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Schizophrenia Research 165 (2015) 6065

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Schizophrenia Research
journal homepage: www.elsevier.com/locate/schres

Impaired facial emotion recognition in individuals at ultra-high risk for


psychosis and with rst-episode schizophrenia, and their associations
with neurocognitive decits and self-reported schizotypy
Su Young Lee a,b,1, Minji Bang a,c,1, Kyung Ran Kim a,c, Mi Kyung Lee a, Jin Young Park a,d, Yun Young Song a,e,
Jee In Kang a,c, Eun Lee a,c, Suk Kyoon An a,c,f,
a

Section of Affect and Neuroscience, Institute of Behavioral Science in Medicine, Yonsei University College of Medicine, Seoul, South Korea
Department of Psychiatry, Cheil General Hospital & Women's Healthcare Center, Dankook University College of Medicine, Seoul, South Korea
c
Department of Psychiatry, Yonsei University College of Medicine, Severance Hospital, Seoul, South Korea
d
Department of Psychiatry, Yonsei University College of Medicine, Gangnam Severance Hospital, Seoul, South Korea
e
Department of Psychiatry, Seoul National Hospital, Seoul, South Korea
f
Graduate Program in Cognitive Science, Yonsei University, Seoul, South Korea
b

a r t i c l e

i n f o

Article history:
Received 10 January 2015
Received in revised form 17 March 2015
Accepted 22 March 2015
Available online 10 April 2015
Keywords:
Facial emotions recognition
Schizotypy
Ultra-high risk for psychosis
First-episode
Schizophrenia
Decit
Neurocognition

a b s t r a c t
Objective: This study aims to quantify facial emotion recognition abnormalities and their relation to
neurocognitive dysfunction and schizotypy in individuals at ultra-high risk (UHR) for psychosis and patients
with rst-episode schizophrenia (FES).
Methods: Forty individuals at UHR for psychosis, 24 patients with FES and 46 normal controls performed a facial
emotion recognition task that presented facial photographs encompassing all basic emotions. The perceptual
aberration scale and revised social anhedonia scale were employed for self-reported assessment of schizotypy.
An intellectual functioning (IQ) test and a broad battery of neurocognitive tests were conducted. Emotional
task performance indexed by accuracy rate of specic emotion was compared among three groups. The correlation of accuracy rate with neurocognitive tests and schizotypy scales were analyzed within each clinical group.
Results: A recognition decit of facial emotions was present in both clinical groups, even after adjusting for IQ and
gender as covariates. This emotional decit showed few signicant relationships with broad range of individual
neurocognitive measures. Meanwhile, this decit demonstrated signicant relationships with schizotypy,
especially perceptual aberration in each clinical group.
Conclusions: Facial emotion recognition decit may not only be present in FES patients, but may already have
evolved prior to the onset of overt psychotic symptoms. This emotion recognition decit may be linked to a
perceptual aberration and largely independent of broad range of neurocognitive dysfunction.
2015 Elsevier B.V. All rights reserved.

1. Introduction
Facial emotion recognition, or the ability to infer others' emotional
states, is essential for adaptive social interaction. Decit in facial
emotion recognition is a widely replicated nding in patients with
schizophrenia, including rst-episode patients (Edwards et al., 2001,
2002; Green et al., 2005; Addington et al., 2006; Kohler et al., 2010;
Savla et al., 2013). This decit is considered as a unique feature of
schizophrenia, going beyond neurocognitive impairment (Edwards

Corresponding author at: Department of Psychiatry, Yonsei University College of


Medicine, Seoul, South Korea, Severance Hospital, Yonsei University Health System, 50-1
Yonsei-ro, Seodaemun-gu, Seoul, 120-752, South Korea. Tel.: + 82 2 2228 1585;
fax: +82 2 313 0891.
E-mail addresses: ansk@yuhs.ac, ansk@yonsei.ac.kr (S.K. An).
1
These two authors contributed equally to this study as rst authors.

http://dx.doi.org/10.1016/j.schres.2015.03.026
0920-9964/ 2015 Elsevier B.V. All rights reserved.

et al., 2001; An et al., 2003; Kohler et al., 2003, 2010), although there
have been some contentions that emotional decit may be secondary
to general neurocognitive impairment (Kohler et al., 2000; Addington
et al., 2006).
In recent years, facial emotion recognition decit has been investigated in the putative prodromal, ultra-high-risk (UHR) phase of schizophrenia. Individuals at UHR, presenting attenuated but clinically
meaningful psychotic symptoms have elevated risk of transition into
frank psychosis (Yung and McGorry, 1996), while they are relatively
less contaminated by secondary morbidity with chronic illness accompanied by marked neurocognitive decline (Fusar-Poli et al., 2012a).
Impaired facial emotion recognition in individuals at UHR have been
demonstrated in a number of investigations (Addington et al., 2008;
van Rijn et al., 2011; Amminger et al., 2012a, 2012b; Green et al.,
2012; Thompson et al., 2012; Wolwer et al., 2012) including a metaanalysis (Fusar-Poli et al., 2012b). Furthermore, impairment in facial

S.Y. Lee et al. / Schizophrenia Research 165 (2015) 6065

emotion recognition has remained apparent even after adjusting for


intellectual dysfunction (IQ) and/or psychopathology (van Rijn et al.,
2011; Amminger et al., 2012a, 2012b; Comparelli et al., 2013; Bliksted
et al., 2014) while it was also reported that social cognition and
neurocognition are closely related in clinical high risk individuals
(Yong et al., 2014). Because there has been growing evidence that social
cognition and neurocognition are distinct constructs (Sergi et al., 2007;
Green et al., 2008; Eack et al., 2010), facial emotion recognition decit
may be an independent disease-related marker, not just consequence
of neurocognitive decit.
As a potential intermediate phenotype, facial emotion recognition
decit has been investigated in line with schizotypy, which reects
genetic vulnerability to schizophrenia (Meehl, 1962, 1990). Previous
studies reported that facial emotion recognition was related to the
individual differences in psychometrically dened psychosis-proneness
in nonclinical populations (Shean et al., 2007; Germine and Hooker,
2011; Abbott and Green, 2013) and adolescents with schizotypal personality disorder (Wickline et al., 2012). In particular, both self-reported
scales of perceptual aberration and social anhedonia have been considered to be closely related with facial emotion recognition (Shean et al.,
2007; Germine et al., 2011; Abbott and Green, 2013). Perceptual aberration measures the abnormal awareness of one's own body and blurring
of self-boundaries (Chapman et al., 1978; Meehl, 1990). Since an ability
to judge other's emotions was closely linked to subject's own emotional
feeling elicited by other's facial expression (Buchanan et al., 2010),
individuals who have aberrant perceptual experience and selfboundary problems may have more difculty in recognizing and attributing one's emotions to other. Social anhedonia, characterized by lack
of social pleasure and reduced desire to engage in social interaction
(Chapman et al., 1994; Kwapil, 1998), has been suggested to be associated with neural mechanisms responsible for face emotion processing
(Germine et al., 2011). Reduced capacity for hedonic experience in social
situations may affect one's own emotional experience on facial expression of other, so it may be hard to exactly recognize other's emotion.
Furthermore, perceptual aberration and social anhedonia have been
considered as important indicators reecting core features of schizotypy
(Lenzenweger, 1994, 2006) and predicting increased risk for the development of psychosis (Chapman et al., 1994; Kwapil, 1998; Gooding
et al., 2005). Thus, taken together, schizotypy including aberration of
self-other discrimination and reduced hedonic capacity may play an
important role in underlying mechanism of facial emotion recognition
decits in schizophrenia.
To date, the relationship between emotion recognition decit and
schizotypy along with comprehensive neurocognitive impairment has
rarely been investigated in UHR individuals and rst-episode schizophrenia (FES) patients. We hypothesized that there would be a facial
emotion recognition decit in both clinical groups, and then explored
whether facial emotion recognition decit was related to the broad
battery of individual neurocognitive impairments. If this decit is
largely independent of neurocognitive impairment, it should be present
beyond intellectual dysfunction and grossly uncorrelated with the
broad battery of individual neurocognitive impairments in each clinical
group. Finally, we also hypothesized that if facial emotion recognition
decit may be linked to inability to discriminate the self and other
and/or reduced capacity to experience pleasure, this decit should be
associated to schizotypy scales of perceptual aberration and social
anhedonia in each clinical group.
2. Methods
2.1. Participants
The present study was conducted as part of the Green Program for
Recognition and Prevention of Early Psychosis (GRAPE) project in
Seoul and details of inclusion and exclusion criteria are described
elsewhere (An et al., 2010; Kang et al., 2014). Forty UHR individuals,

61

24 FES patients and 46 normal controls (NC) were invited to participate


in this study between April 2008 and December 2011. All participants
were evaluated and diagnosed using the Structured Clinical Interview
for DSM-IV (SCID-IV; First et al., 1996a, 1996b). UHR individuals were
diagnosed according to the Criteria of the Prodromal Syndromes from
the Structured Interview for Prodromal Syndromes (SIPS; McGlashan
et al., 2003) and met at least one of the three criteria of prodromal syndrome: (1) attenuated positive prodromal syndrome (APPS); (2) brief
intermittent psychotic syndrome (BIPS); or (3) genetic risk and deterioration syndrome (GRDS). In FES patients, the mean duration of illness
after developing frank psychotic symptoms was 9.5 (SD = 10.8)
months. The recruitment of schizophrenia patients typically occurred about 1.5 months after hospitalization, as soon as outpatient
maintenance medication levels had been stabilized. The majority
(21/24) of FES patients were in a nearly-remitted state and their positive symptoms, assessed by the Scale for Assessment of Positive
Symptoms (SAPS; Andreasen, 1984), were equivocal or at a mild
level. The positive symptoms of the remaining (3/24) patients were
moderate.
Written informed consent was obtained from all participants after
the procedure had been fully explained and the study was reviewed
and approved by the Institutional Review Board of Severance Hospital
and Severance Mental Health Hospital. For participants under the age
of 18 years, we also obtained the informed consent of their parents.
Table 1 shows demographic and clinical proles of the participants.
2.2. Procedures
The facial emotion recognition task consisted of 53 colored facial
photographs. The facial stimuli were selected from standardized photographs of Japanese and Caucasian Facial Expressions of Emotion and
Neutral Faces (Matsumoto and Ekman, 1988). This selection was
based on the results of our previous standardization study (Ha et al.,
2011) in a Korean cohort (n = 143) with a criterion of consensus
from more than 70% of observers, which yielded eight happiness,
eight surprise, seven sadness, six disgust, four anger, four fear, eight
contempt and eight neutral facial photographs. This emotion task
presented the stimuli in pseudorandom order to participants and
asked them to choose an emotional category that best describes the
emotional state of the person in the photograph shown. A forcedchoice format was used and the participant had to choose from the
categories of happiness, surprise, sadness, disgust, anger, fear and
contempt which were shown below the facial photograph. While
eight neutral faces were also included, there was no choice for neutral
among the responses. The stimulus presentation time was 7 s and
another 7 s was allowed for choice of an emotional category.
Neurocognitive function was assessed using a broad battery of
individual neurocognitive tests, as described in our previous study
(Bang et al., in press). The battery consisted of the California Verbal
Learning Test (learning 15 trials, short delay free recall, long delay
free recall), Rey-Osterrieth Complex Figure Test (immediate recall and
delayed recall), 37 Continuous Performance Test (sensitivity, d),
Verbal and Spatial 2-back Test, Trail-Making Test-Part B, Controlled
Oral Words Association Test, Design Fluency Test, Stroop Test and
Wisconsin Card Sorting Test. The score from each assessment was converted to a z-score based on the performance of NC subjects. Intellectual
functioning (IQ) was also assessed using the K-WAIS (Korean-Wechsler
Adult Intelligence Scale; Wechsler, 1981; Kim and Lee, 1995).
Chapman's self-reports of perceptual aberration scale (Chapman
et al., 1978) and revised social anhedonia scale (Chapman et al., 1976)
were used to assess experiential features of schizotypy (Chapman
et al., 1994). The perceptual aberration scale contains 35 truefalse
items that assess body-image aberration, including unclear boundaries
of the body, feeling of unreality of parts of one's body, and perceptions
of the change in spatial relationship of one's body parts (Chapman
et al., 1978). The revised social anhedonia scale consists of 40 true-

62

S.Y. Lee et al. / Schizophrenia Research 165 (2015) 6065

Table 1
Demographic and clinical proles of normal controls, individuals at ultra-high-risk (UHR) for psychosis, and rst-episode schizophrenia (FES) patients.

Age (years)
Education (years)
Gender (M/F)
SIPS-dened prodromal status (BIPS/APS/GRDS)
DSM-IV subtype
(paranoid/undifferentiated/residual)
Perceptual aberration1,2
Social anhedonia1,2,3
IQ2
Positive symptoms (SAPS, summary score)
Negative symptoms (SANS, summary score)
Antipsychotic medications
Naive/medicated3
Chlorpromazine equivalent dose (mg/day)a

Normal
controls
(n = 46)

Individuals at UHR for


psychosis
(n = 40)

First-episode schizophrenia
patients
(n = 24)

Statistical
analysis

p-Value

20.8 (3.5)
13.2 (1.9)
25/21

19.9 (3.6)
12.8 (2.0)
25/15
10/37/5

20.5 (3.3)
13.3 (2.3)
8/16

F(2, 109) = 0.86


F(2, 109) = 0.54
2 = 5.20

p = 0.427
p = 0.583
p = 0.074

29/2/2
3.9 (4.0)
10.1 (5.5)

9.0 (6.5)
23.3 (7.9)

7.7 (7.2)
16.7 (7.7)

F(2, 107) = 8.68


F(2, 107) =

p b 0.001
p b 0.001

105.8 (12.5)

104.1 (11.8)
3.5 (2.4)
7.0 (4.1)

96.0 (15.7)
6.0 (2.7)
9.4 (5.5)

37.55
F(2, 109) = 4.71
t = 3.88
t = 1.95

p = 0.011
p b 0.001
p = 0.056

24/16
138.2 (84.4)

1/23
454.7 (307.6)

2 = 19.64
t = 4.60

p b 0.001
p b 0.001

SIPS: Structured Interview for Prodromal Syndromes (McGlashan et al., 2003); BIPS: Brief Intermittent Psychotic Symptom Prodromal Syndrome; APS: Attenuated Positive Symptom
Prodromal Syndrome; GRDS: Genetic Risk and Deterioration Prodromal Syndrome; SAPS: Scale for Assessment of Positive Symptoms (Andreasen, 1984); SANS: Scale for Assessment
of Negative Symptoms (Andreasen, 1983); Perceptual aberration scale (Chapman et al., 1978) and Revised social anhedonia scale (Chapman et al., 1976) (2 UHR data were missing).
1
A signicant difference between normal controls and UHR individuals for psychosis (Bonferroni corrected p b 0.05).
2
A signicant difference between normal controls and FES patients (Bonferroni corrected p b 0.05).
3
A signicant difference between UHR individuals and FES patients (Bonferroni corrected p b 0.05).
a
Kroken et al. (2009).

false items that assess traits of subjective anhedonic experience to nonphysical situations including talking and exchanging expressions of
feelings (Chapman et al., 1976). The internal consistencies of both
schizotypy scales were 0.90 and 0.92 respectively.
Clinical interviews and psychopathology assessments were conducted using the SAPS (Andreasen, 1984; 020; total of four global subscale
scores), the Scale for Assessment of Negative Symptoms (SANS;
Andreasen, 1983; 025; total of ve global subscale scores). They
were administered by a psychiatrist (KKR) on the day of recruitment.
Each participant then received a packet of questionnaires including
the perceptual aberration scale (Chapman et al., 1978) and revised
social anhedonia scale (Chapman et al., 1976). The facial emotion
recognition task and the neurocognitive tests were conducted by a
masters-level psychologist (LMK) within a week of recruitment.

3. Results
3.1. Facial emotion recognition task performances
There was a signicant difference in accuracy rate in the facial
emotion recognition task between the three groups after adjusting for
IQ and gender [F(2, 105) = 10.3, p b 0.001; Table 2]. Post-hoc analyses
with Bonferroni correction revealed that the FES group (corrected
p b 0.001; Cohen's d = 1.23) and UHR group (corrected p = 0.023,
Cohen's d = 0.67) were worse than controls. There was no signicant
difference in facial emotion recognition performance between the two
clinical groups after adjusting for IQ and gender (corrected p = 0.132;
Cohen's d = 0.58).

3.2. Relation to neurocognitive function test and schizotypy scales


2.3. Data analysis
Facial emotion recognition task performance was quantied using
accuracy rate (%) for emotion recognition. To examine primary group
differences, multivariate analysis of variance was performed with the
group as a between-subject factor, accuracy rate for emotion recognition as a within-subject factor, and IQ and gender as covariates. Posthoc analysis with Bonferroni adjustment was conducted. Effect size
was calculated as Cohen's d (Cohen, 1988).
The relationship of the accuracy rate (%) of facial emotion recognition task with scores of schizotypy scales and the broad range of individual neurocognitive tests were explored using partial correlation analysis
with IQ and gender as covariates. A signicance level of 0.05 was used
for all statistical tests.

Regarding neurocognitive function, the exploratory correlation


analysis between facial emotion recognition task and neurocognitive
performance covarying with IQ and gender indicated no signicant
relationships in UHR group, while there were signicant relationships
between Rey complex gure test results for immediate recall (r =
0.44, uncorrected p = 0.043) and design uency (r = 0.47, uncorrected
p = 0.029), and facial emotion recognition accuracy rate in the FES
group (Supplementary Table 1).
In regard of schizotypy scales, there were signicant relations of
accuracy rate in the facial emotion recognition with perceptual aberration in both the UHR (r = 0.59, n = 34, corrected p b 0.001) and
FES groups (r = 0.55, n = 20, corrected p = 0.017), after adjusting
for IQ and gender. For social anhedonia, it was found to be related at a

Table 2
Accuracy rate (%) of emotions in normal controls, individuals at ultra-high-risk (UHR) for psychosis, and rst-episode schizophrenia (FES) patients.

Accuracy rate

Normal controls
(n = 46)

Individuals at UHR for psychosis


(n = 40)

First-episode schizophrenia patients


(n = 24)

ANCOVA with IQ and gender as covariates


Statistical
analysis

Post-hoc

Corrected
p-valuea

88.0 (9.4)

80.7 (12.4)

72.6 (15.5)

F(2, 105) = 10.0


p b 0.001

N vs. U
N vs. S
U vs. S

0.023
b0.001
0.132

Bonferroni-corrected p-value.

S.Y. Lee et al. / Schizophrenia Research 165 (2015) 6065

trend level with facial emotion recognition in schizophrenia


(r = 0.45, n = 20, corrected p = 0.070), and not in the UHR group
(r = 0.09, n = 34, corrected p N 0.999; Fig. 1) after adjusting for IQ
and gender.
4. Discussion
This study investigated whether facial emotion recognition decit is
present and, more importantly, examined the relationship between
facial emotion recognition performance and schizotypy as well as a
broad battery of neurocognitive tests in UHR individuals and rstepisode schizophrenia patients. The main ndings were that a recognition decit of facial emotions was present in both clinical groups, even
after adjusting for IQ and gender as covariates. While facial emotion
recognition decit showed few signicant relationships with some
visuo-spatial neurocognitive measures only in the FES group, this decit
was signicantly associated with schizotypy, especially Chapman's
perceptual aberration scale in each clinical group.
The facial emotion recognition decit was present in not only the
rst-episode schizophrenia, but also the UHR group, even after adjusting
for the confounding effect of IQ and gender. This nding is essentially
consistent with the recent ndings that individuals at UHR and rstepisode patients showed facial emotion recognition decits, even after
adjusting for intellectual function (IQ) and/or psychopathology (van
Rijn et al., 2011; Amminger et al., 2012a, 2012b; Comparelli et al.,
2013; Bliksted et al., 2014). In addition, this emotion recognition

63

impairment exhibited only few signicant correlations with individual


neurocognitive measures in the FES group and no signicant correlation
was shown in the UHR group after adjusting the IQ and gender effects.
Although some previous studies reported associations between social
cognition and neurocognition in individuals at clinical high risk for
psychosis (Yong et al., 2014) and schizophrenia patients (Kohler et al.,
2010; Ventura et al., 2013), there is growing evidence that signicant
social cognitive decits remained independent of neurocognitive decits
in both genetic (Eack et al., 2010) and clinical high risk individuals
(Amminger et al., 2012b; Comparelli et al., 2013; Bliksted et al., 2014).
The inconsistency in recent ndings may be partly due to differences in
clinical status of participants and task designs (types of stimuli, presentation methods of stimuli and response sheets, levels of difculty, etc.). To
integrate the present ndings in UHR and rst-episode patients with the
previous researches mentioned above, facial emotion recognition
impairment is suggested to be largely independent from neurocognitive
dysfunction in at least at-risk and rst-episode phases of schizophrenia.
Regarding schizotypy, perceptual aberration was found to be related
to facial emotion recognition decit in both clinical groups, even after
adjusting for IQ and gender. Since abilities to experience emotions
based on one's own somatic state and discriminate self from others
are essential for facial emotion recognition (Adolphs, 2002; Goldman
and Sripada, 2005; Shanton and Goldman, 2010), aberrant bodily
experience and blurring of self-boundaries could be barrier for accurate
source attribution of emotional feeling to other's facial expression.
Therefore, this nding suggests that perceptual aberration may share

Fig. 1. Relationship between accuracy rate (%) of the facial emotion recognition and Chapman's schizotypy scales in (A) individuals at ultra-high risk (UHR) for psychosis and (B) rstepisode schizophrenia (FES) patients.

64

S.Y. Lee et al. / Schizophrenia Research 165 (2015) 6065

common pathogenetic mechanisms with facial emotion recognition


decit in the UHR and FES groups. Meanwhile social anhedonia was
related at a trend level to emotion recognition decit in the FES group,
after adjusting for IQ and gender. Recently, it was proposed that selfreported anhedonia may not reect the reduced capacity to experience
pleasure rather may be associated with episodic memory, identityrelated beliefs (Strauss and Gold, 2012). Thus, the relations of facial
emotion recognition ability with reported social anhedonia could be
confounded by other factors. Further study is needed to explore the
relations using by the variable forms of the anhedonia assessments.
The study had several limitations. First, some of the UHR participants
were medicated. However, their antipsychotic medications were smalldose atypical drugs that had been taken for less than 1 month. A recent
review (Hempel et al., 2010) found no substantial improvement in facial
emotion recognition decit after treatment by typical or atypical antipsychotic drugs. Furthermore, there was no difference in accuracy rate
between the medicated (n = 16) and unmedicated UHR groups (n =
24; p = 0.989) in the present study. Thus, although we cannot
completely rule out their existence, the effects of medication on emotional tasks appear to be too small to change our main ndings. Next,
due to small sample size and different proportion of stimuli of specic
emotional categories, we cannot conduct separate analyses of accuracy
rate of each specic emotion.
In conclusion, the facial emotion recognition decit, which may not
only be present in rst-episode psychotic patients, but may also emerge
prior to the onset of overt psychotic symptoms, appears to be largely
independent of broad domains of neurocognitive dysfunction. Schizotypy
of perceptual aberration may share common pathogenetic mechanisms,
including self-boundary problems, with facial emotion recognition decit.
Therefore, further research should focus on the possible role of
sociocognitive factors such as theory of mind and self-experience disturbance, schizotypy in facial emotion recognition decits, which provide
critical clues regarding abnormal emotional processing in schizophrenia.
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.schres.2015.03.026.
Role of funding source
This work was supported by a National Research Foundation of Korea (NRF) grant
funded by the Korean government (MSIP) (No. 2010-0024264 and No. 2010-0026833).
The funding source had no further role in study design, in the collection, analysis and
interpretation of data, in the writing of the report, and in the decision to submit the
paper for publication.
Contributors
ASK, LE, and KJI conceived the idea and designed the study. KKR, PJY, SYY, and LMK
were involved in subject recruitment, data acquisition, and the literature searches. ASK
conducted the analyses and interpretation of data. LSY and BMJ managed the literature reviews and wrote the rst draft of the manuscript. BMJ revised the analyses and provided
the critical revision of the manuscript. All authors contributed to and have approved the
nal manuscript.
Conict of interest
The authors do not have any conict of interest to disclose.
Acknowledgments
Funding for this study was provided by a National Research Foundation of Korea
(NRF) grant funded by the Korean government (MSIP) (No. 2010-0024264 and No.
2010-0026833).

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