doi:10.1093/scan/nst014
SCAN (2014) 9, 505^512
Disrupted neural processing of emotional faces in
psychopathy
Oren Contreras-Rodrı́guez,1,2 Jesus Pujol,1 Iolanda Batalla,3 Ben J. Harrison,1,4 Javier Bosque,5
Immaculada Ibern-Regàs,6 Rosa Hernández-Ribas,1,2 Carles Soriano-Mas,1,2 Joan Deus,7 Marina López-Solà,1,2
Josep Pifarré,3 José M. Menchón,2 and Narcı́s Cardoner1,2
1
MRI Research Unit, CRC Mar, Hospital del Mar, Barcelona, Spain, 2Department of Psychiatry, Bellvitge University Hospital, Bellvitge Biomedical
Research Institute (IDIBELL), CIBERSAM, Barcelona, Spain, 3Gestió de Serveis Sanitaris (GSS), Hospital de Santa Maria and Biomedical Research
Institute, Lleida, Spain, 4Melbourne Neuropsychiatry Centre, Department of Psychiatry, University of Melbourne and Melbourne Health, Australia,
5
Medical Service, Centre Penitenciari de Ponent, Lleida, Spain, 6Department of Justice, Generalitat de Catalunya, Barcelona, Spain, and
7
Department of Clinical and Health Psychology, Autonomous University of Barcelona, Barcelona, Spain
Psychopaths show a reduced ability to recognize emotion facial expressions, which may disturb the interpersonal relationship development and successful social adaptation. Behavioral hypotheses point toward an association between emotion recognition deficits in psychopathy and amygdala
dysfunction. Our prediction was that amygdala dysfunction would combine deficient activation with disturbances in functional connectivity with cortical
regions of the face-processing network. Twenty-two psychopaths and 22 control subjects were assessed and functional magnetic resonance maps were
generated to identify both brain activation and task-induced functional connectivity using psychophysiological interaction analysis during an emotional
face-matching task. Results showed significant amygdala activation in control subjects only, but differences between study groups did not reach
statistical significance. In contrast, psychopaths showed significantly increased activation in visual and prefrontal areas, with this latest activation
being associated with psychopaths affective–interpersonal disturbances. Psychophysiological interaction analyses revealed a reciprocal reduction in
functional connectivity between the left amygdala and visual and prefrontal cortices. Our results suggest that emotional stimulation may evoke a
relevant cortical response in psychopaths, but a disruption in the processing of emotional faces exists involving the reciprocal functional interaction
between the amygdala and neocortex, consistent with the notion of a failure to integrate emotion into cognition in psychopathic individuals.
Keywords: psychopathy; face recognition; fMRI; functional connectivity; amygdala
INTRODUCTION
Psychopathy is characterized by the presence of callous and unemotional personality traits (Hare, 2003). The apparent emotional insensitivity of psychopaths is thought to be closely related to a reduced
ability to discriminate affective cues in others, which in turn may disturb the normal development of interpersonal relationships and successful social adaptation (Blair and Coles, 2000; Blair, 2006; Corden
et al., 2006).
There is strong evidence to suggest that the recognition of fearful and
sad emotional facial expressions is impaired in psychopathy (Blair and
Coles, 2000; Blair et al., 2001; Stevens et al., 2001; Montagne et al., 2005;
Dadds et al., 2006; Dolan and Fullam, 2006; Mitchell et al., 2006), while
other studies have reported deficits in the recognition of disgust
(Kosson et al., 2002; Hansen et al., 2008). Although less consistently
observed, some studies have also indicated that the perception of faces
with a positive emotional valence (e.g. happiness) may be altered in
psychopaths (Dolan and Fullam, 2006; Hastings et al., 2008; Pham
and Philippot, 2010), which is broadly consistent with other evidence
that they show decreased subjective arousal (Eisenbarth et al., 2008) and
abnormal brain responses (Deeley et al., 2006) to happy faces, as well as
reduced startle reflex inhibition (Levenston et al., 2000) and
Received 9 July 2012; Accepted 27 January 2013
Advance Access publication 5 February 2013
We thank the collaboration of the Secretaria de Serveis Penitenciaris, Rehabilitació i Justı́cia Juvenil and the
Centres Penitenciaris de Catalunya. This work was supported in part by the Fondo de Investigaciones Sanitarias de
la Seguridad Social of Spain (PI050884 and PI050884), the Ministerio de Ciencia e Innovación of Spain (SAF201019434) and the Departament de Justı́cia de la Generalitat de Catalunya. Dr Harrison is supported by a National
Health and Medical Research Council of Australia (NHMRC) Clinical Career Development Award (628509). Dr SorianoMas is funded by a ‘Miguel Servet’ contract from the Carlos III Health Institute (CP10/00604). Drs Deus and LopezSola are members of the Research Group SGR-1450 of the Catalonia Government.
Correspondence should be addressed to Dr Jesus Pujol, Department of Magnetic Resonance, CRC Mar, Hospital
del Mar, 25-29 Passeig Marı́tim, 08003 Barcelona, Spain. E-mail: [email protected]
electrodermal responses (Herpertz et al., 2001) to pleasant stimulation.
These studies, taken together with knowledge that fear recognition is
generally more difficult than happiness recognition (Elfenbein and
Ambady, 2002), suggest that psychopaths may show a general impairment of emotional processing, as opposed to a specific deficit in the
processing of negative cues (Cleckley, 1976; Herpertz et al., 2001).
Emotional face processing involves a distributed brain network,
including occipital areas, the fusiform gyrus, the amygdala and prefrontal regions (Haxby et al., 2000; Ishai et al., 2005). The activity in
the elements of this network is modulated via their well-established
reciprocal connections (Pessoa et al., 2002; Fairhall and Ishai, 2007;
Pujol et al., 2009). The amygdala is central to emotional face recognition due to its specific role in stimuli saliency detection (Davidson
et al., 2000; Adolphs, 2008).
The hypotheses generated from the large body of behavioral data
commonly point toward an association between the deficit in facial
affect recognition and amygdala dysfunction in antisocial individuals
(Marsh and Blair, 2008). In support of this notion, neuroimaging studies have found abnormal amygdala response to fearful facial expressions (Marsh et al., 2008; Jones et al., 2009) in children and adolescents
showing callous–unemotional traits. In normal student populations,
subjects scoring above average on callous–unemotional traits in the
Psychopathy Personality Inventory (Lilienfeld and Andrews, 1996)
showed reduced amygdala and medial frontal cortex activation
(Gordon et al., 2004; Han et al., 2011) together with increased visual
cortex and prefrontal cortex activation (Gordon et al., 2004) during the
processing of emotion facial expressions. Despite this evidence, very few
imaging studies have been conducted in adult populations that formally
satisfy psychopathy criteria (Hare, 2003). One study reported abnormal
activity in visual regions in response to fearful and happy faces in criminal psychopaths (Deeley et al., 2006).
ß The Author (2013). Published by Oxford University Press. For Permissions, please email: [email protected]
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There is increasing evidence that brain alterations in psychopathy
also involve neural connectivity. We recently identified reduced functional connectivity between frontal and posterior cingulate cortices in
criminal psychopaths under resting-state imaging conditions (Pujol
et al., 2011). Aberrant functional connectivity of the posterior cingulate
cortex has also been identified during an auditory target detection
‘oddball’ task in association with interpersonal and affective symptoms
of psychopathy (Juárez et al., 2013). Another study demonstrated abnormal microstructural integrity in the uncinate fasciculus, which is
the white matter pathway linking the anterior temporal and amygdala
region with the orbitofrontal cortex (Craig et al., 2009). Motzkin et al.
(2011) confirmed both reduced structural integrity in the right uncinate fasciculus and reduced functional connectivity of the frontal cortex
with both the amygdala and posterior cingulate cortex. Specifically
using emotional face stimulation, Marsh et al. (2008) identified
reduced functional connectivity between the amygdala and ventromedial prefrontal cortex during the processing of fearful expressions
in their children and adolescents with callous–unemotional traits.
The primary aim of the current study was to comprehensively examine brain activation and functional connectivity responses in criminal
psychopaths when performing a validated emotional face-recognition
task (Hariri et al., 2000). This task served to assess implicit processing
of general emotional stimulation in psychopaths, including both positive and negative emotional cues. Our hypothesis was that psychopaths
would demonstrate a disruption between putative emotional and cognitive components of the face-processing network. Specifically, we predicted that they would demonstrate reduced functional connectivity
between the amygdala and the other network key regions. Consistent
with prior studies, we also expected decreased activation in limbic
regions in psychopaths combined with increased activation of neocortical areas, presumably indicating compensatory neural processes
(Levenston et al., 2000; Kiehl et al., 2001; Glenn et al., 2009; Gordon
et al., 2004; Jones et al., 2009).
MATERIALS AND METHODS
Participants
Twenty-two psychopathic men (Hare, 2003) with a documented history of severe criminal offense were assessed and compared with 22
non-offender control subjects. Characteristics of both samples are fully
described in Table 1 and in a previous report (Pujol et al., 2011).
A total of 105 convicted subjects were initially evaluated using a
comprehensive clinical protocol. The sample showed a mean
Psychopathy Checklist-Revised (PCL-R) score (Hare, 2003) of 27.8
and served to select individuals for functional magnetic resonance
(fMRI) evaluation according to the following criteria (i) total PCL-R
score >20 or PCL-R Factor 1 >10, (ii) documented severe criminal
offense, (iii) absence of Diagnostic and Statistical Manual of Mental
Disorders-Fourth Edition (DSM-IV) Axis I diagnosis with the exception of past history of substance abuse, (iv) absence of DSM-IV Axis II
diagnosis, apart from antisocial personality disorder, (v) absence of
symptomatic medical and neurological illness, (vi) normal IQ according to the Wechsler Adult Intelligence Scale-Third Edition-Revised
(WAIS-III-R; Wechsler, 1997) (sample total IQ in mean s.d. is
108 14) and (vii) obtaining subject-specific full administrative permissions and special police custody during the fMRI assessment day,
which was limited to 23 individuals (valid cases, n ¼ 22).
Psychopathy assessment
Information for rating the PCL-R was collected by a trained senior
psychiatrist from a comprehensive semi-structured interview with the
inmate and a review of his institutional files and all available additional
information. For the PCL-R, each of the 20 items was scored 0, 1 or 2,
Table 1 Characteristics of study groups
Mean s.d.
Characteristics
Age, years (range)
Gender, men
Vocabulary WAIS-III
Education, years
Handedness (left/right)
PCL-R total
PCL-R Factor 1
PCL-R Factor 2
Comorbidities
DSM-IV-R Axis I diagnosisa
Hamilton Depression Scale score
Hamilton Anxiety Scale score
Y-BOCS, total score
DSM-IV-R Axis II diagnosisb
Impulsiveness Scale, total score
Sensitivity to punishment
Sensitivity to reward
Controls
Psychopaths
40.6 9.5 (28–61)
22
10.3 2.3
10.5 2.3
2/20
0.8 1.9
0.4 1.1
0.3 0.6
39.8 9.2 (28–64)
22
10.9 3.0
9.0 2.7
1/21
27.8 4.5*
12.5 2.2*
13.2 4.7*
None
0.4 1.0
0.8 1.1
00
None
34 15
5.8 4.9
7.1 4.6
None
1.9 2.1*
1.8 3.2
0.5 2.2
None
53 23*
8.1 5.5
11.9 5.5*
*P < 0.01.
a
Except history of substance abuse.
b
Except APD.
APD ¼ antisocial personality disorder; PCL-R ¼ psychopathy checklist-revised; Y-BOCS ¼ Yale–Brown
Obsessive–Compulsive Scale.
depending on the degree to which it was exhibited. The Spanish version of PCL-R was used (Hare, 2003). The internal consistency of the
assessment was tested for the whole 105-subject sample obtaining a
Cronbach’s coefficient of 0.79 (inter-item correlation mean ¼ 0.36)
for PCL-R total score.
Offense history
All 22 individuals were incarcerated in correctional institutions situated in Catalonia (Spain). The mean ( s.d.) completed incarceration
time at inclusion was 88 63 months (range 12–251 months). The
mean time of accumulated sentences was 243 127 months (range
96–546 months). All were violent armed offenders. Twenty-one of
the individuals had committed violent robberies. Fifteen individuals
were convicted murderers. Twelve individuals had a criminal record
prior to the age of 15 years. None of them had a sexual offense record.
Substance use/abuse and medical records
Although we sought to recruit a group of relatively ‘pure’ psychopaths,
we avoided excessive subject exclusion from associated medical factors
in an attempt to maximally provide a generally representative inmate
psychopath population. No subject had consumed alcohol (except for
one sporadic consumer) or relevant amounts of psychoactive substances for at least 2 months prior to the assessment (verified using
drug-urine testing). A total of five individuals showed a history of
alcohol abuse and fifteen individuals had been sporadic consumers
of alcohol. Sixteen individuals had a history of other psychoactive
substance use.
None of the subjects had suffered from any relevant symptomatic
medical illness prior to the study. Four individuals showed positive
testing for asymptomatic HIV, four additional individuals for asymptomatic hepatitis B virus and three for asymptomatic hepatitis C virus.
None of them presented with neurological complications.
The sample of healthy non-offender subjects were recruited from the
community matching the psychopathy group by age, sex and scores on
the Vocabulary subscale of WAIS-III and also underwent a comprehensive medical and psychiatric assessment (Table 1). All cases and
control subjects gave written informed consent after receiving a
Disrupted neural face processing in psychopathy
complete description of the study, which was approved by local research and ethics committees (IMIM Hospital del Mar, Barcelona and
Hospital Universitari Arnau de Vilanova, Lleida). The investigation
was carried out in accordance with the Declaration of Helsinki.
Emotional face-matching task
Subjects were assessed using a modified version of the emotional facematching task originally reported by Hariri et al. (2000). The task was
identical to that described in our previous studies (Pujol et al., 2009;
Cardoner et al., 2011). Briefly, during each 5 s trial, subjects were
presented with a target face (center top) and two probes faces
(bottom left and right) and were instructed to match the probe expressing the same emotion to the target by pressing a button in either
their left or right hand. An fMRI block consisted of six consecutive
trials in which the target face was either happy or fearful, and the probe
faces included two out of three possible emotional faces (happy, fearful
and angry). As a control condition, subjects were presented with 5 s
trials of ovals or circles in an analogous configuration and were instructed to match the shape of the probe to the target.
A total of six 30 s blocks of faces (three happy and three fearful) and
six 30 s blocks of the control condition were presented interleaved in a
pseudo-randomized order. A fixation cross was interspersed between
each block. The paradigm was presented visually on a laptop computer
running Presentation Software (http://www.neurobehavioralsystems.
com). MRI-compatible high-resolution goggles (VisuaStim Digital
System, Resonance Technology Inc., Northridge, CA, USA) were
used to display the stimuli. Subjects’ task responses were registered
using a right- and a left-hand response device based on optical fiber
transmission (NordicNeuroLab Inc., Bergen, Norway).
Image acquisition and preprocessing
A 1.5 T Signa Excite system (General Electric, Milwaukee, WI, USA)
equipped with an eight-channel phased-array head coil and single-shot
echo-planar imaging (EPI) software was used. Functional sequences
consisted of gradient recalled acquisition in the steady state [time of
repetition (TR) ¼ 2000 ms; time of echo (TE) ¼ 50 ms; pulse
angle ¼ 908] within a field of view of 24 cm, with a 64 64 pixel matrix
and with a slice thickness of 4 mm (inter-slice gap ¼ 1 mm). Twentytwo interleaved slices, parallel to the anterior–posterior commissure
(AC–PC) line, were acquired to cover the whole brain. The sequence
first included four additional dummy volumes to allow the magnetization to reach equilibrium.
Imaging data were transferred and processed on a Microsoft
Windows platform running MATLAB version 7 (The MathWorks
Inc., Natick, MA, USA). Image preprocessing was performed in
SPM5 (Statistical Parametric Mapping Software, http://www.fil.ion.
ucl.ac.uk/spm/) and involved motion correction, spatial normalization
and smoothing using a Gaussian filter (full-width at half-maximum of
8 mm). Data were normalized to the standard SPM-EPI template and
re-sliced to 2 mm isotropic resolution in Montreal Neurological
Institute (MNI) space. We excluded data from one psychopathic individual and one control from the larger original samples of 23 subjects, because of technical problems during fMRI.
Statistical analyses
Behavioral analysis
The Statistical Package for the Social Sciences (SPSS) version 15.0 was
used. Behavioral measurements were compared using independent
sample Student’s t-test. Task performance was analyzed using repeated
measures analysis of variance with ‘accuracy’ and ‘reaction time’ (fearful faces, happy faces and shapes) as the within-subject factor and
SCAN (2014)
507
‘study group’ (controls and psychopaths) as the between-subject
factor to assess interactions.
Functional MRI analysis
Main task effects. First-level (single-subject) SPM contrast (.con)
images were estimated for the following three tasks effects of interest:
all faces > shapes, fear faces > shapes and happy faces > shapes. Four
regressors were used in these analyses to model conditions separately
corresponding to fearful, happy, shapes and baseline. A hemodynamic
delay of 4 s was considered and a high-pass filter was used to remove
low-frequency noise (1/128 Hz). The resulting first-level contrast
images were then carried forward to subsequent second-level
random-effects (group) analyses. One-sample t-test was used to
assess the main task effects and two-sample t-test to assess group differences within the network activated by the task (identified with a
group conjunction analysis).
Psychophysiological interactions analysis
One established method for characterizing functional connectivity
within brain networks in the context of experimental tasks is ‘psychophysiological interaction’ (PPI) analysis (Friston et al., 1997). Using
PPI analysis, abnormal functional connectivity between key regions of
the ‘face-processing network’ has been characterized in social phobia
(Pujol et al., 2009; Danti et al., 2010), autism spectrum disorder (Monk
et al., 2010) and obsessive–compulsive disorder (Cardoner et al., 2011).
A series of PPI analyses were carried out in SPM5 (Friston et al.,
1997) to assess the influence of task (the ‘psychological factor’) on the
strength of functional coupling (‘functional connectivity’) between the
amygdala and the emotional face network (voxels activated during
task) and between the network (selected regions of interest, ROIs)
and the amygdala.
The placement of source ROIs was determined from a global
(group-combined) analysis of the ‘all faces > shapes’ contrast. The
fMRI signal time course was extracted at peak activation for right (x,
y, z: 32, 86, 8) and left (22, 92, 8) visual cortices; right (40,
54, 22) and left (40, 56, 26) fusiform gyri; right (28, 0, 26)
and left (22, 2, 26) amygdalae; and right (50, 22, 22) and left
(46, 20, 24) prefrontal cortices. The fMRI signal time course for each
selected ROI was obtained using the first eigenvariate value from a 4
mm radial sphere placed on these anatomical coordinates.
As in previous studies (Pujol et al., 2009; Cardoner et al., 2011), a
first-level analysis was performed for each subject to map areas where
fMRI signal was predicted by the cross-product (PPI interaction term)
of the ‘physiological’ (deconvolved time course of the given ROI) and
the ‘psychological’ factors (regressors representing the experimental
paradigm). Separate models were performed for the contrasts all
faces > shapes, fearful faces > shapes and happy faces > shapes. Both
the physiological and the psychological factors were included in the
final SPM model as confound variables.
First-level individual contrast images were then included in a second-level random-effects (group) analysis to assess task-induced reciprocal functional connectivity between the amygdala and the
emotional face network. Amygdala to emotional face network connectivity was masked by task activation map (group conjunction analysis)
and network (selected ROIs) to amygdala connectivity by an anatomical mask of the amygdala created with the Wake Forest University
(WFU) PickAtlas (Maldjian et al., 2003). Although our primary target
was the amygdala, connectivity for each selected ROI was additionally
explored within the entire emotional face network (see Supplementary
material for further details).
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Correlation analysis
Voxel-wise correlation analyses were performed in SPM5 to map the
association between psychopathy severity (using total PCL-R scores,
Factor 1 and Factor 2 as regressors) and both brain activation and taskinduced functional connectivity in the psychopathy group.
Thresholding criteria
Group-level brain activation and task-induced functional connectivity
maps were thresholded at PFDR < 0.05, whole-brain corrected.
Between-group differences and within-group correlations within the
network of interest were considered significant when involving a minimum cluster extension of 200 voxels at P < 0.01, uncorrected.
RESULTS
Behavioral performance
Control subjects and psychopaths showed a similar performance
during the emotional face task (Table 2). There was no significant
interaction between study group and task condition with regards to
task accuracy [F(2,84) ¼ 1.3, P ¼ 0.27] nor a significant main effect of
group [F(1,42) ¼ 1.3, P ¼ 0.26]. There was, however, a main effect of
task condition [F(2,84) ¼ 4.7, P < 0.01] to which overall accuracy for
fearful faces was lower than for happy faces (P ¼ 0.04) and shapes
(P ¼ 0.009).
There was no significant interaction between study group and task
condition with regards to reaction time [F(2,84) ¼ 0.2, P ¼ 0.82] and
no significant main effect of group [F(1,42) ¼ 0.2, P ¼ 0.63]. There was
a main effect of task condition [F(2,84) ¼ 165.1, P < 0.0001] to which
reaction time for fearful face was slower than for both happy faces
(P < 0.0001) and shapes (P < 0.0001), and happy faces slower than
shapes (P < 0.0001).
Functional MRI
Brain response to emotional faces
Brain activation for the ‘faces > shapes’ contrast in both groups bilaterally included a large extension of the visual cortex, the fusiform
gyrus, the posterior part of the parietal lobe, the hippocampus, superior brainstem, and medial and lateral prefrontal areas. Additional activation was identified in the right amygdala in control subjects, but
not in psychopaths. Psychopaths, on the other hand, showed significant activation in the basal ganglia and thalamus. Between-group comparisons showed that relative to control subjects, psychopaths
demonstrated significantly greater activation of visual areas, medial
frontal cortex and the left prefrontal cortex (Figure 1 and Supplementary Table S1). No brain region showed significantly greater activation
in control subjects.
Separate analyses for the contrasts ‘fearful faces > shapes’ and ‘happy
faces > shapes’ showed a brain activation pattern similar to the pattern
obtained for the ‘all faces > shapes’ contrast. Between-group comparisons also demonstrated significantly greater activation of visual areas,
medial frontal cortex and the left prefrontal cortex in psychopaths
relative to control subjects (Supplementary Table S2).
To test post hoc a potential effect of task difficulty on group differences in brain activation, we repeated the analyses for the contrasts
‘fearful faces > shapes’, ‘happy faces > shapes’ and ‘all faces > shapes’
using accuracy and reaction time measurements as covariates. We
found comparable results before and after the covariation, which indicates no relevant task difficulty effect.
Functional connectivity (PPI) analysis
With this analysis, we set out to test for group differences in reciprocal
functional connectivity between the amygdala and other key
Table 2 Emotional face task performance [accuracy and reaction time (RT)]
Conditions
Shapes, correct, %
RT (ms)
Fearful, correct, %
RT (ms)
Happy, correct, %
RT (ms)
Mean s.d.
Controls
Psychopaths
100 0
874 155
99.0 2.78
1831 561
100 0
1262 322
100 0
886 222
96.5 9.63
1883 482
99.0 4.74
1341 395
t-value
P-value
–
0.2
1.2
0.3
1.0
0.7
–
0.83
0.24
0.75
0.32
0.47
components of the emotional face-processing network. We report results for ‘all faces > shapes’ contrast only, as separate analyses for fearful and happy conditions showed amygdala connectivity changes
comparable to the global (all faces) pattern.
Functional connectivity between amygdala and
emotional face network
We found consistent task-induced functional connectivity between the
left amygdala (seed) and both the visual cortex and left fusiform gyrus
only in control subjects (Figure 2 and Supplementary Table S3). A
between-group comparison confirmed that psychopaths had a significant reduction in functional connectivity between the left amygdala
and visual areas, the fusiform gyrus, parietal/frontal cortices and the
thalamus (Supplementary Table S4). No significant within- or between-group findings were observed in the right amygdala PPI
analysis.
Functional connectivity between network ROIs and amygdala
(i) PPI analyses centered on the visual extrastriate regions did not
demonstrate significant functional connectivity with the amygdalae.
(ii) The fusiform gyri did not show significant task-induced functional
connectivity with the amygdalae in any group (no main effects), but
between-group differences were significant for the right fusiform gyrus
analysis. That is, because control subjects showed a tendency toward
increased connectivity between the right fusiform gyrus and amygdalae
and psychopaths showed the opposite pattern, there was a significant
between-group difference in the functional connectivity of these regions (Figure 3). (iii) Finally, the prefrontal regions also showed no
evidence of significant task-induced functional connectivity with the
amygdalae.
The complete PPI analyses’ results for the visual extrastriate cortex,
fusiform gyrus and prefrontal regions are reported in Supplementary
Tables S3 and S4.
Correlation with the severity of psychopathy
We found a significant positive correlation between PCL-R Factor 1
and frontal cortex activation in the psychopathy group. The anatomy
of this finding partially overlapped with areas showing abnormally
increased activation in this group (Figure 4 and Supplementary
Table S5). In contrast, PCL-R Factor 2 was negatively correlated
with task activation in frontoparietal cortex, visual areas and diencephalic–mesencephalic structures. The correlation analysis was repeated
controlling for total months spent in prison. A similar correlation
strength was observed with regards to PCL-R Factor 1 (e.g. r ¼ 0.72
without control vs r ¼ 0.72 controlling for incarceration time in medial
prefrontal cortex), but the correlations were no longer significant for
PCL-R Factor 2. These results indicate that the severity of the interpersonal and affective deficits (Factor 1), as opposed to antisocial
behavior (Factor 2) and incarceration time, accounted for increased
Disrupted neural face processing in psychopathy
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509
Fig. 1 Brain regions activated during the emotional face-matching task in the controls (C) and psychopaths (P) subjects and between-group differences (P > C), masked by group conjunction activations.
Fig. 2 Task-induced functional connectivity of the left amygdala in control (C) and psychopathic (P) subjects, and between-group differences (P > C). The boxplots illustrate group mean functional connectivity
strength between the left amygdala seed (green spot) and right visual cortex (green cross). R ¼ right hemisphere.
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O. Contreras-Rodri¤guez et al.
Fig. 3 Task-induced functional connectivity between the right fusiform gyrus and the amygdalae in control (C) and psychopathic (P) subjects, and between-group differences (P > C) within a PickAtlas (Maldjian
et al., 2003) mask of the amygdala. The boxplots illustrate group mean functional connectivity strength between the right fusiform gyrus seed (green spot) and the right amygdala (green cross). R ¼ right
hemisphere.
Fig. 4 Correlations between PCL-R Factor 1 and task-related activation in psychopaths. The plot illustrates the correlation between psychopathy severity and medial prefrontal cortex activation MNI coordinates
(x, y, z: 0, 36, 40 mm).
frontal activations during emotional face processing. PCL-R total
scores were not significantly correlated with task activation
measurements.
PCL-R total scores, Factor 1 and Factor 2 were not significantly
correlated with task-induced functional connectivity measurements.
DISCUSSION
We have conducted a functional neuroimaging study comparing criminal psychopaths and control subjects during the execution of an emotional face-matching task. While behavioral performance was similar
between the two groups, fMRI findings revealed relevant differences
suggesting a generally distinct neural processing of this emotional
stimulation. On the one hand, psychopaths showed greater activation
of neocortical areas involving both visual and prefrontal cortices,
whereas they also showed a reciprocal decrease in task-induced functional connectivity between the amygdala and the visual and prefrontal
cortices. The observed pattern of results suggests that differences in the
neural processing of emotional faces may combine both deficient
(limbic) and compensatory (neocortical) operations. Relevantly, further correlation analyses revealed a positive association between PCL-R
scores Factor 1 and brain activation in areas mostly related to the
putative compensatory processes.
Behavioral studies assessing the recognition of emotional face expressions have generally reported performance deficits in psychopaths
Disrupted neural face processing in psychopathy
and individuals with psychopathic traits (Blair et al., 2001, 2004;
Kosson et al., 2002; Dadds et al., 2006; Dolan and Fullam, 2006),
which seem to contrast with our current findings. However, it is
likely that the discrepancy is explained by the implicit, as opposed to
explicit, emotional processing demands of our face matching task. That
is, participants in our study were instructed to perceptually match
correct face expressions, rather than to explicitly label each emotional
expression. Supporting this interpretation, other fMRI studies have
generally reported an absence of performance deficits in such populations in the context of implicit emotional face-processing tasks (Deeley
et al., 2006; Marsh et al., 2008; Jones et al., 2009).
The explicit component in the current task involves the visual
matching of facial features, which notably relies on visual perceptual
(neocortical) abilities (Goodale and Milner, 1992). Performance success in the psychopath group may arguably be related to the efficient
use of visual and frontal cortex resources. Prior functional imaging
studies have reported cortical hyperactivity during other emotional
tasks in psychopath cohorts (Intrator et al., 1997; Kiehl et al., 2001;
Müller et al., 2003; Glenn et al., 2009), which has been generally interpreted as reflecting compensatory neural operations. Importantly,
the implicit component in our task involves an inherent limbic system
(hippocampus and amygdala) engagement due to the biological salience of human emotional faces (Hariri et al., 2000). Our findings
suggest that this implicit limbic system engagement is disrupted in
psychopaths. Amygdala activation during the task was only significant
in control subjects, while functional connectivity between the amygdala and cortical regions was significantly reduced in psychopaths. To
this end, a relevant question emerges with regards to the context to
which emotion brain processing is deficient in psychopaths. According
to Newman’s response modulation theory, the neural processing of
visual emotional content should be less altered in psychopaths if emotional cues are the central focus of attention (Hiatt et al., 2004; Glass
and Newman, 2009; Newman et al., 2010). In other words, the implicit
nature of our task may have contributed to emphasize emotional
system deficiencies in psychopaths showing an overselective attention
(Hiatt et al., 2004).
The visual occipitotemporal cortex and the amygdala are tightly
coupled during face perception (Haxby et al., 2000; Fairhall and
Ishai, 2007; Smith et al., 2009). Functional connectivity with the fusiform gyrus is strengthened specifically by emotional faces (Fairhall and
Ishai, 2007) and modulated by anxiety-related personality traits (i.e.
harm avoidance and sensitivity to punishment) and emotional abilities
in general (Japee et al., 2009; Pujol et al., 2009), which are known to be
blunted in some psychopathic individuals (Cleckley, 1976; Hare, 2003).
Overall, our finding of a functional connectivity reduction within the
visual-fusiform-amygdala pathway is consistent with the studies reporting reduced affective responses to facial expressions in psychopaths (Patrick et al., 1993; Blair et al., 1997; Levenston et al., 2000;
Herpertz et al., 2001; Marsh et al., 2011). More broadly, a disruption of
amygdala functional connectivity is consistent with the abundant data
suggesting that amygdala alterations contribute prominently to impaired stimulus-reinforcement learning in psychopaths (Kiehl et al.,
2001; Birbaumer et al., 2005; Blair, 2006).
Our data, therefore, may assist in further delineating the functional
anatomy of disturbed neural processing of emotional stimulation in
psychopaths. Importantly, functional connectivity disruption may
occur at multiple stages of the normal emotion processing flow.
Indeed, the alteration between visual input areas and the amygdala
observed in the present study implicates a pathway relevant for the
detection of stimulus saliency (Adolphs, 2008). Other studies have
previously demonstrated anatomical and functional disruption between the anterior temporal/amygdala region and the orbitofrontal
cortex (Marsh et al., 2008; Motzkin et al., 2011). This processing
SCAN (2014)
511
pathway is relevant to signal stimulus reinforcing value (reward expectancies) in the context of associative learning (Schoenbaum et al., 1998,
2003; Baxter et al., 2000). Finally, significantly impaired functional
connectivity has also been identified between the medial frontal
cortex and the posterior cingulate cortex, which are connections relevant to the large-scale integration of the emotional and cognitive components of decision-making in a moral context (Motzkin et al., 2011;
Pujol et al., 2011; Juárez et al., 2013).
As mentioned above, this study is limited in that we explored neural
processes related mainly to implicit emotional processing and used a
task that may better assess the effect of general emotional stimuli than
the effect of single emotions, as two different emotional expressions are
presented in each trial. Also, the potential effect of incarceration on
brain function was not controlled for using an additional control
group of non-psychopathic prison inmates. The results of our correlation analysis suggest that subjects’ confinement can indeed modulate
the association between antisocial behavior (PCL-R Factor 2) and
brain activation. Nevertheless, our findings indicated that the interpersonal and affective traits in psychopaths (PCL-R Factor 1) accounted
for cortical activation changes with little influence from the length of
the incarceration period.
In conclusion, the neural response to emotional face matching in
criminal psychopaths involved an increase in neocortical activation
combined with reduced task-related functional connectivity between
the cortex and the amygdala. We propose that psychopaths were capable of performing the task similar to control subjects by marshaling
greater involvement of neocortical perceptual resources, but that the
ultimate input to the limbic system was weakened. Therefore, callous
and unemotional psychopaths do appear to exhibit a deficit in the
neural processing of emotional stimuli, which is in broad agreement
with the notion that psychopaths display low ‘somatic’ emotion.
Nevertheless, new research will be of interest to further explore the
‘cognitive’ component of emotional processing in psychopathy to ascertain how their apparent emotional insensitivity translates to various
aspects of their subjective experience.
SUPPLEMENTARY DATA
Supplementary data are available at SCAN online.
Conflict of Interest
None declared.
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