Neural responses to morally laden interactions in female inmates with psychopathy

Abstract

Much of social cognition requires making inferences about the mental and emotional states of others. Moreover, understanding the emotions of others is an important foundation for moral decision-making. Psychopathy is associated with both aberrant emotional understanding and atypical hemodynamic responses when viewing and evaluating morally laden social interactions. In the present functional MRI study, female inmates (N=107) were asked to evaluate the likely emotional state of either the recipient or the initiator of harmful or helpful interactions. Psychopathy was assessed with the Psychopathy Checklist-Revised (PCL-R). PCL-R scores were not associated with differences in confidence or accuracy ratings. However, psychopathy scores were significantly related to increased hemodynamic response in right dorsolateral prefrontal cortex when viewing harmful interactions and decreased functional connectivity from right amygdala to inferior parietal and insula, and from temporal parietal junction to dorsomedial prefrontal cortex. Overall, this work indicates that in females, psychopathy is associated with normal behavioral accuracy and confidence but alterations in neural network activity during moral decision-making.

Full text

NeuroImage: Clinical 30 (2021) 102645
Available online 27 March 2021
2213-1582/© 2021 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Neural responses to morally laden interactions in female inmates
with psychopathy
Keith J. Yoder
a
,
*
, Carla Harenski
b
,
c
, Kent A. Kiehl
b
,
c
, Jean Decety
a
,
d
a
Department of Psychology, University of Chicago, Chicago, IL, USA
b
The Mind Research Network and Lovelace Biomedical, Albuquerque, NM, USA
c
Department of Psychology, University of New Mexico, Albuquerque, NM, USA
d
Department of Psychiatry, and Behavioral Neuroscience, University of Chicago, Chicago, IL, USA
ARTICLE INFO
Keywords:
Emotion understanding
Decision-making
Empathy
Functional connectivity
Functional MRI
Forensic neuroscience - Moral evaluation
Female Psychopathy
ABSTRACT
Much of social cognition requires making inferences about the mental and emotional states of others. Moreover,
understanding the emotions of others is an important foundation for moral decision-making. Psychopathy is
associated with both aberrant emotional understanding and atypical hemodynamic responses when viewing and
evaluating morally laden social interactions. In the present functional MRI study, female inmates (N =107) were
asked to evaluate the likely emotional state of either the recipient or the initiator of harmful or helpful in-
teractions. Psychopathy was assessed with the Psychopathy Checklist-Revised (PCL-R). PCL-R scores were not
associated with differences in condence or accuracy ratings. However, psychopathy scores were signicantly
related to increased hemodynamic response in right dorsolateral prefrontal cortex when viewing harmful in-
teractions and decreased functional connectivity from right amygdala to inferior parietal cortex and insula, and
from temporal parietal junction to dorsomedial prefrontal cortex. Overall, this work indicates that in females,
psychopathy is associated with normal behavioral accuracy and condence but alterations in neural network
activity during moral decision-making.
1. Introduction
Humans, as social creatures, readily attribute emotional and cogni-
tive states to others when engaging in or observing third-party social
interactions. Emotion is an adaptive orienting system that evolved to
guide behavior. Emotion is also an interpersonal communication system
that elicits response from others. Thus, emotions can be viewed both as
intrapersonal and interpersonal states (Decety and Skelly, 2014).
Cognitive (e.g., attentional processes) and emotional processes are not
entirely separate entities. Rather, signals interact and are integrated at
both perceptual and executive levels (Pessoa, 2014).
Psychopathy is a personality disorder which includes a constellation
of traits, such as dishonesty, supercial charm, lack of empathy or guilt,
and impulsive behavior (Cleckly, 1941). Importantly, dysfunctional
socioemotional processing is a core feature of psychopathy (Hare, 2016;
Kiehl, 2015), and atypical emotional processing, such as decits in
empathy, is a risk factor for violent or criminal behavior (Anderson and
Kiehl, 2012; Blair, 2008; Olver and Wong, 2015; Seara-Cardoso and
Viding, 2014). Conicting behavioral and neuroscience investigations
have led to ongoing debates about the specicity of atypical empathic
processing, particularly whether decits are limited to distinct emotions
(e.g. fear and/or sadness) or are more general (Book et al., 2007; Dawel
et al., 2012; Deming et al., 2020; Glass and Newman, 2006; Hastings
et al., 2008; Marsh and Blair, 2008; Seara-Cardoso et al., 2012). While
both cognitive and emotional decits have been documented in in-
dividuals with high levels of psychopathic traits (Anderson et al., 2017),
most neuroscience studies report atypical neural responses during
perception and recognition of the emotions of others (Decety et al.,
2015, 2013b; Deming et al., 2020; Marsh et al., 2013; Sato et al., 2011).
Further, two recent meta-analyses indicate that across a variety of tasks,
psychopathy is marked by atypical neural responses in prefrontal, par-
alimbic, and insular regions (Deming and Koenigs, 2020; Poeppl et al.,
2019).
Socioemotional processing plays a critical role in moral reasoning
(Haidt and Graham, 2007; Van Bavel et al., 2015). Notably, harm
aversion is a crucial component of moral cognition (Decety and Cowell,
2018; Gray et al., 2012; Miller and Cushman, 2013). Studies reporting
moral insensitivity in individuals with psychopathy often interpret these
* Corresponding author at: Department of Psychology 5848 S. University Ave., Chicago, IL, 60637, USA.
E-mail address: kjyoder@uchicago.edu (K.J. Yoder).
Contents lists available at ScienceDirect
NeuroImage: Clinical
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https://doi.org/10.1016/j.nicl.2021.102645
Received 18 December 2020; Received in revised form 24 February 2021; Accepted 22 March 2021

NeuroImage: Clinical 30 (2021) 102645
2
effects as stemming from lack of empathy and callous disregard for
others (Blair, 2007; Cheng et al., 2012; Decety and Cowell, 2014a;
Harenski and Kiehl, 2011; Lockwood, 2016). Using the Moral Founda-
tions framework, which articulates distinct moral domains (Graham
et al., 2011), psychopathy was originally linked to specic reductions in
concern for the domains of harm and fairness (Aharoni et al., 2011;
Glenn et al., 2009a), though more recent work has identied reduced
concern across all domains (Jonason et al., 2015). Conversely, research
utilizing sacricial moral dilemmas has produced conicting results,
with some studies nding associations between psychopathic traits and
greater endorsement of utilitarian judgments among both un-
dergraduates and incarcerated populations (Bartels and Pizarro, 2011;
Koenigs et al., 2012), while others nd no differences in behavioral
responses (Cima et al., 2010; Glenn et al., 2009a; Tassy et al., 2013). A
recent meta-analysis concluded that psychopathy is weakly associated
with abnormal moral decision-making, rather than being characterized
by pronounced or overarching moral decits (Marshall et al., 2018). A
complementary motivational account suggests that psychopathy is
associated with relatively intact moral understanding but a lack of
motivation to apply this moral knowledge (Cima et al., 2010; Glenn
et al., 2009a; Tassy et al., 2013). Moreover, a growing body of neuro-
science evidence suggests that when individuals with psychopathy
provide moral evaluations that are indistinguishable from controls, as is
often the case, they do so by recruiting different brain circuits (Aharoni
et al., 2012; Yoder et al., 2015a).
However, the vast majority of studies examining neural functioning
in psychopathy have included only male participants. Psychopathy is a
well-documented risk factor for violent behavior and criminality in
males (Blais et al., 2014; Guy et al., 2010), and predicts violent recidi-
vism and future violence in prison (Camp et al., 2013; Olver and Wong,
2015). Emerging evidence from adolescents with conduct disorder
suggests that there are important sex differences in the impact of psy-
chopathic traits on brain structure and function (Michalska et al., 2015;
Smaragdi et al., 2017). The rates of female incarceration have risen over
the last decade (Carson and Anderson, 2016), indicating the pressing
importance of investigating psychopathic traits in female offenders and
determining whether the established links between psychopathic traits
and abnormal neural functioning observed in men also manifest in
women.
There is some debate about the specicity of empathic decits in
psychopathy. Empathy is a multifaceted construct which includes af-
fective, cognitive and motivational facets (Decety and Jackson, 2004;
Lockwood, 2016; Shamay-Tsoory, 2009), and each facet seems uniquely
related to moral cognition (Decety and Cowell, 2014b). Affective
empathy includes both the tendency to experience emotional distress in
response to the distress of others, as well as a motivation to respond
appropriately to another person’s emotional state. Cognitive empathy
refers to an individual’s propensity to adopt the perspective of another
person and imagine what another person is thinking or feeling (Shamay-
Tsoory, 2009). Cognitive empathy is closely related to theory of mind,
the ability to infer the beliefs and intentions of others as separate from
oneself (Decety and Jackson, 2004). Though some have argued that sex
differences in empathy are fundamental to psychological differences
(Baron-Cohen and Wheelwright, 2004), decades of research indicates
that sex differences in empathy are large when measured using self-
reports, but quickly diminish, or even become nonexistent, when
using behavioral measures and functional neuroimaging methods, such
as responding to others’ pain (Baez et al., 2017; Eisenberg and Lennon,
1983; Michalska et al., 2013). Some evidence suggests that psychopathy
is associated with reduced accuracy when inferring the emotional states
of others (Brook et al., 2013; Brook and Kosson, 2013), though the
impact of psychopathic traits on emotion processing does not always
replicate in women (e.g., Vitale et al., 2011). Other work indicates high
levels of psychopathic traits are associated with decits in inferring af-
fective states (e.g. emotions) alongside an intact ability to infer cognitive
states (e.g. beliefs) of others (Shamay-Tsoory et al., 2010). Converging
evidence from functional neuroimaging and lesion studies indicate that
the temporoparietal junction (TPJ), which is situated at the posterior
superior temporal sulcus (pSTS), and medial prefrontal cortex (mPFC)
are essential for detecting and representing mental states of others, and
play an important role in cognitive empathy and moral cognition
(Decety and Lamm, 2007; Gallagher and Frith, 2003; Lamm et al., 2007;
Moll et al., 2007; Saxe et al., 2004; Silani et al., 2013; Yoder and Decety,
2014a). In healthy participants, viewing others in pain reliably elicits
response in dorsal anterior cingulate (dACC) and anterior insula (aINS;
Decety et al., 2013a; Fallon et al., 2020; Lamm et al., 2011), core nodes
of the salience network which integrate multiple stimuli to coordinate
cortical and subcortical resources to respond to motivationally relevant
stimuli (Decety, 2011; Harsay et al., 2012; Shackman et al., 2011; Yoder
and Decety, 2018).
Moreover, these regions play critical roles in supporting moral
decision-making (Decety and Yoder, 2017; Krueger and Hoffman, 2016).
Previous work demonstrates that psychopathy, even when not associ-
ated with differences in socio-emotional judgments, is related to atypical
neural responses within these regions, especially pSTS/TPJ, amygdala,
and ventromedial prefrontal cortex (vmPFC), as well as the functional
connectivity with dACC and aINS (Harenski et al., 2010; Yoder et al.,
2015a, 2015b). Moreover, individuals with high levels of psychopathic
traits appear to not encode the pain of others as personally relevant,
though they can make use of this information if it becomes relevant to
the task at hand (Yoder et al., 2015a) or if they are imaging themselves
suffering (Decety et al., 2013a, 2013b). In fact, recent work suggests that
psychopaths do not spontaneously adopt the spatial perspective of
others, and that the magnitude of this dysfunction in altercentric
interference is correlated with real-world callous behaviors (Drayton
et al., 2018).
Given the complexity of the decits in socioemotional processing and
moral cognition in psychopathy, understanding the links between psy-
chopathic traits and moral cognition requires experimental manipula-
tions which focus on specic aspects of socioemotional processing in
ecologically meaningful contexts. In particular, there is good evidence
that just as individuals with high psychopathic traits “know” moral rules
but don’t “care” about them (Cima et al., 2010), such individuals do not
attend to socioemotional information in the same way as individuals
without psychopathy. Psychopathy is associated with reductions in
neural activity and functional connectivity within the salience network
when viewing visual depictions of morally laden scenarios, especially
when the moral content of the scenarios is relevant to the task (Yoder
et al., 2015a). Psychopathy has also been linked to reduced anatomical
connectivity of the uncinate fasciculus (Motzkin et al., 2011; Wolf et al.,
2015), which links the anterior temporal lobe, including amygdala and
aINS, to inferior frontal cortex, including vmPFC.
The rst, and to our knowledge, the only fMRI study of psychopathy
in female inmates found negative associations between PCL-R scores and
hemodynamic responses in right amygdala and rostral ACC during
emotional processing, and in the right TPJ specically during the pro-
cessing of moral scenarios (Harenski et al., 2014). Recent neuroimaging
work in non-incarcerated women identied associations between PCL-R
scores and connectivity, both anatomical white matter integrity (Lind-
ner et al., 2017) and functional connectome dened from resting-state
data (Lindner et al., 2018). These effects were more particularly pro-
nounced for Factor 2 scores, which reect the affective/interpersonal
dimension of psychopathy, suggesting that this dimension of psychop-
athy may be most important for understanding the impact of psycho-
pathic traits on neural functioning in female inmates.
The current study was designed to examine socioemotional pro-
cessing in response to third-party morally laden interactions in female
offenders. The emotional expressions of the protagonists were situated
in the context of dyadic interactions that were either intentionally
harmful or intentionally helpful. Harm and help represent prototypical
morally bad and morally good actions and provide a useful platform for
examining low-level sociomoral cognition (Yoder et al., 2015a). Based
K.J. Yoder et al.

NeuroImage: Clinical 30 (2021) 102645
3
on previous work, it was expected that inmates with higher levels of
psychopathy traits would be less likely to nd harmful outcomes as
salient, leading to reduced hemodynamic response in core nodes of the
salience network, particularly dACC, aINS, and amygdala. Moreover,
psychopathy was expected to be associated with little to no difference in
behavioral responses coincident with a shift towards reliance on pre-
frontal executive control systems, leading to increased response in
dlPFC. This shift was also expected to manifest as reductions in func-
tional connectivity seeded in amygdala and TPJ to other nodes of the
salience network and social cognition networks, such as insula, TPJ, and
dmPFC.
2. Materials and methods
2.1. Participants
115 women in a medium-maximum security state prison completed
all aspects of the study protocol. Eight participants showed excessive
movement in the MRI data (rotation >3 degrees or translation >3 mm)
and were excluded from analysis. Thus, the nal sample consisted of 107
women (M
age
=35.0, SD =8.2, range =20 – 53). Inclusion criteria were
age 18–59 years, female sex (not transitioning), no uncorrectable
auditory or visual decits, ability to speak and understand English,
reading level of at least 5th grade, not currently pregnant, no central
nervous system disease, no current major medical conditions, no hy-
pertension with complications, no lifetime history of psychotic disorder,
no self-reported psychotic disorder (with psychiatric hospitalization) in
a rst degree relative, no traumatic brain injury with loss of con-
sciousness >10 min, no drug use in last three months (self-report or
institution records), and no MRI contraindications such as metal in the
body. One participant was ambidextrous, while the remaining 106 were
right-handed. 65 (61%) of the women had been convicted of at least one
violent crime. The women were compensated for study participation at a
rate proportional to the institutional wages for work assignments at their
correctional facility, and provided written informed consent. All pro-
cedures and materials were approved by the Institutional Review Boards
at the University of Chicago and Ethical and Independent Review
Services.
Psychopathy was assessed using the Hare Psychopathy Checklist-
Revised (Hare, 2003) which was administered by trained research as-
sistants. The PCL-R includes four correlated facets, which can be
grouped into two higher order factors (Hare, 2016). Factor 1 captures
interpersonal and affective dimensions, while Factor 2 captures devel-
opmental, lifestyle, and antisocial aspects of psychopathy. Intelligence
Quotient (IQ) was assessed using the vocabulary and matrix reasoning
subtests from the Wechsler Adult Intelligence Scale 3rd Edition or the
Wechsler Abbreviated Scale of Intelligence 2nd Edition. PCL-R scores
showed small but signicant negative relationships with age (Spear-
man’s rho =-0.19, p =0.049) and IQ (Spearman’s rho =-0.20, p =
0.042). PCL-R scores were not signicantly related to conviction for at
least one violent crime (Odds Ratio =1.17, 95% CI [0.79, 1.73], p =
0.435).
2.2. Task stimuli
Participants completed a task previously used in a population of
incarcerated males (Decety et al., 2015). In each trial, participants were
shown a dyadic interactions depicting either intentional interpersonal
harm or intentional assistance. Depictions consisted of three static im-
ages presented to create apparent motion (image durations of 1.0, 0.2,
and 1.0 s). Following each scenario, participants were shown a cutout of
either the recipient of the behavior or the individual who initiated the
behavior. After a jittered interval (M =3 s, SD =1.2 s), a 2s video clip
appeared next to the cut-out and showed a person making one of six
expressions: happy, sad, frightened, angry, disgust, or in pain. Impor-
tantly, the interaction and cutout did not show a face, so it was possible
to counter-balance actors and expressions with recipients or agents (see
Fig. 1). After the video ended, the nal frame remained on the screen
next to the cutout, and participants were asked “Do you think the person
felt this way?” Participants indicated their response by pressing a key to
stop a red bar which began on the left (“No, not at all”) and moved to the
right (“Yes, denitely”). Trials were separated by a jittered interval (M
=3, SD =1.1 s). Stimuli were presented using the E-Prime 2.0 stimuli
presentation suite (Psychology Software Tools, Pittsburgh, PA, USA).
2.3. MRI acquisitions and analysis
Function images were acquired using the Mind Research Network
1.5 Tesla Siemens Magnetom Avanto Mobile unit (Washington, DC,
USA) which was equipped with a 32-element head coil. Echo-planar
images were acquired using a multiband sequence (posterior-to-ante-
rior phase encoding, multiband factor =12, repetition time/echo time
=350 ms / 39 ms, ip angle =37 degrees, eld of view =248 ×248
mm, matrix =70 ×70, voxel size =3.5 ×3.5 ×3.5 mm
3
). These images
were then realigned and motion-corrected using INRIAign (Freire et al.,
2002). Rather than performing slice-timing correction at this step, the
temporal derivative of each event was included (see below). EPI images
were normalized to the EPI MNI template (Calhoun et al., 2017) before
smoothing with an 8 mm Gaussian kernel. Images were preprocessed
and analyzed using SPM12 (Wellcome Department of Imaging Neuro-
science, London, UK) in MATLAB (MathWorks, Natick, MA, USA).
A general linear modeling (GLM) framework was used, where a ca-
nonical hemodynamic response function was convolved with a boxcar
function representing the onsets and durations of the events of interest.
Specically, the onsets of each scenario through the end of the third
picture, and the onset of each decision phase, beginning at the onset of
the actor cutout through the response. This created six trial regressors:
HarmScene, HelpScene, IdentifyAgentHarm, IdentifyRecipientHarm,
IdentifyAgentHelp, IdentifyRecipientHelp. Temporal derivatives were
also modeled for each event. The beta image pairs for each modeled
event amplitude and temporal derivative were combined into a single
magnitude image which was then passed to the second-level analysis
(Calhoun et al., 2004). Six movement parameters were entered as
nuisance regressors.
Second-level contrasts were derived by combining rst-level contrast
estimates. Psychopathy scores were modeled using either total PCL-R, or
Factor 1 and Factor 2. For each, mean-centered age in months and IQ
were entered as covariates of no interest. For group-based analysis,
participants with PCL-R scores of 30 or above (n =24) were categorized
as high psychopathy, consistent with the “diagnostic” cutoff proposed by
Hare (2003), and scores of 20 or below (n =45) were categorized as low.
Functional connectivity was assessed by modeling a psychophysiologi-
cal interaction between the task contrasts and mean signal extracted
from an anatomically dened right amygdala mask and a 10 mm radius
sphere placed in rTPJ (MNI × = 52, y =-54, z =16) based on previous
work investigating rTPJ connectivity during socioemotional processing
(Yoder et al., 2015a; Yoder and Decety, 2014a). Images were thresh-
olded to achieve family-wise error corrected p <0.05, determined using
the rst-level residual images to estimate smoothness for 3dClustSim
(Cox, 1996).
2.4. Behavioral data analysis
Two separate measures were extracted from the behavioral re-
sponses (Decety et al., 2015). First, the midpoint was subtracted from
the responses and the absolute value was taken to create a “condence”
measure, ranging from 0, the midpoint, to 3, the extreme end of the
scale. Accuracy was evaluated by limiting analyses to those trials where
there was a natural congruence between an individual’s emotion and the
situation: happy expressions for either individuals following a helpful
interaction, angry expressions for the perpetrators of harmful in-
teractions, and pain or sad expressions for victims of harmful
K.J. Yoder et al.

NeuroImage: Clinical 30 (2021) 102645
4
interactions.
Behavioral data were analyzed using complementary approaches in
R (version 4.0.2, R Core Team, 2015). First, repeated-measures analysis
of variance (ANOVA) modeled condence and accuracy in a 2 (Morality:
Harm|Help) ×2 (Actor: Agent|Recipient) basic model using the ‘afex’
package (Singmann et al., 2020) with pairwise comparisons interro-
gated with the ‘emmeans’ package (Lenth, 2020). Once t to the full
model, another model specically examined high and low psychopathy
groups. A complementary multilevel linear modeling (MLM) approach,
as implemented in the ‘lme4′package (Bates et al., 2015), regressed
behavioral responses on Morality and Actor, with participant modeled
using a random intercept. Psychopathy was modeled continuously using
PCL-R scores.
3. Results
The ANOVA for condence identied a marginal main effect of Actor
(F(1,106, F =3.92,
η
2G
=0.003, p =0.050) and a signicant Moral *
Actor interaction (F(1,106), F =15.89,
η
2G
=0.013, p <0.001; Fig. 1B).
Tukey’s comparisons revealed higher condence for recipients than
agents in harmful interactions (p =0.002) and higher condence for
helpful agents than harmful agents (p <0.001). These effects remained
the same when limiting the analysis to only the high and low psychop-
athy groups. No Group effects were signicant (all p >0.3). Modeling
psychopathy scores continuously also did not identify any signicant
effects (all p >0.2), and including psychopathy scores did not signi-
cantly improve model t over a model with just Moral and Actor terms
(Х
2
(4) =6.17, p =0.187).
Accuracy for the subset of trials with clear emotional mapping
revealed a signicant main effect of Moral (F(1, 106) =190.53,
η
2G
=
0.278, p <0.001) and a Moral * Actor interaction (F(1, 106) =9.75,
η
2G
=0.023, p =0.002; Fig. 1C). All pairwise comparisons were signicant
(largest p =0.035 for recipients of harm compared to agents of harm).
Accuracy was highest for recipients of help, then agents of help, agents
and harm, and recipients of harm had the lowest accuracy. As with
condence, restricting the analysis to only high and low psychopathy
individuals produced similar results, though the pairwise difference
between agents and recipients of harm became non-signicant (p =
0.192). No Group effects were signicant (all p >0.3). Modeling psy-
chopathy continuously in an MLM framework produced similar effects,
with psychopathy scores producing no signicant behavioral effects (all
p >0.6) and psychopathy score not improving explanatory power of the
model (Х
2
(4) =0.69, p =0.953).
Viewing harmful social interactions compared to helpful social in-
teractions elicited increased hemodynamic response throughout visual
cortex, much of the social decision-making network, including pSTS/
TPJ, and the core nodes of the salience network – i.e. dACC, aINS
(Fig. 2A, Table S1). In contrast, helpful actions were associated with
greater signal in bilateral caudate, vmPFC, and dlPFC. PCL-R scores
were associated with greater responses in right dlPFC when viewing
harmful compared to helpful interactions. Factor 1 and Factor 2 scores
were not uniquely associated with any signicant clusters.
During the emotion identication phase, decisions about harmful
interactions, compared to helpful interactions, elicited greater response
in lateral occipital cortex, fusiform gyrus, and bilateral inferior frontal
gyrus (IFG) extending into aINS and left inferior parietal (Fig. 2B;
Table S1). Decisions about helpful interactions were associated with
greater response in primary visual cortex, left precentral gyrus, right
aINS, SMA, and right caudate body. Combined with the viewing phase,
these main effects replicate previous whole-brain results using the same
Fig. 1. Task schematic and behavioral responses. A) Sample trial of harmful interaction with pain expression for recipient (top) and angry expression for agent
(bottom). Below are shown plots for the Actor * Moral interaction for condence across all responses (B) and accuracy for trials with clear emotion mappings (C).
K.J. Yoder et al.

NeuroImage: Clinical 30 (2021) 102645
5
task in a sample of incarcerated males (Decety et al., 2015), with the
exception of rTPJ, in which activation was not observed during the
evaluation phase in this study. PCL-R scores were associated with
reduced response in right STS when identifying the emotions of in-
dividuals involved in harmful compared to helpful interactions. Factor 1
scores were specically associated with reduced signal in right STS. No
clusters showed any signicant associations with Factor 2 scores.
When evaluating the emotions of protagonists who initiated harmful
compared to helpful interactions, greater neuro-hemodynamic response
was observed in bilateral IFG and left aINS, dlPFC, and TPJ (Fig. 3A;
Table S2). Identifying the emotional state of actors in helpful scenarios
elicited greater signal in cuneus, SMA, precentral gyrus and caudate.
When identifying the emotions of recipients of helpful compared to
harmful interactions, increased signal was observed in cuneus, SMA,
caudate body, and bilateral dlPFC (Fig. 3B). No regions showed greater
response when identifying recipients of harm compared to help. PCL-R
scores showed no signicant associations when identifying the emo-
tions of agents, but were associated with reduced signal in bilateral pSTS
when identifying the emotional state of the recipients of harm compared
to help (Fig. 3B). Factor 1 scores were not signicantly associated with
either contrast, but Factor 2 scores were signicantly associated with
reduced response in right pSTS, caudate, and ACC (Table S2).
When viewing harmful compared to helpful interactions, right
amygdala demonstrated increased functional connectivity with left aINS
(Fig. 4; Table S3). The rTPJ seed showed increased neuronal coupling
with left medial temporal areas, caudate and right medial and superior
frontal cortex (Fig. 4; Table S4). Right TPJ showed increased connec-
tivity with an overlapping cluster in left parietal, as well as increased
connectivity with precuneus and right parietal. When viewing harmful
compared to helpful interactions, PCL-R scores were associated with
reduced functional connectivity from amygdala to left parietal and right
temporal cortex, and with reduced connectivity from TPJ to left parietal
and parahippocampal gyrus (Fig. 4A).
While identifying emotions for harmful compared to helpful in-
teractions (Fig. 4B), right amygdala demonstrated increased connec-
tivity with a cluster in left parietal cortex extending to TPJ and into
anterior insula. Right TPJ also showed decreased connectivity with right
fusiform gyrus and dACC. PCL-R scores were associated with decreased
amygdala connectivity with precuneus and bilateral pSTS, extending
into left insula. Connectivity between rTPJ and dACC/SMA was also
negatively related to PCL-R scores.
Identifying the emotions of agents who initiated actions (Fig. 5A;
Table S6) elicited reduced connectivity from rTPJ to vmPFC and
increased connectivity with caudate and bilateral postcentral gyri.
Specically focusing on identifying the emotional state of the agent of
the interaction, PCL-R scores were negatively related to connectivity
between right amygdala and left aINS, TPJ, IFG, precuneus (Table S5).
PCL-R scores were not related to functional connectivity seeded in rTPJ
during identication of agent emotions. Factor 2 was specically asso-
ciated with decreased functional connectivity between amygdala and
left pSTS and bilateral aINS.
For recipients (Fig. 5B), TPJ showed greater connectivity with
dACC/SMA. No regions showed signicant functional connectivity in-
creases or decreases with right amygdala when examining harmful
compared to helpful interaction specically for the actor or specically
for the recipient. PCL-R scores were signicantly related to reduced
connectivity between right amygdala and left temporal regions,
including pSTS, and reduced connectivity between right TPJ and SMA.
Factor 2 scores were associated with decreased connectivity between
both amygdala and TPJ with SMA, and between amygdala and right
aINS, inferior frontal gyrus, and inferior parietal cortex.
Fig. 2. Whole-brain results for morally laden content during task phases. Regions more sensitive to harmful (red) or helpful (blue) interactions during the viewing
phase (A) or emotion identication phase (B). Also shown are regions identied by the Harm-Help contrast as having a positive association (green) or negative
association (violet) with PCL-R scores. All regions signicant at FWEp <0.05 (height =0.005, extent =100). (For interpretation of the references to colour in this
gure legend, the reader is referred to the web version of this article.)
K.J. Yoder et al.

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6
Fig. 3. Whole-brain results for identifying emotional stats of different individuals. Regions more sensitive to harmful (red) or helpful (blue) interactions when
evaluating the emotional state of agents who initiated actions (A) or recipients of actions (B). Also shown are regions identied by the Harm-Help contrast as having a
positive association (green) or negative association (violet) with PCL-R scores. All regions signicant at FWEp <0.05 (height =0.005, extent =100). (For inter-
pretation of the references to colour in this gure legend, the reader is referred to the web version of this article.)
Fig. 4. Whole-brain functional connectivity re-
sults for task phases. Regions show increased
(red) or decreased (blue) connectivity with right
amygdala (left) or TPJ (right) during the view
phase (A) or emotion identication phase (B).
Regions where connectivity was negatively asso-
ciated with PCL-R scores are shown in green. All
regions signicant at FWEp <0.05 (height =
0.005, extent =100). (For interpretation of the
references to colour in this gure legend, the
reader is referred to the web version of this
article.)
K.J. Yoder et al.

NeuroImage: Clinical 30 (2021) 102645
7
4. Discussion
The goal of this study was to examine the impact of psychopathic
traits on behavioral and neuro-hemodynamic measures of socioemo-
tional understanding of morally laden interactions in adult female of-
fenders. Overall, and as predicted, psychopathy, whether viewed as a
dichotomous variable or a continuous trait, was not related to differ-
ences in behavioral responses. Condence ratings and behavioral ac-
curacy were not signicantly related to PCL-R scores, and the high and
low psychopathy groups did not signicantly differ on either measure.
Contrary to predictions, psychopathy was not signicantly related to
reduced responses in amygdala or dACC during either third-party
evaluation or identication phases. While women overall did demon-
strate greater dACC response when viewing harmful compared to
helpful interactions, no amygdala response was detected in either phase.
However, psychopathy scores were signicantly related to increased
hemodynamic response in rdlPFC when viewing harmful scenarios and
widespread decreases in functional connectivity seeded in right amyg-
dala and right TPJ. Overall, these results suggest that the nodes of the
salience and social cognition networks respond similarly in female
psychopaths, but the networks are largely disconnected in comparison
to inmates with low levels of psychopathic traits.
The whole-brain results for viewing harmful compared to helpful
interactions is consistent with a large body of work in moral neurosci-
ence and third-party evaluations (Eres et al., 2018; Krueger and Hoff-
man, 2016), with regions important for theory of mind and saliency,
especially bilateral TPJ, insula, and dACC/SMA showing greater
response to intentional harm (Decety and Yoder, 2017; Yoder and
Decety, 2014a). In contrast, core regions of the reward circuitry, namely
vmPFC and caudate, as well as dlPFC demonstrated greater response
when observing helpful interactions (Decety and Porges, 2011).
Right dlPFC response directly replicates previous moral judgment
work using similar stimuli in undergraduates and inmates (Yoder et al.,
2015a; Yoder and Decety, 2014a, 2014b). The dlPFC was the only region
showing signicant associations with PCL-R total score (Fig. 2A). This
result ts with the notion that individuals with high levels of psycho-
pathic traits rely on prefrontal recruitment in order to maintain similar
behavior responses (Glenn et al., 2009b; Yoder et al., 2015a).
When identifying emotions of individuals involved in harmful
compared to helpful interactions, psychopathic traits were associated
with reduced response in a region of right STS extending into deep
pSTS/TPJ (Fig. 2B). Response in pSTS is reliably implicated when
inferring mental states of others in pain (Lamm et al., 2011), but pSTS
also plays important integrative roles for incorporating mental state
information into social decision-making contexts (Carter and Huettel,
2013; Yoder and Decety, 2018). Reduced response in this region was
specically associated with Factor 1, but not Factor 2. Thus, reduced TPJ
response here suggests that women with higher levels of psychopathic
traits, particularly the interpersonal-affective dimension of callousness,
may rely less on others’ mental states when attempting to label
emotional expressions of others. Future work could clarify this rela-
tionship by examining emotional accuracy while varying the amount of
mental state information that is available and testing whether Factor
scores are associated with specic decreases in performance.
When identifying the emotion of the recipient of an interaction
(Harm – Help), PCL-R scores were associated with reduced response in
bilateral pSTS (Fig. 3B). Interestingly, whereas pSTS response when
identifying emotions generally was associated with Factor 1 scores,
Factor 2 scores were associated with reduced pSTS response specically
for identifying the emotions of recipients (Table S2). This dissociation
between Factor 1 and 2 suggests that the Interpersonal/Affective and
Developmental/Lifestyle/Antisocial dimensions of psychopathy may
differentially impact use of mental state information when evaluating
the emotional states of others in general or specically of victims. The
lack of an association between psychopathic traits and amygdala or
dACC response is surprisingly. However, this result could be a
Fig. 5. Whole-brain functional connectivity results for different actors. Regions show increased (red) or decreased (blue) connectivity with right amygdala (left) or
TPJ (right) when identifying agents who initiated actions (A) or recipients (B). Regions where connectivity was negatively associated with PCL-R scores are shown in
green. At right are shown regions where Factor 2 scores were negatively associated with functional connectivity seeded in amygdala (violet) or TPJ (yellow). All
regions signicant at FWEp <0.05 (height =0.005, extent =100). (For interpretation of the references to colour in this gure legend, the reader is referred to the
web version of this article.)
K.J. Yoder et al.

NeuroImage: Clinical 30 (2021) 102645
8
consequence of directly comparing harmful and helpful interactions,
rather than including a neutral condition. Further work is required to
directly test this possibility.
The impact of psychopathic traits was more robust when examining
functional connectivity. When viewing morally laden scenarios (Harm –
Help), PCL-R scores were associated with reduced functional connec-
tivity to left inferior parietal cortex for both the amygdala and TPJ seeds
(Fig. 4). Moreover, the amygdala seed revealed psychopathy-linked
reduced connectivity between right amygdala and right TPJ. These al-
terations in functional connectivity are consistent with recent reports of
disrupted functional networks association with higher psychopathic
traits in incarcerated males (Espinoza et al., 2018; Tillem et al., 2019).
Thus, psychopathy appears to alter connectivity within the social
cognition network when inmates viewed morally laden images.
During the emotion identication phase, PCL-R scores predicted
reduced connectivity between right amygdala and left TPJ. This effect
remained regardless of whether the trial was focused on the agent or the
recipient, suggesting that for individuals with high levels of psycho-
pathic traits the usually aversive salience of interpersonal harm is
disconnected from mental state representations (Buckholtz and Marois,
2012). For agents, PCL-R was also related to reduced connectivity to
aINS. This ts with previous work demonstrating reduced aINS response
during face processing among adolescent females with conduct disorder
(Fairchild et al., 2014). This is particularly important given the role of
the insula in salience processing and signaling motivationally relevant
information (Harsay et al., 2012; Krueger and Hoffman, 2016). The
negative relationship between PCL-R and amygdala-insula coupling
suggests that individuals with high levels of psychopathic traits don’t
encode violent others as personally salient, potentially because they
don’t view others behaving antisocially as unexpected. This would be
consistent with studies linking increased psychopathic traits in the
general population to reduced amygdala connectivity (e.g., Dotterer
et al., 2020; Waller et al., 2019; Yoder et al., 2015b). However, future
studies could directly test this effect using violation of expectation
paradigms.
Interestingly, while Factor 1 scores were not signicantly associated
with any changes in functional connectivity during the recipient iden-
tication phase, higher Factor 2 scores were associated with reductions
in connectivity, specically to dACC/SMA. Some previous work with
undergraduate and incarcerated males found that callous-unemotional
traits were specically linked to reduced connectivity with dACC and
right amygdala (Yoder et al., 2015b, 2015a). Moreover, large-scale in-
vestigations of functional connectivity in incarcerated males has linked
Factor 1, rather than Factor 2, to altered network connectivity, partic-
ularly with the salience network (Espinoza et al., 2018; Thijssen and
Kiehl, 2017). Thus, the somewhat surprising link with Factor 2 in the
current study suggests that the dimensions of psychopathy may impact
different neural systems in women and men.
5. Conclusion
Overall, the results of our study replicate previous work demon-
strating links between higher levels of psychopathic traits and wide-
spread decreases in functional connectivity seeded in amygdala and TPJ
during socioemotional processing and decision-making. Importantly,
the current study extends these ndings to incarcerated females with
psychopathic traits, a population that is severely understudied. Much
previous work has highlighted specic links between psychopathy and
reduced hemodynamic response and connectivity within neural net-
works anchored by amygdala, dACC, and aINS. However, these results
provide important preliminary evidence that the antisocial dimension of
psychopathy is more important than the affective/interpersonal
dimension for explaining this effect in women.
CRediT authorship contribution statement
Keith J. Yoder: Methodology, Software, Writing - original draft,
Writing - review & editing, Visualization. Carla Harenski: Data cura-
tion, Validation, Writing - original draft. Kent A. Kiehl: Data curation,
Project administration, Writing - original draft. Jean Decety: Concep-
tualization, Methodology, Writing - original draft, Writing - review &
editing, Funding acquisition.
Declaration of Competing Interest
The authors declare that they have no known competing nancial
interests or personal relationships that could have appeared to inuence
the work reported in this paper.
Acknowledgments
The work was supported by the National Institutes of Health [grant
number R01MH109329].
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.nicl.2021.102645.
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