Download Facial Expression Recognition, Fear Conditioning, and Startle

Facial Expression Recognition, Fear Conditioning, and
Startle Modulation in Female Subjects with Conduct
Disorder
Graeme Fairchild, Yvette Stobbe, Stephanie H.M. van Goozen, Andrew J. Calder, and Ian M. Goodyer
Background: Recent behavioral and psychophysiological studies have provided converging evidence for emotional dysfunction in
conduct disorder (CD). Most of these studies focused on male subjects and little is known about emotional processing in female subjects
with CD. Our primary aim was to characterize explicit and implicit aspects of emotion function to determine whether deficits in these
processes are present in girls with CD.
Methods: Female adolescents with CD (n ⫽ 25) and control subjects with no history of severe antisocial behavior and no current psychiatric
disorder (n ⫽ 30) completed tasks measuring facial expression and facial identity recognition, differential autonomic conditioning, and
affective modulation of the startle reflex by picture valence.
Results: Compared with control subjects, participants with CD showed impaired recognition of anger and disgust but no differences in facial
identity recognition. Impaired sadness recognition was observed in CD participants high in psychopathic traits relative to those lower in psychopathic traits. Participants with CD displayed reduced skin conductance responses to an aversive unconditioned stimulus and impaired autonomic
discrimination between the conditioned stimuli, indicating impaired fear conditioning. Participants with CD also showed reduced startle magnitudes across picture valence types, but there were no significant group differences in the pattern of affective modulation.
Conclusions: Adolescent female subjects with CD exhibited deficits in explicit and implicit tests of emotion function and reduced
autonomic responsiveness across different output systems. There were, however, no differences in emotional reactivity. These findings
suggest that emotional recognition and learning are impaired in female subjects with CD, consistent with results previously obtained in male
subjects with CD.
Key Words: Conduct disorder, emotion, face recognition, female,
psychopathy
C
onduct disorder (CD) is a psychiatric diagnosis characterized by increased levels of aggressive and antisocial
behavior. Although CD is less common in females than
males (1,2), it is nevertheless the second most frequently diagnosed psychiatric disorder in female adolescents (3–5). Conduct
disorder in female adolescents is associated with negative psychosocial outcomes including early pregnancy (6) and increased
rates of morbidity, substance dependence, criminality, and psychiatric illness in adulthood (7,8).
We and others have argued that deficits in emotional learning
and recognition contribute to the etiology of antisocial behavior
(9 –12). Although there is converging evidence for the presence
of such deficits in male adolescents with CD (13,14), little is
known about emotional learning, recognition, or reactivity in
female adolescents with CD. This study addresses these gaps in
the literature.
Facial expressions are an important channel of social communication, carrying information about others’ emotional states.
Conduct disorder is associated with impaired social functioning
that may stem from difficulties in perceiving others’ feelings. We
therefore assessed our participants’ ability to recognize facial
From the Developmental Psychiatry Section (GF, YS, IMG), Department of
Psychiatry, Cambridge University, Cambridge; School of Psychology
(SHMvG), Cardiff University, Cardiff, Wales; and Medical Research Council Cognition and Brain Sciences Unit (AJC), Cambridge, United Kingdom.
Address correspondence to Graeme Fairchild, Ph.D., Developmental Psychiatry Section, Cambridge University, Douglas House, 18b Trumpington
Road, Cambridge, CB2 8AH, UK; E-mail: [email protected].
Received Sep 4, 2009; revised Feb 18, 2010; accepted Feb 20, 2010.
0006-3223/$36.00
doi:10.1016/j.biopsych.2010.02.019
expressions. Given previous findings in male subjects (14), we
predicted impaired anger and disgust recognition in girls with
CD. We also hypothesized that variation in psychopathic traits
would influence recognition of fear and sadness (14,15). The
Benton Facial Recognition Test (16) assessed for potential group
differences in face perception skills.
We studied fear conditioning as an objective measure of
emotional learning. Skin conductance responses (SCRs) to conditioned stimuli positive (CS⫹) were measured before and after
the CS⫹ were paired with an aversive unconditioned stimulus
(US) to examine transfer of fear responses from the US to the
CS⫹. Patients with anxiety disorders show enhanced fear conditioning (17), whereas fear-conditioning deficits are observed in
adult psychopaths (18 –21) and male subjects with CD (13).
Consequently, we predicted impaired conditioning in female
subjects with CD.
Finally, we assessed affective modulation of the startle
reflex, a sensitive index of emotional reactivity (22–26).
Eyeblink startle reflexes to an acoustic probe are typically
attenuated when pleasant images are viewed and potentiated
by negative images (27). This pattern of modulation is proposed to result from priming of appetitive or defensive
motivational systems by the visual images (28). Affective
startle modulation has been used to investigate emotionrelated psychopathology, with anxious individuals showing
increased (29) and psychopaths showing reduced (30 –32)
potentiation by negative images. Previous work in male
adolescents with CD or children with oppositional defiant
disorder (ODD) did not reveal aberrant patterns of affective
modulation, but overall startle magnitudes were reduced in
both groups compared with control subjects (13,33). We
therefore predicted reduced startle magnitudes but a normal
pattern of affective modulation in female subjects with CD.
BIOL PSYCHIATRY 2010;68:272–279
© 2010 Society of Biological Psychiatry
G. Fairchild et al.
Methods and Materials
Participants
Fifty-five female adolescents aged 14 to 18 years were recruited from schools, pupil referral units, and the Cambridge
Youth Offending Service. Twenty-five participants had CD or
ODD (three had ODD only). Most (n ⫽ 22) participants with
CD/ODD had adolescence-onset CD/ODD (i.e., onset of symptoms and functional impairment after age 10 [34]). For brevity, the
term CD refers to the overall group with disruptive behavior
disorders. We also tested 30 age- and sex-matched healthy
control subjects (no lifetime CD/ODD and no current psychiatric
illness). The Local Research Ethics Committee approved the
study and all participants provided written informed consent.
All participants were in midpuberty to postpuberty (Tanner
Stage III or above [35]) and were tested 5 to 12 days after the
onset of menstruation (early- to mid-follicular phase) because
startle magnitudes and facial expression recognition accuracy
may vary during the menstrual cycle (36,37).
Exclusion criteria included full-scale IQ ⬍75 as estimated
using matrix reasoning and vocabulary subtests of the Wechsler
Abbreviated Scale of Intelligence (38), presence of pervasive
developmental disorder (e.g., autism) or chronic physical illness,
and current steroid medication use.
Participants were assessed for CD, ODD, attention-deficit/
hyperactivity disorder (ADHD), major depressive disorder
(MDD), generalized anxiety disorder, obsessive compulsive disorder, and posttraumatic stress disorder using the Schedule for
Affective Disorders and Schizophrenia for School-Age ChildrenPresent and Lifetime version (39). Separate diagnostic interviews
were carried out with participants and their caregivers.
Psychopathic traits were measured using the Youth Psychopathic traits Inventory (YPI) (40). Participants with total scores ⱖ
2.5 were classified as being high in psychopathic traits (41). We
assessed callous-unemotional traits using the callous-unemotional dimension YPI subscale (40). Anxiety symptoms were
measured using the Revised Children’s Manifest Anxiety Scale
(42). The Adolescent Alcohol and Drug Involvement Scale
assessed alcohol and substance use (43). Socioeconomic status
was estimated using the occupation of the participant’s caregiver
using the Standard Occupational Classification 2000 (44).
Facial Identity Perception
The Benton Facial Recognition Test (16) assesses participants’
ability to match pictures of unfamiliar faces and was used to
screen for basic face perception deficits. Participants are asked to
identify a target face(s) from an array of six faces, presented
under different illumination or head orientation conditions.
Facial Expression Recognition
The emotion hexagon task was used to assess facial expression recognition ability (45). Participants were asked to label
morphed facial expression continua spanning the following six
expression pairs: happiness-surprise, surprise-fear, fear-sadness,
sadness-disgust, disgust-anger, and anger-happiness (Figure S1
in Supplement 1). For example, for happiness-surprise, facial
images of happy and surprised expressions were morphed to
create a series of pictures ranging across five ratios (90%–10%,
70%–30%, 50%–50%, 30%–70%, and 10%–90%). Morphed faces
were presented individually on a computer monitor in random
order. Each face was presented for a maximum of 5 sec and
participants were asked to label the expression displayed. After a
practice block, participants completed five blocks, with each
BIOL PSYCHIATRY 2010;68:272–279 273
block containing one instance of each of the 20 morphed faces
(and four instances of each expression). For each expression, the
total score ranged from 0 to 20, with 50%-50% morphed images
not being scored.
Aversive Conditioning
Skin Conductance Recording. Electrodermal activity was
measured at the distal phalanges of the index and middle fingers
of the nondominant hand, using a skin conductance transducer
(TSD203) and amplifier (GSR100C) connected to an MP150
system (all BIOPAC Systems, Goleta, California). The electrodes
of the transducer were filled with skin conductance paste, and
electrodermal activity was sampled at 50 Hz. The task computer
sent digital markers to the MP150 system to indicate slide onset
and offset and also onset of the white noise tone. Data were
analyzed offline using AcqKnowledge 3.8.1 (BIOPAC Systems).
Fear Conditioning Procedure. We assessed differential conditioning (CS⫹ ⫽ blue slides and conditioned stimulus negative
[CS–] ⫽ red slides) with partial (56%) reinforcement during
acquisition, following Bechara and Damasio (46). Briefly, we
used monochrome slides as the visual conditioned stimuli (CS),
a loud (97 dB) aversive white noise tone lasting 1000 msec as the
US, and the amplitude of the SCR in the 7-sec period following CS
presentation as the dependent measure of the conditioning
process. The colored slides were presented for 3 sec with a
10-sec interslide interval. The aversive tone was presented
binaurally via headphones. When presented with the CS⫹
(reinforced trials), the white noise tone occurred 2 sec after slide
onset. The conditioned SCR amplitude within the 7-sec analysis
window was quantified using the peak-to-peak function in
AcqKnowledge and the slope function to determine the direction
of the change (positive or negative).
The procedure involved four phases: habituation (HAB),
acquisition 1 (ACQ1), acquisition 2 (ACQ2), and extinction
(EXT). During the habituation phase, the average SCR elicited by
the CS⫹ was compared with that elicited by the CS– (two of each
slide type were presented). In the acquisition phases, the average
SCR to the unreinforced CS⫹ was compared with the average
SCR to the CS⫺. Acquisition 1 comprised the first four unreinforced CS⫹, five reinforced CS⫹, and five presentations of the
CS–, presented in pseudorandom order. Acquisition 2 involved
the same combination of CS⫹ and CS– slides in a different order.
The EXT phase comprised six unreinforced CS⫹ and three CS–
trials. Again, average SCRs to the CS⫹ and CS– were compared.
After the experiment had finished, participants were asked to
recall salient aspects of the task to ensure that they had been
paying attention, i.e., how many and which colors they had seen
and the number of slides and the color that had been paired with
the aversive sound.
Affective Modulation of the Startle Reflex
We modified the design employed by Patrick et al. (30).
Participants viewed nine positive, nine neutral, nine sad, nine
disgusting, and nine fearful images from the International Affective Pictures System (47) (see [13] for International Affective
Pictures System numbers and normative valence and arousal
ratings). Slides were presented in a single, fixed, pseudorandom
sequence. Each slide was displayed for 10 sec with an interslide
interval of 10 sec.
Eyeblink responses to the startle probes were measured using
silver/silver chloride electrodes positioned over the orbicularis
oculi muscle (48). Electromyographic data were recorded at 1000
Hz using an EMG100C amplifier module (BIOPAC Systems), with
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274 BIOL PSYCHIATRY 2010;68:272–279
G. Fairchild et al.
Controls (n = 30)
Conduct Disorder (n = 25)
100
90
Correct recognition (%)
a bandpass of 30 Hz to 500 Hz. A 97-dB white noise probe lasting
100 msec was presented binaurally via headphones. To reduce
the impact of habituation, only 30 slides were accompanied by
the startle probe (6 from each slide category). The slides were
presented in blocks to examine for possible effects of habituation. Probe presentation was varied relative to slide onset (3500,
4500, or 5500 msec after onset).
Startle responses were quantified offline using AcqKnowledge functions “Max” and “Min” in the electromyographic channel using an analysis window beginning 30 msec after and
terminating 100 msec after startle probe onset. These values were
subtracted from baseline Max and Min values within the 50-msec
period before probe onset to yield integrated values for startle
magnitude.
**
***
80
70
60
50
40
30
20
10
0
Anger
Disgust
Fear
Happiness Sadness
Surprise
Emotional expression depicted
Data Analyses
Chi-square and independent t tests were used to investigate
group differences in demographic and personality characteristics. Independent t tests compared groups on the Benton Facial
Recognition Test. All other statistical tests are described in the
Results section. Where the data violated sphericity, Huynh-Feldt
or Greenhouse-Geisser correction was applied as appropriate
(49). Effect sizes are reported as r equivalent (50) (abbreviated to
r; small ⱖ.10, medium ⱖ.30, large ⱖ.50; [51]) or partial etasquared. Analyses were conducted using SPSS 11.5 (SPSS, Inc.,
Chicago, Illinois).
Figure 1. Accuracy of facial expression recognition by group. Relative to
control subjects, participants with conduct disorder showed impairments in
anger and disgust recognition. **p ⬍ .01, ***p ⬍ .005.
Results
Facial Expression Recognition
The emotion hexagon task results are shown in Figure 1. The
data were not normally distributed and could not be transformed
to a normal distribution. Mann-Whitney tests were therefore used
to compare groups on the six expressions separately, using an
alpha level of .008 (i.e., .05/6) to control for multiple comparisons.
Relative to control subjects, CD participants showed significant deficits in recognition of anger (Z ⫽ ⫺2.70, p ⫽ .007, r ⫽
.35) and disgust (Z ⫽ ⫺2.86, p ⫽ .004, r ⫽ .37) but not fear,
happiness, sadness, or surprise (all p ⬎ .1).
Confusion matrices showing which emotion labels were
selected if the target emotion was misidentified are provided in
Table S1A and Table S1B in Supplement 1.
The anger and disgust recognition deficits were still significant (both p ⫽ .03; r ⫽ .30 and r ⫽ .31, respectively) after
equating groups on estimated IQ (p ⫽ .13) by removing eight
high IQ control subjects (⬎118 on the Wechsler Abbreviated
Scale of Intelligence). This procedure reduced sample size; thus,
an alpha of .05 was used. To rule out the possibility that the
group findings were driven by comorbid MDD or ADHD, we
omitted participants with these disorders and repeated the
analyses. The findings for anger and disgust were significant
(both p ⫽ .01, r ⫽ .33) when participants with MDD were
excluded. Following exclusion of participants with ADHD, the
disgust deficit was significant (p ⬍ .01, r ⫽ .35) and the anger
deficit was of borderline significance (p ⫽ .055, r ⫽ .27).
Demographic Characteristics
The groups were matched for age, ethnicity, and socioeconomic status, but control subjects were of higher intelligence
than CD participants (p ⬍ .005; Table 1). Compared with control
subjects, significantly more CD participants reported regular use
of tobacco [␹2(1) ⫽ 27.5, p ⬍ .001], alcohol [␹2(1) ⫽ 8.5, p ⬍
.005], and cannabis [␹2(1) ⫽ 15.5, p ⬍ .001]. Conduct disorder
Table 1. Participant Characteristics
Age (years, mean ⫾ SD)
Estimated IQ (mean ⫾ SD)
MDD Diagnosis
ADHD Diagnosis
Psychopathic Traits (YPI)
Anxiety
SES
Low
Middle
High
Ethnicity
Caucasian
Nonwhite
Regular Use of:
Tobacco
Alcohol
Cannabis
Control Subjects
(n ⫽ 30)
CD (n ⫽ 25)
p Value
15.3 ⫾ .7
108.3 ⫾ 14.0
0a
0a
1.94 ⫾ .35
11.5 ⫾ 6.9
15.6 ⫾ 1.0
97.2 ⫾ 11.0
2
5
2.44 ⫾ .35
13.0 ⫾ 6.3
.279
.002
5
10
15
4
0
10
29
1
23
2
3 (10%)
11 (37%)
3 (10%)
20 (80%)
19 (76%)
15 (60%)
⬍.001
.396
.799
.448
⬍.001
.002
⬍.001
Socioeconomic status information was unavailable for one conduct disorder participant.
ADHD, attention-deficit/hyperactivity disorder; CD, conduct disorder;
MDD, major depressive disorder; SES, socioeconomic status; YPI, Youth
Psychopathic traits Inventory.
a
The presence of major depressive disorder or attention-deficit/hyperactivity disorder was an exclusion criterion for the control group.
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participants also had higher levels of psychopathic (p ⬍ .001)
and callous-unemotional (p ⬍ .001) traits. There were no group
differences in self-reported anxiety.
Facial Identity Recognition
There was no group difference in face recognition [t (53) ⫽
1.13, p ⫽ .26]. Mean (⫾ SD) score for control subjects ⫽ 46.4/54
(⫾ 2.9) and for CD participants ⫽ 45.6/54 (⫾ 2.5).
Effect of Psychopathic Traits on Facial Expression Recognition
Given our a priori hypothesis of impairments in fear and
sadness recognition in CD participants high in psychopathic
traits, we examined the relationship between YPI score and
expression recognition by splitting the CD sample using the YPI
cutoff of 2.5. Figure 2 shows facial expression recognition
accuracy in high and lower psychopathy CD subgroups.
Comparing these subgroups revealed deficits in recognition
of sadness (Z ⫽ ⫺2.96, p ⫽ .003, r ⫽ .53), but no other emotions,
BIOL PSYCHIATRY 2010;68:272–279 275
G. Fairchild et al.
Lower psychopathy (n = 14)
Higher psychopathy (n = 11)
SCR ( siemens)
100
90
Correct recognition (%)
A
0.2
80
70
60
50
40
30
20
10
0.1
0.0
-0.1
-0.2
0
Disgust
Fear
Happiness Sadness
HAB
Surprise
Emotional expression depicted
B
Figure 2. Effect of psychopathic traits on facial expression recognition,
considering participants with conduct disorder only. Participants high in
psychopathic traits, as measured using total scores on the Youth Psychopathic traits Inventory, showed a specific deficit in recognition of sadness
relative to conduct disorder participants lower in psychopathic traits.
***p ⬍ .005.
in those high in psychopathic traits. This effect was not accounted for by subgroup differences in IQ (p ⫽ .48) or Benton
Facial Recognition Test performance (p ⫽ .60). Repeating these
analyses using callous-unemotional traits yielded similar results
for sadness (Z ⫽ ⫺2.17, p ⫽ .03, r ⫽ .41).
Only one control scored above the YPI cutoff, preventing us
from using the above method to investigate effects of psychopathic traits on facial expression recognition in control subjects.
However, neither overall psychopathic nor callous-unemotional
traits were significantly correlated with sadness or fear recognition in control subjects using Spearman’s rho.
Aversive Conditioning
Data were unavailable for eight participants due to technical
or experimenter error or inability to tolerate the procedure.
Recall score did not differ between groups (p ⫽ .95); both could
articulate the experimental contingencies.
Autonomic Measures
The SCR data were not normally distributed, so they were
normalized using a log(SCR ⫹ 1) transformation. Raw values are
shown in the figures for ease of interpretation.
2.5
Controls (n = 25)
Conduct Disorder (n = 23)
2.0
1.5
1.0
0.5
0.0
US1
US2
US3
US4
US5
US6
US7
US8
US9
US10
Unconditioned stimulus number
Figure 3. Skin conductance responses (SCRs) to the 10 presentations of the
aversive unconditioned stimulus, by group. Although both groups showed
marked habituation of SCRs to the unconditioned stimulus over time, control subjects showed significantly larger SCRs than conduct disorder participants across all trials. US, unconditioned stimulus.
SCR ( siemens)
Anger
Skin conductance response ( siemens)
Control CS+
Control CS-
***
ACQ1
ACQ2
0.2
EXT
CD CS+
CD CS-
0.1
0.0
-0.1
-0.2
HAB
ACQ1
ACQ2
EXT
Conditioning phase
Figure 4. Mean (⫾ SE) skin conductance responses to blue test slides (conditioned stimulus positive unpaired with unconditioned stimulus, solid line
and closed symbols) and red control slides (conditioned stimulus negative,
dashed line and open symbols) across conditioning phases in: (A) control
and (B) conduct disorder groups. Control participants showed enhanced
differential conditioning, as shown by a larger difference between skin
conductance responses to the conditioned stimulus positive and the conditioned stimulus negative during acquisition phase 1 and acquisition phase
1, relative to conduct participants. ACQ1, acquisition phase 1; ACQ2, acquisition phase 2; CD, conduct disorder; CS–, conditioned stimulus negative;
CS⫹, conditioned stimulus positive; EXT, extinction phase; HAB, habituation
phase; SCR, skin conductance response.
We first examined whether SCRs to the US differed over time
and by group, using repeated-measures analysis of variance
(ANOVA) with time as within-subjects factor and group as
between-subjects factor (10 ⫻ 2). This revealed effects of time
[F (4.61,212.03) ⫽ 26.38, p ⬍ .001, ␩p2 ⫽ .37] and group [F(1,46) ⫽
5.18, p ⬍ .05, ␩p2 ⫽ .10] but no interaction (F ⬍ 1). Skin
conductance responses to the US were lower in CD participants
than control subjects (Figure 3). Additionally, SCRs to the US
declined strongly over time in both groups.
Group differences in autonomic conditioning were assessed
using a mixed-model ANOVA with group (control, CD) as a
between-subjects factor and CS type (CS⫹, CS⫺) and conditioning phase (HAB, ACQ1, ACQ2, EXT) as within-subjects factors
(2 ⫻ 2 ⫻ 4). This revealed effects of CS type [F (1,46) ⫽ 21.01, p ⬍
.001, ␩p2 ⫽ .31] and conditioning phase [F (3,138) ⫽ 5.78, p ⬍
.005, ␩p2 ⫽ .11] but not group [F (1,46) ⫽ 3.11, p ⫽ .08].
Underlying the phase effect, SCRs were larger during HAB than
ACQ1 or ACQ2 (both p ⱕ .01). Underlying the CS type effect,
subjects showed larger SCRs to the CS⫹ than the CS– (p ⬍ .001).
We also observed significant group ⫻ CS type [F (1,46) ⫽ 3.98,
p ⫽ .05, ␩p2 ⫽ .08] and conditioning phase ⫻ CS type
[F (1.47,67.76) ⫽ 4.10, p ⬍ .05, ␩p2 ⫽ .08] interactions. Breaking
down the former, control subjects exhibited greater SCR differentiation between CS types than CD participants (Figure 4), as
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276 BIOL PSYCHIATRY 2010;68:272–279
Startle Reflex Modulation by Affective Valence
Data were unavailable for seven participants due to technical
or experimenter error or parents withholding consent for their
children to participate in this experiment.
The startle data were not normally distributed, so they were
normalized using a square root transformation. Absolute values
are provided in Figure 5 for ease of interpretation.
We ran a repeated-measures ANOVA with slide category as a
within-subjects factor and group as a between-subjects factor
(5 ⫻ 2). This revealed effects of slide category [F (4,180) ⫽ 14.79,
p ⬍ .001, ␩p2 ⫽ .25] and group [F (1,45) ⫽ 4.61, p ⬍ .05, ␩p2 ⫽
.09] but no interaction effect (p ⫽ .09). Pairwise comparisons
between slide categories showed reduced startle magnitudes to
the acoustic probe when participants viewed positive slides,
relative to all negative slides (all p ⬍ .005). Startle magnitudes
were larger when viewing disgusting and fearful slides compared
with neutral slides (both p ⬍ .005) and when viewing disgusting
compared with sad slides (p ⬍ .005). Thus, startle magnitudes
were significantly modulated by slide category.
Underlying the group effect, CD participants exhibited lower
startle magnitudes across all slide categories (Figure 5). This
effect remained significant (p ⬍ .05, ␩p2 ⫽ .15) following
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20
Eyeblink startle response (mV)
shown using separate repeated-measures ANOVAs for each
group, which revealed an effect of CS type in control subjects
[F (1,24) ⫽ 31.45, p ⬍ .001, ␩p2 ⫽ .57] but not CD participants
[F (1,22) ⫽ 2.46, p ⫽ .13].
The CS type ⫻ phase interaction was driven by a divergent
pattern of SCRs to the respective CS types between habituation
and acquisition 1 and 2. That is, the difference in SCRs between
the CS⫹ and CS– was much greater during acquisition 1 and
2, relative to habituation. There was, however, no significant
group ⫻ CS type ⫻ phase interaction.
To ensure that group differences in autonomic conditioning
were not explained by IQ differences, we ran an analysis of
covariance (ANCOVA) with IQ as a covariate. The IQ was a
significant covariate, but after accounting for IQ, all results
except the effect of CS type remained significant and a main
effect of group emerged [F (1,45) ⫽ 12.76, p ⬍ .001, ␩p2 ⫽ .22].
To examine the impact of comorbidity, we excluded participants
with ADHD and reran the analyses. The group ⫻ CS type
interaction was not significant but had a similar effect size
[F (1,41) ⫽ 3.42, p ⫽ .07, ␩p2 ⫽ .08]. Crucially, there was still no
effect of CS type in this noncomorbid CD subgroup [F (1,17) ⫽
1.52, p ⫽ .23]. The group ⫻ CS type interaction was significant
[F (1,44) ⫽ 4.24, p ⬍ .05, ␩p2 ⫽ .09] following exclusion of
participants with MDD.
To investigate the possibility that reduced US responsiveness
caused the conditioning impairments, we excluded seven CD
participants with small SCRs to the US (mean values ⬍ .2 ␮S
across 10 US trials). There was no effect of CS type in the CD
subgroup with normal SCRs to the US [F (1,15) ⫽ 2.0, p ⫽ .17].
In separate ANCOVAs controlling for tobacco, alcohol, or
cannabis use, the group ⫻ CS type interaction remained significant in each case (all p ⬍ .05, ␩p2 ⱖ .09). Finally, we explored
whether psychopathic traits influenced fear conditioning. In an
ANCOVA with psychopathic traits as a covariate, this variable
was not a significant covariate when considering the entire
sample. We also assessed for differences in fear conditioning
between the low and high psychopathy CD subgroups (Figure S2
in Supplement 1). There was no effect of subgroup status (p ⫽
.73) nor a subgroup ⫻ CS type interaction (p ⫽ .59). Neither
subgroup showed an effect of CS type (both p ⬎ .12).
G. Fairchild et al.
18
Controls (n = 24)
Conduct Disorder (n = 23)
16
14
12
10
8
6
4
2
0
Positive
Neutral
Sad
Disgusting
Fearful
Slide valence
Figure 5. Mean (⫾ SE) startle reflex magnitudes to a 97-dB acoustic probe
when viewing pictures of different affective valence, by group. Compared
with control subjects, conduct disorder participants exhibited reduced startle magnitudes (p ⬍ .05) regardless of slide valence, although the pattern of
affective modulation did not differ significantly between groups. mV, millivolt.
exclusion of participants with average startle responses ⬍2.5 mV
(nonresponders to the startle probe [31]) and following statistical
adjustment for differences in IQ and psychopathic traits (both
p ⬍ .05). Furthermore, it was marginally significant following
exclusion of participants with MDD (p ⫽ .06, ␩p2 ⫽ .08) or
ADHD (p ⫽ .06, ␩p2 ⫽ .08).
The influence of psychopathy on affective modulation was
explored further by splitting the CD sample into high and low
psychopathy subgroups. There was no subgroup effect on overall
startle magnitudes (p ⫽ .88) or a psychopathy subgroup ⫻ slide
category interaction (p ⫽ .42; Figure S3 in Supplement 1). Hence,
there was no evidence for reduced affective modulation in the high
relative to the low psychopathy CD subgroup.
Finally, group effects on startle magnitude remained significant
when controlling for differences in tobacco (p ⬍ .05, ␩p2 ⫽ .11),
cannabis (p ⫽ .05, ␩p2 ⫽ .08), or alcohol use (p ⬍ .005, ␩p2 ⫽ .18).
Discussion
The objective of this study was to investigate emotional
recognition, learning, and reactivity in female adolescents with
CD. Consistent with predictions, female subjects with CD
showed impaired recognition of anger and disgust relative to
control subjects. This pattern was similar to that previously
observed in male subjects with early-onset CD (14) and adults
with impulsive aggression problems (52). Although impaired
anger recognition in CD may be considered counterintuitive
given evidence for hostile biases in social information processing
in aggressive individuals (53), our data provide further evidence
for reduced, rather than increased, sensitivity to hostile facial
signals in CD. This observation is important because facial
expressions convey information about the feelings and intentions of others. In particular, angry expressions can be considered social punishment signals, informing the observer that they
should stop their current behavioral action (54).
In addition to showing that female subjects with CD scored
higher than control subjects on measures of psychopathic and
callous-unemotional traits, we demonstrated that variation in
these personality traits influenced recognition of sad expressions.
However, contrary to predictions, variation in psychopathic traits
did not affect fear recognition. Several studies have demonstrated
impaired fear and sadness recognition in children (15,55) and
G. Fairchild et al.
adults (56 –58) with psychopathic traits, although conflicting
findings are reported (59,60).
The present findings on startle reflex modulation do not
provide clear evidence for aberrant modulation by affective
valence in female subjects with CD. Earlier research in boys with
CD or ODD also did not reveal an abnormal pattern of affective
modulation (13,33). These data indicate that physiological sensitivity to the emotional valence of visual stimuli is intact in some
individuals with CD, and as a group they do not show an
aberrant pattern of affective modulation as observed in adult
psychopaths (30 –32,61). Furthermore, splitting the CD sample
into those high and low in psychopathic traits did not reveal
deficient affective modulation in the former. The CD participants
in this study did, however, show reduced startle responses to the
acoustic probe used to elicit the startle reflex, regardless of slide
affective valence, consistent with previous results (13,33).
Further evidence for reduced autonomic responsiveness in
female subjects with CD comes from our aversive conditioning
experiment. Although both groups displayed strong SCR habituation to the aversive US, responses to this stimulus were consistently lower in participants with CD than control subjects. With
respect to autonomic conditioning to neutral stimuli, we observed a group ⫻ CS type interaction, underpinned by control
subjects showing increased SCRs to the CS⫹ (which predicted
the US) relative to the CS– (which did not predict the US),
whereas CD participants failed to differentiate between these
stimuli. Female subjects with CD therefore showed impaired fear
conditioning, consistent with previous data from male adolescents with CD (13) and adult psychopaths (18 –21). Longitudinal
studies have shown that impaired fear conditioning in early
childhood may predict involvement in criminal activity by age 23
(62), whereas enhanced conditioning may act as a protective
factor (63).
Theoretical Implications
Our results, demonstrating deficits in emotional recognition
and learning in CD, may help to explain why individuals with CD
experience interpersonal difficulties and problems in learning
from punishment. These impairments did not appear to be
explained by lower cognitive ability (a general deficit) in the CD
group, because all results remained significant following adjustment for IQ differences or exclusion of high IQ control subjects.
Additionally, our nonaffective control tasks (assessing facial
identity recognition and awareness of the CS⫹-US contingency
in the conditioning experiment) showed no group differences,
providing further evidence for a disproportionate impairment in
emotional functioning in CD. Because conditioning deficits and
reduced startle magnitudes are reported in patients with amygdala lesions (64 – 67), our findings may be interpreted as evidence for amygdala dysfunction in CD. However, the lack of
deficits in fear recognition or affective modulation in female
subjects with CD is problematic for this position because amygdala lesions are associated with impairments in these processes
(68 –70). Further research using neuroimaging techniques is
required to investigate the neural basis of the behavioral and
autonomic differences reported in this study.
Our results provide indirect support for the delayed-onset
pathway model of antisocial behavior in female subjects (71). This
proposes that female subjects with adolescence-onset CD should
show neuropsychological vulnerabilities in common with male
subjects with early-onset CD, even though the former show a delay
in the emergence of their clinical phenotype. A key question for
future research is why, despite the presence of these neuropsycho-
BIOL PSYCHIATRY 2010;68:272–279 277
logical vulnerabilities, female subjects with CD generally do not
exhibit severe antisocial behavior until adolescence (1,72).
Five limitations are noted. First, the sample was relatively
small, which may have made it difficult to demonstrate aberrant
affective modulation of startle due to power limitations. Second,
because we had to analyze the facial expression recognition data
using nonparametric statistics, we were unable to control for
group differences in IQ using ANCOVA procedures. We instead
equated groups for IQ by omitting high IQ control subjects but
cannot exclude the possibility that group differences in facial
expression recognition were partially driven by IQ. Third, conflating early-onset and adolescence-onset forms of CD (plus CD
and ODD) was not optimal. These findings thus require replication in a larger sample, ideally with a prospective design to avoid
using retrospective reports of symptom onset (the fourth limitation). Fifth, using a similar aversive noise as the US in our
conditioning task and as the acoustic probe in our startle
experiment was not ideal.
Conclusions
This study provides evidence for deficits in emotional recognition and learning in female subjects with CD, consistent with
previous results in male subjects with early-onset CD. Our
findings therefore suggest that neural systems involved in emotional recognition and learning may be compromised in CD. We
found no clear evidence for reduced emotional reactivity but
instead observed a generalized deficit in autonomic reactivity in
female subjects with CD.
The study was funded by Wellcome Trust Project Grant
Number 069679 and completed within the National Institute for
Health Research Collaboration for Leadership in Applied Health
Research and Care for Cambridgeshire and Peterborough. AJC
was supported by the Medical Research Council, project code
U.1055.02.001.00001.01.
We thank our participants and their parents and teachers for
taking part in the study. We also thank the Cambridge Youth
Offending Service and the schools and pupil referral units for
their help with recruitment.
The authors report no biomedical financial interests or potential conflicts of interest.
Supplementary material cited in this article is available
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