Article

Association of Impaired Facial Affect Recognition with Basic Facial and Visual Processing Deficits in Schizophrenia

McLean Hospital, Belmont, Massachusetts, USA.
Biological psychiatry (Impact Factor: 10.26). 04/2009; 65(12):1094-8. DOI: 10.1016/j.biopsych.2009.01.026
Source: PubMed
ABSTRACT
Impaired emotion recognition has been reported in schizophrenia, yet the nature of this impairment is not completely understood. Recognition of facial emotion depends on processing affective and nonaffective facial signals, as well as basic visual attributes. We examined whether and how poor facial emotion recognition in schizophrenia is related to basic visual processing and nonaffective face recognition.
Schizophrenia patients (n = 32) and healthy control subjects (n = 29) performed emotion discrimination, identity discrimination, and visual contrast detection tasks, where the emotionality, distinctiveness of identity, or visual contrast was systematically manipulated. Subjects determined which of two presentations in a trial contained the target: the emotional face for emotion discrimination, a specific individual for identity discrimination, and a sinusoidal grating for contrast detection.
Patients had significantly higher thresholds (worse performance) than control subjects for discriminating both fearful and happy faces. Furthermore, patients' poor performance in fear discrimination was predicted by performance in visual detection and face identity discrimination.
Schizophrenia patients require greater emotional signal strength to discriminate fearful or happy face images from neutral ones. Deficient emotion recognition in schizophrenia does not appear to be determined solely by affective processing but is also linked to the processing of basic visual and facial information.

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Available from: Yue Chen
BRIEF REPORT
Association of Impaired Facial Affect Recognition with
Basic Facial and Visual Processing Deficits in
Schizophrenia
Daniel Norton, Ryan McBain, Daphne J. Holt, Dost Ongur, and Yue Chen
Background: Impaired emotion recognition has been reported in schizophrenia, yet the nature of this impairment is not completely
understood. Recognition of facial emotion depends on processing affective and nonaffective facial signals, as well as basic visual attributes.
We examined whether and how poor facial emotion recognition in schizophrenia is related to basic visual processing and nonaffective face
recognition.
Methods: Schizophrenia patients (n 32) and healthy control subjects (n 29) performed emotion discrimination, identity discrimination,
and visual contrast detection tasks, where the emotionality, distinctiveness of identity, or visual contrast was systematically manipulated.
Subjects determined which of two presentations in a trial contained the target: the emotional face for emotion discrimination, a specific
individual for identity discrimination, and a sinusoidal grating for contrast detection.
Results: Patients had significantly higher thresholds (worse performance) than control subjects for discriminating both fearful and happy
faces. Furthermore, patients’ poor performance in fear discrimination was predicted by performance in visual detection and face identity
discrimination.
Conclusions: Schizophrenia patients require greater emotional signal strength to discriminate fearful or happy face images from neutral
ones. Deficient emotion recognition in schizophrenia does not appear to be determined solely by affective processing but is also linked to
the processing of basic visual and facial information.
Key Words: Cognitive, emotion recognition, face recognition, neu-
roscience, perception, schizophrenic
F
acial affect recognition is impaired in schizophrenia (1,2).
This behavioral impairment has been linked to specific
brain mechanisms responsible for affective processing,
such as those mediated in the amygdala (3–5). It is important,
however, to note that recognition of facial emotion also relies on
perceptual signals and nonaffective face information (6,7). Pa-
tients with schizophrenia are deficient at processing basic visual
information (8,9) and at detecting and recognizing facial images
that are without emotional content (10 –13). It has been sug-
gested that impaired emotion recognition in schizophrenia is
secondary to deficient visual processing (14). Also, some re-
searchers have posited that the deficit in emotion recognition is
secondary to a generalized deficit associated with schizophrenia
(15). Yet, performance in emotion recognition and in basic
perception tasks has not been directly compared in schizophre-
nia patients. This comparison would provide a direct test of the
hypothesis that impaired emotion recognition is associated with
basic perceptual processing in schizophrenia.
In this study, emotion discrimination performance was as-
sessed in schizophrenia patients and then compared with basic
visual processing (contrast detection), as well as nonaffective
identity discrimination, using a psychophysical approach. Face
identity discrimination was used as a nonaffective comparison of
face recognition ability, since it depends on similar information
processes to facial emotion recognition. Contrast detection was
used as a measure of basic visual processing, since contrast
provides basic perceptual inputs for almost all vision-related
tasks. Each of these assessments used psychophysical methods
to index the level of signal strength required to perform the task.
The employment of these three tasks in the same patients
allowed direct comparison of behavioral capacities across visual
and emotional domains and permitted inference regarding the
roles of affective, nonaffective, and basic visual processing in
emotion recognition in schizophrenia. We hypothesized that
performance on face identity discrimination and contrast detec-
tion tasks would account for a sizeable proportion of the
variance in facial emotion discrimination in patients.
Methods and Materials
Subjects
Thirty-two schizophrenia patients and 29 normal control
subjects participated. Inclusion criteria were age 18 to 65 years,
no recent history of drug or alcohol abuse (past 6 months), no
neurological problems, and IQ 70. Patients were diagnosed
with schizophrenia (n 18) or schizoaffective disorder (n 14)
using the Structured Clinical Interview for DSM-IV (SCID-IV).
Demographic and clinical characteristics of the sample are listed
in Table 1. All subjects gave written informed consent, and the
protocol was approved by the Institutional Review Board of
McLean Hospital.
Procedures
Emotion Discrimination. The targets were face images gen-
erated from the NimStim Face Stimulus Set (http://www.
macbrain.org)(16). The images contained happy, fearful, or
neutral expressions. The task was to indicate which of two
sequentially presented face images, one with a specific emo-
tional intensity and the other with a neutral expression, was more
From McLean Hospital (DN, RM, DO, YC), Belmont; Massachusetts General
Hospital (DJH), Charlestown; and Department of Psychiatry (DJH, DO,
YC), Harvard Medical School, Belmont, Massachusetts.
Address reprint requests to Yue Chen, Ph.D., Harvard University Medical
School, Department of Psychiatry, 115 Mill Street, Room G06, Centre
Building, Belmont MA 02478; E-mail: ychen@mclean.harvard.edu.
Received October 8, 2008; revised January 20, 2009; accepted January 21,
2009.
BIOL PSYCHIATRY 2009;xx:xxx0006-3223/09/$36.00
doi:10.1016/j.biopsych.2009.01.026 © 2009 Society of Biological Psychiatry
ARTICLE IN PRESS
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fearful or happier (Figure 1A). Additional details about this and
the other task procedures are provided in Supplement 1.
Identity Discrimination. The targets were face images with
neutral expressions, either the original images of two individuals
or images morphed between them (Figure 1B). The task was to
determine which of two face images was identical to a face image
presented immediately prior.
Contrast Detection. The target was a sinusoidal grating (2
cycles/degree) displayed at varying contrast levels. The task was
to indicate during which interval, the first or second, the target
was present; a blank screen was present during the other
interval.
Analysis. The critical measure for the tasks was the just
noticeable difference (JND) threshold between the target and
comparison, at which subjects performed at a criterion level. The
thresholds were compared using a two-way repeated measures
analysis of variance (ANOVA) (emotion type and diagnosis).
Thresholds for contrast detection and identity discrimination
were compared using Student t tests. To examine how nonaffec-
tive perceptual and clinical variables contribute to emotion
discrimination performance in patients, multiple regression anal-
yses were performed.
Results
Emotion Discrimination
Patients had significantly higher overall thresholds than con-
trol subjects for discriminating between emotional and neutral
Figure 1. (A) Emotion discrimination. Emotional in-
tensity of the face images was manipulated by mor-
phing a neutral face image and an emotional face
image of the same individual. Six levels of emotion
intensity were used: 0, 6, 12, 24, 48, and 100%. The
greater an emotion intensity level, the easier the
emotion discrimination task. Photographs of two in-
dividuals, a male individual and a female individual,
were used. Each face image was presented for 400
msec, with a 500 msec interstimulus interval. (B)
Identity discrimination. Morphed images were cre-
ated by morphing together two separate faces (i.e.,
two different individuals) such that the resultant im-
age contained varying proportions of each of the two
original face images. The difference between the two
comparison face images in the second presentation
could be 5, 12.5, 25, 50, or 100%. A 100% difference
would entail a comparison of the original (nonmor-
phed) face photographs of two separate individuals.
A 5% difference would entail comparison of two mor-
phed images: 47.5% of individual #1 and 52.5% of
individual #2, or 52.5% individual of #1 and 47.5% of
individual #2. Difference levels between two compar-
ison face images varied across trials according to the
method of constant stimuli. Presentation One lasted
for 600 msec, and Presentation Two lasted for 1200
msec. There was a 500-msec interval between the
two presentations.
2 BIOL PSYCHIATRY 2009;xx:xxx D. Norton et al.
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facial expressions (F 10.55, df 1, 59, p .002) (Table 2). For
both groups, thresholds were lower for discriminating happiness
than fear (F 19.8, df 1, 59, p .001) (Figure 2). The
interaction between the type of emotion and group was also
significant (F 7.58, df 1, 59, p .008), indicating that patients
were differentially impaired in their ability to discriminate fear.
Post hoc comparisons between groups were significant for
fear discrimination (t 3.94, df 59, p .001, Bonferroni
corrected) but only approached significance for happiness dis-
crimination (t 2.21, df 59, p .07, Bonferroni corrected).
Consistent with this was a larger effect size (ES) for group in fear
discrimination (ES .99) than happiness discrimination, which
also had a considerable group effect size (ES .55). Summary
and analysis of the performance accuracies, from which the
above perceptual thresholds are derived, are included in Sup-
plement 1.
Identity Discrimination and Visual Detection
Face identity discrimination thresholds were higher for pa-
tients than control subjects, but the group difference was not
significant (t 1.76, df 52, p .09). Contrast detection
thresholds were significantly higher for patients than in control
subjects (t 4.33, df 52, p .001).
Correlations between emotion recognition and perceptual/
clinical variables are included in Figure 3 and Supplement 1.
Multiple Regression Analyses
Multiple linear regression analysis included the five factors
that were significantly correlated with fear discrimination perfor-
mance in patients: identity discrimination thresholds, contrast
detection thresholds, Positive and Negative Syndrome Scale
(PANSS) negative scores, PANSS general scores, and IQ. With all
these variables included, the model accounted for a large portion
of the variance in fear discrimination performance in the patients
(R
2
.60). Among these independent variables, only identity
discrimination (p .02) and contrast detection thresholds (p
.01) significantly predicted fear discrimination performance. Fur-
ther analysis using backward stepwise regression included only
the identity discrimination and contrast detection factors and
accounted for a similar amount of variance (R
2
.54) to the
original regression analysis.
For happiness discrimination, the same analysis showed that
the five variables in consideration predicted a smaller amount of
the performance variance than they did for fear discrimination
(R
2
.38). Only IQ was a significant predictor for happiness
discrimination performance (p .01), accounting for a moderate
amount of performance variance (R
2
.20).
Discussion
This study found that schizophrenia patients had significantly
elevated thresholds for emotion discrimination. Interestingly,
impaired fear discrimination was predicted by basic perceptual
performance, namely, contrast detection and face identity dis-
Table 1. Demographic and Clinical Information of the Sample
Control Subjects
(n 29)
Patients
(n 32)
Age 40.7 (14.6) 41.8 (9.8)
Sex 12 males, 17 females 17 males, 15 females
Education
b
15.6 years (2.2) 13.6 years (2.1)
Parental Education 14.1 years (3.1) 13.5 years (3.3)
Verbal IQ
a
110.4 (9.2) 98.9 (14.0)
BDI
b
2.9 (5.3) 12.1 (9.9)
Illness Duration 18.9 years (10.9)
PANSS Positive 15.5 (6.3)
PANSS Negative 16.8 (7.8)
PANSS General 31.1 (7.52)
Chlorpromazine Equivalent 565.9 mg (349.7)
Numbers in parentheses indicate standard deviation.
BDI, Beck Depression Inventory; PANSS, Positive and Negative Syn-
drome Scale.
a
Groups differ significantly at p .05.
b
Groups differ significantly at p .001.
Table 2. Summary of Results
Group Fear Discrimination Happiness Discrimination Contrast Detection Identity Discrimination
Control Subjects 17.82 (6.33) 15.46 (5.94) 2.66 (.16) 67.11 (8.69)
Patients 32.73 (20.35) 22.69 (17.40) 2.36 (.33) 72.55 (13.67)
Means and standard deviations (in parentheses) of thresholds for each of the four visual tasks. For all tasks, smaller numbers indicate better performance.
For emotion discrimination (happiness and fear), the threshold represents the level of emotional intensity needed for reliable detection. For contrast
detection, it is the level of contrast (in log units) needed for detecting the target. For identity discrimination, it is the proportion of a given individual in the
image that is morphed between two individuals.
Figure 2. (A) Example of performance scores on fear discrimination by a
patient (right panel) and a control subject (left panel). The horizontal lines
denote 80% accuracy level, and the vertical lines mark the stimulus level
needed for each subject to reach 80% accuracy (the threshold). (B) Individ-
ual subjects’ thresholds for fear discrimination and happiness discrimina-
tion. The ordinate, in a log scale, denotes the values of the threshold. The
abscissa denotes the subject groups and type of emotion discrimination
evaluated. The lower the threshold, the better the performance.
D. Norton et al. BIOL PSYCHIATRY 2009;xx:xxx 3
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crimination, whereas impaired happiness discrimination was not
predicted by these two perceptual variables, but rather by IQ.
Most previous studies of facial emotion recognition in schizo-
phrenia have found that patients make poor judgments classify-
ing and labeling different emotional expressions (1,2). Extending
this work, the present study found that patients performed
poorly on a task where only one emotional expression was
presented at a time. This result suggests that patients have
difficulty detecting the presence of a given emotion. Classifica-
tion and detection of facial emotion are two distinct but closely
related processes (17). How the deficits in these two emotion
processes are related in schizophrenia remains to be explored.
The connection between affective processing systems (e.g.,
amygdala) and visual processing systems (e.g., striate and extra-
striate cortex) has been a topic of intense research. Damage to
the amygdala results in lower activity in the visual cortex during
emotion recognition (18). Presumably, changes in activity levels
within early visual areas also influence activity within the amyg-
dala. The current study found that schizophrenia patients’ per-
formance in contrast detection and nonaffective face recognition
predicted their fear discrimination performance, suggesting that
the known deficits in the visual and affective processing domains
are associated in schizophrenia. It is not clear whether deficient
visual processing leads to deficient affective processing in
schizophrenia or vice versa. Examining the effects of modulating
signals in one domain (e.g., physical attributes of the visual
stimulus) on performance in the other (e.g., affect discrimina-
tion) may help clarify this issue. Also, other aspects of social
cognitive dysfunction in schizophrenia, particularly those that
rely on abstract representations of other people, may not be
associated with basic perceptual processing abnormalities. This
possibility should be examined in future studies.
Impaired performance on both fear and happiness discrimi-
nation seems to suggest an emotion recognition problem that is
not confined to specific affect categories. However, further
analysis revealed that the impairment in fear discrimination was
predicted by visual and nonaffective face discrimination but not
other variables such as IQ or PANSS scores. In contrast, the
impairment in happiness discrimination was predicted by IQ but
not other variables, suggesting that dysfunctions of distinct brain
systems are implicated in these two domains of emotion discrim-
ination. The result of differential associations in patients is
consistent with previous findings that happiness discrimination
and fear discrimination rely on different facial features (mouth vs.
eyes) (19) and involve different brain mechanisms (20). The
selective association between performance in fear discrimination
and contrast detection in patients is also consistent with the
known connections between the magnocellular pathway (which
processes contrast information) and the amygdala (which pro-
cesses fear information) (6).
In sum, the results of this study, along with previous studies,
suggest that impairment in emotion recognition in schizophrenia
can no longer be viewed solely as a problem of affective
processing: basic perceptual processing deficits appear to play
an integral role. Therefore, novel therapeutic interventions that
aim to improve social cognition in schizophrenia patients should
account for the role of perceptual factors.
This work was supported in part by grants from the National
Institutes of Health (NIH) and Harvard University.
We thank Dr. Ken Nakayama for help during the initial phase
of the study, Dr. Jejoong Kim for his comments on an earlier
version of the article, and Dr. Caitlin Ravichandran for her help
with statistical analysis.
The authors report no biomedical financial interests or other
conflicts of interest.
Supplementary material cited in this article is available
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  • Source
    • "b where y is the proportion of trials judged correctly, x equals the presentation time of the grating, and a and b are two curve-fitting parameters (Norton et al., 2009). The threshold was defined as the minimum presentation time where the accuracy value of the function reached 80%. "
    [Show abstract] [Hide abstract] ABSTRACT: Individuals with depression show depleted concentrations of the inhibitory neurotransmitter GABA in occipital (visual) cortex, predicting weakened inhibition within their visual systems. Yet, visual inhibition in depression remains largely unexplored. To fill this gap, we examined the inhibitory process of center-surround suppression (CSS) of visual motion in depressed individuals. Perceptual performance in discriminating the direction of motion was measured as a function of stimulus presentation time and contrast in depressed individuals (n=27) and controls (n=22). CSS was operationalized as the accuracy difference between conditions using large (7.5°) and small (1.5°) grating stimuli. Both depressed and control participants displayed the expected advantage in accuracy for small stimuli at high contrast. A significant interaction emerged between subject group, contrast level and presentation time, indicating that alterations of CSS in depression were modulated by stimulus conditions. At high contrast, depressed individuals showed significantly greater CSS than controls at the 66ms presentation time (where the effect peaked in both groups). The results' specificity and dependence on stimulus features such as contrast, size and presentation time suggest that they arise from changes in early visual processing, and are not the results of a generalized deficit or cognitive bias.
    Full-text · Article · Apr 2016
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    • "Our findings therefore suggest that impaired facial emotion perception in schizophrenia is due at least in part to under-recruitment of regions involved in processing perceptual features of faces and the detection of changes in facial expressions, in contrast or in addition to other processes that contribute to facial emotion perception (e.g., dysfunction at the level of associating a perception with emotional knowledge). Our findings are consistent with previous research reporting sensory contributions to facial emotion processing deficits in schizophrenia (e.g., Butler et al., 2009; Norton et al., 2009; Turetsky et al., 2007). Furthermore, the similar findings in core regions involved in face perception in relatives suggest that this under-recruitment is associated with the genetic/familial liability to schizophrenia. "
    [Show abstract] [Hide abstract] ABSTRACT: Deficits in facial emotion perception in schizophrenia may be a marker of disorder liability. Previous functional magnetic resonance imaging (fMRI) studies investigating these deficits have been limited by task demands that may recruit other impaired cognitive processes in schizophrenia. We used a family study design along with a passive viewing task during fMRI to investigate brain activation abnormalities underlying facial emotion perception in schizophrenia and examine whether such abnormalities are associated with the genetic liability to the disorder. Twenty-eight schizophrenia patients, 27 nonpsychotic relatives, and 27 community controls passively viewed images of facial emotions during an fMRI scan. Analyses revealed hypoactivation in face processing areas for both patients and relatives compared to controls, and hyperactivation in relatives compared to both patients and controls for frontal regions implicated in emotion processing. Results suggest that activation abnormalities during facial emotion perception are manifestations of the genetic liability to schizophrenia, and may be accompanied by compensatory mechanisms in relatives. Studying mechanisms in nonpsychotic relatives is a valuable way to examine effects of the unexpressed genetic liability to schizophrenia on the brain and behaviour. Copyright © 2015 Elsevier B.V. All rights reserved.
    Full-text · Article · Jul 2015 · Schizophrenia Research
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    • "Face visual processing impairments in face recognition may also be associated with patients' clinical characteristics such as chronicity of the disease (Kucharska-Pietura et al., 2005) or severity of the symptomatology, in particular negative symptoms (Chen et al., 2012; Chen et al., 2009; Norton et al., 2009; Ventura et al., 2013). Perceptual deficits during face processing seem to be intact at the behavioral level in UHR individuals and early onset schizophrenia patients, corroborating the hypothesis that these deficits might appear as the disease progresses. "
    [Show abstract] [Hide abstract] ABSTRACT: Facial emotion processing has been extensively studied in schizophrenia patients while general face processing has received less attention. The already published reviews do not address the current scientific literature in a complete manner. Therefore, here we tried to answer some questions that remain to be clarified, particularly: are the non-emotional aspects of facial processing in fact impaired in schizophrenia patients? At the behavioral level, our key conclusions are that visual perception deficit in schizophrenia patients: are not specific to faces; are most often present when the cognitive (e.g. attention) and perceptual demands of the tasks are important; and seems to worsen with the illness chronification. Although, currently evidence suggests impaired second order configural processing, more studies are necessary to determine whether or not holistic processing is impaired in schizophrenia patients. Neural and neurophysiological evidence suggests impaired earlier levels of visual processing, which might involve the deficits in interaction of the magnocellular and parvocellular pathways impacting on further processing. These deficits seem to be present even before the disorder out-set. Although evidence suggests that this deficit may be not specific to faces, further evidence on this question is necessary, in particularly more ecological studies including context and body processing. Copyright © 2015. Published by Elsevier Ltd.
    Full-text · Article · Apr 2015 · Neuroscience & Biobehavioral Reviews
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