulate cortex (ACC) for primary versus secondary psychopaths. Primary psychopaths exhibited a pattern of activity in the dorsal and ventral ACC consistent with enhanced fear expression, while secondary psychopaths exhibited a pattern of activity in these regions consistent with fear inhibition. These results contradict the low-fear model of psychopathy and suggest that the low fear observed for psychopaths in previous studies may be specific to secondary psychopaths.

Keywords: amygdala; anxiety; fMRI; fear conditioning; psychopathy.

FIGURE 1

Design of the experiment. (A) An example of the stimulus timing for the CS+ and CS- trials. (B) An example of the visual display. (C) An enlarged example of the rating bar that was present on the bottom of the visual display.

FIGURE 2

Behavioral data indicates an interaction between psychopathy and anxiety on both UCS expectancy and SCR measures and psychopaths show larger differential activity in the left amygdala compared to the control group. (A) All groups give larger UCS expectancy rating for the CS+ relative to the CS-. The control group shows a trend for larger differential UCS expectancy ratings in the high anxiety group compared to the low anxiety group. There was no such trend for the psychopath group. (B) Psychopaths in the low anxiety group (primary) show a trend toward a larger differential SCR compared to Psychopaths in the high anxiety group. There was no such trend in the control group. (C) Brain map showing larger differential activity in the left amygdala for psychopaths. (D) Bar graph of the data from the amygdala cluster. Error bars depict the standard error of the mean. The colors on the brain map correspond to the F-values on the color scale.

FIGURE 3

(A) Brain regions showing an interaction between psychopathy and anxiety. (B) The interaction effects were due to anxiety increasing differential responses to the CS+ versus CS- in the control group, and decreasing differential responses in the psychopaths.

FIGURE 4

The dorsal ACC shows an interaction between psychopathy and anxiety characterized by the control group showing that anxiety increased differential responses while the psychopath group shows anxiety decreased differential responses. The vmPFC shows an interaction between psychopathy and anxiety characterized by the control group showing that anxiety decreased differential responses while the psychopath group shows anxiety increased differential responses.