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Original Article |

Brain Response to Empathy-Eliciting Scenarios Involving Pain in Incarcerated Individuals With Psychopathy

Jean Decety, PhD; Laurie R. Skelly, PhD; Kent A. Kiehl, PhD
JAMA Psychiatry. 2013;70(6):638-645. doi:10.1001/jamapsychiatry.2013.27.
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Importance A marked lack of empathy is a hallmark characteristic of individuals with psychopathy. However, neural processes associated with empathic processing have not yet been directly examined in psychopathy, especially in response to the perception of other people in pain and distress.

Objective To identify potential differences in patterns of neural activity in incarcerated individuals with psychopathy and incarcerated persons serving as controls during the perception of empathy-eliciting stimuli depicting other people experiencing pain.

Design In a case-control study, brain activation patterns elicited by dynamic stimuli depicting individuals being harmed and facial expressions of pain were compared between incarcerated individuals with psychopathy and incarcerated controls.

Setting Participants were scanned on the grounds of a correctional facility using the Mind Research Network's mobile 1.5-T magnetic resonance imaging system.

Participants Eighty incarcerated men were classified according to scores on the Hare Psychopathy Checklist–Revised (PCL-R) as high (27 men; PCL-R, ≥30), intermediate (28 men; PCL-R, 21-29), or low (25 men; PCL-R, ≤20) levels of psychopathy.

Main Outcome Measure Neurohemodynamic response to empathy-eliciting dynamic scenarios revealed by functional magnetic resonance imaging.

Results Participants in the psychopathy group exhibited significantly less activation in the ventromedial prefrontal cortex, lateral orbitofrontal cortex, and periaqueductal gray relative to controls but showed greater activation in the insula, which was positively correlated with scores on both PCL-R factors 1 and 2.

Conclusions and Relevance In response to pain and distress cues expressed by others, individuals with psychopathy exhibit deficits in the ventromedial prefrontal cortex and orbitofrontal cortex regardless of stimulus type and display selective impairment in processing facial cues of distress in regions associated with cognitive mentalizing. A better understanding of the neural responses to empathy-eliciting stimuli in psychopathy is necessary to inform intervention programs.

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Figures

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Figure 1. Tasks used to example neural processes involved in empathy. A, An example of the last frame of the pain interactions task. In this task, 48 visual scenarios depicting pain and 48 control scenarios without pain were used. Each scenario consisted of a 3-part frame capture taken from videos of live actors, presented at the rate of 1000, 200, and 1000 milliseconds to simulate biological motion. The scenarios depicted people intentionally harming another person by actions such as striking, cutting, pinching, or crushing that person's hands, feet, arms, legs, fingers, or toes. Control stimuli included sequences in which 2 people interacted, but no harm or pain occurred. No heads or faces were visible in the scenarios. Data were collected in 2 runs, with each 7 minutes. B, An example of the pain expression task. Video clips showed a natural pain response in which individuals displayed brow lowering, orbit tightening, and either pursing/pressing of the lips or opening/stretching of the mouth. These movements have consistently been attributed to the facial expression of pain. After 8 of the clips were shown, participants were asked whether the previous clip had featured a male or a female. Data in this task were acquired in one 8-minute run.

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Figure 2. Groupwise and continuous measures of hemodynamic response in the right anterior insular cortex. Blood oxygen level dependence response increased as a function of the degree of psychopathy (as measured by the Hare Psychopathy Checklist–Revised [PCL-R]) during the viewing of both types of empathy-eliciting stimuli, interactions in which one person caused pain to another (interactions) and facial expressions of pain (expressions). A, Histogram of responses of all participants stratified into 3 groups. B, Anatomical location of cluster of interest (circled) superimposed on the sample-specific diffeomorphic anatomical registration through exponentiated lie algebra (DARTEL)–normalized T1 template at Montreal NeuroIogical Institute (MNI) coordinate x = 34. C and D, The groupwise effects seen in part A were expanded to examine the contribution of continuous factor 1 and factor 2 PCL-R subscores, representing the affective/interpersonal and lifestyle/behavioral features of psychopathy, respectively. Values used for A, C, and D are the contrast estimates per participant averaged across the 3-mm sphere centered on the cluster peak at MNI coordinates (26, 28, −8), from the contrast of scenarios with pain/harm content vs scenarios with no pain/harm in the pain interactions task, and from the contrast of dynamic pain expressions vs dynamic baseline stimuli in the pain expressions task. Error bars indicate the standard error of the mean. H indicates high psychopathy (PCL-R, ≥30); L, low psychopathy (PCL-R, ≤20); and M, intermediate psychopathy (PCL-R, 21-29). * P < .001. † P < .01. ‡ P < .05.

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Figure 3. Neurohemodynamic activity in the ventromedial prefrontal cortex (vmPFC) and lateral orbitofrontal cortex (lOFC) decreases as a function of total psychopathy score during the viewing of 2 types of empathy-eliciting stimuli, interactions in which one person caused pain in another (interactions) and facial expressions of pain (expressions). At the center, the clusters illustrated in the figure are indicated on the study-specific T1 template, circled in violet for the vmPFC and blue for the lOFC. At left and right, per-subject contrast estimates averaged across the 3-mm sphere surrounding the peak voxel in each cluster (Montreal NeuroIogical Institute [8, 30, −10] for the vmPFC and [42, 48, −12] for the lOFC) are expanded for the entire sample (N = 70) as a function of the Hare Psychopathy Checklist–Revised (PCL-R) total score.

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