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Christian G. Kohler, M.D. Objective: The authors used color photo- tensity was better than recognition of mild
graphs of emotional and neutral expres- intensity. However, patients showed less
sions to investigate recognition patterns of benefit from increased intensity for all
Travis H. Turner, B.S.
five universal emotions in schizophrenia. emotions combined, and the difference
Warren B. Bilker, Ph.D. Method: Twenty-eight stable outpatients was most pronounced for fear. Thus, pa-
with schizophrenia (19 men and nine tients were more impaired than healthy
women) and 61 healthy subjects (29 men comparison subjects in identifying high-in-
Colleen M. Brensinger, M.S.
and 32 women) completed an emotion tensity expressions, even though this was
discrimination test that presented mild an easier task than identifying low-inten-
Steven J. Siegel, M.D., Ph.D. and extreme intensities of happy, sad, an- sity expressions. In the comparison of pat-
gry, fearful, disgusted, and neutral faces, terns of errors, patients and healthy sub-
Stephen J. Kanes, M.D., Ph.D. balanced for gender and ethnicity. Analy- jects differed only in misattributions of
ses evaluated accuracy of identifying emo- neutral expressions; patients overattrib-
Raquel E. Gur, M.D., Ph.D. tions as a function of intensity, diagnosis,
uted disgusted expressions and underat-
and gender of poser and rater.
tributed happy expressions.
Ruben C. Gur, Ph.D. Results: Patients performed worse than
comparison subjects on recognition of all Conclusions: Patients with schizophre-
emotions and neutral faces combined, in- nia were impaired in overall emotion rec-
cluding mild and extreme expressions. For ognition, particularly fear and disgust,
specific emotions, patients performed and did not benefit from increased emo-
worse on recognition of fearful, disgusted, tional intensity. Error patterns indicate
and neutral expressions. For all emotions that patients misidentified neutral cues as
except disgust, recognition of extreme in- negatively valenced.
a Top row: neutral and mild-intensity happy, sad, angry, fearful, disgusted expressions. Bottom row: neutral and extreme-intensity happy, sad,
angry, fearful, disgusted expressions.
FIGURE 2. Recognition of Facial Emotions by Patients With Schizophrenia and Healthy Comparison Subjects
100
Comparison
subjects (N=61)
Patients (N=28)
80
Percent Correct
60
40
20
0
Mild Extreme Mild Extreme Mild Extreme Mild Extreme Mild Extreme
Happiness Sadness Anger Fear Disgust Neutral
Emotion
FIGURE 3. Error Profile of Patients With Schizophrenia and cated in fear processing, are affected in schizophrenia. We
Healthy Comparison Subjects for Neutral Expressionsa recently noted a lack of amygdala activation in patients
with schizophrenia during discrimination of positive from
negative emotions (22).
Disgust was not well recognized in either the compari-
son group or the patient group, but it was worse in pa-
tients. In contrast to the other emotions, disgust was bet-
ter recognized in mild-intensity expressions and almost
never identified as neutral. This finding lends support to
the possibility that disgust is not a primary emotion but,
rather, a combination of other emotions.
Comparison Subjects Patients
Impaired recognition of neutral or nonemotional faces
(N=61) (N=28)
in the schizophrenia group may have implications for un-
6.1 (43%) Happy 8.7 (29%) derstanding symptoms. During an acute psychotic epi-
sode, people with schizophrenia frequently misinterpret
4.5 (32%) Sad 8.7 (29%)
as significant neutral occurrences that are personally irrel-
2.3 (16%) Angry 2.9 (10%) evant. Perhaps even stable patients are more likely to
0.6 (4%) Afraid 3.1 (10%) identify neutral facial expressions as emotional, imputing
negative valence to such expressions.
0.7 (5%) Disgusted 6.9 (23%)
The lack of difference between groups for recognition of
14% Percent for neutral 30%
sad expressions accords with our previous finding that sad
recognition is less impaired in schizophrenia (12, 35).
However, the lack of deficit in recognition of anger in
a Figure shows misidentification patterns of neutral faces as happy,
schizophrenia was less expected. On the basis of clinical
sad, angry, fearful, or disgusted faces expressed in average frequen-
cies and percentages of overall error rate. The overall error rate for symptoms, we expected that people who are more prone
identifying neutral expressions is also presented. to paranoid thinking and hostility will also be more likely
to misinterpret anger and show a different error pattern.
were lower for fearful, disgusted, and neutral expressions Perhaps such deficits can be seen in study groups contain-
but not for happy, sad, and angry expressions. ing more paranoid patients.
Patients with schizophrenia differed not only in emo- Limitations of our study include the demographic dif-
tion recognition rates but also in the pattern of error rates, ferences between patients and the comparison group, the
specifically for neutral faces. Neutral expressions were relatively small number of subjects in the patient group,
more commonly mistaken as sad or happy followed by and the focus on stable patients. The patient group was
disgusted in the schizophrenia group, and as happy fol- more likely to be male, non-Caucasian, and older than
lowed by sad in the comparison group. Patients misidenti- comparison subjects, although the difference was signifi-
fied neutral cues as emotional, showing a negative bias. cant only for age. Because patients were clinically stable,
Previously we reported a positive error bias in schizophre- most had undergone long-term treatment at our center
nia (10, 35), but this was in the context of discriminating and were older than the comparison group. However,
sad from happy emotions. Walker et al. (36) described a there is no evidence that emotion recognition abilities
trend toward greater deficit in recognition of negative change with age, and our statistical analyses indicated
emotions in schizophrenia on a battery of eight different that neither age nor gender and race of rater accounted for
emotions, including five that are considered universally the findings. The schizophrenia group was small because
recognized. Error patterns of neutral faces were not exam- of the selection criteria for stability, which included partial
ined separately in these studies. or complete remission of positive symptoms and no hos-
As in previous studies, happy expressions were the best pitalization within the past 6 months. Comparisons re-
recognized of all emotions across groups. Happy expres- garding possible effects of typical or atypical antipsychotic
sions represent the only universally recognized positive medication on emotion recognition were not possible be-
emotion, in contrast to multiple negative emotions. We cause only four patients were receiving typical antipsy-
have observed little overlap in action units of facial expres- chotic medication only.
sions (37) for happy compared with sad, angry, and fearful Another limitation of the study is that subjects were
expressions (31). The unique facial configuration of action asked only to identify the emotion, not rate the intensity.
units may explain the better recognition of happy expres- In an earlier study (12), we used an emotion recognition
sions, even at low intensity. test that investigated the ability to correctly identify the in-
The recognition deficit for fearful expressions was ex- tensity of expression for happy and sad emotions using a
pected because mesial temporal lobe structures, impli- forced choice design. Since the present test included 96
items, we were concerned that an additional task would 3. Edwards J, Pattison PE, Jackson HJ, Wales RJ: Facial affect and
produce fatigue in patients. affective prosody recognition in first-episode schizophrenia.
Schizophr Res 2001; 48:235253
Finally, the high recognition rate for happy expressions 4. Kerr SL, Neale JM: Emotion perception in schizophrenia: spe-
in both patients and comparison subjects, which ap- cific deficit or further evidence of generalized poor perfor-
proached ceiling levels, may be unavoidable because mance? J Abnorm Psychol 1993; 102:312318
happy is the only positive universal emotion. The majority 5. Salem JE, Kring AM, Kerr SL: More evidence for generalized
poor performance in facial emotion perception in schizophre-
of universally recognized emotions are of negative va- nia. J Abnorm Psychol 1996; 105:480483
lence. Although surprise has been included as a positive 6. Silver H, Shlomo N, Turner T, Gur RC: Perception of happy and
emotion in some earlier studies, this is not necessarily sad facial expressions in chronic schizophrenia: evidence for
valid because the valence of surprise depends on the trig- two evaluative systems. Schizophr Res 2002; 55:171177
7. Mueser KT, Doonan R, Penn DL, Blanchard JJ, Bellack AS,
gering event. In our previous study examining emotion
Nishith P, DeLeon J: Emotion recognition and social compe-
recognition (12), we evaluated outpatients who were con- tence in chronic schizophrenia. J Abnorm Psychol 1996; 105:
sidered stable enough for testing but not yet clinically sta- 271275
ble. In that study, overall errors on the emotion recogni- 8. Penn DL, Combs DR, Ritchie M, Francis J, Cassisi J, Morris S,
tion task were associated with greater severity of both Townsend M: Emotion recognition in schizophrenia: further in-
vestigation of generalized versus specific deficit models. J Ab-
negative and positive symptoms, including alogia, atten- norm Psychol 2000; 109:512516
tion, hallucinations, and thought disorder. In the present 9. Mandal MK, Jain A, Haque-Nizamie S, Weiss U, Schneider F:
study, the association with performance was found pre- Generality and specificity of emotion-recognition deficit in
dominately for negative symptoms, probably because the schizophrenic patients with positive and negative symptoms.
Psychiatry Res 1999; 87:3946
positive symptoms were attenuated in this clinically stable
10. Schneider F, Gur RC, Gur RE, Shtasel DL: Emotional processing
group. in schizophrenia: neurobehavioural probes in relation to psy-
Future studies may examine the possible effect of treat- chopathology. Schizophr Res 1995; 17:6775
ment on emotion recognition abilities. A previous study 11. Bryson G, Bell M, Lysaker P: Affect impairment in schizophre-
nia: a function of global impairment or a specific cognitive def-
(38) showed improved emotion recognition with amelio-
icit. Psychiatry Res 1997; 71:105113
ration of symptoms in acutely ill patients. This change was 12. Kohler CG, Bilker W, Hagendoorn M, Gur RE, Gur RC: Emotion
attributed to practice effects, despite a comparison group recognition deficit in schizophrenia: association with symp-
of patients with schizophrenia in remission who exhibited tomatology and cognition. Biol Psychiatry 2000; 48:127136
no such improvement. The emotion recognition test was 13. Gur RE, Turetsky BI, Cowell PE, Finkelman C, Maany V, Gross-
man RI, Arnold SE, Bilker WB, Gur RC: Temporolimbic volume
limited by the use of only 12 faces representing six emo- reductions in schizophrenia. Arch Gen Psychiatry 2000; 57:
tions. Few studies have explored the specificity of emotion 769775
recognition deficit to schizophrenia compared with other 14. Nelson MD, Saykin AJ, Flashman LA, Riordan HJ: Hippocampal
disorders, particularly bipolar disorder. A recent report volume reduction in schizophrenia as assessed by magnetic
resonance imaging: a meta-analytic study. Arch Gen Psychiatry
(39) described impaired emotion recognition in patients
1998; 55:433440
with bipolar I disorder, specifically for fear and disgust. 15. Adolphs R, Tranel D, Hamann S, Young AW, Calder AJ, Phelps
Finally, functional imaging studies using different emo- EA, Anderson A, Lee GP, Damasio AR: Recognition of facial
tional categories and contrasting groups with and without emotion in nine individuals with bilateral amygdala damage.
schizophrenia may establish the neural substrates of emo- Neuropsychologia 1999; 37:11111117
16. Gur RC, Erwin RJ, Gur RE, Zwil AS, Heimberg C, Kraemer HC: Fa-
tion recognition deficits in schizophrenia. cial emotion discrimination, II: behavioral findings in depres-
sion. Psychiatry Res 1992; 42:241251
Presented in part at the annual meeting of the Society of Biological 17. Ekman P, Friesen WV: Unmasking the Face. Englewood Cliffs,
Psychiatry, Philadelphia, May 1618, 2002. NJ, Prentice-Hall, 1975
Received October 29, 2002; revision received May 27, 2003; ac- 18. Elfenbein HA, Ambady N: On the universality and cultural
cepted July 8, 2003. From the Neuropsychiatry Section, Department specificity of emotion recognition: a meta-analysis. Psychol
of Psychiatry, University of Pennsylvania, Philadelphia. Address re- Bull 2002; 128:203235
print requests to Dr. Kohler, Neuropsychiatry Section, 10 Gates Bldg., 19. Erwin RJ, Gur RC, Gur RE, Skolnick B, Mawhinney-Hee M,
Hospital of the University of Pennsylvania, 3400 Spruce St., Philadel- Smailis J: Facial emotion discrimination, 1: task construction
phia, PA 19104; kohler@bbl.med.upenn.edu (e-mail).
and behavioral findings in normal subjects. Psychiatry Res
Supported by NIMH grants MH-01839, MH-60722, MH-64045, and 1992; 42:231240
MO1-RR-0040.
20. Gur RC, Sara R, Hagendoorn M, Marom O, Hughett P, Macy L,
Turner T, Bajcsy R, Posner A, Gur RE: A method for obtaining 3-
dimensional facial expressions and its standardization for use
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