Neural processing of dynamic emotional facial expressions in psychopaths

Abstract

Facial expressions play a critical role in social interactions by eliciting rapid responses in the observer. Failure to perceive and experience a normal range and depth of emotion seriously impact interpersonal communication and relationships. As has been demonstrated across a number of domains, abnormal emotion processing in individuals with psychopathy plays a key role in their lack of empathy. However, the neuroimaging literature is unclear as to whether deficits are specific to particular emotions such as fear and perhaps sadness. Moreover, findings are inconsistent across studies. In the current experiment, 80 incarcerated adult males scoring high, medium, and low on the Hare Psychopathy Checklist-Revised (PCL-R) underwent functional magnetic resonance imaging (fMRI) scanning while viewing dynamic facial expressions of fear, sadness, happiness, and pain. Participants who scored high on the PCL-R showed a reduction in neuro-hemodynamic response to all four categories of facial expressions in the face processing network (inferior occipital gyrus, fusiform gyrus, and superior temporal sulcus (STS)) as well as the extended network (inferior frontal gyrus and orbitofrontal cortex (OFC)), which supports a pervasive deficit across emotion domains. Unexpectedly, the response in dorsal insula to fear, sadness, and pain was greater in psychopaths than non-psychopaths. Importantly, the orbitofrontal cortex and ventromedial prefrontal cortex (vmPFC), regions critically implicated in affective and motivated behaviors, were significantly less active in individuals with psychopathy during the perception of all four emotional expressions.

Figure 1

Amygdala response for each facial expression does not show significant difference between psychopaths and controls. (A) All emotional expressions for all participants greater than baseline thresholded for viewing purposes at p<0.001, with spatial threshold of k>50 voxels (red circles indicate amygdala). (B) Mean contrast estimates in the left amygdala for each emotional expression type for controls participants (individuals who scored <20 on the PCL-R) and for psychopaths (individuals who scored >30 on the PCL-R) (C) Mean contrast estimates in the right amygdala for each emotional expression type for each group.

Figure 2

The response in the dorsal insula is greater in psychopaths. (A) Greater activity in psychopaths as compared to controls for pain expressions (red circles indicate anterior dorsal insular cortex) (B) Mean contrast estimates in the left anterior insula for each emotional expression for control participants (individuals who scored <20 on the PCL-R) and for psychopaths (individuals who scored >30 on the PCL-R) (C) Mean contrast estimates in the right anterior insula for each emotional expression for each group.