mia Recognition Accuracy and Response Bias to Happy and Sad Facial Expressions in Patients With Major Depression imon A. Surguladze ‘King's College London Carl Senior Asion University Andrew W. Young University of York Gildas Brébion, Michael J. Travis, and Mary L. Phillips King’s Colleye London Impaired facial expression recognition has been associated with features of major depression, which could undetie some of the dificltes in seca ineractions in these pains. Pals with major ‘epresive disorder and age- an gendersmatched healthy volueers judged the emotion of 100 fil sul displaying different intensities of sadness and hap sand neural expressions presented for sort (100 ms} and ong (2.000 ms) duraons. Compared with heathy vlumters, depressed patients demonsrated subtle impuimens in discrimination accuracy and a predominant bias away fom the ieateaion as huppy of mildly happy expressions. The authors suggest hut ia depressed patie, dhe inability to aur nay undelete impaired interpersonal uncioing. Defining features of unipolar depression include depressed ‘mood and anhedonia, which, with increasing severity of illness, can lead to a restriction of affective range and social dysfunction. ‘The ability to recognize facial expressions displayed by others is, highly developed in human and nonhuman primates and is ob- served actoss many cultures (Ekman & Friesen, 1971), In de= pressed patients, however, depressed mood hhas been associated ‘with specific abnormalities in the identification of facial expres sions (Cooley & Nowicki, 1989; Wexler, Levenson, Warrenburg, & Price, 1994), negative cognitions regarding the sell, and dys functional appraisal of social events and situations (Beck, 1976). ‘These abnormalities may lead to impaired interpersonal function ing (eg... Gotlib & Asarnow, 1979). Previous studies have examined the nature of the impairment in perception of facial expressions in depressed patients. Some in- vestigators exploring discrimination accuracy of facial emotional stimuli in these patients have provided evidence fora generalized deficit in the recognition ofall emotions (and even in the recox- nition of nonemotional stimuli) Deficits have been demonstrated, for example, in the recognition of faces expressing. happiness (laeger, Borod, & Pesclow, 1987), sadness and interest (Rubinow ‘Simon A. Surguladze, Section of Neuroscience & Eetio, Division of Payohological Modine, Insite of Psyehiany, King’s College London, London: Andrew W. Young. Department of Psychology. Univesity of York. Heslington, York. United Kingdom: Carl Seaior. Neuroscience Resear Instr, Aston University, Birmingham, United Kingdom: Git as Brébion, Michsel J. Tris, and Mary L, Philips, Divison of Pyeho- logical Meine, Institute of Psychiatry, Kings College London. “This sty wes soppoted bythe James McDonnell Pew undation, We ‘hank S. Rabo Hesketh fr help with dats analysis and Cris Andre for “sippor in imal peepration, ‘Conespondence concerning this ace shouldbe adresse to Simon A ‘Surguladze, Division of Poychologial Medicine. PO, Box 63, Inte of ‘Paychiaty, Kins College London, De Crespgny Par, London SES BAF, ‘United Kingdom. E-mail phasis hop ela uk 2 ly identity subule change in fail expression displays by others in soa stations & Post, 1992), and fear, anger, surprise, disgust, happiness sad ness, and indifference (Persad & Polivy, 1993), In one study, however, impairments in performance of bath visuospatial and affective tasks (identification of neural happy, sad, fearful, and angry expressions) were demonstrated in depressed patients (AS- thana, Mandal, Khurana, & Haque-Nizami, 1998), suggestive of 1 general visual pereeptve rather thun a specific emotion recog- nition deficit, In another study, although depressed patients were not signii- ‘cantly impaired in tasks requiring matching pictures of emotional fees, they were impsired in. verbal labeling of all emotional anger, happiness, sadness, fear, disgust, surprise) and neutral (Feinberg, Rifkin, Schaffer, & Walker, 1986) faces. These findings were interpreted as evidence of a specific deficit inthe expressive domain rather than a visual perceptual deficit in these patients ‘Conversely, depressed patients compared with healthy volun- teers have been reported to be significantly impaired inthe recog nition of both sad and happy, but not neutral, faces (Mikhailova, Vidimirova, Iznak, Tsusulkovskaya, & Sushko, 1996). In this ‘study, depressed patients retested in remission did not demonstrate this deficit in emotion processing, suggesting a state rather than trait deficit in emotion processing in depression. ‘Other studies have revealed emotion-specitic abnormalities in depressed patients, with patients demonstrating negative percep- ‘wal bias (Le., recognizing significantly more sadness in facial expressions than healthy volunteers: Bouhuys, Geers, & Gordijn, 1999; RC. Gur et al, 1992; Hale, 1998; Matthews & Antes, 1992), There have been addtional reports in depressed patients of impaired recognition of positive facial expressions (Murphy et al. 1999; Sustow, Junghanas, & Arolt, 2001), diminished emotional responses to pleasant pictorial stimuli (Sloan. Strauss, Quirk, & Sajatovic, 1997; Sloan, Strauss, & Wisner, 2001), and increased, response times to happy compared with sad emotional words. Findings to date from studies examining emotion processing in, depressed patients ate, therefore, inconsistent, with evidence for and against the presence of a general visual perceptual dei Material may be protected by copyright law (Title 17, U.S. Code)RECOGNITION AND RESPONSE BIAS IN DEPRESSION 213, ‘evidence for impaired identiieation ofall categories of emotion, and evidence for impairments in the identification of specie ‘emotions. ‘There are several potential explanations for dhe discrepant find- ings. First, there were differences in the types of patient popul tions recruited and examined in the studies, In some studies, patients were restricted to those with unipolar depression (et, Feinberg et al. 1986; Juegeret ul, 1987; Persad & Polivy, 1993), ‘whereas in others, both unipolar and bipolar depressed paints were examined (R. C. Gur etal, 1992; Rubinow & Pest, 1992), Second, there were differences across the studies in the types of stimuli used. In some of the studies, facial expressions from a standardized series (Ekman & Friesen, 1976) were used (Feinberg et al, 1986; Persad & Polivy, 1993), whereas other investigators used novel seies of photographs (Asthana etal, 1998; R. C. Gur ct al, 1992) of schematic fares (Bouhuys et al. 1999: Suslow et al, 2001), Furthermore, diferent categories of emotional expres- sion (negative or postive) have been use in the different stodies, "Third, the ability of depressed patints to identity facial expres- sions of milder intensity or those presented for shorter durations remains unexplored. In everyday life, humans process a wide range of emotional stimuli displayed by others, including signals [ess intense than prototypical facial expressions from standardized series or those displayed for brief rather than long durations. Studies using event-related potentials and rapid presentation of facial expressions have demonstrated that healthy paricipants were able to discriminate between emotional and neutral facial expressions presented for durations as brief as 100 to 200 ms Glunghoefer, Bradley, Elbert, & Lang, 2001; Sato, Kochivams, Yoshikawa, & Matsumura, 2001). It has been argued that the recognition of rapid presentations of emotional expressions might, be impuired in depressed patients because of general slowing of cognitive processes (Cooley & Nowicki, 1989). The ability of depressed patients to identity rapid presentations of facial expres- sions remains unexamined, however. ‘Previous finding in healthy participants have also demonstrated that accuracy in recognition of facial expressions decreases as the Intensity of emotional expression displayed in the face is reduced (ex. Calder, Young, Rowland, & Percett, 1997). Iti possible that specific impairments in the identification of subtle changes in emotional expression, rather than in the identification of prototyp= ical displays of emotion, may exist in depressed patients. As noted, intact matching of prototypical displays of emotion has been ‘demonstrated in these patients (Feinberg et al, 1986). There is, therefore, 8 rationale for the examination of the ability of de- pressed patients to identify facial expressions presented for shor ‘durations or depicting milder intensities af emotion, Finally, although there is evidence from previous studies for the presence of impaired recognition aceuracy and a negative response bias to facial expressions in depressed patients, the nature of the ‘lationship between these processes in depressed patients has not been examined, ‘We timed to examine the recognition accuracy of and response bias toward positive and negative facial expressions in patients ‘with unipolar depression and healthy volunteers. We chose happy and sad emotional expressions. reasoning that these emotional splays might be of particular relevance to the negative schemata demonstrated by depressed patients, in partculur, the negative cognitions regarding the abilities ofthe self compared with others (Beck, 1976). It is, therefore, possible that depressed patents identify with displays of sadness, but not happiness, in others. We used happy, neural, and si facial expressions ftom a standardized series (Ekman & Friesen, 1976) presented at different durations and transformed with computer softwate (Facial Expressions of Emotion: Stimuli and Tests; Young, Perret, Calder, Sprengel- meyer, & Fkman, 2002) to depict different intensities of emotion ‘We were interested in examining measures of recog. feuracy and response bias. There are two commonly used ap- proaches to derive these measures: signaletcetion theory, with the discrimination measured’ and the bias measure C(e., Stas law & Todorov, 1999), and the two-high threshold HT) theory with the discrimination accuracy measure Pr and the response bias measure Br (Conwin, 1994). The latter approach is especially useful when numhers of criteria items (targets) and distractrs, ler, as was the case inthe curent study. We, therefore, used the 2HT theory to compute measures of recognition or discrimination accuracy and response bias to happy and sad facial expressions in both groups. In this study, the discrimination accuraey measure represented the ability to discriminate among neueal, happy. and sau expressions. The response bias measure reflected the tendency of participants when uncertain ubout the eategoryto which a facial expression should belong. to eategorize the expression as emo- tional (happy of sad) rater than neutral Findings from previous studies enabled us to make several predictions in depressed patients, Hypothesis I: We predicted 8 negative response bias toward facial expressions such that (a) depressed patients would demonstrate a smaller response bias to happy expressions (e., compared with healthy volunteers, they would les fre= quently identify happy and neutral faces as happy) and (b) depressed patients would have & sreater response bias to sad expressions (ic, compared with healthy volunteers, they \Would more frequently identify sad and neutral faces as sod), Hypothesis 2: We predicted a reduced recognition accuracy ‘of happy and sad favial expressions overall compared with healthy volunteers. Hypothesis 3: We predicted « significantly greater negative response bias and impaired recognition accuracy in response to expressions presented for shorter rather than longer dura- ‘ions and those expressions depiting milder rather than more severe intensities of emotion, Hypothesis 4: We predicted a significant positive corelation between the magnitude of the negative response bias and impairment in recognition accuracy and the severity of de- pression measured by standardized rating scales. Method Participants ‘Tweny-seven patents meeting Diagnostic and Statistica! Manual of Mental Disorders fort edition; Aseria PechiaticAssecation, 1984) eriteria for major depressive disorder were recruited fom inpatient and ‘outpatient services of the Bethlem Royal and Maudsley Hospital. All tients hada chronic, rcurent depressive disorder, and noe was tse I the fist episode of ines, The mean duration of illness (since frst, Material may be protected by copyright law (Title 17, U.S. Code)214 SURGULADZE EF AL. esode ia patens was 10.1 years median duration of ines = 9 yeah [Ava coro! group 29 healthy volunour without» history’ of Upresion were erated fom the local community and from 2 ool of employes a the Institute of Psyehiany. ‘They were matched with paints forage, ender, and educational achievement (Table). Biel approval wa ‘obtained frm the Ftical Comme of the South London and Matisley ‘Trust and Insitute of Pychiany. All paiipants were righthand (Ol field, 1971), Patients were excluded from the study if they reported 3 history of mana. psychosis, alcoholism, o organic brain syomte or if they cored les than 24 onthe Mini-Meatal State Exam Folin, Folin, & Mellagh, 1975). AI! paripunts competed the Recognition Memory ‘Tes-Faces(Watrington, 1984) as a measure of nonemosional fice percep tion. Depressed pints didnot differ significantly from controls inp Torance on this tsk, 436.1) = 1.7, p > 05 (ee Table D All pacipants completed the Beck Depression Inventory (BDI; Bech, ‘Ward, Mendelson, Mock, & Exbaugh. 1961. Controls wih a sore higher, than 9 on the BDI or with a history of depression were excluded fom he ‘iy. The mean BDI soe f the controls was sgrtcamy lower than that ofthe patients. 31.8) = = 122, p< 01. The Hamilton Depression Rating Seale HHAMD; Hamiton, 1960) was also complete for each paint (26 “Table 1). To ensore thatthe experimenter was unawate ofthe depression severity rating of patloats during tak perfomance, these ratings were called afer patients participate ia the task ll patents were taking some ype of antidepressant medication; selective scotonin uptake in hiitors (n= 8), serotonin and noradrealin reuptake inhibitoes(n = 8), ‘moncamine oxidase inhibitors (n= 4, siecle antidepressants (n = 3), nocadenain reuptake init (= 2), mitaapine cn —1) tum (x = 5, and otber mood stabilizers, including caramarepine and Imotiine wd Procedure A facial expression recognition task was developed to present facia expressions at different intensities and fr diferent uso In ths ts atcipans viewed randomized pictures n a computer sereen of 10 fact Table Demographic and Clinical Data Varite Patiems (n= 27) Contos = 29) ‘Mean age (yeas) ™ 69. 430 sD m2 He Gender Female Is na Male 2 2 Education Ww bs 1s sD 2 ness duration (year) a ion sD 83 RMT ™ 387 46 sD 69 42 AMD ” 69 SD 3s abl a 0 a1 SD 99 ase Nowe. RMIT = Recognition Memory Tesi-Faces: HAMD Depression Rating Sele: BDI = Beck Depression Inventor. spe Dh Hsin “emits fom a sadacdlzed series (Yeung eta, 2002), each displaying ‘xpress of bappines, sess, oF neal expressions. Both heppy and ‘al faces wore posemod within the same task t© avoid tsk-dependent ‘sjstomati ears and allow fora det eompyrison of responses Raph and sd faces. Fach emotional fail expression was mowed wig im [UY software with the facial expression ofthe sme invita to depict ‘vo ferent intensities (50% and 100%) of the emaion, ad each Was ‘hen presented vie during the ask: for 100 ms and 2.000 ms. Ta the sane tusk, 10 neural faces were presented at two durations cach: 100 ms and 2,010 ms Paricipats, therfore, viewed 100 stimu during the ‘experiment 10 facial denies, each displaying two emotions, happy and Sa attwo diferent ienstes of emotion and for evo diferent durations. Each face was presented individually. with an interim ineral of 1,500 ms. during the ist 00 ms of which was displayed a fixation ross, Panicipuns were inated that they ould view either emotional (Gal or happy) or acuta faces and were requested to label each fia expression a¢ happy, sa, or acuta hy moving. a computer joystick cordingly in one ofthe Uxee dictions. Before tetng il partipans performed s practice Wilt ensure they were able to perform he tsk Statistical Analysis: Rav: data wor wansfrma ino measures of accuracy and eesponse bias scoring tothe 2HT medel Corvin, 1994), Discrimination secracy was ‘computed for the wo separate subsets of targets (eter sad a apy faces (targets) vs. curl faces fiswactos): Pr ~ (numberof hits + 05) number of targets + 1) ~ (oumber of fake slrms + 0Snumber of sistactes ~ 1), Response bis was computed according to false-lem scores (tendency label u neural face 35 happy oe Sa) i two separate subsets of sad or happy faces sersis neutral faces (sar): r= umber of false alarms + OSioumber of eiseactors + (1 ~ Pr) Discrimination accuracy and response bss values were, therefore, cm ted wit regard o measures of ecngeton ascorcy of metal wells motional facial expression. High accuracy ves woold ince an ability w discriminate acurtely among sad, BappS: end neural expe sons Higher response bas sorss Would indicate eden to msde newwal faces a enetional (either slo happy) Results Response Accuracy Hecause the data were not normally distributed, they were log-iransformed, Log-traasformed scores of response accuracy ‘were entered in 2 X 2 X 2 repeated measures analysis of variance (ANOVA) with emotion (sad, happy), intensity (50% and 100%), and duration (100, 2,000 ms) as within-subject factors and group (patients, controls) as the between-suhject factor. There were sev= ‘ral significant main effects: emotion, FU. 42) ~ 176.1, p< Ols imensity, FU, 42) = 197.7, p < 01; duration, F(1, 42) = 69.2, p< 01; and group, FUN, 42) ~ 26.2, p <.O1. The degrees of freedom are smaller than expected (S4) because of some missing data ‘Comparison of the mean values for diserimination accuracy ‘indicated that in both groups, these significant effects were the result of sad expressions being recognized loss accurately than happy ones, expressions with higher intensity being recognized ‘more accurately than those with lower intensity, and stimuli with longer durations being recognized mote accurately than those with shorter durations. Patients were less accurate overall compared, with contol, Significant interactions were observed for the following: Emo: tion x Group, FUL, 42) 2 7.9, p < 01; Duration % Group, £4, Material may be protected by copyright law (Title 17, U.S. Code)