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88 views12 pages

Fearless Feedback

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Maria
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© © All Rights Reserved
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Biological Psychology 93 (2013) 352–363

Contents lists available at SciVerse ScienceDirect

Biological Psychology
journal homepage: [Link]/locate/biopsycho

Fearless Dominance and reduced feedback-related negativity


amplitudes in a time-estimation task – Further neuroscientific
evidence for dual-process models of psychopathy
Stefan Schulreich a,b,c,∗,1 , Daniela M. Pfabigan c,1 , Birgit Derntl d,e,f , Uta Sailer c,g
a
Languages of Emotion, Cluster of Excellence at Freie Universität Berlin, 14195 Berlin, Germany
b
Emotion Psychology and Affective Neuroscience, Department of Education and Psychology, Freie Universität Berlin, 14195 Berlin, Germany
c
Social, Cognitive and Affective Neuroscience Unit, Faculty of Psychology, University of Vienna, 1010 Vienna, Austria
d
Institute for Applied Psychology, Faculty of Psychology, University of Vienna, 1010 Vienna, Austria
e
Department of Psychiatry, Psychotherapy and Psychosomatics, RWTH Aachen University, 52074 Aachen, Germany
f
Jülich Aachen Research Alliance (JARA), Translational Brain Medicine, 52074 Aachen, Germany
g
Faculty of Psychology, Box 500, 40530 Gothenburg, Sweden

a r t i c l e i n f o a b s t r a c t

Article history: Dual-process models of psychopathy postulate two etiologically relevant processes. Their involvement
Received 27 August 2012 in feedback processing and its neural correlates has not been investigated so far. Multi-channel EEG
Accepted 10 April 2013 was collected while healthy female volunteers performed a time-estimation task and received nega-
Available online 19 April 2013
tive or positive feedback in form of signs or emotional faces. The affective-interpersonal factor Fearless
Dominance, but not Self-Centered Impulsivity, was associated with reduced feedback-related negativ-
Keywords:
ity (FRN) amplitudes. This neural dissociation extends previous findings on the impact of psychopathy
Psychopathy
on feedback processing and further highlights the importance of distinguishing psychopathic traits and
Fearless Dominance
Dual-process models
extending previous (neuroscientific) models of psychopathy.
Feedback processing © 2013 The Authors. Published by Elsevier B.V. Open access under CC BY-NC-ND license.
Event-related potentials
ERPs
sLORETA
FRN
ACC
RCZa

1. Introduction group (Edens, Marcus, Lilienfeld, & Poythress, 2006; Marcus, John,
& Edens, 2004). Moreover, this also indicates more than one causal
Psychopathy is a construct characterized by a number of deficits factor in the etiology of psychopathy.
in adaptation and affective processing – lack of empathy, fear-
lessness, deficits in aversive and passive avoidance learning, and 1.1. Dual-process models of psychopathy
antisocial behavior among others (Cleckley, 1941; Hare, 2003; Hare
& Neumann, 2008). Although primarily studied in offenders, there Dual-process models (e.g., Fowles & Dindo, 2009; Patrick &
is a growing number of investigations in the general population, Bernat, 2009) relate two potential etiological dimensions to the
as psychopathy is not restricted to incarcerated offenders (Hall & higher order factors of frequently applied psychometric instru-
Benning, 2006) but rather considered as a construct with a dimen- ments in the assessment of psychopathy in offenders, e.g. the PCL-R
sional latent structure and not representing a qualitatively discrete (Psychopathic Checklist-Revised; Hare, 2003) or in the general pop-
ulation, e.g. the PPI-R (Psychopathy Personality Inventory-Revised;
Alpers & Eisenbarth, 2008; Lilienfeld & Andrews, 1996). The first
model dimension (“Trait Fearlessness” in the model of Patrick &
Bernat, 2009) focuses on emotional-interpersonal aspects and is
related to an arrogant interpersonal style, lack of empathy and
∗ Corresponding author at: Languages of Emotion, Cluster of Excellence at Freie
reduced fear reactivity. The second model dimension (“External-
Universität Berlin, 14195 Berlin, Germany. Tel.: +49 030 838 57857.
izing Vulnerability”, Patrick & Bernat, 2009) is associated with an
E-mail address: [Link]@[Link] (S. Schulreich). impulsive, socially deviant lifestyle. In the PPI-R, they are psy-
1
These authors contributed equally to the work reported in this article. chometrically operationalized in form of the higher-order factors

0301-0511 © 2013 The Authors. Published by Elsevier B.V. Open access under CC BY-NC-ND license.
[Link]
S. Schulreich et al. / Biological Psychology 93 (2013) 352–363 353

Fearless Dominance and Self-Centered Impulsivity, respectively. involvement of the RCZ in remedial action than a signaling function
Both dimensions of psychopathic personality are thought to reflect as stated in the RLT.
etiologic pathways that can be already found in childhood psy- Another ERP repeatedly investigated during feedback
chopathology (Fowles & Dindo, 2009). The label “Externalizing processing is the P3(b) component, peaking between 200 and
Vulnerability” emphasizes the link to externalizing psychopathol- 600 ms at posterior electrode sites (Yeung & Sanfey, 2004). This
ogy (Patrick, Hicks, Krueger, & Lang, 2005) – one of two broad classical P3 component seems to index the task relevance of a stim-
factors underlying the most common mental disorders, in particu- ulus (Coles, Smid, Scheffers, & Otten, 1995) and resource allocation
lar the one associated with conduct disorder, antisocial behavior, (Israel, Chesney, Wickens, & Donchin, 1980; Kahneman, 1973).
alcohol and drug abuse among others (Krueger, 1999). However, One influential theory links the classical P3 with context-updating
psychopathy cannot be sufficiently described by externalizing psy- of working memory, i.e. revisions of mental representations by
chopathology because the latter was unrelated to the unique stimuli classified as new after comparison with previous stimuli
variance of the emotional-interpersonal dimension of psychopathy (Donchin & Coles, 1988, 1998; Polich, 2007).
(Patrick et al., 2005). These ERPs in error monitoring have been associated with sev-
A dual-process perspective might allow new insights in the eral personality traits in previous studies, for instance with trait
(neurocognitive) mechanisms underlying these pathways to psy- anxiety or anxiety disorders (Gu, Ge, Jiang, & Luo, 2010; Hajcak,
chopathic personality and the core deficits of psychopathy such McDonald, & Simons, 2003; Ladouceur, Dahl, Birmaher, Axelson, &
as deficits in behavioral adaptation or passive avoidance learn- Ryan, 2006) and the Behavioral Inhibition System (BIS; Boksem,
ing (Newman & Kosson, 1986; Newman, Patterson, Howland, & Tops, Wester, Meijman, & Lorist, 2006; De Pascalis, Varriale, &
Nichols, 1990). Dinn and Harris (2000) suggested that behavioral D’Antuono, 2010). The question arises if these electrophysiologi-
adaptation deficits found in ASPD (antisocial personality disorder) cal components are also linked to psychopathy, in particular the
individuals with psychopathic traits might be related to inade- FRN, consistent with the suggestion of Dinn and Harris (2000) of
quate processing of feedback information. Previous studies already impaired feedback processing underlying the behavioral adapta-
reported neurocognitive dissociations between the two dimen- tion deficits found.
sions of psychopathy, for instance in affect recognition (Gordon, The majority of studies related to psychopathy investigated
Baird, & End, 2004) or executive functions such as attention and internal error monitoring (i.e. ERN; Brazil et al., 2009, 2011; Munro
inhibition (Carlson & Thái, 2010; Carlson, Thái, & McLarnon, 2009). et al., 2007; von Borries et al., 2010) with inconsistent results. As far
The aim of our study was to investigate now feedback processing as feedback processing is concerned, two studies reported no FRN
– another potentially relevant neurocognitive mechanism – from a amplitude modulation related to psychopathy in a probabilistic
dual-process perspective of psychopathy. gambling task (von Borries et al., 2010) and in a visual Go/No Go task
(Varlamov, Khalifa, Liddle, Duggan, & Howard, 2010). With regard
1.2. Feedback processing and psychopathy to the P3 component, but unrelated to feedback processing, PPI-
R Self-Centered Impulsivity was associated with reduced frontal
A brain structure that has been associated with feedback P3 amplitudes in an oddball task (Carlson et al., 2009), whereas
processing is the dorsal anterior cingulate cortex (dACC; Holroyd PPI-R Fearless Dominance was associated with increased P3 ampli-
& Coles, 2002; Holroyd, Pakzad-Vaezi, & Krigolson, 2008; Miltner, tudes in a continuous performance task (Carlson & Thái, 2010). A
Braun, & Coles, 1997; Ullsperger & Von Cramon, 2003). It is an area meta-analysis of Gao and Raine (2009) showed inconsistent, task-
supposed to be fundamental to response-reinforcement associa- dependent effects on the P3 for psychopathy.
tions (Rushworth, Behrens, Rudebeck, & Walton, 2007), behavioral
monitoring and adaptation (e.g. Holroyd & Coles, 2002), and there- 1.3. The present study
fore a plausible candidate for explaining behavioral adaptation
deficits in psychopathy. Importantly, none of the studies investigating error monitoring
Electrophysiologically, external feedback after the occurrence focused on specific psychopathic traits in a multi-dimensional fash-
of an error elicits a negative event-related potential (ERP) called ion, as also discussed in Pfabigan, Alexopoulus, Bauer, Lamm, and
feedback-related negativity (FRN) with a typical peak amplitude Sailer (2011). This creates two potential problems for investigating
within 200–300 ms. Behaviorally, the FRN was shown to be asso- associations between psychopathy and feedback processing. First,
ciated with the degree of learning from negative feedback in an psychopathic traits might be differentially related to error moni-
emotion recognition task and a probabilistic learning task (Frank, toring. Working with a unitary construct (i.e. total scores instead
D’Lauro, & Curran, 2007; Frank, Woroch, & Curran, 2005). of specific psychopathic traits/higher-order factors) could obscure
Reinforcement Learning Theory (RLT; Baker & Holroyd, 2009, potential associations with both, the FRN and ERN. Second, categor-
2011; Holroyd & Coles, 2002) suggests that reward-prediction error ical grouping of dimensional data (i.e. splitting subjects into low-
signals are transmitted via the mesencephalic dopamine system to and high-scoring groups) leads to a loss of information about indi-
the dACC eliciting the FRN. As the FRN is sensitive to the unpre- vidual differences (MacCallum et al., 2002). From a dual-process
dictability of the outcome, its amplitude becomes smaller in the perspective, each individual is located on two functionally inter-
course of learning the specific action-outcome association, enabling related dimensions rather than belonging to qualitatively discrete
a switch from external (i.e. via external feedback information) groups of psychopaths and non-psychopaths. To overcome these
to internal error monitoring (i.e. comparing actual and intended shortcomings we investigated the potentially differential asso-
behavior) indexed by a functional related component called error- ciations between dimensional psychopathic traits and feedback
related negativity (ERN), peaking earlier than the FRN, about 100 ms processing.
after erroneous response (Falkenstein, Hohnsbein, Hoormann, & Therefore, we used the PPI-R (Alpers & Eisenbarth, 2008), which
Blanke, 1991; Gehring, Gross, Coles, Meyer, & Donchin, 1993; is applicable also in the low and moderate range of psychopathy,
Holroyd & Coles, 2002). This is called backward propagation after enabling us to investigate potential etiological processes across a
learning (Holroyd & Coles, 2002). In particular, the rostral cingu- broader dimensional range in an undergraduate/graduate sample
late zone anterior (RCZa), which is part of the dACC, is sensitive at the University of Vienna. Moreover, we investigated a female
to both forms of error monitoring and also reflects these learning- only sample to control for any gender differences that might occur
dependent dynamics (Mars et al., 2005). However, van der Veen, and to enhance our knowledge about this less-studied population.
Röde, Mies, van der Lugt, & Smits, (2011) proposed rather an Participants performed a modified time-estimation task (Miltner
354 S. Schulreich et al. / Biological Psychology 93 (2013) 352–363

Fig. 1. Trial time sequence.

et al., 1997) and received negative and positive feedback in form The PPI-R is a self-report questionnaire for measuring psychopathy. Internal
of signs and emotional faces, resulting in four (2 × 2) experimental consistency is satisfying with a reported Cronbach alpha of .85. The PPI-R consists of
eight subscales, which form two higher-order factors (Benning, Patrick, Bloningen,
conditions.
et al., 2005). Scores for the higher-order factors were calculated as in Benning
According to the low-fear hypothesis of psychopathy (Lykken, et al. (2003), Carlson and Thái (2010) and Carlson et al. (2009). The mean of the z-
1957, 1995) behavioral adaptation deficits after punishment in psy- transformed scales Fearlessness, Social Influence, and Stress Immunity scores added
chopaths are due to a fundamental fear deficit. This suggests a link up to the higher-order factor Fearless Dominance score, whereas the mean of the
to PPI-R Fearless Dominance – a dimension reflecting among oth- z-transformed scales Blame Externalization, Rebellious Nonconformitiy, Machiavel-
lian Egocentricity, and Carefree Nonplanfulness scores added up to the higher-order
ers low fear in terms of psychometric (Benning, Patrick, Bloningen, factor Self-Centered Impulsivity score. The subscale Coldheartedness did not fit into
Hicks, & Iacono, 2005; Benning et al., 2003) and psychophysiologi- this two-factor solution and was therefore not included.
cal data such as inhibition of the fear-potentiated startle response In contrast to the interrelated PCL-R factors, the orthogonal nature of the PPI-
(e.g. Anderson, Stanford, Wan, & Young, 2011; Benning, Patrick, & R higher-order factors Fearless Dominance and Self-Centered Impulsivity (Benning
et al., 2003) renders it an even more promising instrument to disentangle the differ-
Iacono, 2005; Dindo & Fowles, 2011), reduced skin conductance
ent mechanisms potentially relevant in those etiological pathways (Patrick & Bernat,
response to aversive pictures (Benning, Patrick, & Iacono, 2005), 2009) and core impairments typically seen in psychopathy.
and deficient fear-conditioning (López, Poy, Patrick, & Moltó, 2012). Our sample showed considerable variability in PPI-R total score, in all subscales
Since our behavior is crucially guided by feedback processes the and in the higher-order factors Fearless Dominance and Self-Centered Impulsivity.
question arises whether psychopathic traits affect this capacity and The comparison of our sample with the norm sample of female students (n = 204)
provided in the manual showed that PPI-R total scores ranged from percentile ranks
we hypothesize that in particular Fearless Dominance would be
3.40% (score: 229) to 96.60% (score: 316) in our sample. Furthermore, the mean
associated with impaired feedback processing indicated by reduced score of 273.90, which corresponds to a percentile rank of 48.50% indicating that
FRN amplitudes and reduced behavioral adaptation after negative our sample represents well the norm sample. However, in addition to students,
feedback. Moreover, we expected decreased neuronal source activ- the German version of the PPI-R has also been applied in a forensic sample, where
higher scores were reported, as one would expect from a valid measure (Alpers &
ity in the rostral cingulate zone anterior (RCZa) for high Fearless
Eisenbarth, 2008). Fearless-Dominance scores ranged from −1.43 and 1.13 and Self-
Dominance due to the demonstrated link to feedback processing Centered Impulsivity scores from −1.56 and 1.52. These scores represent average
(Mars et al., 2005; Ullsperger & Von Cramon, 2003; van der Veen z-scores of the respective subscales and thus indicate ranges from below to above
et al., 2011). Furthermore, feedback processing might be impaired one standard deviation of the raw scores and thereby sufficient variability.
to a greater degree when socio-emotional stimuli like faces are
presented as compared to signs due to the social and affective 2.2. Stimuli and paradigm
deficits seen in psychopathy. Possible personality effects on P3 were
explored without specific hypotheses. Participants sat comfortably about 70 cm in front of a 19-in. cathode ray tube
monitor (Sony GDM-F520; 75 Hz refresh rate) in a sound-attenuated room. Stimulus
presentation and EEG data collection (Pentium IV, 3.00 GHz) were synchronized by
2. Methods E-Prime software (Psychology Software Tools, Inc., Pittsburgh, PA).
A modified version of a time estimation task (Miltner et al., 1997) was used as
2.1. Participants and measures experimental paradigm (Fig. 1). Each trial started with the presentation of a black
fixation dot on a gray screen for 1000 ms. Subsequently, the dot was replaced by a
We investigated an undergraduate/graduate sample of 24 women. Two of them black star which remained on the screen for 250 ms. The star indicated the starting
had to be excluded from further analysis due to movement and blink artifacts. One point of the time estimation. Following the star, a blank gray screen was presented
subject had to be excluded due to a history of social anxiety, depression and psy- for max. 2000 ms. During this period, participants were asked to indicate the elapse
chiatric treatment. The remaining 21 women were aged between 21 and 29 years of one second by pressing a keyboard button. Following the button press, the blank
(mean age = 24.29 years, SD = 1.95) and were enrolled as students or graduates of gray screen lasted another 600 ms, after which subjects were provided with feed-
the University of Vienna. All participants were right-handed (Edinburgh Handed- back for 1000 ms indicating whether the estimation had been correct or incorrect.
ness Inventory; Oldfield, 1971) and had normal or corrected-to-normal vision. All The inter-trial-interval varied between 400 and 600 ms. Feedback was provided
participants gave written informed consent prior to the experiment. The study was performance-based, but task difficulty was adjusted to the individual performance
conducted in accordance with the Declaration of Helsinki (World Medical Association, level. Each participant started with the same criteria: positive feedback was pro-
revised 2000) and local guidelines of the University of Vienna. vided if the button press fell within the time window of 900–1100 ms after star
After EEG data collection, all subjects completed the German version of the onset. The width of this time window was adjusted automatically based on the indi-
Psychopathic Personality Inventory-Revised (PPI-R; Alpers & Eisenbarth, 2008).2 Fur- vidual performance on the preceding trial (Johnson & Donchin, 1978; Miltner et al.,
thermore, a shortened version of the SCID (Structural Clinical Interview for DSM-IV; 1997). Following a trial with positive feedback, the time window became narrower
Wittchen, Wunderlich, Gruschwitz, & Zaudig, 1996) was administered to screen as 10 ms were subtracted; following a trial with negative feedback, the time window
for mental disorders. Participants did not receive any financial remuneration and became wider as 10 ms were added. Thus, global probability of positive and negative
participated voluntarily. feedback stimuli was approximately 50% during the whole experiment. Feedback
stimuli were equiluminescent, comparable in size, and either emotional faces or
signs (all 4 cm × 5 cm in size) were used. Facial feedback stimuli were photographs
of a female poser of the Pictures of Facial Affect (Ekman & Friesen, 1976). The happy
2
In addition, all subjects completed the German Version of the Liebowitz Social facial expression indicated positive feedback; the angry facial expression indicated
Anxiety Scale (LSAS; Stangier & Heidenreich, 2004) and the Experience of Emotions negative feedback. Sign feedback stimuli were an X and an O. The assignment of X
Scale (German: Skalen zum Erleben von Emotionen; Behr & Becker, 2004). Since these and O to positive and negative feedback was counterbalanced across participants.
data fall beyond the scope of this article, they will not be presented in the present Feedback valence was explained in the instruction. Thus, there were four feedback
context. conditions – negative face feedback, negative sign feedback, positive face feedback
S. Schulreich et al. / Biological Psychology 93 (2013) 352–363 355

and positive sign feedback. The whole experiment consisted of 20 training trials and applied for the absolute trial-by-trial adjustment of time estimation as dependent
400 experimental trials. The experimental trials were divided into four blocks: two variable.
blocks with facial feedback stimuli, and two with sign feedback stimuli. Blocks with
facial and sign feedback stimuli were presented alternately. To recall the assign- 2.4.2. ERP data
ment of positive and negative feedback stimuli, detailed instruction was given prior Artifact-free trials were averaged per subject and per feedback condition (neg-
to each block. Half the participants started with a facial feedback block, the other ative faces, negative signs, positive faces, and positive signs). Subsequently, FRN
half with a sign feedback block. Data collection was paused every 50 trials to offer amplitudes were scored at electrode sites FCz and Cz in all conditions as the peak-
subjects a short rest. The whole EEG data collection lasted about 45 min. to-peak voltage difference between the most negative local peak and the voltage of
the immediately preceding positive peak 140–350 ms after feedback onset, in line
2.3. Electrophysiological recording and preprocessing with previous peak detection methodology (e.g. with detection intervals beginning
150 or 160 ms post-stimulus; Hajcak, Moser, Holroyd, & Simons, 2006; Holroyd,
Multi-channel EEG was recorded from 61 Ag/AgCl ring electrodes which were Nieuwenhuis, Yeung, & Cohen, 2003). If no FRN peak was apparent, the difference
embedded equidistantly in an elastic cap (EASYCAP GmbH, Herrsching, Germany; score was set to zero. Electrode sites FCz and Cz were repeatedly used in previous
model M10) with a sterno-clavicular reference (Stephenson & Gibbs, 1951). Ver- literature (e.g. Holroyd & Coles, 2002; Holroyd et al., 2003; Yeung & Sanfey, 2004)
tical and horizontal electrooculogram (EOG) was recorded with a bipolar setting and visual inspection showed pronounced ERP deflections at these electrode sites
from electrodes placed on the outer canthi, 1 cm above and below the left eye in the time range mentioned above. A difference wave approach (e.g. Miltner et al.,
for off-line eye-movement correction. Subject- and channel-specific parameters for 1997) was not undertaken as the FRN seems to be an integrative result of differ-
eye-movement correction were obtained in two pre-experimental calibration trials ent processes in both the negative and positive feedback condition as described
(Bauer & Lauber, 1979). Furthermore, a template matching procedure was applied in the introduction (Baker & Holroyd, 2011; Holroyd et al., 2008). P3 amplitudes
to minimize blink artifacts (cf. Lamm, Fischmeister, & Bauer, 2005). A skin scratch- were scored at electrode site Pz as the most positive peak within 200–600 ms after
ing procedure (Picton & Hillyard, 1972) kept the electrode impedances below 2 k, feedback onset (Yeung & Sanfey, 2004).
as measured with a manual impedance meter. Signals were amplified using an AC FRN peak measures were subjected to a general linear model with the within
amplifier set-up with a time constant of 10 s (Ing. Kurt Zickler GmbH, Pfaffstät- subject factors electrode site (FCz vs. Cz), valence (negative vs. positive) and form
ten, Austria). All signals were recorded within a frequency range of .016–125 Hz (face vs. signs) and the between-subject factors Fearless Dominance and Self-
and sampled at 250 Hz for digital storage. In addition, individual three-dimensional Centered Impulsivity as regressors. In addition, we also analyzed FRN peak latencies
electrode coordinates of 17 pre-defined electrode positions (referenced to nasion, with the same approach as well as FRN peak amplitudes with the total score of the
inion, and the two preauricular electrodes) were measured for all participants with PPI-R to compare the effects for the psychopathic traits (dual-process perspective)
a photogrammetric scanner (3D-PHD; Bauer et al., 2000). Off-line, a standard head with those of the overall score (unitary-construct perspective). P3 peak measures
model was fit into these predefined locations, whereupon the remaining electrodes were subjected to the same general linear model except for the within-subject factor
were interpolated using a radial basis function, based on the equidistant montage electrode site (as there is only one, Pz). Although collinearity, i.e. highly correlated
of the electrode cap. predictors, was not found for the PPI-R derived measures, zero-order correlations
EEGLAB 6.03b (Delorme & Makeig, 2004) was used for off-line data analysis. A between Fearless Dominance as well as Self-Centered Impulsivity and FRN ampli-
low-pass filter with a cut-off frequency of 30 Hz (roll-off 6 dB/octave) was applied tudes were calculated in a second analysis. Moreover, in order to discuss potential
to the EEG data. Data were segmented into individual trials, starting 200 ms before differential effects of the psychopathic traits Fearless Dominance and Self-Centered
feedback onset and lasting for 1100 ms. The 200 ms prior to feedback onset served Impulsivity, it is not sufficient to find a significant effect for one factor and a not
as baseline interval. Artifact-afflicted trials that depicted voltage values exceeding significant results for the other (Gelman & Stern, 2006; Niewenhuis, Forstmann, &
±75 ␮V or voltage drifts of more than 50 ␮V were discarded from further analysis. Wagenmakers, 2011). Consequently, we tested for differences between correlations
Extended infomax independent component analysis (ICA; Bell & Sejnowski, 1995; for Fearless Dominance and Self-Centered Impulsivity in each feedback condition
Lee, Girolami, & Sejnowski, 1999) was applied to single-subject data of two partic- with four specific tests for dependent correlations per electrode site (T2 statistic;
ipants to detect and correct for residual eye movement-related activity (Delorme, Steiger, 1980). The specificity of the FRN-related effects was also tested by applying
Sejnowski, & Makeig, 2007). the same general linear model to the ERP amplitudes to the positivity prior to the
FRN and the P3 after the FRN at electrode sites FCz and Cz. In addition, the associ-
ation between time estimation or behavioral adaptation and FRN amplitude in the
2.4. Statistical analysis respective conditions was tested with zero-order correlations.

Participants received negative and positive feedback in form of signs and emo-
2.4.3. Source activity
tional faces, resulting in the within-subject factors valence (negative vs. positive
In order to corroborate our ERP findings and address our hypothesis on ros-
feedback) and form (face vs. sign feedback). For FRN analyses an additional within-
tral cingulate zone anterior (RCZa) activity we applied source localization as an
subject factor electrode site was included (FCz vs. Cz). Fearless Dominance and
additional method to explore brain activity. Source localization was conducted
Self-Centered Impulsivity served as between-subject factors. As dependent vari-
by means of standardized low resolution brain electromagnetic tomography soft-
ables, behavioral data and brain electric activity by means of ERPs and source
ware (sLORETA; Pascual-Marqui, 2002). sLORETA provides a linear, minimum norm
localization (sLORETA; Pascual-Marqui, 2002) were analyzed. The level of signifi-
inverse solution that estimates the distribution of the electrical neuronal activity in
cance was set at p < .05 for all tests. Correlation coefficients (r) or partial eta-squared
three-dimensional space by assuming that neighboring neurons are simultaneously
(2p ) are reported indicating the effect sizes (r < .10 and 2p < .05 representing small
and synchronously activated, and produces images of electric neuronal activity
effects, r < .30 and 2p around .10 representing medium effects, and r > .50 and 2 > .20
without localization bias (Greenblatt, Ossadtchi, & Pflieger, 2005; Pascual-Marqui,
representing large effects; Cohen, 1973, 1988). All statistical tests are two-tailed. Sta-
2002). sLORETA computes the electric activity at each voxel as the squared stan-
tistical analyses were performed using SPSS (version 19; SPSS, Inc., IBM Corporation,
dardized magnitude of the estimated current density. The sLORETA solution space
NY).
is restricted to cortical gray matter and hippocampus, defined via the MNI (Montreal
Neurological Institute) reference brain and subdivided into 6239 voxels, with a spa-
2.4.1. Questionnaire and behavioral data tial resolution of 5 mm × 5 mm × 5 mm. The sLORETA method has been validated in
Pearson intercorrelations between scores of the PPI-R subfactors, Fearless Dom- several simultaneous EEG/fMRI studies (e.g. Mobascher et al., 2009; Olbrich et al.,
inance and Self-Centered Impulsivity were calculated. For the time estimation task, 2009) and has also been applied to feedback processing (Santesso et al., 2011). The
the overall number of correct responses was calculated. Then average time estima- individual electrode positions which had been acquired with the photogrammetric
tion was calculated per subject and condition as the mean interval between cue scanner (Bauer et al., 2000) were cross-registered to the standard Talairach space
onset and button press. Subsequently, for each subject and separately for all four (Talairach & Tournoux, 1988) and reconciled with the estimated cortical activation
conditions (negative faces, negative signs, positive faces, and positive signs), the patterns. A regularization parameter of zero was used for transformation of elec-
absolute trial-by-trial adjustment of time estimation was calculated (Miltner et al., trode mean amplitudes into a three-dimensional distribution of cortical activation,
1997). Higher values indicate overall larger behavioral adaptation after feedback. thus achieving the smoothest of all possible solutions. Overall signal-to-noise-ratio
For the behavioral data, the first trial of each block and after each rest between was set to 100 during the transformation process.
blocks was discarded from this analysis because of feedback change and rest. We decided to use a region of interest (ROI) approach to address our spe-
The association between personality and time estimation was tested using a cific hypothesis. In contrast to ROIs based on rather broad Brodmann areas as in
general linear model with the within-subject factors valence (positive vs. negative Santesso et al. (2011), we created spherical regions of interest (ROIs) covering
feedback) and form (face vs. sign feedback) as well as the between-subject factors the anterior rostral cingulate zone for each hemisphere. The RCZa was repeat-
Fearless Dominance and Self-Centered Impulsivity as continuous variables. Such a edly shown to be associated with error monitoring and feedback processing (Mars
model provides within- and between-subject main effects and interactions as well as et al., 2005; Ullsperger & Von Cramon, 2003, 2004; van der Veen et al., 2011),
parameter estimates for the regression of the between-subject psychopathic traits Our ROIs were centered at ±8, 30, 32 mm, according to the stereotactic coor-
on time estimation in all conditions. Regression parameter estimates should provide dinates of Talairach and Tournoux (1988) as in Picard and Strick (1996) and in
valid information about the unique contributions of Fearless Dominance and Self- Mars et al. (2005), who found this area involved in error processing. In contrast
Centered Impulsivity as no substantial collinearity is expected for these two PPI-R to Mars et al. (2005), we used the nonlinear Yale MNI to Talairach converter
derived measures (and indeed was not found, see results). The same model was algorithm (described in Lacadie, Fulbright, Rajeevan, Constable, & Papademetris,
356 S. Schulreich et al. / Biological Psychology 93 (2013) 352–363

Fig. 2. The red spots illustrate the two bilateral spherical seeds (8 mm) in the RCZa used for sLORETA ROI regression analysis. (For interpretation of the references to color
in this figure legend, the reader is referred to the web version of the article.)

2008; applet: [Link] to search for cor- estimates in the separate conditions across valence. No other effects
responding MNI coordinates, which are −8, 30, 35 and 9, 30, 35, respectively. As in were significant (all p > .15). Means and standard deviations for time
Mars et al. (2005) the spheres had a radius of 8 mm. The location of the ROIs is
estimation and absolute trial-by-trial adjustment in time estima-
illustrated in Fig. 2.
Zero-order correlations between the average electric activity in these ROIs tion data are presented in Table 2 for all conditions.
between 140 and 300 ms post-stimulus and Fearless Dominance and Self-Centered
Impulsivity were calculated for all feedback conditions. Differences between corre-
lations for Fearless Dominance and Self-Centered Impulsivity in the four feedback
conditions were tested with four specific tests for dependent correlations (T2 statis- 3.2. ERP data
tic; Steiger, 1980). This specific timeframe was chosen because of the early negativity
onset visible in some individual ERP averages. When we tested for potential outliers
Regarding FRN amplitudes, the general linear model revealed
by calculating Z-scores of the RCZa mean activity, one additional subject turned out
as a biasing outlier (e.g. Z = 4.01 for negative faces) and had to be excluded from anal- significant effects for valence, F (1,18) = 18.97, p < .01, 2p = .51, indi-
ysis. This was probably due to technical problems in peripheral electrodes visible in cating that the FRN amplitude was larger for negative than for
the scalp topography, which is not crucial for FRN and P3 analysis, but presumably positive feedback, and for form, F (1,18) = 66.89, p < .01, 2p = .79,
for source analysis. Therefore source analysis was carried out on the 20 remaining
indicating larger amplitudes for faces than for signs. There was no
subjects.
effect for electrode site, F (1,18) = .39, p = .54. Moreover, no inter-
action reached significance (all p > .06). Mean peak amplitudes,
3. Results latencies, and standard deviations are displayed in Table 3. Grand
averages for the four conditions are displayed in Fig. 3.
3.1. Questionnaire and behavioral data Regarding psychopathic traits, there was a between-subjects
effect for Fearless Dominance, F (1,18) = 8.88, p < .01, 2p = .33. As
Pearson intercorrelations of all PPI-R scales and higher-order hypothesized, parameter estimates (Table 4) indicate an inverse
factors are provided in Table 1. The rather orthogonal nature of relation between Fearless Dominance and feedback processing in
the PPI-R higher-order factors in contrast to PCL-R factors (Benning all feedback conditions at both electrode sites, i.e. higher scoring
et al., 2003; Hare, 2003) was also evident in our sample, as there was subjects displayed reduced FRN amplitudes, significant for negative
no significant correlation between Fearless Dominance and Self- faces and positive faces and positive signs at least at one electrode
Centered Impulsivity (r = −.05, p = .83). site, FCz or Cz. The confidence intervals of regression slopes were
In the time estimation task, participants were correct on about substantially overlapping and there were no significant interaction
half of the trials for face feedback (48.50%) and sign feedback effects between Fearless Dominance and the within-subject fac-
(47.43%) as would be expected by applying the adaptive criterion tors electrode site, valence and form, (all p > .13). Together with the
for correctness of performance (see Section 2). Time estimation overall between-subject effect this indicates a more generalized
values were higher before negative than positive feedback, F pattern of reduced FRNs in higher-scoring subjects. There was no
(1,18) = 37.16, p < .01, 2p = .67, indicating that on average partic- significant between-subject effect for Self-Centered Impulsivity, F
ipants responded after too long time intervals in error trials. There (1,18) = .98, p = .34, indicating that this psychopathic trait is rather
was no significant difference between faces and signs, F (1,18) = .10, unrelated to feedback processing.
p = .76. Unexpectedly, there was a significant between-subjects Zero-order Pearson correlation coefficients indicate that Fear-
effect for Self-Centered Impulsivity, F (1,18) = 14.46, p < .01, 2p = less Dominance is associated with reduced FRN amplitudes
.46. Respective parameter estimates were significant for all con- (Table 4). Moreover, the zero-order correlation coefficients of Fear-
ditions (all p < .05), indicating longer estimated time intervals for less Dominance and Self-Centered Impulsivity were significantly
subjects with higher Self-Centered Impulsivity scores. In addition, different for negative faces and positive signs when applying the T2
there was a significant interaction effect between valence and Self- test statistic (Steiger, 1980) as illustrated also in Table 4. Descrip-
Centered Impulsivity, F (1,18) = 7.70, p = .01, 2p = .30, which was, tively, all the regression parameters and correlations pointed
however, qualified by substantially overlapping confidence inter- in different directions when comparing the two psychopathic
vals of the parameter estimates in the separate conditions across traits. The relationship between Fearless Dominance and feedback
valence. Fearless Dominance was unrelated to time estimation, F processing is also illustrated by simple regression lines in Fig. 4.
(1,18) = .04, p = .84. No other effects were significant (all p > .08). This effect for Fearless Dominance cannot be explained by differ-
The absolute trial-by-trial adjustment in time estimation was ences in FRN latencies as there were no significant between-subject
larger after negative than after positive feedback, F (1,18) = 118.35, effect (p > .88) or parameter estimates in the four feedback condi-
p < .001, 2p = .87, but there was no significant difference between tions (p > .28), when running the same GLM for FRN peak latency
faces and signs, F (1,18) = 2.28, p = .15. Although there was a as the dependent variable. Zero-order correlations were also not
significant interaction between valence and Self-Centered Impuls- significant (all p > .24).
ivity, F (1,19) = 5.73, p = .03, 2p = .24, this result was qualified by When applying a unitary construct perspective, run-
substantially overlapping confidence intervals of the parameter ning the same GLM for total PPI-R score did not reveal a
S. Schulreich et al. / Biological Psychology 93 (2013) 352–363 357

Note: Fearless Dominance and Self-Centered Impulsivity were the mean of the z-scores of the respective subscales. FD scales were Fearlessness, Social Influence, and Stress Immunity. SCI scales were Blame Externalization,
Table 2

27.81 [5.09]
Means [and standard deviations] for time estimation and absolute trial-by-trial
adjustment in time estimation (in ms).

.15

.06
−.23
.04

−.38

−.22
.43
.30
−.05

.03
CH
Measure Condition Mean [SD]

Time estimation Negative faces 1128.16 [196.94]


Negative signs 1127.65 [184.00]

37.14 [3.86]
Positive faces 1039.32 [150.59]
Positive signs 1028.45 [111.66]
.77*

.71*

.44*
.56*
.23
.17
.36
−.06

−.01
Absolute trial-by-trial Negative faces 169.24 [49.13]
ME

adjustment in time Negative signs 175.22 [50.97]


estimation Positive faces 111.11 [29.56]

54.57 [10.96]
Positive signs 123.76 [39.81]
.79*

.59*

.76*

.57*
.28

.38
−.39

.00
RNC

significant between-subject effect (p = .65) nor significant


parameter estimates for the separate conditions (all p > .06).
Regarding P3 amplitudes, the main effect for valence was not
significant (p = .09), whereas we found a significant effect for
29.19 [5.03]

form, F (1,18) = 6.15, p = .02, 2p = .26, indicating that P3 ampli-


.56*

−.53*
.86*

tudes were larger for faces. Grand averages for the four conditions
−.25
.06
−.05

.40
CNP

are displayed in Fig. 5. The between-subject effects and all of


the parameter estimates of Fearless Dominance and Self-Centered
24.71 [6.40]

Impulsivity were not statistically significant (all p > .46). Moreover,


no significant interactions emerged (all p ≥ .07). Zero-order Pear-
.49*
−.34
−.14
−.34
.08

−.40

son correlation coefficients also indicate that Fearless Dominance


BE

and Self-Centered Impulsivity are unrelated with P3 amplitudes (all


p > .43).
Therefore, effects seem to be specific for the FRN, also indicated
.00 [.70]

by the non-significant main, interaction or between-subject effects


.78*

−.47*
.17
−.05

.20
SCI

applying the same GLM to the positivity prior to the FRN and the
P3 after FRN at electrode sites FCz and Cz (all p > .10).
With regard to behavioral measures, there were no significant
39.24 [7.02]

correlations between FRN amplitude at FCz and Cz and time esti-


.59*

mation or absolute trial-by-trial adjustment of time estimation in


.18
.01

.01
StI

the respective conditions (all p > .16).

3.3. Source analysis


46.52 [5.38]
Means [and standard deviations] on the diagonal and bivariate zero-order correlations for PPI-R scales.

.55*

.68*
.38

We observed decreased RCZa activity for higher levels of Fear-


SI

less Dominance in the FRN-time range for negative faces, whereas


Self-Centered Impulsivity was unrelated to RCZa activity across
14.71 [4.79]

all conditions (Table 5). No other effects were significant (all


Carefree Nonplanfulness, Rebellious Nonconformity, and Machiavellian Egocentricity.

p > .07).
.56*

.76*
F

4. Discussion
.00 [.68]

Although there is a considerable body of evidence for behav-


ioral and neural correlates of psychopathy, feedback processing has
.55*
FD

not been investigated with respect to specific psychopathic traits


so far. Applying a dual-process perspective enabled us to find a
relationship that previous studies focusing on a unitary construct
273.90 [21.48]

of psychopathy could not establish. Considering the theoretically


postulated role of low fear in behavioral deficits in psychopathy
PPI-R

(Lykken, 1957, 1995), we hypothesized that in particular the psy-


chopathic trait Fearless Dominance – an emotional-interpersonal
Significantly different from 0 (p ≤ .05)

factor associated with high dominance, low anxiety, venturesome-


ness and low fear-reactivity (Benning et al., 2003; Benning, Patrick,
PPI-R Machiavellian Egocentricity
PPI-R Rebellious Nonconformity
PPI-R Self-Centered Impulsivity

PPI-R Carefree Nonplanfullness

& Iacono, 2005) – would be associated with impaired feedback


PPI-R Blame Externalization

processing.
PPI-R Fearless Dominance

As expected, we found an overall between-subjects effect for


PPI-R Coldheartedness
PPI-R Stress Immunity
PPI-R Social Influence

Fearless Dominance as well as significant regression parameter


PPI-R Fearlessness

estimates in the negative face, the positive face and positive signs
PPI-R Total Score

condition (and descriptively the same relation for negative signs)


in the GLM. There were no significant differential effects for faces
and signs or negative and positive feedback. Together, this might
Table 1

indicate a rather generalized reduction of FRN amplitudes in


*

higher Fearless Dominance. In contrast, Self-Centered Impulsivity


358 S. Schulreich et al. / Biological Psychology 93 (2013) 352–363

Fig. 3. Grand averages for all feedback conditions (N = 21) at electrode sites FCz and Cz. Approximate FRN windows between peak minima (156 ms) and maxima (312 ms)
are displayed.

as well as total PPI-R score were not significantly related to Evidence for this specific relation between Fearless Domi-
feedback processing. Moreover, zero-order correlation coefficients nance and brain activity associated with feedback processing was
for Fearless Dominance partly differ from the coefficients for also found in our sLORETA results for negative faces. Fearless
Self-Centered Impulsivity. Thus, our findings suggest that Fearless Dominance, but not Self-Centered Impulsivity, was negatively cor-
Dominance might uniquely contribute to impaired feedback related with activity in the rostral cingulate zone anterior (RCZa)
processing. for negative face feedback, although for the other conditions no

Table 3
Means [and standard deviations] for FRN amplitudes.

Measure Condition FCz Cz


Mean [SD] Mean [SD]

FRN amplitude Negative faces −6.44 [3.23] −6.50 [2.82]


Negative signs −4.51 [2.88] −3.89 [2.93]
Positive faces −4.66 [2.04] −4.76 [2.60]
Positive signs −2.06 [2.14] −1.90 [2.04]

FRN latency Negative faces 236.57 [37.78] 211.52 [32.80]


Negative signs 227.05 [36.00] 212.76 [32.54]
Positive faces 231.62 [43.91] 208.19 [34.79]
Positive signs 234.22 [27.69] 214.53 [40.75]

Note: For FRN latency only trials with detectable negativity were included.

Table 4
GLM regression parameter estimates (B) with confidence intervals (CI) and effect sizes (2 ), as well as zero-order Pearson correlation coefficients (r) between PPI-R Fearless
Dominance and Self-Centered Impulsivity and FRN amplitude in the four feedback conditions at electrode sites FCz and Cz.

Condition Fearless Dominance

FRN (Fcz) FRN (Cz)

B CI 2p r B CI 2p r

Negative faces 1.47 [−.58, 3.53] .11 .33a 2.06* [.32, 3.81] .26 .51* , a
Negative signs 1.40 [−.57, 3.37] .11 .34 .83 [−1.24, 2.90] .04 .20
Positive faces 1.46* [.17, 2.75] .24 .49* 1.54 [−.19, 3.28] .16 .41
Positive signs 1.90* [.66, 3.13] .37 .61* , a 2.01* [.91, 3.12] .45 .66* , a

Condition Self-Centered Impulsivity

FRN (Fcz) FRN (Cz)

B CI 2p r B CI 2p r

Negative faces −1.69 [−3.67, .29] .15 −.39 a


−.67 [−2.35, 1.01] .04 −.19a
Negative signs −.47 [−2.37, 1.43] .02 −.13 −.62 [−2.62, 1.37] .02 −.16
Positive faces −.30 [−1.54, .95] .01 −.13 −.26 [−1.93, 1.41] .01 −.09
Positive signs −.34 [−1.53, .84] .02 −.14a −.30 [−.76, 1.37]
a
Correlation coefficients of Fearless Dominance and Self-Centered Impulsivity are significantly different from each other in the respective condition (p ≤ .05).
*
Significantly different from 0 (p ≤ .05).
S. Schulreich et al. / Biological Psychology 93 (2013) 352–363 359

Fig. 4. Scatter plots and fitted regression lines with Fearless Dominance as independent variable and FRN amplitude as the dependent variable for electrode sites FCz and Cz
illustrated separately for the four feedback conditions.

significant effects could be found. The RCZa is a key area for inter- This is what we have found. Theories emphasizing processing of the
nal and external error monitoring (Mars et al., 2005; Ullsperger & affective/motivational significance and subjective stimulus eval-
Von Cramon, 2001, 2003, 2004). uation in error monitoring (Gehring & Willoughby, 2002; Pailing
& Segalowitz, 2004; Yeung, Holroyd, & Cohen, 2005) would also
4.1. Integration with theories of psychopathy predict impaired error monitoring in case of an affective deficit pre-
venting the use of affective information to determine salience. From
Our hypotheses were derived from dual process models (Fowles this perspective, feedback might have been less salient for subjects
& Dindo, 2009; Patrick & Bernat, 2009) as well as from the low- high in Fearless Dominance.
fear hypothesis of psychopathy (Lykken, 1957, 1995). On the one An alternative to affective-based theories of psychopathy is the
hand, the neural dissociation between Fearless Dominance and response modulation theory (Newman & Lorenz, 2003). Accord-
Self-Centered Impulsivity observed in this study strongly sup- ing to Newman and Baskin-Sommers (2011), response modulation
ports the value of dual-process models of psychopathy – in line is an early attentional process necessary for self-regulation and
with previous studies focusing on different processes like execu- behavioral adaptation. The theory postulates that psychopaths are
tive functions related to the P3 component (Carlson & Thái, 2010; impaired in suspending a dominant response set (i.e. ongoing
Carlson et al., 2009) or affect recognition (Gordon et al., 2004). On approach behavior), integrating contextual information, and shif-
the other hand, our results support the low-fear hypothesis, which ting attention to the evaluation of the response, which might be
states that deficits in behavioral adaptation are the result of a fear reflected in impaired internal or external error monitoring. A defi-
deficit. Thus, we expected in particular a contribution of Fearless ciency in feedback processing might therefore indirectly reflect an
Dominance, a dimension of psychopathy incorporating among oth- impaired process at an earlier stage. However, the model does cur-
ers low fear, to a reduced FRN, an ERP component, which has been rently not offer an explanation why the socio-emotional dimension
associated with behavioral adaptation (Frank et al., 2007, 2005). Fearless Dominance in contrast to Self-Centered Impulsivity would
be specifically related to impaired feedback processing.

Table 5
Zero-order Pearson correlation coefficients (r) between Fearless Dominance or Self- 4.2. Integration with neuroscientific studies about feedback
Centered Impulsivity and mean current source density (A/m2 ) in the RCZa (bilateral processing in psychopathy and related constructs
spherical ROIs, 8 mm) between 140 and 300 ms post-feedback in the four conditions.

Condition Fearless Dominance Self-Centered Impulsivity Our results extend the limited body of evidence on feedback
r r processing in psychopathy and show that the latter is related
Negative faces −.45* .08 to reduced FRN amplitudes – a relationship which has not been
Negative signs −.41 .15 established by previous studies relying on a unitary construct of
Positive faces −.39 .09 psychopathy. von Borries et al. (2010) found no difference in the
Positive signs .03 .01
FRN between psychopathic violent offenders and controls in a prob-
*
Significantly different from 0 (p ≤ .05). abilistic learning task. Neither did Varlamov et al. (2010) find any
360 S. Schulreich et al. / Biological Psychology 93 (2013) 352–363

has been linked to the emotional-interpersonal dimension (i.e.


“Trait Fearlessness) of psychopathy whereas high BAS to the second
social-deviance dimension (i.e. “Externalizing Vulnerability”; Ross,
Benning, Patrick, Thompson, & Thurston, 2009; Wallace, Malterer,
& Newman, 2009). High BIS has been associated with larger ERN
amplitudes in a Flanker Task (Boksem et al., 2006) and with larger
FRN amplitudes in an instrumental Go/No-Go learning task (De
Pascalis et al., 2010); which is consistent with our findings of
reduced FRN amplitudes for higher Fearless Dominance. Another
clinically relevant dimension, which has been specifically related
to the social-deviance dimension of psychopathy, is externalizing
psychopathology (Patrick et al., 2005). The latter has been associ-
ated with reduced ERN amplitudes in a flanker task (Bernat, Nelson,
Steele, Gehring, & Patrick, 2011) but not with reduced FRN ampli-
tudes after feedback in a gambling task (Bernat et al., 2011). Thus,
one could hypothesize that Self-Centered Impulsivity is unrelated
to the FRN amplitude variation. In fact, we found no significant
relation between Self-Centered Impulsivity and FRN amplitudes.
These overlapping results with regard to related constructs clearly
emphasize the benefits of a dual-process perspective.
An additional remark to be made is that apart from a distinc-
tion of internal and external error monitoring, the latter might
Fig. 5. Grand averages for all feedback conditions (N = 21) at electrode site Pz. also be sub-divided on the basis of the kind of feedback involved.
Approximate P3 windows between peak minima (212 ms) and maxima (496 ms) For instance, Pfabigan et al. (2011) found enhanced FRN ampli-
are displayed. tudes for more antisocial compared to less antisocial individuals
after monetary but not after emotional-social feedback. Although
this study did not investigate psychopathy or specific psycho-
difference in the FRN between psychopathic and non-psychopathic pathic traits, it demonstrates the importance of the type of reward
patients with comorbid personality disorder and controls in a used. In contrast to their results, we observed reduced FRN ampli-
visual Go/No Go task. Although Munro et al. (2007) and Varlamov tudes for Fearless Dominance in the socio-emotional domain (facial
et al. (2010) reported also correlational data between ERPs and feedback), whereas no monetary reward was included in our
PCL-R scores, they did not analyze the factor scores. Moreover, experiment–neither in the task nor in form of remuneration of
this analysis was restricted to violent offenders at a maximum participation. Hence, future studies might compare non-monetary
security forensic hospital (Munro et al., 2007) or subjects with with monetary reward/feedback in individuals with psychopathic
personality disorder detained at medium and high levels of secu- traits.
rity (Varlamov et al., 2010), potentially reducing the variation in
underlying psychopathic dimensions and thus statistical power to 4.3. Integration with neuroscientific models of feedback
detect more specific associations as reported for Fearless Domi- processing and psychopathy
nance here. Another type of external error monitoring is reflected
in the “observed ERN” (oERN), which is elicited when processing On a neuro-computational level, our results give rise to the
the action-outcomes of other observed individuals. This oERN was question how psychopathic traits are involved in the interac-
reduced in psychopathic violent offenders (Brazil et al., 2011). ting mechanisms thought to be central to feedback processing.
Although the authors found an oERN impairment in psychopaths, According to its recent formulation, Reinforcement Learning
future studies might also investigate possible differential contrib- Theory (Baker & Holroyd, 2011; Holroyd et al., 2008) postulates
utions of psychopathic traits. that intrinsic activity of the ACC, which generates the N200 com-
As far as internal monitoring is concerned, von Borries et al. ponent, is suppressed by an extrinsic dopamine reward signal
(2010) observed reduced ERN amplitudes in psychopathic offen- reflected by a component called feedback correct-related positivity
ders in a probabilistic learning task, as well as Dikman and Allen (fCRP)/reward-positivity, resulting in the FRN. Thus, the FRN ampli-
(2000) for the related construct of low socialization. In contrast, tude visible in difference waves (contrasting negative vs. positive
Munro et al. (2007) reported reduced ERN amplitudes in psy- feedback) or FRN amplitude differences between waves for nega-
chopaths in an emotional face flanker task, but not in a standard tive and positive feedback (as measured separately in our study)
letter flanker task. Similarly, Brazil et al. (2009) found intact early might be the result of an interaction of these processes. Thus,
error monitoring (ERN) but deficiencies in later stages of error mon- future research should try to disentangle N200 and fCRP when
itoring/error awareness (Pe) in psychopaths and Brazil et al. (2011) investigating the association with specific psychopathic traits. The
observed similar ERNs in response to one’s own action. Applying alteration in feedback processing associated with Fearless Domi-
a dual-process perspective might also reveal differential contrib- nance might be in the intrinsic activity of the ACC, associated with
utions of psychopathic traits and offer an explanation for these response conflict (Yeung, Botvinick, & Cohen, 2004) or in the extrin-
inconsistent results. sic signals from the mesencephalic dopamine system. In addition to
A consistency check with studies investigating internal and the analysis of event-related potentials, frequency-based methods
external error monitoring in other personality or clinical con- might be a promising and complementary approach. For instance
structs that have been related to psychopathy should provide theta-activity (4–8 Hz) has been associated with response con-
additional information about the value of dual-process models. For flict, performance monitoring and affective processing (Luu, Tucker,
instance, two of the three conceptual brain systems proposed by & Makeig, 2004; Nigbur, Cohen, Ridderinkhof, & Stürmer, 2011;
the Reinforcement Sensitivity Theory (Gray & McNaughton, 2000), Nigbur, Ivanova, & Stürmer, 2011).
the Behavioral Inhibition System (BIS) and the Behavioral Acti- A different aspect of Reinforcement Learning Theory is that –
vation System (BAS) have been linked to psychopathy. Low BIS when learning the action-outcome associations – also enhanced
S. Schulreich et al. / Biological Psychology 93 (2013) 352–363 361

FRN amplitudes could in principle indicate impaired adaptation which could be due to differences in socio-emotional salience.
when back propagation (Holroyd & Coles, 2002) does not take place. However, differences between faces and signs could be equally
However, the paradigm used ensured that feedback remained due to other stimulus characteristics (e.g. differences in complex-
salient throughout the whole task due to the adaptive fashion of the ity).
feedback criteria (see Section 2). Thus, it is reasonable to assume
that reduced FRN amplitudes indicate altered feedback processing.
Feedback processing is not specifically discussed in current neu- 4.5. Methodological considerations
roscientific models of psychopathy and associated brain areas like
the RCZa have to be included in neuroscientific models of psychopa- Our study has some limitations to be considered. Especially
thy. In contrast to Blair’s (2005) integrated emotion system (IES) the rather small sample size renders the present data as prelim-
model of psychopathy, which focuses on the (orbito)frontal cor- inary. Although our study had sufficient power to detect general
tex and amygdala, Kiehl (2006) included the ACC in his extended effects of Fearless Dominance on feedback processing, detection
paralimbic system dysfunction model of psychopathy. However, of more subtle effects, especially interaction effects (e.g. concern-
a detailed account for specific psychopathic traits is missing in ing feedback condition factors), is more difficult given the reduced
his model. The dACC has connections with paralimbic and subcor- power. Further investigations are clearly needed if one wants
tical regions like the orbitofrontal cortex (Morecraft & Van Hoesen, to address for instance the question if feedback variants differ-
1998; van Hoesen, Morecraft, & Vogt, 1993) and the mesencephalic entially modulate the relationship between Fearless Dominance
dopamine system (Crino, Morrison, & Hof, 1993). This points and feedback processing. Another limitation is that only female
toward an interaction of affective/motivational and cognitive pro- participants were recruited for the present study. Therefore, our
cesses, which is consistent with effects of Fearless Dominance on results add to the limited literature regarding psychopathic traits
feedback processing. Apart from our findings related to feedback in healthy females but raise concerns regarding the generalizabil-
processing and the dACC, other neuroscientific evidence should ity with respect to the male population. However, as mentioned
also be incorporated into a neurocognitive dual-process model of before, there is some overlap in structure and correlates of core fea-
psychopathy. As already mentioned briefly, previous studies also tures of psychopathy in men and women (Cale & Lilienfeld, 2002;
found dissociations in executive functions (Carlson & Thái, 2010; Hare & Neumann, 2006; Salekin, Rogers, & Sewell, 1997; Vitacco,
Carlson et al., 2009) or affect recognition (Gordon et al., 2004). An Neumann, & Jackson, 2005; Vitale & Newman, 2001). Differences
integrative view also should include models not specifically cre- were primarily found in aspects central to Self-Centered Impuls-
ated for psychopathy, e.g. Reinforcement Learning Theory (Baker & ivity (e.g. impulsivity, disinhibition) and not Fearless Dominance
Holroyd, 2011; Holroyd & Coles, 2002; Holroyd et al., 2008), Rein- (Verona & Vitale, 2006). This increases the probability that our main
forcement Sensitivity Theory (RST; Corr, 2010; Gray & McNaughton, result can be generalized to the male population. Nevertheless,
2000), and models of decision making (e.g. Rushworth et al., constructive replications with male or mixed gender participants
2007). would be needed.
As far as generalizability is concerned, one needs to be
4.4. Additional findings cautious in drawing inferences for a special segment on the
psychopathy continuum, namely high-end psychopathy that is
Interestingly, Self-Centered Impulsivity was associated with of most clinical interest in terms of diagnosis and interven-
higher values in time estimation (i.e. underestimation of the pas- tion. An undergraduate/graduate sample does not capture the
sage of time). This contrasts the time estimation literature on same variability in the high-end of psychopathic traits as for
impulsivity (for a review see Wittmann & Paulus, 2008), which indi- instance a psychopathic offender sample. Although our samples
cates lower values in time estimation (i.e. overestimation of the shows variability over a large range of the psychopathic traits,
passage of time) in impulsive individuals. However, Wittmann and it is an open and interesting research question if the reported
Paulus (2008) pointed out that this altered time perception seems relationships also holds for high-end psychopathy. One would
to take place especially when subjects are not able to act on their hypothesize this to be the case given the dimensionality of the
impulsive urges, for example in situations of delayed reward and construct. Thus, replications in incarcerated high-end psychopaths
confrontation with the passage of time. In contrast our task did not would be desirable, although possible differences might also be
present a mere passage of time (i.e. passive waiting), but an active attributable to potentially confounding factors like institutional-
time estimation, which might explain the differences. In addition, ization or substance abuse (Lilienfeld, 1996; Sellbom & Verona,
impulsivity and psychopathy are both multidimensional and only 2007), which need to be addressed accordingly. A comparison
partly overlapping constructs (Poythress & Hall, 2011), which could of high- and low-end groups, should also be a powerful test
account for the differences. This might also be true for findings of for the relationship between Fearless Dominance and feedback
reduced FRNs in impulsive individuals (Onoda, Abe, & Yamaguchi, processing as well as it would address generalizability. Although
2010). the conclusions that could be drawn for high-end psychopathy
Despite the significant impact of psychopathic traits on neural are preliminary, our study has higher generalizability for the
correlates of feedback processing, we observed no effects of psy- general population, which is of special interest for personality
chopathy on absolute trial-to-trial adjustment of time estimation. research.
This is what one would expect when considering that FRN ampli-
tude and this behavioral adaptation measure were also not related,
i.e. FRN amplitudes do not mediate behavioral change. Our mea- 5. Conclusion
sure might not perfectly indicate behavioral adaptation as only
absolute trial-to-trial changes in estimation time irrespective of The present study demonstrated a neural dissociation between
the direction of change were analyzed. Furthermore, for improv- different aspects of psychopathic personality associated with
ing performance in the time-estimation task, feedback might need recent dual-process models. Fearless Dominance, but not Self-
to provide additional directional information (Miltner et al., 1997). Centered Impulsivity, was associated with impaired feedback
Some further remarks have to be made about the main effects processing, indicated by decreased FRN amplitudes. The current
found. Both the FRN as well as the P3 are larger for emotional faces data strongly favor to incorporate the dual process perspective in
than for signs in both positive and negative feedback conditions, (neuroscientific) models of psychopathy.
362 S. Schulreich et al. / Biological Psychology 93 (2013) 352–363

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