Original Paper
Received: July 31, 2007
Accepted after revision: April 22, 2008
Published online: $ $ $
Psychopathology 739
DOI: 10.1159/000XXXXXX
Attribution Biases in Schizophrenia:
Relationship to Clinical and Functional
Impairments
Alex S. Cohen a Tasha M. Nienow b Thomas J. Dinzeo c Nancy M. Docherty d
a
Department of Psychology, Louisiana State University, Baton Rouge, La., b Department of Psychiatry and
Biobehavioral Sciences, University of California, Los Angeles, Calif., c Department of Psychiatry, Yale University,
New Haven, Conn., and d Department of Psychology, Kent State University, Kent, Ohio, USA
Key Words
Schizophrenia ⴢ Facial emotions ⴢ Social and occupational
functioning ⴢ Attribution bias scores ⴢ Decoding ability
Abstract
Background: Patients with schizophrenia exhibit impairment in their ability to accurately recognize facial emotions
in others, and the severity of this emotion perception deficit
has been associated with poorer functioning. However, the
mechanisms underlying facial emotion perception deficits
are poorly understood. There is evidence to suggest that patients, particularly those with certain positive symptoms,
may misinterpret other people’s facial expressions as having
an overly negative valence. The present study examined the
degree to which attribution biases in facial emotion perception are associated with psychiatric symptomatology and
social and occupational impairments. Sampling and Methods: The error profiles from a facial emotion perception test
were analyzed and compared for 67 schizophrenic state hospital inpatients and 21 nonpsychiatric controls. Attribution
bias scores were separately computed for each of six types
of emotion. Results: The error profiles were remarkably similar for patients as a group and controls. Within the patient
group, severity of positive symptoms was associated with
more ‘fear’ misperceptions. Patients with relatively high lev-
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els of ‘anger’ misperceptions tended to have more severe
disorganization and negative symptoms and more pronounced functional impairments. Interestingly, patients
who erroneously reported seeing relatively high levels of
‘shame’ and ‘happiness’ showed better functioning and less
severe symptoms. Conclusions: Attribution biases appear to
play a role in contributing to functional impairments in patients with schizophrenia. The lack of an isomorphic attribution bias across patients highlights the importance of considering schizophrenia heterogeneity when attempting to
understand and treat social cognitive deficits.
Copyright © 2008 S. Karger AG, Basel
Introduction
Patients with schizophrenia have shown marked social cognitive deficits, particularly in their ability to accurately recognize facial emotions [1]. Moreover, the severity of these deficits has been associated with poorer
functioning across a number of social and occupational
domains [2, 3]. However, the underlying mechanism by
which emotion perception deficits occur is largely unclear. Based mostly on evidence that emotion perception
deficits are modestly correlated with impaired neuropsychological performance [4, 5], some researchers have proAlex Cohen, PhD
Department of Psychology, Louisiana State University
206 Audubon Hall
Baton Rouge, LA 708080 (USA)
Tel. +1 225 578 7017, Fax +1 225 578 4125, E-Mail [email protected]
10.06.2008 10:30:47
posed that emotion perception deficits reflect impairment in basic neurocognitive processes [5, 6]. There is
reason to suspect that, at least for some patients, emotion
perception deficits are also driven by higher-order cognitive disruptions, notably attribution biases. Attribution
biases are motivational and cognitive perceptual biases
that color an individual’s perception of their environment [7]. With regard to schizophrenia, it may be the case
that patients erroneously interpret others as having an
overly negative emotional valence and this attribution
bias interferes with their ability to effectively function in
social and occupational settings. The present study examined the degree to which attribution biases in facial
emotion perception are related to severity of schizophrenia symptoms and functional impairments. Understanding the underpinnings of emotion perception deficits in
this manner is particularly timely given current efforts to
develop social cognition rehabilitation programs for use
with schizophrenia patients [8].
There is good reason to think that attribution biases
are important for understanding emotion perception
deficits in schizophrenia. First, an attribution bias towards seeing facial emotions as overly negative in valence
has been observed in other psychiatric disorders, including depression [9], body dysmorphic disorder [10], conduct disorder [11] and bipolar disorder [12]. Second, the
application of attribution theory to schizophrenia research has been helpful for understanding certain schizophrenic processes, notably paranoia and delusions of persecution [13, 14], hallucinations [15, 16] and depression
[17]. Finally, support for an attribution bias in facial emotion perception in patients with schizophrenia has been
found. Kohler et al. [18] reported that patients, compared
to nonpsychiatric controls, incorrectly endorsed seeing
significantly more negative emotions (‘disgust’, and to a
lesser extent ‘fear’) in neutral-valenced facial expressions.
However, patients and controls did not differ in the error
profiles of nonneutral faces, suggesting that this attribution bias may be limited to neutral stimuli, at least for
patients as a group. In the present study, we compared the
error profiles from a facial emotion perception test between patients and healthy controls with the expectation
that patients would erroneously report seeing negatively
valenced emotions, particularly anger and fear, more so
than controls. A related goal of this study involved determining the extent to which these attribution biases were
associated with ‘real world’ social and occupational dysfunctions.
When discussing schizophrenia, it is important to acknowledge the considerable heterogeneity across patients
2
PSP739.indd 2
Psychopathology 739
in most aspects of the disorder. Given the improbability
that an isomorphic attribution bias is present in all or
even most patients, it seems more plausible that attribution biases for different ‘types’ of emotions would manifest in patients with different types of symptom presentations. Based on evidence that patients with paranoid psychotic processes have relatively global attribution biases
compared to nonparanoid patients [13], a reasonable supposition would be that attribution biases for negative
emotions might be more pronounced in patients with
prominent positive symptoms. In an examination of this
issue, Peer et al. [19] found that ‘disgust’ misperceptions
from a facial emotion perception test were associated
with more severe paranoid symptoms. A secondary aim
of the present project was to examine the relationship between symptoms and attribution biases for five common
emotion types. In particular, we were interested in determining whether patients with positive symptoms would
evidence attribution biases for ‘anger’- and ‘fear’-based
emotions.
Methods
This study was part of a larger investigation into the emotional, physiological, and neuropsychological correlates of social
functioning. Approval from all relevant human subjects review
boards was obtained, and all subjects gave written voluntary informed consent prior to participating in the study. A fuller description of the methodology is provided elsewhere [20, 21]. The
descriptive and clinical data for the patient group are presented
in table 1.
Participants
The patient group consisted of 67 individuals who met the
DSM-IV [22] criteria for schizophrenia or schizoaffective disorder based on information obtained from the Schedule for Affective Disorders and Schizophrenia (SADS) [23]. These patients
were recruited from an inpatient psychiatric state hospital, and
the majority of the patients were hospitalized under a forensic
status (i.e., forensic evaluation, restoration of competency to stand
trial, or being found not guilty by reason of insanity by a court of
law). Patients were excluded if they had a Global Assessment of
Functioning (GAF) score [22] below 30, evidence of mental retardation, history of organic disorder or significant head trauma (requiring overnight hospitalization), DSM-IV current alcohol or
drug abuse, or a significant history of alcohol or drug abuse or
dependence suggestive of substance-related organic damage.
The control group consisted of 21 university support staff and
community volunteers. The control group was matched to the
patient group in age, gender, and parental Socioeconomic Index
[24]. Exclusion criteria included meeting DSM-IV criteria for any
current psychotic or substance use disorder, or having a history
suggestive of the possibility of organic damage, as above.
Cohen /Nienow /Dinzeo /Docherty
10.06.2008 10:31:02
Table 1. Spearman’s correlations between the attribution bias scores and the functioning and symptom sever-
ity scores for patients (n = 67)
Functioning measures
Attribution bias categories3
happiness
Functioning1
Social functioning
Global functioning
Symptom measures2
Core positive symptoms
Disorganization symptoms
Negative symptoms
Anxiety-depression symptoms
0.31*
0.18
0.12
0.03
–0.11
–0.03
anger
fear
sadness
shame
–0.30*
–0.42**
–0.16
–0.07
0.05
–0.01
0.00
0.31*
0.11
0.28*
0.30*
0.07
0.31*
–0.03
0.16
0.25*
–0.10
0.01
0.00
0.03
–0.29*
–0.37*
–0.15
–0.01
Significant r values are in italics. * p < 0.05, ** p < 0.01.
1
Higher scores reflect better functioning.
2 Higher scores reflect more severe symptomatology.
3 Higher scores reflect a more severe attribution bias.
Procedures
Attribution biases were measured using the Facial Emotion
Identification Test (FEIT) [25]. Patients were presented with 19
black-and-white still photographs of individuals’ faces and then
asked to identify the primary emotion from six different emotions. These emotions included: happiness, anger, fear, sadness,
surprise and shame [26]. Using the procedures outlined in Peer et
al. [19], attribution bias scores were computed for each of the emotion categories as a proportion between the number of times that
specific category was erroneously selected and the total number
of errors. For example, the ‘fear’ bias score was computed by dividing the number of incorrect ‘fear’ responses by the total number of errors. As noted by Hogg and Craig [27], proportion scores
violate the homogeneity of variance assumption for parametric
statistical analysis. To compensate for this, we employed the following arcsine transformation suggested in Hogg and Craig [27]:
arcsin(SQRT[(y + 3/8)/(n + 3/4)]), where y = the number of errors
of interest reported for each subject and n = the total number of
errors. Furthermore, for reasons explicated below, we used nonparametric statistics for all analyses examining attribution bias
scores.
Functioning
Social and occupational functioning was measured using the
Social Functioning Scale (SFS) [28]. The SFS is a 79-item questionnaire that assesses seven distinct yet highly correlated domains of
social behavior including: social engagement, interpersonal behavior, independence-performance, recreational activities, prosocial behavior, independence-competence, and employment/occupation. A global social functioning score was computed by
summing the seven individual t-score-transformed subscale
scores (norms in Birchwood [28]). The SFS has been shown to
have acceptable alpha coefficients (0.80), sensitivity and construct
validity in patients with schizophrenia and nonpsychiatric controls [28]. Higher SFS scores reflect better social functioning.
Attribution Biases in Schizophrenia
PSP739.indd 3
General functioning was measured using the GAF [22]. Ratings were made by one of three graduate-level researchers who
demonstrated adequate reliability based on independent reviews
of 10 videotaped SADS interviews (intraclass correlation coefficient values = 0.83). The GAF was not administered to controls in
the present study. Higher GAF scores reflect better overall functioning.
Global intellectual functioning (IQ) was estimated using the
Shipley Institute of Living Scale [29]. This scale has been found to
be highly correlated with full-scale WAIS-R IQ scores [28].
Symptom Severity
The Scale for the Assessment of Positive Symptoms (SAPS)
[30] and the Scale for the Assessment of Negative Symptoms
(SANS) [31] were used to measure patients’ symptom severity.
Three symptom domain scores were computed for the present
study, which included a core positive (i.e., SAPS global hallucination and delusion items), core disorganization (i.e., SAPS global
bizarre behavior and formal thought disorder items), and negative (i.e., SANS global items, except the inattention score) factors.
We also computed a ‘depression-anxiety’ factor (i.e., anxiety,
guilt, suicidality and depression items), identified in a recent factor analytic study [32] of the expanded 24-item Brief Psychiatric
Rating Scale [33]. Ratings were made by one of three graduatelevel researchers who demonstrated adequate reliability based on
independent reviews of 10 videotaped SADS interviews (intraclass correlation coefficient values for each of the individual factor scores were 1 0.70). Higher scores reflect more severe symptoms.
Analyses
The analyses were conducted in three steps. First, we compared the patients and controls on demographic variables. Second, we compared patients and controls in accuracy on the emotion perception test with the expectation that patients would perform worse. As part of these analyses, we computed and compared
Psychopathology 739
3
10.06.2008 10:31:03
attribution bias scores for patients and controls with the expectation that patients would more frequently misinterpret faces as
having an overly angry and fearful valence. Finally, we computed
correlations to determine the relationship between the attribution bias scores, symptom ratings and functioning scores. Unless
otherwise noted, all of the distributions for the variables were
normally distributed (skew values less than 1.5). For all analyses
examining the attribution bias scores or symptom ratings, we employed nonparametric statistics because the data were not normally distributed. All analyses were two-tailed.
Results
Patients versus Controls: Descriptive and
Demographic Variables
Means and standard deviations were separately computed and compared between patients and nonpatient
controls for age (41.29 8 8.55 and 39.38 8 10.97 years,
respectively), education (11.94 8 1.96 and 14.24 8 1.45
years, respectively), IQ (80.61 8 10.63 and 101.38 8
11.47, respectively), gender composition (27 and 33%
male, respectively), ethnic composition (33 and 57% Caucasian, respectively) and social functioning (106.96 8
7.65 and 122.83 8 3.85, respectively) variables. Controls
had significantly higher levels of education and better intellectual, social and general functioning than patients,
but the two groups did not differ in any other respect.
Regarding patient clinical characteristics, patients were
relatively stable (core positive syndrome = 3.49 8 2.66,
disorganization syndrome = 2.77 8 2.29, negative syndrome = 4.58 8 3.54 and anxiety factor = 8.35 8 2.12)
and were functionally impaired (GAF score = 41.29 8
8.25). Eighty-eight percent of the patients were being prescribed atypical antipsychotic medications, 42% mood
stabilizers and 9% antidepressant medications.
Patients versus Controls: Emotion Perception
Accuracy and Attribution Bias Scores
A t test comparing patients and controls in FEIT accuracy suggested that patients produced significantly
more errors (mean = 8.84, SD = 3.23) than controls
(mean = 5.71, SD = 2.26) [t(86) = 4.12, p ! 0.001]. Thus,
consistent with prior research [1], patients showed a deficit in emotion recognition ability.
Means, standard deviations and ranges for the attribution bias scores were computed. Across both groups,
‘happiness’ misperception scores ranged from 0 to 0.50
(means 8 SD = 0.13 8 0.12 and 0.06 8 0.13 for patients
and controls, respectively), ‘anger’ misperception scores
ranged from 0 to 0.57 (means 8 SD = 0.13 8 0.15 and
4
PSP739.indd 4
Psychopathology 739
0.17 8 0.16 for patients and controls, respectively), ‘fear’
misperception scores ranged from 0 to 0.29 (means 8
SD = 0.08 8 0.08 and 0.11 8 0.10 for patients and controls, respectively), ‘sadness’ misperception scores ranged
from 0 to 0.50 (means 8 SD = 0.17 8 0.13 and 0.17 8
0.16 for patients and controls, respectively), ‘surprise’
misperception scores ranged from 0 to 1.00 (means 8
SD = 0.31 8 0.19 and 0.32 8 0.18 for patients and controls, respectively), and ‘shame’ misperception scores
ranged from 0 to 0.50 (means 8 SD = 0.19 8 0.14 and
0.17 8 0.15 for patients and controls, respectively). We
had concerns about these distributions because there
were a large number of ‘zero’ values for some of the categories (percent of zero scores ranged from 12 to 46%).
Therefore, nonparametric statistics were used for all
analyses examining the attribution bias scores. A MannWhitney U test, computed to compare the two groups on
attribution bias scores, suggested that the groups significantly differed only on the ‘happiness’ (Z = –2.57, p !
0.01) categories (all other p values 10.10). Thus, in contrast to our predictions, patients, as a group, did not demonstrate attribution biases towards negative emotions.
Patient Group Analyses: the Relationship between
Attribution Biases, Symptom Severity and Functional
Impairment
Spearman rank correlations were computed between
the attribution biases, symptom severity and functional
impairment scores (table 1). Given that ‘surprise’ is neither inherently positively nor negatively emotionally valenced, we excluded this variable to reduce the overall
number of analyses. There were three main findings.
First, severity of ‘anger’ misperceptions was significantly
associated with poorer overall social and global functioning. ‘Anger’ misperceptions were not significantly associated with core positive symptoms as expected, but were
significantly associated with more severe disorganization
and negative symptoms. Second, ‘fear’-based misperceptions tended to occur in individuals with pronounced
core positive symptoms and depressive/anxious symptoms but were not significantly associated with functioning. Third, ‘happiness’ and ‘shame’ misperceptions were
significantly associated with better clinical and functional state in some respects. Patients who tended to erroneously report seeing ‘happiness’ tended to have better social functioning and those who erroneously reported seeing ‘shame’ tended to have better overall functioning and
less severe core positive and disorganization symptoms.
Cohen /Nienow /Dinzeo /Docherty
10.06.2008 10:31:03
To our knowledge, this study is one of the first to examine the relationship between functioning ability,
symptom severity and attribution biases in facial emotion perception in patients with schizophrenia. For the
most part, as in Kohler et al. [18], patients as a group did
not differ from controls in these attribution biases (when
evaluating emotionally expressive faces) raising doubts
about whether there is an isomorphic attribution bias
that characterizes schizophrenia patients as a group.
However, within the patient group, attribution biases for
emotion showed important clinical and functional correlates. In general, these findings suggest that certain
types of attribution biases, particularly for anger-, fearand shame-based emotions, are important for understanding schizophrenia pathology across the heterogeneous manifestations of the disorder. Several findings
from this study bear further discussion.
Evidence from this study suggests that patients who
misinterpret others’ faces as having an angry emotional
valence tend to have poorer functioning than other patients. ‘Anger’ misperceptions were not associated significantly with core positive symptoms as hypothesized but
were associated with more severe disorganization and
negative symptoms. When attempting to explain this, it
is important to note that patients with disorganization
symptoms have shown lower levels of hemispheric specialization than other patients [34], and there is growing
evidence for a right hemispheric dominance for emotion
processing, particularly for ‘anger’-based emotions [35].
Thus, disorganization symptoms and ‘anger’-based attribution biases may reflect abnormal right hemispheric
functioning. An alternate explanation concerns the fact
that a majority of patients in this sample were hospitalized for forensic reasons, and some of the patients probably had maladaptive personality traits (e.g. antisocial
traits) that may have interfered with functioning. Thus,
it could be the case that, as has been noted in adolescents
with conduct disorder [11], personality traits contributed
to an ‘angry’ attribution bias. Finally, it is possible that
increased ‘anger’ misperceptions reflected a more global
angry disposition related to a severe illness state. In support of this view, a link between increased self-reported
feelings of anger and increased chronicity of illness has
been reported [36]. While far from conclusive, the idea
that disorganization and negative symptoms may be related to attribution biases and these biases may be associated with functional impairment is relatively novel and
intriguing for the generation of future hypotheses.
Individuals with ‘fear’, ‘anger’ and ‘shame’/’happiness’
misperceptions each showed a relatively distinct pattern
of clinical correlates suggesting that different types of attribution biases are related to different pathological processes. While these results should be interpreted cautiously, it may be the case that certain types of attribution
styles demarcate coherent schizophrenia subtypes, each
with relatively specific symptom and functional correlates. In other words, there may be something fundamentally different about patients who erroneously see ‘anger’
in others’ faces versus patients that erroneously see
‘shame’ or ‘fear’. If true, this finding would be important
in its implications for our understanding of schizophrenia heterogeneity. From a treatment perspective, the present findings are also important for developing cognitivebehavioral interventions aimed at reducing the impact of
maladaptive attribution and cognitive distortions on patients’ functioning. Understanding how patients process
information from their environment may be very informative for designing efficacious, individually tailored
treatments. While clearly in its early stages of validation,
the facial emotion perception test appears to hold promise as a measure of attribution biases in schizophrenia.
It is also important to consider the potential contribution that methodological issues made to the present findings. First, as noted by Kohler et al. [18], there are limitations with using the FEIT, including restricted stimulus
set and limited use of ethnicity and age representation
across the facial stimuli. Moreover, the use of photographic stills has limited ecological validity for understanding ‘real-life’ emotion perception occurring in dyadic interactions across multiple sensory domains. Our
use of FEIT stimuli was also a limitation in that it did not
allow for a more sophisticated examination of whether
attribution biases occurred at the ‘encoding’ versus ‘decoding’ stages of processing [37, 38]. Second, the patient
group was primarily comprised of chronic patients who
may be considered atypical in some respects. In particular, antisocial characteristics, illicit drug abuse and florid
psychosis were probably much more pronounced in this
sample than patients as a whole. As we lacked information on these characteristics, we were unable to determine their effect on the present findings. Third, no attempt to control for type II errors was made due to the
exploratory nature of this study, so it is possible that these
significant findings could be spurious. Fourth, the control sample was relatively small compared to the patient
group and we were unable to examine the relationship
between attribution biases and functional impairments
in nonpatient controls. Given that emotional biases ap-
Attribution Biases in Schizophrenia
Psychopathology 739
Discussion
PSP739.indd 5
5
10.06.2008 10:31:03
pear to have functional consequences for individuals who
are not schizophrenic [9], it may be the case that these
biases reflect a more general marker of pathology rather
than a pathognomonic sign of schizophrenia. Fifth, the
study was ill-equipped to examine the role of basic cognitive processes (e.g. attention, memory) in facial emotion
recognition ability. Finally, this study was cross-sectional
in design and it would be important to examine the covariance between symptoms, functioning and attribution biases over time using a longitudinal design. An important next step in this line of research would be to replicate the present study in a sample of stable outpatients
using a more comprehensive facial emotion perception
test.
The present findings have relevance for efforts to develop remediation interventions that address deficits in
social cognition and emotion perception. Namely, successful remediation strategies may benefit by taking into
account the extent to which attribution biases are related
to patients’ impaired facial emotion perception ability.
Moreover, attribution biases may vary considerably across
patients and may reflect different underlying pathophysiological processes. Further research is needed to clarify
the role that attribution biases play in schizophrenia pathology across the heterogeneous manifestations of the
disorder.
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