Brain Response to Empathy-Eliciting Scenarios Involving Pain in Incarcerated Individuals With Psychopathy
http://archpsyc.jamanetwork.com/article.aspx?articleid=1681369ABSTRACT 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.
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.
Psychopathy
is a personality disorder characterized by affective and interpersonal
deficits as well as social deviance and poor behavioral control. As
measured by the Hare Psychopathy Checklist–Revised (PCL-R),1
psychopathy comprises interpersonal, affective (factor 1), and lifestyle
and antisocial (factor 2) features.
The
interpersonal/affective component of psychopathy is largely defined by a
lack of empathy and attachment, as well as a callous lack of regard for
others. Empathy, the natural
capacity to share and understand the affective states of others, is at
the heart of the first of the disorder's core components. The construct
of empathy is complex and involves social, emotional, and motivational
facets. The primary component of empathy, empathic sensitivity (or
empathic arousal), refers to the automatic sharing of the affective
states of others and is a crucial prerequisite to the experience of
empathic concern (ie, other-oriented emotional response congruent with the perceived welfare of someone in need).
Interconnected subcortical regions, including the brainstem, amygdala,
and hypothalamus, and cortical regions such as the insula, orbitofrontal
cortex (OFC), and ventromedial prefrontal cortex (vmPFC), form the
essential neural circuit of
empathy.3- 5 Empathic sensitivity is a
phylogenetically ancient and basic form of intraspecies communication,
and it is the first component of
empathy to develop in children.4,6,7
The vicarious sharing of another's negative state provides a strong
signal that can promote empathic concern, and the lack of such signals
during development can impede the process of normal socialization.7,8 To
be motivated to help another, one needs to be affectively, empathically
aroused and anticipate the cessation of mutually experienced personal
distress.9,10
Empathic sensitivity may thus
serve as a catalyst in promoting empathic concern for others: the lack
of this signal would make the engagement of empathic concern and
prosocial behavior much less likely. The
perception of
others' pain or physical distress usually acts as a prosocial signal,
notifying others that their conspecific is at risk, attracting their
attention, and motivating helping behavior,12 and has become a fruitful
avenue to investigate the neural mechanisms underpinning affective
processing and
empathy.<br><br>In healthy participants,
functional magnetic resonance imaging (fMRI) studies 6,8,13- 19 of
empathy have demonstrated reliable activation of a neural network that
overlaps substantially with regions engaged when one experiences pain
and when one perceives, anticipates, or even imagines pain happening to
others. The activated neural network includes the anterior insular
cortex (AIC), dorsal anterior cingulate cortex (dACC), anterior
midcingulate cortex (aMCC), supplementary motor area (SMA),
somatosensory cortex, amygdala, periaqueductal gray, and
vmPFC.20<br><br>The neural response to the distress of
others, such as pain, is thought to reflect an aversive response in the
observer that may act as a trigger to inhibit aggression or prompt
motivation to help.
Hence,
examining the neural response of individuals with psychopathy as they
view others being hurt or expressing pain may be an effective probe into
the neural processes underlying affective and empathic deficits in
psychopathy. To date, no fMRI study has investigated
the neural response to
empathy-eliciting stimuli in incarcerated
individuals with
psychopathy. Previous research21- 23 showed that these
people understand the emotional state of others without “sharing” their
feelings or being aroused by their emotional states. Thus, one can
anticipate different hemodynamic response in the neural network involved
in the
perception of pain between individuals with
psychopathy,
especially for participants scoring high on the PCL-R. An alternative
hypothesis draws on research showing that children and adolescents with
callous-unemotional traits are reward-oriented, insensitive to
punishment cues, lack emotional responsiveness to distress cues, and may
show both reactive and instrumental aggression.24 In support of this
hypothesis, one study23 found that
male adolescent offenders with high
callous-unemotional traits exhibited atypical neural dynamics of pain
empathy processing (measured with event-related
brain potentials) in the
early stages of affective arousal coupled with relative insensitivity
to actual pain. Another neuroimaging study25 documented strong
activation of the amygdala (as well as the pain network), which
correlated with a measure of sadism, in youth with aggressive conduct
disorder when they observed people being hurt.<br><br>To
investigate the neural mechanisms underlying
empathy for pain in adults
with
psychopathy, 80 incarcerated
male volunteers, stratified into 3
groups, were scanned using fMRI. Participants classified as having a
high level of
psychopathy (n = 27) were those who scored 30 or above on
the PCL-R (of a possible 40), those classified as having intermediate
psychopathy (n = 28) scored between 21 and 29, and volunteers scoring 20
or below (n = 25) were classified as low-psychopathy controls.
Well-matched groups from the prison population are used to isolate
differences due to
psychopathy and eliminate confounding factors
possible in the direct comparison of incarcerated people with
psychopathy with community controls.<br><br>Furthermore, the
inclusion of participants from across the scoring spectrum allowed us
to investigate differences at a groupwise and a continuous level using
both PCL-R total and factor 1 and 2 scores. The neurohemodynamic
activity was measured while participants attended to visual scenarios
depicting individuals being physically hurt and dynamic facial
expressions of pain; these stimuli have been used in numerous fMRI
studies6,8,13- 19,23,25- 30 investigating the neural underpinnings of
empathy for pain in healthy children, adolescents, and adults. Moreover,
having 2 sets of stimuli,
ie,
pain interactions (2 persons interacting without the faces of the
protagonists) and facial expressions of pain may help us identify which
component of
empathy is dysfunctional in
psychopathy. The former class
of stimuli requires a cognitive understanding of a social interaction
with a negative outcome, which is associated with the engagement of the
network supporting mental state inference and the
perception of pain in
others8; the latter also induces activation in the OFC and vmPFC, which
are prefrontal regions that play a pivotal role in adaptive responses to
emotionally relevant situations and the production of an affective
state.
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