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Impaired recognition of affect in facial expression in depressed patients
BIOL PSYCHIATRY 1992;31:947-953
947
Impaired Recognition of Affect .in Facial Expression in Depressed Patients David R. Rubinow and Robert M. Post
Measures of recognition of seven affects in facial and verbal expressions to 17 depressed patients and 31 controls were administered. Depressed patients were significantly im. paired in the recognition of affect in the facial, but not verbal, expressions. Among the seven affects examined, depressed patients made significantly or near significantly fewer correct matches for sad, happy, and interested face items. The performance of the depressed patients was similar to thai obserw,d by Kolb and Taylor in patients with right, but not left, hemisphere cortical excisions. The neurobiology of facial recognition is reviewed, and the relevance of the observed perceptual deficit in depressed patients to the pathophysiology and symptomatology of depression is discussed. Neuropsychological approaches to the study of affective disorder are useful in several respects. First, they are of clear phenomenological relevance, as cognitive and perceptual deficits are well-described features of affective illness (Weingartner and Silberman 1984). Second, they offer the potential for identification of pathophysiologic mechanisms. Thus, studies of patients with unilateral brain lesions or commissurotomies have permitted the neuroana~lomic and hemispheric localization of defined cognitive processes. Some neuropsychologic and cerebral laterality investigations to date provide evidence for frontotemporo-hippocampal dysfunction in affective disorder that, consistent with Flor-Henry's suggestion, preferentially involves the right hemisphere (Flor-Henry 1969; Uytdenhoef et al 1983; Silberman and Weingartner 1986). However, findings in other studies are more suggestive of left hemisphere or bilateral dysfunction (Davidson et al 1987; Robinson et al 1984; Altshuler et al 1990; Davidson and Tomarken 1989). These discrepancies notwithstanding, cognitive/perceptual me&~ures offer the promise of identifying discrete areas of cerebral dysfunction that may underlie the symptoms of affective disorders. One cognitive task, facial recognition, offers promise as an investigational tool in the study of affective disorders both because of' the extent to which this cognitive process has been localized neuroanatomically and because of its potential role in interpreting and determining social behavior (Gruzelier et al 1988; Kolb and Taylor 1981; Leonard et al 1985). Kolb and Taylor (1981) demonstrated that unilateral excision of right hemisphere cortical tissue (temporal, frontal, or parietooccipital) for treatment of epilepsy resulted in impaired perception of emotion in facial expression, whereas perception of emotion in verbal expression was similarly impaired by excision of left hemisphere cortical tissue.
From the Biological Psychialry Branch, National Institute of Mental Health, Betbes~.a,Maryland. Address reprint requests to David R. Rubinow, MD, Section on Behaviotal Endocrinology, Biglc,~ic.alpsychiatry B;anch. Natio~al Institute of Mental Health, Building 10, Room 3N238, 9000 Rockville Pike, Bcthesda, MD 20892. Re~eiv~ January IS, 1991; revised December 8, 1991. © 1992 Society of ~iological Psychiatry
0006-3223/92/$05.00
948
BIOLPSYCHIATRY
D.R. Rubinow and R.M. Post
1992;31:947-953
These authors concluded that the left hemisphere plays a role in verbal affective expression, whereas the right predominates in visual recognition of emotions. In the following study, we employed the measures of perception of emotion in facial and verbal expression described by Kolb and Taylor to evaluate the performance of patients with affective disorder and to determine whether evidence exists for a lateralized perfolmance deficit in the perception of emotion. Methods
Subjects The subjects participating in this study were 17 inpatients (mean age +- SD - 39 _ 10.9, 2 men and 15 women) on a National Institute of Mental Health (NIMH) affective disorder clinical research unit and 31 normal volunteers (mean age +- SD - 31 ± 10.7, I 1 men and 20 women). Inpatients had affective disorder (7 bipolar !, 5 bipolar II, 5 unipolar) diagnosed by Research Diagnostic Criteria (Spitzer et al 1978) and, more recently, DSM-III-R criteria (APA 1987) and were at least moderately depressed at the time of testing (Bunney-Hamburg Depression Scale scores 97) (Bunney and Hamburg 1963). Both patients and controls were medication free at the time of testing, as well as free of medical or neurological illness. Ten patients had a history of prior electroeonvulsive therapy (ECT). No subject had a substance abuse diagnosis.
Procedure The ~rception of affect in facial and verbal expression was assessed by a nonverbal photograph-matching test and a sentence-matching test (respectively) as described by Kolb and Taylor (1981). In brief, in the photograph-matching test, the subject is shown a series of 48 photographs of faces and must match each face with one of seven key photographs that most closely expresses the same affect. Each key photograph depicts an affect described by Ekman and colleagues (Ekman et a11973) as a verbally categorizable emotion. The affects represented are sadness, fear or terror, happiness or' amusement, anger, disgust or contempt, surprise, and interest or attention. In the sentence-matching test, the subject is ,provided with a list of these affects and ~en asked to select the one that best characterizes the affect of a person described in each of 48 sentences. These instruments were kindly provided by Dr. Kolb and were administered in an identical fashion to that described by Kolb and Taylor (1981).
Statistics Peribrmance comparisons were made as follows. The mean number of incorrect answers for both the face-matching and sentence-word-matching tasks was determined for patients and controls; a corrected mean score was also calculated after eliminating particularly difficult task items, defined as those incorrectly answered by more than 50% of the controls. The mean number of incorrect matches was also calculated for each of the above-described seven affects. Finally, the number of subjects incorrectly matching more than half of the face or wore items associated with a particular affect was determined. Effects of diagnosis, test (face versus sentence matching), and affect (sadness, fear, etc.) were determined by analysis of variance with repeated measures (ANOVA-R) with one between-subject (diagnosis) ~ d two within-subject (test, affect) variables. If ANOVA
Facial Recognition in Depression
toOLPSYCHIATRY 1992;31:947-953
949
effects were significant, post-hoc between-group differences were analyzed with unpaired Student's t-tests and z-tests for comparison of proportions. The relationship between test performance and ratings of depression and anxiety was examined with Pearson productmoment correlation coefficients, as were the relationships between test performance and patient historical variables (e.g., duration of illness, number of hospitalizations). Test performance in males and females and in patients with and without a history of ECF was compared with Student's t-tests. Results ANOVA-R showed significant effects of diagnosis (p < 0.05), test (p < 0.0001), affect (p < 0.0001), and the interactive terms diagnosis by test (p < 0.005), diagnosis by affect (p < 0.05), test by affect (p < 0.0001), and diagnosis by test by affect (p < 0.05), These results in general reflect impaired performance of depressed patients rel:~ ~e to controls, with impairments significantly greater on one test (face matching) and for several specific affects. Depressed patients showed significant impairment on the face-matching test compared with controls (mean errors ± SD = 19.6 ± 5.4 and 15.4 ± 3.3 for patients and controls, respectively, t = 2.92 andp < 0.005). In contrast, the mean error scores for the sentenceword-matching test were highly comparable in patients and controls (mean _ SD = 8.4 __. 3.6 and 7.7 --. 2.6, respectively, r = 0.78, p = NS). Differences in performance between patients and controls were not affected when scores were "corrected" by eliminating those items incorrectly identified by more than half of the controls (face matching, t = 3.02, p < 0.01; sentence-word-matching, t = 1.35, p = NS). No significant differences were seen in test performance between those with (~ = 10) and those without (n = 7) a history of ECT; in fact, non significant increased numbers of errors were seen on both face-matching and sentence-word-matching tests in those without a history of ECT (21.6 versus 18.2 and 9.3 versus 7.8~, respectively). Although the patient sample contained only two men, no significant gender-related differences were seen in the control group on either matching test (p > 0. I for beth); again, the men showed a nonsignificant increase in errors on both tests (16.6 versus 14.7 and 8.8 versus 7.1), which, if anything, would bias in a direction opposite to that of our findings. When matching performance for individual ,Lffects was examined in a post-hoc fashion, patients compared to controls made significan~ly fewer correct matches for sad and interested face items (t = 3.25, p < 0.005, t -'- 2.12, p < 0.05) and near significantly fewer matches for happy items (t = 2.05, p = 0.052), and significantly fewer matches on the surprise sentence-word items (t = 3.21, p < 0.005). No particular affect was selected significantly more frequently by patients or controls. The patients showed significantly improved performance on the fear items of t~e sentence..wor~-metehing test (t = 2.22, p < 0.05). Comparison of the number of subjects providing incorrect answers for more than half of the items associated with a particular affect showed a significant increase in the proportion of depressed patients scoring incorrectly on more ~han half of the sad face-matching items (z -~ 3.09, p < 0.005). No significant relationship was identified between performance on the face-matching or sentence-word-matching test and observer ratings of the severity of depression or anxiety in depressed patients. Similarly, no significant relationships were observed between test performance and the following patient historical variables: duration of illness, total number of depres~eA or manic episodes, number of hospitalizations, age of onset of illness, current age. Finally, perfor-
950
BIOLPSYCHIATRY
D.R. Rubinow and R.M. Post
1992;31:94/-953
90
m
Normal Depressed Right Hemisphere Lesions*
80
Left Hemisphere Lesions*
o (.3
'°r
.,,ooKo,b.to,,.,
=u rt
60
50 t
.
-
-
Facial Expression Mat.ching
-
~
Verbal F'xpression Matching
Figure 1. Eepressed patients show impaired performance on the matching of emotion in facial expression similarto that observedin patients with right hemispherecortical excisions. Performance of depressed patients on the matchingof emotion in verbal expression is similar to that of controls.
mance on face and sentence-word-matching tests was significantly correlated in controls (r = .65, p < 0.0001) but not in patients (r = 0.20, p = NS).
Discussion We have demonstrated that depressed patients scored significantly lower than controls on the perception of emotion in facial, but not verbal, expression. Kolb and Taylor (1981) determined a matchin~ answer to be correct if selected by 70% or greater of their control subjects. The mean percentage of correct items selected by our controls on the matching tests was 68% for facial and 84% for verbal. In contrast, the mean percentage of correct responses for depressed patients was 59% for facial and 83% for verbal. The impairment of facial emotional matching seen in the depressed patients is comparable to a mean percentage of correct matches of approximately 59% in neurological patients with right hemisphere cortical excisions (Koib and Taylor 1981). The verbal emotional matching scores in our depressed patients were comparable to those of our controls and the righthemisphere-lesion patients of Kolb and Taylor and were higher than patients with left hemisphere cortical excisions (see Figure 1). Our data, then, suggest considerable and relatively selective right hemispheric dysfunctio~l in affective disorder patients, consistent with other reports of impaired spatial
Facial Recognitionin Depression
BIOLPSYCHIATRY 1992;31:947-953
951
versus nonspatial performance and greater right hemispheric impairment in patients with affective disorder (Gmzelier et al 1988; Silberman and Weingartner 1986). Davidson et al (1987) have observed impaired spatial compared with verbal performance in depressed patients, with the spatial defects associated with an absence of the expected activation of the right posterior temporoparietal area on electroencephalograph (EEG). Abnormal right temporoparietooccipital EEG activity was also observed by Gruzelier (Gruzelier and Liddiard 1989) in schizophrenic patients in association with a deficit in facial recognition memory, suggesting that our findings may not be specific for affective disorder. Mixed performance of the depressed patients on the sentence-word items surprise (impaired performance) and fear (improved performance) suggests, as noted elsewhere (Henriques and Davidson 1990; Davidson and Tomarken 1989), that patients may also differ from controls on measures of predominantly left hemispheric function. Nonetheless, the overall comparable performance of patients and controls on the sentence-word-matching test stands in marked contrast to the relatively impaired performance by patients in the facematching test, with this contrast suggesting that the differences seen on the face-matching test cannot be attributed to motivational factors. The significant diagnosis by test interaction s-~.n on ANOVA-R also supports this interpretation. The difference in performance in depressed patients further appears to be a state rather than a trait phenomenon. Patient historical variables (illness and treatment characteristics) were not related to test performance. Also, preliminary data in five medication-free euthymic patients reveal no differences in perception of emotion it, facial expression compared with controls, again suggesting the depression state-dependent nature of the impaired performance. Noteworthy in this regard, however, is the description by Henriques and Davidson (1990) of the depression state-indel~endentappearance of regional b~in electrical asymmetry in patients with a past history of depression. Thus, decreased right-sided posterior and left-sided anterior activation was obset'ved in both currently depressed and previously depressed patients (with no medication history and at least one year of euythmic mood) compared with subjects with no prior history of depression. The importance of facial recognition is suggested by identifcation in the amygdala, superior temporal sulcus, inferior temporal visual cortex, parietal cortex, and frontal codex (Perrett et al 1982) of neurons that respond selectively or predominantt.yto faces. Identification of these "facial neurons" in the amygdala and temporal cortex is consistent vdth ~he prosopagnosia (facial agnosia) associated with inferior occipitotemporal damage (Meadows 1974; Perrett et a11982) and with the inappropriate reaction to faces observed following amygdala and temporal lobe lesions in the Kluver-Bucy syndrome (Kluver and Bucy 1939; Horel et al 1975). Dysfunction of the facial recognition system, therefore, may not only represent a perceptual deficit but may directly translate into behavioral alterations, perhaps via amygdalar projections to cortical reg.~ons(e.g., orbitofrontal cortex) believed important in behavioral regulation (Rolls 1990). Although face-responsive neurons have been identified in both hemispheres and faci~,|perception appears to occur bilaterally, facial recognition, that is, the comparison of stimulus faces with internal representations, shows hemispheric asymmetry with right hemispheric specialization (Marzi et al 1985). In addition to the overall deficit ir~perception of emotion in facial expressions, the dep~ssed pat.ientswere particularly ~npaired in their ability to recognize sadness, happiness, and interest, but not anger, surprise, disgust, or fear; that is, there appeared to be a selective impairmentof those items ~-eflc~tingf f f ~ most pertinent to manic depressive illness. Leonard et al (1985) and Perrett ct al (1982) have identified neurons that differentially respond to faces on the basis of the t y ~ of facial expression. As such, our data might suggest the~pres-
952
BIOLPSYCHIATRY 1992;31:947-953
D.R. Rubinow and R.M. Post
ence of selective dysfunction of certain components of the facial recognition system, either the face perception neurons or their cortical inputs. Alternatively, if tbe fuce-responsive neurons in the amygdala are part of an association mechanism for emotional response to faces as suggested by Leonard et al (1985), the selective recognition abnormalities that we observed might reflect or contribute to the affect association or access dysfunction observed in affective disorder, that is, persistent sadness with anbedonia and apathy. This interpretation would suggest that affective illness is characterized by deficits in both receptive (perceptual) as well as expressive (behavioral) function. Thus the deficient recognition of emotion in facial expression may reflect misperceptions of emotions ("emotional dysphasia") as well as produce or contribute to inappropriate behavioral responses ("behavioral dyspraxia"). The misreading of facial emotions, then, may be one manifestation of the inability of the depressed patient to employ external and internal emotional cues to modify behavior and alter self-perceptions. This inability of depressed patients to employ experiential and emotional cues is suggested by other neuropsychological studies. Silberman et ai (1983) demonstrated that depressed patients did not show the expected improved recall performance with high emotional words, despite their being able to properly order the words with respect to emotional valence. Additionally, Szostak et al (1990) recently demonstrated that depressed patients manifest a major deficit in implicit learning; that is, they are ramble to improve their test performance despite earlier experience with the same cognitive task, an improvement seen in Alzheimer's patients as well as normal controls. Finally, although we cannot with certainty assert that the deficit in recognition of facial expression does not reflect a more general problem with facial perception, the significant diagnosis by test by affect interaction suggests that the deficit is ,selective for certain facial expressions and is therefore unlikely to represent a nonspecific perceptual problem. Recognition of emotion in facial expressions is a perceptual-interpretive process that is highly developed in human and nonhuman primates, reflecting its social and behavioral importance. Human infants may recognize emotion and facial expression when only several months of age (Trevarthen 1985), and it has been suggested that disruption of the face-processing system contributes in a major fashion to the inappropriate social behavior and social ostracism that follows damage to the amygdala (Perrett et al 1982; Kling and Steklis 1976). Further investigation of the nature and extent of the deficit in recognition of emotion in facial expression in affective disorder may provide greater understanding of the symptomatology and underlying neural substrates of depression. The authors acknowledge with considerablegratitude Dr. Teresa Huggins' significant contributions to this paper.
References Altshuler LL, Devinsky O, Post RM, Theodore W (1990): Depression, anxiety, and temporal lobe epilepsy. Arch Neurol 47:284-288. Americai~ Psychiatric Association (1987): Diagnosticand Statistical Manual of Mental Disorder,% 3rd ed, rev. Washington, DC: American Psychiatric Association Press, Bunney WE Jr, Hamburg DA (1963)" Methods for reliable longitudinal observation of behavior: Development of a method for systematic observation of emotional behavior on psychiatric wards. Arch Gen Psychiatry 9:280-294. Davidson RJ, Tom.ken AJ (1989): Laterality and emotion: An electrophysiological approach. In Belier F, Grafinan J (eds), Handbook of Neuropsychology, 3rd ed. New York: Elsevier, pp 419-441.
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Davidson RJ, Chapman JP, Chapman LJ (1987): Task-dependent EEG asymmetry discriminates between depressed and non-depressed subjects. Psychophysiology 24:585. Ekman P, Friesen WV, Ellsworth P (i973): Emotion in the Haman Face. Toronto: Pergamon. Fief-Henry P (1969): Psychoses and temporal lobe epilepsy: A controlled investigation. Epilepsia 10:363-395. Gruzelier J, Liddiard D (I 989): The neuropsycbologyof schizophreniain the context of topographical mapping of electrocorticai activity. In Maurer K (ed), Topographic Brain Mapping of EEG and Evoked Potentials. Berlin: Springer-Verlag, pp 421-437. Gmzelier J, Seymour K, Wilson L, Jolley A, Hirsch S (1988): Impairments on neuropsychologic tests of temporohippocampal and frontohippocampal functions and word fluency in remitting schizophrenia and affective disorders. Arch Gen Psychiatry 45:623-629. Henriques JB, Davidson P.J (1990): Regional brain electrical asymmetries discriminate between previously depressed and healthy control subjects. J Abnorm Psychol 99:22-31. Horel JA, Ke~tingEG, Misantone LG (1975): Partial Klu,~er-Bucysyndrome produced by destroying neocortox or amygdaia. Brain Res 94:347-359. Kling A, Steklis HD (1976): A neural substrate for afliliative behavior in nonhuman primates. Brain Belrav Evol 13:216-238. iKluver H, Bucy PC (1939): Preliminary analysis of functions of the temporal lobes in monkeys. Arch Neurol Psychiatr 42:979-1000. I(olb B, Taylor L (1981): Affective behavior in patients with localized cortical excisions: Role of lesion site and side. Science 214:89-91. Leonard CM, Rolls ET, Wilson FAW, Baylis GC (1985): Neurons in the amygdala of the monkey with responses selective for faces. Behav Brain Res 15:159-176. Marzi CA, Tassinari G, Tressoldi PE, Barry C, Grabowska A (1985): Hemispheric asymmetry in face perception tasks of different cognitive requirement. Hum Neurobiol 4:15-20. Meadows JC (1974): The anatomical basis of prosopagnosia. J Neurol Neurosurg Psychiatry 37:489-501. Perrett DI, Rolls El', Caan W (1982): Visual neurones responsive to faces in the monkey temporal cortex. Exp Brain Res 47:329-342. Robinson RG, Kubos KL, Staff LB, Rao K, Price TR (1984): Mood disorders in stroke patients: Importance of location of lesion. Brain 107:81-93. Rolls ET (1990): A theory of emotion, and its application to understanding the neural basis of emotion. Cogn Emot 4:161-190. 5ilberman EK, Weingartner H (1986): Hemispheric lateralization of functions related to emotion. Brain Cogn 5:322-353. Silberman EK, Weingartner H, Leraia M, Byrnes S, Post RM (1983): Processing of emotional properties of stimuli by depressed and normal subjects. J Nerv blent Dis 171:10-14. Spitzer RL, Endicott J, Robins E (1978): Research diagnostic criteria: Rationale and reliability. Arch Gen Psychia,'ry 35:773-782. $zostak CM, Kling MA, Gold PW, Post RM, Weingartner H (1990): Implicit memory is impaired in major depression. Abstracts of the American Psychiatry Association's 143rd Annual Meeting. Trevarthen C (!985): Facial expressions of emotion in mother-infant interaction. Neurobiology 4:21-32. Uytdenhoef P, Po~elange P, Jacquy J, Charles G, Linkowski P, Mendlewicz J (1983): Regi,~nal cerebral blood flow and lateralized hemispheric dysfunction in depression. Br J Psychiatry 143:128-132. Weingartner H, Silberman E (1984): Cognitive changes in depression. In Post RM, Ballenger JC (eds) Neurology of Mood Disorders. Baltimore: Williams & Wilkins, pp 121-135.
947
Impaired Recognition of Affect .in Facial Expression in Depressed Patients David R. Rubinow and Robert M. Post
Measures of recognition of seven affects in facial and verbal expressions to 17 depressed patients and 31 controls were administered. Depressed patients were significantly im. paired in the recognition of affect in the facial, but not verbal, expressions. Among the seven affects examined, depressed patients made significantly or near significantly fewer correct matches for sad, happy, and interested face items. The performance of the depressed patients was similar to thai obserw,d by Kolb and Taylor in patients with right, but not left, hemisphere cortical excisions. The neurobiology of facial recognition is reviewed, and the relevance of the observed perceptual deficit in depressed patients to the pathophysiology and symptomatology of depression is discussed. Neuropsychological approaches to the study of affective disorder are useful in several respects. First, they are of clear phenomenological relevance, as cognitive and perceptual deficits are well-described features of affective illness (Weingartner and Silberman 1984). Second, they offer the potential for identification of pathophysiologic mechanisms. Thus, studies of patients with unilateral brain lesions or commissurotomies have permitted the neuroana~lomic and hemispheric localization of defined cognitive processes. Some neuropsychologic and cerebral laterality investigations to date provide evidence for frontotemporo-hippocampal dysfunction in affective disorder that, consistent with Flor-Henry's suggestion, preferentially involves the right hemisphere (Flor-Henry 1969; Uytdenhoef et al 1983; Silberman and Weingartner 1986). However, findings in other studies are more suggestive of left hemisphere or bilateral dysfunction (Davidson et al 1987; Robinson et al 1984; Altshuler et al 1990; Davidson and Tomarken 1989). These discrepancies notwithstanding, cognitive/perceptual me&~ures offer the promise of identifying discrete areas of cerebral dysfunction that may underlie the symptoms of affective disorders. One cognitive task, facial recognition, offers promise as an investigational tool in the study of affective disorders both because of' the extent to which this cognitive process has been localized neuroanatomically and because of its potential role in interpreting and determining social behavior (Gruzelier et al 1988; Kolb and Taylor 1981; Leonard et al 1985). Kolb and Taylor (1981) demonstrated that unilateral excision of right hemisphere cortical tissue (temporal, frontal, or parietooccipital) for treatment of epilepsy resulted in impaired perception of emotion in facial expression, whereas perception of emotion in verbal expression was similarly impaired by excision of left hemisphere cortical tissue.
From the Biological Psychialry Branch, National Institute of Mental Health, Betbes~.a,Maryland. Address reprint requests to David R. Rubinow, MD, Section on Behaviotal Endocrinology, Biglc,~ic.alpsychiatry B;anch. Natio~al Institute of Mental Health, Building 10, Room 3N238, 9000 Rockville Pike, Bcthesda, MD 20892. Re~eiv~ January IS, 1991; revised December 8, 1991. © 1992 Society of ~iological Psychiatry
0006-3223/92/$05.00
948
BIOLPSYCHIATRY
D.R. Rubinow and R.M. Post
1992;31:947-953
These authors concluded that the left hemisphere plays a role in verbal affective expression, whereas the right predominates in visual recognition of emotions. In the following study, we employed the measures of perception of emotion in facial and verbal expression described by Kolb and Taylor to evaluate the performance of patients with affective disorder and to determine whether evidence exists for a lateralized perfolmance deficit in the perception of emotion. Methods
Subjects The subjects participating in this study were 17 inpatients (mean age +- SD - 39 _ 10.9, 2 men and 15 women) on a National Institute of Mental Health (NIMH) affective disorder clinical research unit and 31 normal volunteers (mean age +- SD - 31 ± 10.7, I 1 men and 20 women). Inpatients had affective disorder (7 bipolar !, 5 bipolar II, 5 unipolar) diagnosed by Research Diagnostic Criteria (Spitzer et al 1978) and, more recently, DSM-III-R criteria (APA 1987) and were at least moderately depressed at the time of testing (Bunney-Hamburg Depression Scale scores 97) (Bunney and Hamburg 1963). Both patients and controls were medication free at the time of testing, as well as free of medical or neurological illness. Ten patients had a history of prior electroeonvulsive therapy (ECT). No subject had a substance abuse diagnosis.
Procedure The ~rception of affect in facial and verbal expression was assessed by a nonverbal photograph-matching test and a sentence-matching test (respectively) as described by Kolb and Taylor (1981). In brief, in the photograph-matching test, the subject is shown a series of 48 photographs of faces and must match each face with one of seven key photographs that most closely expresses the same affect. Each key photograph depicts an affect described by Ekman and colleagues (Ekman et a11973) as a verbally categorizable emotion. The affects represented are sadness, fear or terror, happiness or' amusement, anger, disgust or contempt, surprise, and interest or attention. In the sentence-matching test, the subject is ,provided with a list of these affects and ~en asked to select the one that best characterizes the affect of a person described in each of 48 sentences. These instruments were kindly provided by Dr. Kolb and were administered in an identical fashion to that described by Kolb and Taylor (1981).
Statistics Peribrmance comparisons were made as follows. The mean number of incorrect answers for both the face-matching and sentence-word-matching tasks was determined for patients and controls; a corrected mean score was also calculated after eliminating particularly difficult task items, defined as those incorrectly answered by more than 50% of the controls. The mean number of incorrect matches was also calculated for each of the above-described seven affects. Finally, the number of subjects incorrectly matching more than half of the face or wore items associated with a particular affect was determined. Effects of diagnosis, test (face versus sentence matching), and affect (sadness, fear, etc.) were determined by analysis of variance with repeated measures (ANOVA-R) with one between-subject (diagnosis) ~ d two within-subject (test, affect) variables. If ANOVA
Facial Recognition in Depression
toOLPSYCHIATRY 1992;31:947-953
949
effects were significant, post-hoc between-group differences were analyzed with unpaired Student's t-tests and z-tests for comparison of proportions. The relationship between test performance and ratings of depression and anxiety was examined with Pearson productmoment correlation coefficients, as were the relationships between test performance and patient historical variables (e.g., duration of illness, number of hospitalizations). Test performance in males and females and in patients with and without a history of ECF was compared with Student's t-tests. Results ANOVA-R showed significant effects of diagnosis (p < 0.05), test (p < 0.0001), affect (p < 0.0001), and the interactive terms diagnosis by test (p < 0.005), diagnosis by affect (p < 0.05), test by affect (p < 0.0001), and diagnosis by test by affect (p < 0.05), These results in general reflect impaired performance of depressed patients rel:~ ~e to controls, with impairments significantly greater on one test (face matching) and for several specific affects. Depressed patients showed significant impairment on the face-matching test compared with controls (mean errors ± SD = 19.6 ± 5.4 and 15.4 ± 3.3 for patients and controls, respectively, t = 2.92 andp < 0.005). In contrast, the mean error scores for the sentenceword-matching test were highly comparable in patients and controls (mean _ SD = 8.4 __. 3.6 and 7.7 --. 2.6, respectively, r = 0.78, p = NS). Differences in performance between patients and controls were not affected when scores were "corrected" by eliminating those items incorrectly identified by more than half of the controls (face matching, t = 3.02, p < 0.01; sentence-word-matching, t = 1.35, p = NS). No significant differences were seen in test performance between those with (~ = 10) and those without (n = 7) a history of ECT; in fact, non significant increased numbers of errors were seen on both face-matching and sentence-word-matching tests in those without a history of ECT (21.6 versus 18.2 and 9.3 versus 7.8~, respectively). Although the patient sample contained only two men, no significant gender-related differences were seen in the control group on either matching test (p > 0. I for beth); again, the men showed a nonsignificant increase in errors on both tests (16.6 versus 14.7 and 8.8 versus 7.1), which, if anything, would bias in a direction opposite to that of our findings. When matching performance for individual ,Lffects was examined in a post-hoc fashion, patients compared to controls made significan~ly fewer correct matches for sad and interested face items (t = 3.25, p < 0.005, t -'- 2.12, p < 0.05) and near significantly fewer matches for happy items (t = 2.05, p = 0.052), and significantly fewer matches on the surprise sentence-word items (t = 3.21, p < 0.005). No particular affect was selected significantly more frequently by patients or controls. The patients showed significantly improved performance on the fear items of t~e sentence..wor~-metehing test (t = 2.22, p < 0.05). Comparison of the number of subjects providing incorrect answers for more than half of the items associated with a particular affect showed a significant increase in the proportion of depressed patients scoring incorrectly on more ~han half of the sad face-matching items (z -~ 3.09, p < 0.005). No significant relationship was identified between performance on the face-matching or sentence-word-matching test and observer ratings of the severity of depression or anxiety in depressed patients. Similarly, no significant relationships were observed between test performance and the following patient historical variables: duration of illness, total number of depres~eA or manic episodes, number of hospitalizations, age of onset of illness, current age. Finally, perfor-
950
BIOLPSYCHIATRY
D.R. Rubinow and R.M. Post
1992;31:94/-953
90
m
Normal Depressed Right Hemisphere Lesions*
80
Left Hemisphere Lesions*
o (.3
'°r
.,,ooKo,b.to,,.,
=u rt
60
50 t
.
-
-
Facial Expression Mat.ching
-
~
Verbal F'xpression Matching
Figure 1. Eepressed patients show impaired performance on the matching of emotion in facial expression similarto that observedin patients with right hemispherecortical excisions. Performance of depressed patients on the matchingof emotion in verbal expression is similar to that of controls.
mance on face and sentence-word-matching tests was significantly correlated in controls (r = .65, p < 0.0001) but not in patients (r = 0.20, p = NS).
Discussion We have demonstrated that depressed patients scored significantly lower than controls on the perception of emotion in facial, but not verbal, expression. Kolb and Taylor (1981) determined a matchin~ answer to be correct if selected by 70% or greater of their control subjects. The mean percentage of correct items selected by our controls on the matching tests was 68% for facial and 84% for verbal. In contrast, the mean percentage of correct responses for depressed patients was 59% for facial and 83% for verbal. The impairment of facial emotional matching seen in the depressed patients is comparable to a mean percentage of correct matches of approximately 59% in neurological patients with right hemisphere cortical excisions (Koib and Taylor 1981). The verbal emotional matching scores in our depressed patients were comparable to those of our controls and the righthemisphere-lesion patients of Kolb and Taylor and were higher than patients with left hemisphere cortical excisions (see Figure 1). Our data, then, suggest considerable and relatively selective right hemispheric dysfunctio~l in affective disorder patients, consistent with other reports of impaired spatial
Facial Recognitionin Depression
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versus nonspatial performance and greater right hemispheric impairment in patients with affective disorder (Gmzelier et al 1988; Silberman and Weingartner 1986). Davidson et al (1987) have observed impaired spatial compared with verbal performance in depressed patients, with the spatial defects associated with an absence of the expected activation of the right posterior temporoparietal area on electroencephalograph (EEG). Abnormal right temporoparietooccipital EEG activity was also observed by Gruzelier (Gruzelier and Liddiard 1989) in schizophrenic patients in association with a deficit in facial recognition memory, suggesting that our findings may not be specific for affective disorder. Mixed performance of the depressed patients on the sentence-word items surprise (impaired performance) and fear (improved performance) suggests, as noted elsewhere (Henriques and Davidson 1990; Davidson and Tomarken 1989), that patients may also differ from controls on measures of predominantly left hemispheric function. Nonetheless, the overall comparable performance of patients and controls on the sentence-word-matching test stands in marked contrast to the relatively impaired performance by patients in the facematching test, with this contrast suggesting that the differences seen on the face-matching test cannot be attributed to motivational factors. The significant diagnosis by test interaction s-~.n on ANOVA-R also supports this interpretation. The difference in performance in depressed patients further appears to be a state rather than a trait phenomenon. Patient historical variables (illness and treatment characteristics) were not related to test performance. Also, preliminary data in five medication-free euthymic patients reveal no differences in perception of emotion it, facial expression compared with controls, again suggesting the depression state-dependent nature of the impaired performance. Noteworthy in this regard, however, is the description by Henriques and Davidson (1990) of the depression state-indel~endentappearance of regional b~in electrical asymmetry in patients with a past history of depression. Thus, decreased right-sided posterior and left-sided anterior activation was obset'ved in both currently depressed and previously depressed patients (with no medication history and at least one year of euythmic mood) compared with subjects with no prior history of depression. The importance of facial recognition is suggested by identifcation in the amygdala, superior temporal sulcus, inferior temporal visual cortex, parietal cortex, and frontal codex (Perrett et al 1982) of neurons that respond selectively or predominantt.yto faces. Identification of these "facial neurons" in the amygdala and temporal cortex is consistent vdth ~he prosopagnosia (facial agnosia) associated with inferior occipitotemporal damage (Meadows 1974; Perrett et a11982) and with the inappropriate reaction to faces observed following amygdala and temporal lobe lesions in the Kluver-Bucy syndrome (Kluver and Bucy 1939; Horel et al 1975). Dysfunction of the facial recognition system, therefore, may not only represent a perceptual deficit but may directly translate into behavioral alterations, perhaps via amygdalar projections to cortical reg.~ons(e.g., orbitofrontal cortex) believed important in behavioral regulation (Rolls 1990). Although face-responsive neurons have been identified in both hemispheres and faci~,|perception appears to occur bilaterally, facial recognition, that is, the comparison of stimulus faces with internal representations, shows hemispheric asymmetry with right hemispheric specialization (Marzi et al 1985). In addition to the overall deficit ir~perception of emotion in facial expressions, the dep~ssed pat.ientswere particularly ~npaired in their ability to recognize sadness, happiness, and interest, but not anger, surprise, disgust, or fear; that is, there appeared to be a selective impairmentof those items ~-eflc~tingf f f ~ most pertinent to manic depressive illness. Leonard et al (1985) and Perrett ct al (1982) have identified neurons that differentially respond to faces on the basis of the t y ~ of facial expression. As such, our data might suggest the~pres-
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D.R. Rubinow and R.M. Post
ence of selective dysfunction of certain components of the facial recognition system, either the face perception neurons or their cortical inputs. Alternatively, if tbe fuce-responsive neurons in the amygdala are part of an association mechanism for emotional response to faces as suggested by Leonard et al (1985), the selective recognition abnormalities that we observed might reflect or contribute to the affect association or access dysfunction observed in affective disorder, that is, persistent sadness with anbedonia and apathy. This interpretation would suggest that affective illness is characterized by deficits in both receptive (perceptual) as well as expressive (behavioral) function. Thus the deficient recognition of emotion in facial expression may reflect misperceptions of emotions ("emotional dysphasia") as well as produce or contribute to inappropriate behavioral responses ("behavioral dyspraxia"). The misreading of facial emotions, then, may be one manifestation of the inability of the depressed patient to employ external and internal emotional cues to modify behavior and alter self-perceptions. This inability of depressed patients to employ experiential and emotional cues is suggested by other neuropsychological studies. Silberman et ai (1983) demonstrated that depressed patients did not show the expected improved recall performance with high emotional words, despite their being able to properly order the words with respect to emotional valence. Additionally, Szostak et al (1990) recently demonstrated that depressed patients manifest a major deficit in implicit learning; that is, they are ramble to improve their test performance despite earlier experience with the same cognitive task, an improvement seen in Alzheimer's patients as well as normal controls. Finally, although we cannot with certainty assert that the deficit in recognition of facial expression does not reflect a more general problem with facial perception, the significant diagnosis by test by affect interaction suggests that the deficit is ,selective for certain facial expressions and is therefore unlikely to represent a nonspecific perceptual problem. Recognition of emotion in facial expressions is a perceptual-interpretive process that is highly developed in human and nonhuman primates, reflecting its social and behavioral importance. Human infants may recognize emotion and facial expression when only several months of age (Trevarthen 1985), and it has been suggested that disruption of the face-processing system contributes in a major fashion to the inappropriate social behavior and social ostracism that follows damage to the amygdala (Perrett et al 1982; Kling and Steklis 1976). Further investigation of the nature and extent of the deficit in recognition of emotion in facial expression in affective disorder may provide greater understanding of the symptomatology and underlying neural substrates of depression. The authors acknowledge with considerablegratitude Dr. Teresa Huggins' significant contributions to this paper.
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