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Decety Et Al. (2013)
Decety Et Al. (2013)
Importance: A marked lack of empathy is a hallmark mediate (28 men; PCL-R, 21-29), or low (25 men; PCL-R,
characteristic of individuals with psychopathy. How- ⱕ20) levels of psychopathy.
ever, neural processes associated with empathic process-
ing have not yet been directly examined in psychopa- Main Outcome Measure: Neurohemodynamic re-
thy, especially in response to the perception of other sponse to empathy-eliciting dynamic scenarios revealed
people in pain and distress. by functional magnetic resonance imaging.
Objective: To identify potential differences in patterns Results: Participants in the psychopathy group exhib-
of neural activity in incarcerated individuals with psy- ited significantly less activation in the ventromedial pre-
chopathy and incarcerated persons serving as controls frontal cortex, lateral orbitofrontal cortex, and peri-
during the perception of empathy-eliciting stimuli de- aqueductal gray relative to controls but showed greater
picting other people experiencing pain. activation in the insula, which was positively correlated
with scores on both PCL-R factors 1 and 2.
Design: In a case-control study, brain activation pat-
terns elicited by dynamic stimuli depicting individuals Conclusions and Relevance: In response to pain and
being harmed and facial expressions of pain were com- distress cues expressed by others, individuals with psy-
pared between incarcerated individuals with psychopa- chopathy exhibit deficits in the ventromedial prefrontal
thy and incarcerated controls. cortex and orbitofrontal cortex regardless of stimulus type
and display selective impairment in processing facial cues
Setting: Participants were scanned on the grounds of of distress in regions associated with cognitive mental-
a correctional facility using the Mind Research Net- izing. A better understanding of the neural responses to
work’s mobile 1.5-T magnetic resonance imaging sys- empathy-eliciting stimuli in psychopathy is necessary to
tem. inform intervention programs.
P
SYCHOPATHY IS A PERSONAL- vational facets.3-5 The primary compo-
ity disorder characterized by nent of empathy, empathic sensitivity (or
affective and interpersonal empathic arousal), refers to the auto-
deficits as well as social de- matic sharing of the affective states of
viance and poor behavioral others and is a crucial prerequisite to the
control. As measured by the Hare Psy- experience of empathic concern (ie, other-
chopathy Checklist–Revised (PCL-R),1 oriented emotional response congruent
psychopathy comprises interpersonal, af- with the perceived welfare of someone in
fective (factor 1), and lifestyle and anti- need).4 Interconnected subcortical re-
Author Affiliations: social (factor 2) features. The interper- gions, including the brainstem, amyg- Author Aff
Departments of Psychology sonal/affective component of psychopathy dala, and hypothalamus, and cortical re- Departmen
(Drs Decety and Skelly) and is largely defined by a lack of empathy and gions such as the insula, orbitofrontal (Drs Decety
Psychiatry and Behavioral attachment, as well as a callous lack of re- cortex (OFC), and ventromedial prefron- Psychiatry
Neuroscience (Dr Decety), The gard for others.2 Empathy, the natural ca- tal cortex (vmPFC), form the essential neu- Neuroscien
University of Chicago, Chicago, pacity to share and understand the affec- ral circuit of empathy.3-5 Empathic sensi- University
Illinois; and Departments of Illinois; and
Psychology and Neuroscience,
tive states of others,3 is at the heart of the tivity is a phylogenetically ancient and Psychology
University of New Mexico, and first of the disorder’s 2 core components. basic form of intraspecies communica- University
Mind Research Network, The construct of empathy is complex tion, and it is the first component of em- Mind Resea
Albuquerque (Dr Kiehl). and involves social, emotional, and moti- pathy to develop in children.4,6,7 The vi- Albuquerqu
Contrast Estimate
Contrast Estimate
0.5 x = 34 2 2
0.0 0 0
– 0.5 –2 –2
– 1.0 –4 –4
r = 0.449∗ r = 0.298† r = 0.256‡ r = 0.257‡
– 1.5 –6 –6
L M H L M H 0 5 10 15 0 5 10 15 20
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. Hindicates high psychopathy (PCL-R, ⱖ30); L, low psychopathy (PCL-R, ⱕ20); and M, intermediate
psychopathy (PCL-R, 21-29). *P⬍ .001. †P ⬍.01. ‡P ⬍.05.
had greater activation than did those in the psychopa- volved in emotional and cognitive aspects of mentaliz-
thy group during each task in the right vmPFC and the ing, including the vmPFC, OFC, pSTS, dmPFC, IPL,
right lateral OFC (Figure 3). In addition, 4 regions were dACC, and dorsal striatum.
more active in psychopathic individuals for painful in- The amplified involvement of the AIC in participants
teractions but more active in controls for facial expres- with psychopathy is surprising because of the well-
sions of pain. This pattern was observed in the dmPFC, documented role of this region in the experience of
angular gyrus, pSTS, and IFG (eFigure). empathy (Figure 2). The AIC is a polysensory cortex
involved in mapping internal states of bodily and sub-
DISCUSSION jective feeling. With extensive reciprocal connections
with limbic forebrain areas,40 it is the most consistently
To better understand the deficits in socioemotional in- activated region across all studies of empathy for pain,20
formation processing in individuals with psychopathy, even when there is no explicit cognitive demand to
the current study used 2 classes of stimuli that have been empathize with another individual.41 Moreover, gray
extensively applied during the past decade to chart the matter reduction has been observed in the insula in
neural network underpinning empathy in healthy adults individuals scoring high on psychopathy tests, 42
and children.6,8,13,14,27-30 although the stereotaxic coordinates are different
In the pooled analyses of all 70 participants ana- between their study and ours (posterior insula vs ante-
lyzed, collapsed across PCL-R scores, expected patterns rior insula, respectively). A previous fMRI study25 of
of activation were observed during perception of people empathy in children with aggressive conduct disorder
being hurt and facial expressions of pain. The former elic- and psychopathic tendencies, using similar stimuli,
ited activity in the AIC, dACC, aMCC, amygdala, and reported similar findings. Increased activity was
SMA, and the latter recruited activity in the fusiform gy- detected in the AIC as well as reduced response in the
rus, AIC, pSTS, and IFG. OFC when children with conduct disorder were pre-
There were significant differences, however, in sev- sented with stimuli depicting others in pain. A recent
eral brain regions engaged between the 2 extreme groups. case study43 reported on a patient who, despite com-
When viewing people being hurt, individuals with psy- plete destruction of the insula, experienced all aspects
chopathy showed greater activation in the AIC, as well of feelings and emotions, including empathy. This indi-
as in the dorsal striatum, dmPFC, and pSTS, 3 regions cates that the role of the insula in emotion and empathy
involved in the cognitive dimension of mentalizing.39 Con- is complex and far from being understood. In addition,
trol participants showed greater signal increase in the peri- it has been proposed from network analysis that the
aqueductal gray, vmPFC, and lateral OFC, a circuit with insula and ACC form the core of a network that facili-
reciprocal connections with the amygdala and hypothala- tates the detection of important environmental
mus involved in the regulation and mediation of emo- stimuli.44 The pSTS and medial prefrontal cortex are
tional and affective behavior.9,10 part of the cognitive mentalizing network (processing
When viewing facial expressions of pain, fusiform gyrus intentions and understanding social interaction) and
activity was equivalent between groups. The high- have been reported in previous research using similar
scoring psychopathy group again displayed greater ac- stimuli. 8 , 1 4 The augmented involvement of these
tivation bilaterally in the AIC. However, in this case, low- regions, including the AIC, in individuals with psy-
scoring incarcerated control participants had greater chopathy supports a cognitive assessment strategy of
activation than those with psychopathy in regions in- these scenarios rather than an affective processing.
Contrast Estimate
Contrast Estimate
4
tive vs cognitive theory of mind processing in criminal
2 0
offenders with antisocial personality disorder with high
0
psychopathy features as well as in participants with lo- –1
–2
calized lesions in the OFC or dorsolateral prefrontal cor- –4
–2
tex. The authors found that individuals with psychopa- –6
r = – 0.262
–3
r = – 0.258
Contrast Estimate
3
IPL, pSTS, and IFG were significantly less active during 2
1
the viewing of facial expressions of pain in the psychopa- 0
–1
thy group, but significantly more active than in controls –2
–3
while watching individuals hurting others. According to –4 –5
one network model,39 ventral regions such as the OFC –6
r = – 0.305
–7
r = – 0.331
mentalizing, while dorsal regions such as the dmPFC, PCL-R Total Score PCL-R Total Score