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Hemispheric Asymmetries in the Perception of Emotional and Neutral Faces
HEMISPHERIC ASYMMETRIES IN THE PERCEPTION OF EMOTIONAL AND NEUTRAL FACES 1 Jennifer McLaren and Susan E. Bryson (Dalhousie University, Halifax, Nova Scotia, Canada)
Attention has focused recently on whether the perception of facial emotion is mediated asymmetrically by the human brain. Most investi gators (e.g., Buchtel, Campari, DeRisio and Rota, 1978; McKeever and Dixon, 1981; Safer, 1981) report a left visual field - right hemisphere (LVF-RH) advantage for the processing of all emotional expressions, with some (Ley and Bryden, 1979; Suberi and McKeever, 1977) claiming that this effect is independent of the well established LVF-RH superiority for face recognition. To date, it remains to be determined whether such findings reflect factors other than the emotion per se. Most studies of perceived emotion have used tasks involving memory (e.g., some variant of a delayed match ing task), higher-order visual processing (as required when categorizing or labelling emotion) and/or short stimulus exposures (e.g., 150 msecs). In related work (see Moscovitch, Scullion and Christie, 1976; Sergent, 1982), each of these has been shown to favour right as opposed to left hemisphere processes. Thus, it is possible that any or all of these factors contribute to, or even account for the previously reported LVF-RH advantage for the perception of emotional expressions. Additional support for this possibility comes from the work of Reuter Lorenz and her colleagues (Reuter-Lorenz and Davidson, 1981; Reuter Lorenz, Givis and Moscovitch, 1983). In their task, the demands on memory and visual analysis were minimized, and relatively long stimulus exposures were used ( -250 msecs). Subjects simply responded to the more emotional of two faces (happy and neutral or sad and neutral) presented simultaneously, one to each visual field. Rather than producing on overall 1 The data presented here were drawn from an M.A. thesis submitted by the first author. A version of this paper was presented at the annual meeting of the Canadian Psychological Asso ciation, Ottawa, June, 1984. This work was supported by grant A-8234 from The Natural Sciences and Engineering Research Council of Canada to S.E. Bryson.
Cortex (1987) 23, 645-654
646
Jennifer McLaren and Susan E. Bryson
LVF-RH superiority, responses were faster to sad faces in the LVF and faster to happy faces in the right visual field (RVF). Such findings have been taken as support for the claim that the two cerebral hemispheres are differentially specialized for the processing of positive and negative emo tion. Evidence from studies using physiological measures (e.g., Dimond and Farrington, 1977) or clinical populations (see Sackheim, Greenberg, Wieman, Gur, Hungerbuhler and Geschwind, 1982, for a review) appear to suggest the same, although in the latter the focus is on the production rather than the perception of facial emotion. An alternative interpretation of the Reuter-Lorenz et al. (1981, 1983) pattern of results is that subjects were simply using different strategies to process positive and negative emotion. Let us assume, for example, that subjects were simply looking for the face whose features were not in repose. Work in our laboratory (McLaren, 1984) suggests that an analytic (or left hemisphere) strategy (Bradshaw and Nettleton, 1981) might be employed to detect single features such as the mouth in happy faces. On the other hand, detection of sad faces might be facilitated by a holistic (or right hemisphere) strategy, since their features more closely resemble those of the neutral faces. These strategies, if employed, would give little information about the perception of emotion per se. The present experiment was designed to explore the possibility that factors other than emotion (e.g., memory, short stimulus exposures) might contribute to the overall LVF-RH advantage generally reported for per ceived emotion. To this end, we followed the methodology of Reuter Lorenz et al. (1981, 1983) by presenting two faces (of the same poser) simultaneously, one to each visual field, for a relatively long period of time. One face showed an emotional expression and the other was neutral; the only difference between the stimuli in each visual field was the emo tional expression. Thus, any visual field asymmetry must be due to the emotion. Rather than responding to the more emotional face, as in the Reuter-Lorenz et al. studies, subjects responded to the face that made them feel better or worse. The intent here was to focus attention on the emotion and not merely 6n particular facial features. Our task has the added advantage of requiring responses to neutral as well as to emotional faces (e.g., to the neutral of neutral-sad and to the happy of neutral-happy, in the "feel-better" condition). Unlike Reuter-Lorenz et al. and, to our knowledge, other investigators of hemispheric asymmetries in perceived emotion, we presented the faces in both their normal and mirror-image orientations. This was to ensure that any perceptual asymmetries did not merely reflect differences in the side of the face that was most expressive (e.g., Campbell, 1978; Heller and Levy, 1981; Sackheim and Gur, 1981). Such controls may be particularly important when using posed emotion (see Thompson, 1985, for a review
Asymmetry in the perception of emotion
647
of the literature on asymmetries of posed vs. spontaneous expressions of emotion). Because depression has been shown to interfere with right hemisphere functioning (Tucker, Stenslie, Roth and Shearer, 1981), we also screened our subjects for current mood. The main question of interest was whether, under conditions com parable to those of Reuter-Lorenz et al., these methodological changes would yield an overall LVF-RH superiority, or differential asymmetries for positive and negative emotion. While minimizing the possible role of factors such as memory, higher-order visual analysis and/or short expo sure durations, there was also an opportunity to evaluate the relative effects of responses to neutral versus emotional expressions. Finally, given the preponderance of sex differences in this (e.g., McKeever and Dixon, 1981; Safer, 1981) and related work (see McGlone, 1980, for a review), we examined the effects of subjects' sex on the perception of laterally presented facial expressions.
MATERIALS AND METHOD
Subjects
Twenty-four students (12 males, 12 females) received credit points toward an introductory psychology course for participating in the experiment. The subjects ranged in age from 17 to 23 years and averaged 18.8 years. Each reported a right foot preference and was strongly right-handed as assessed by Bryden's (1977) handedness questionnaire. All had normal vision and did not require corrective lenses. None scored above 12 on Beck's Depression Inventory (B.D.I.; Beck, Ward, Mendelson, Mock and Erbaugh, 1961), which has been shown to be a valid measure of depression in a university population (Bumberry, Oliver and McClure, 1978).
Stimuli
Slides of faces were from Ekman and Friesen's (1975) pictures of facial affect. A total of eight posers were used. Four of the posers (three male, one female) presented with neutral, sad, open mouth happy (OMH)., and closed mouth happy (CMH) expressions, and the otherfour posers (one male, three female) presented with only neutral, sad, and OMH expressions. The posers and emotional expres sions were essentially the same as those used by Reuter-Lorenz et al. (1983). The faces were photographed in both their normal and mirror-image orien tations. Each emotional face was paired with a neutral face from the same poser. Every possible combination of normal and mirror-image emotional and neutral faces was presented, such that each emotional face appeared four times on each side. Thus, there were 160 slides in all. The slides from two of the posers (one male, one female) with sad and open mouth happy expressions paired with neutral faces were used in practice block of 32 trials.
648
Jennifer McLaren and Susan E. Bryson
The remaining 128 slides were presented in two experimental blocks, each consisting of 64 trials. Each block contained a different random ordering of the slides. The only constraint on randomness was that the emotional face did not appear in the same visual field on more than four consecutive trials. Apparatus and Procedure
The slides were rear projected on to a 50 by 40 em Elmo translucent screen by means of a Kodak carousel projector (Model 860H) and Gerbrand's shutter (Model G-1165). The projected image of each face was 5 by 6.5 em, which subtended 4.1 deg. horizontally when viewed from 70 em. A PDP-11/03 com puter regulated the presentation of stimuli, and recorded latency and accuracy of responses. A photo-electric corneal reflection device was used to monitor eye movements during stimulus presentations. The system was recalibrated before the practice block and each of the experimental blocks. Eye movements which deviated from the fixation point by 0.5 deg. caused a brief tone to sound, providing feedback to the subjects. Trials associated with eye movements were excluded from the analysis. Subjects were seated at a table, opposite the viewing screen in a dimly lit room (luminance 5.5 lux), and were asked to place their chin in a chin rest. They initiated each trial by pressing a foot pedal, while fixating a small central dot on the screen. Following a 250 msecs, warning interval, the slides were presented for 250 msecs such that one face was projected to LVF-RH and the other face to the RVF-LH. Two response keys were positioned side by-side on the table in front of the subject. Subjects attended two separate experimental sessions, one week apart, each lasting approximately one hour. They responded in one session, to the face that made them feel better, and in the other session, to the face that made th~m feel worse (i.e., the sad of sad-neutral and the neutral of neutral-happy). The order of the tasks was counterbalanced. Half the subjects of each sex responded with the middle and index fingers of their right hand; the other half used their left hand. They indicated their choice by pressing the appropriate key with the finger corresponding to the side of the selected stimuli. Subjects were encouraged to respond as quickly but as accurately as possible, and were given 32 practice trials before each of the experimentals sessions. RESULTS
In this experiment subjects responded to faces which made them feel better or worse. In both cases, responses were made to neutral as well as to emotional faces (e.g., in the "worse" condition, to the sad of neutral-sad and to the neutral of neutral-happy). In order to compare responses to neutral and emotional faces, mean reaction time and accuracy scores to all neutral and to all emotional faces in each visual field were computed for each subject. A four-way analysis of variance was then carried out on both reaction time and accuracy data. Sex and response hand were between
Asymmetry in the perception of emotion
649
subject variables, and stimulus-type (emotional or neutral) and visual field of target stimulus (i.e., the "correct" stimuli for the given task) were repeated measures. Overall, responses were faster to emotional faces (783 msecs) than to neutral ones (852 msecs), F = 24.61; d.f. = 1, 20; p < .001. There was also amain effect ofvisualfieldin both reaction time(F = 7.84; d.f. = 1, 20; p <.05) and accuracy (F = 5.71; d.f. = 1, 20; p <.01). Performance was better when the target face was presented to the LVF (805 msecs, 85%, vs. 831 msecs, 81%, for the RVF). In addition, each analysis showed a sig nificant interaction between stimulus-type and visual field (F = 23.65; d.f. = 1, 20; p <.001; and F = 22.84; d.f. = 1, 20; p <.001 for reaction time and accuracy, respectively). Responses were both faster and more accurate to emotional faces presented in the LVF (738 msecs, 90%; RVF = 828 msecs, 78%) and to neutral faces presented in the RVF (834 msecs, 85%; LVF = 871 msecs, 80%). Data from responses to emotional faces were then analyzed separately from those to neutral faces. The purpose was to clarify the interaction of stimulus-type by visual field, and to examine the effects of positive versus negative emotion. Figure 1 shows
-LVF
~RVF
iE
Responses to emotional faces
~ SAO
Fig. 1 - Mean reaction times and accuracy of res· ponses to sad, open mouth happy (OMH) and closed mouth happy (CMH) faces by visual field, and to neutral faces by emotional compari son and visualfield. (Note that the sad, neutral (OMH), and neutral (CMH) data were generated by the ''feel worse" condition and the OMH, CMH, and neutral (sad) data by the ''feel better" condi tion.)
8 :H
a:H
0. -
-
••
Responses to neutral faces
NEUTRAL (SAO)
NEUTRAL (OMH)
NEUTRAL (CMH)
REACTION TIMES AND ACCURACY
650
Jennifer McLaren and Susan E. Bryson
the mean reaction time and accuracy scores for each emotional compar ison (i.e. the type of emotional expression paired with the neutral face) and visual field. Separate five-way analyses of variance were performed on these data, with sex, order of task and response hand as between subject variables, and emotional comparison and visual field as repeated measures. Tukey's tests were used for post-hoc analysis of all significant interactions. Responses to Emotional Faces
A main effect of visual field was found for both reaction time (F = 37.60; d.f. = 1, 20; p<.Ol) and accuracy (F = 24.61; d.f, = 1, 20; p <.01). Responses to emotional faces in the LVF were faster (738 msecs) and more accurate (90.3%) than to those in the RVF (828 msecs, 77.5%) This finding obtained for all emotions except OMH, for which there appears to be a ceiling effect. As with previous work (Strauss and Mos covitch, 1981; Reuter-Lorenzetal., 1983; DudaandBrown, 1984),0MH faces were recognized faster and more accurately than the other expres sions, and thus seemed to be easier to distinguish. Responses to sad faces were less accurate than those to CMH faces, indicating that sad faces were the most difficult to discriminate from neutral ones. Overall then, res ponses to emotional faces showed no evidence of differential asymmetries for happy and sad expressions. Both were processed better in the LVF. Further support for this is provided by the only other test which reached significance. Analysis of reaction time to emotional faces rev ealed an interaction between response hand and visual field (F = 4.52; d.f. = 1, 20; p <.05). These scores (excluding left hand responding males who showed no visual field asymmetry), in order from fastest to slowest, were LVF-left hand response (721 msecs), LVF-right hand response (755 msecs), RVF-left hand response (780 msecs), and RVF-right hand res ponse (875 msecs). Suberi and McKeever's (1977) model predicts this ordering when all stimuli are processed by the RH and responses are primarily controlled by either the right or left hemisphere. For example, stimuli presented to the LVF are projected to and processed by the RH, which in tum initiates left hand responses; under these same conditions, right hand responses would require a subsequent transfer to the LH, and thus more processing time. To summarize the main findings, responses were both faster and more accurate to emotional faces in the LVF. This effect obtained for both positive (happy) and negative (sad) expressions, and for both male and female subjects. The data also suggest that independent of the responding hand, all emotional stimuli were selectively processed by the RH.
Asymmetry in the perception of emotion
651
Responses to Neutral Faces
Analysis of neutral face responses yielded a main effect of visual field in reaction time (F = 4.49; d.f. = 1, 20; p < .05). Responses to neutral faces in the RVF (834 msecs) were faster than to those in the LVF (870 msecs). The accuracy data also showed a non-significant trend (F = 3.95; d.f. = 1, 20; p < .1) toward superior responding to the RVF (84.7%, LVF = 80%). These findings are consistent with those for emotional faces, in that responses were superior when the emotional stimuli were presented to the LVF, although in this case subjects were not responding to the emotional expressions. In addition, and also consistent with the data for emotional faces, a main effect of emotional comparison for reaction time (F = 24.96; d.f. = 2, 40; p < .01) and for accuracy (F = 45.34; d.f. = 2, 40; p <.01) revealed that responses to neutral faces paired with OMH faces were superior to those paired with either CMH or sad faces. DISCUSSION
This study was designed to investigate further the hemispheric asym metries reported for the perception of facial emotion. The main question of interest was whether the LVF-RH superiority commonly found reflects the emotion per se, or other factors known to favour RH processes (Moscovitch, Scullion and Christie, 1976; Sergent, 1982). To this end, our task had no memory component, and relatively long stimulus exposure durations were used (250 msecs). Two faces (happy or sad paired with neutral) were presented simultaneously, one to each visual field, and subjects simply responded to the one that made them feel either better or worse. This task not only encourages attention to the emotion itself (rather than merely to particular facial features), but has the added advantage of requiring responses to neutral as well as to emotional faces. The main finding was that a LVF-RH advantage obtained for emo tional faces regardless of the type of emotion expressed, and in both the "better" and "worse" conditions. Furthermore, there was a systematic ordering of visual field and response hand latencies, with LVF-left hand being fastest and RVF-right hand being slowest. This constitutes strong evidence for the conclusion that all emotional stimuli were being pro cessed by the RH (Suberi and McKeever, 1977). The present findings extend earlier reports of a LVF-RH superiority for perceived emotion (e.g., Buchtel, Campari, DeRisio and Rota, 1978; Hirshman and Safer, 1982; Ley and Bryden, 1979; Suberi and McKeever, 1977) by showing that this effect persists despite the use of a methodology less favourable to
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Jennifer McLaren and Susan E. Bryson
the RH. In addition, the finding of a RVF advantage for neutral faces indicates that the LVF effect for emotional faces is due to the emotional expressions and not merely to the faces themselves. In fact, the RVF superiority for neutral faces may be a product of the LVF advantage for emotional faces (when there was a neutral face in the RVF there was an emotional face in the LVF). This interpretation is consistent with previous reports that emotional faces produce a stronger LVF advantage than neutral faces (Ley and Bryden, 1979; Suberi and McKeever, 1977). Additional support for this comes from our finding that responses to neutral faces were slower than those to emotional faces. This suggests that subjects first find the emotional face, and are faster when it satisfies the response criterion (e.g., happy face when responding to what makes them feel better) than when they must switch and respond to the neutral face (paired with sad when responding to what makes them feel better). Despite the similarity in methodology, we did not replicate the Reuter Lorenz et al. (1981, 1983) finding of differential VF asymmetries for positive and negative emotion (i.e., RVF for happy faces and LVF for sad faces). Our methodology differed from theirs in only two respects. Sub jects responded to the face that made them feel better or worse (rather than to the more emotional face), and we used mirror-image as well as normally oriented stimuli. Current work in our laboratory indicates that it is essential to include mirror-image faces to control for asymmetries in the expression of emotion. Indeed, VF asymmetries which have been attri buted to hemispheric differences may actually reflect asymmetries in the stimuli (Bryson, McLaren, Wadden and MacLean, in preparation). In summary, the results of this experiment provide strong support for the conclusion that all emotional expressions are processed better by the RH. Despite the use of a methodology less biased toward RH functioning, a LVF-RH advantage obtained for the perception of both positive and negative emotions, and regardless of whether subjects were looking for what made them feel bett~r or worse. ABSTRACf
This study was designed to investigate hemispheric asymmetries in the per ception of both positive and negative emotion, while minimizing extraneous factors known to favour right hemisphere processes. Pairs of faces (happy-neutral or sad-neutral) were presented, one to each visual field, and subjects responded to the face that made them feel either better or worse. Performance was superior when th~ emotional faces were presented to the left visual field- right hemisphere. This occurred in both the better and the worse conditions, and for both sexes. Indeed, the data indicate that all emotional stimuli were being processed by the right hemisphere, and that the effect for emotional faces is due to the expressions and not merely the faces themselves.
Asymmetry in the perception of emotion
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REFERENCES
BECK, A.T., WARD, C.H., MENDELSON, M., MOCK, J., and ERBAUGH, J. An inventory for measuring depression. Archives of General Psychiatry, 4: 53-63, 1961. BRADSHAW, J.L., and NETILETON, N.C. The nature of hemispheric specialization in man. Behavioral and Brain Sciences, 4: 51-91, 1981. BRYDEN, M.P. Measuring handedness with questionnaires. Neuropsychologia; 15: 617 624, 1977. BUCHTEL, H.A., CAMPARI, F., DERISIO, C., and ROTA, R. Hemispheric differences in discriminative reaction time to facial expressions. Italian Journal of Psychology, 5: 159-169, 1978. BUMBERRY, W., OLIVER, J.M., and McCLURE, J.N .. Validation of the Beck Depression Inventory in a university population using psychiatric estimate as the criterion. Journal of Consulting and Clinical Psychology, 46: 150-155, 1978. CAMPBELL, R. Asymmetries in interpreting and expressing a posed facial expression. Cortex, 14: 327-342, 1978. DIMOND, S.J., and FARRINGTON, L. Emotional responses to films shown to the right or left hemisphere of the brain measured by heart rate. Acta Psychologica, 41: 255-260, 1977. DUDA, P., and BROWN, J. Lateral asymmetry of positive and negative emotions. Cortex, 20: 253-261, 1984. EKMAN, P., and FRIESEN, W. Pictures of Facial Affect. Palo Alto, CA.: Consulting Psy . chologists, 1976. HELLER, W., and LEVY, J. Perception and expression of emotion in right-handers and left-handers. Neuropsychologia; 19: 263-272, 1981. HIRSHMAN, R.S., and SAFER, M.A. Hemisphere differences in perceiving positive and negative emotions. Cortex; 18: 569-580, 1982. LEY, R.G., and BRYDEN, M.P. Hemispheric differences in processing emotions and faces. Brain and Language, 7: 127-138, 1979. McGLONE, J. Sex differences in human brain organization: A critical survey. The Behav ioral and Brain Sciences; 3: 215-227, 1980. McKEEVER, W.F., and DIXON, M.S. Right-hemisphere superiority for discriminating memorized from non-memorized faces: Affective imagery, sex, and perceived emo tionality effects. Brain and Language, 12: 246-260, 1981. MCLAREN J. Hemispheric asymmetries in the perception of emotional faces: Effects of sex and task demands. Unpublished master's thesis, Dalhousie University, Halifax, Nova Scotia, Canada, 1984. MOSCOVITCH, M., SCULLION, D., and CHRISTIE, D. Early versus late stages of processing and their relation to functional hemispheric asymmetries in face recognition. Journal of Experimental Psychology: Human Perception and Performance, 2: 401-416, 1976. REUTER-LORENZ, P., and DAVIDSON, R.J. Differential contributions of the two cerebral hemispheres to the perception of happy and sad faces. N europsychologia, 19: 609-614, 1981. REUTER-LORENZ, P., GIVIS, R.P., and MOSCOVITCH, M. Hemispheric specialization and the perception of emotion: Evidence from right-handers and from inverted and non-inverted 1eft-handers. Neuropsychologia, 21: 687-692, 1983. SACKEIM, H.A., GREENBERG, M.S., WEIMAN, A.L., GUR, R.C., HUNGERBUHLER, J.P., and GESCHWIND, N. Hemispheric asymmetry in the expression of positive and nega tive emotions. Archives of Neurology, 39: 210-218, 1982. SACKEIM, H.A., and GuR, R.C. Lateral asymmetry in intensity of emotional expression. Neuropsychologia, 16: 473-482, 1978. SAFER, M.A. Sex and hemisphere differences in access to codes for processing emotional expressions and faces. Journal of Experimental Psychology: General, 100: 86-100, 1981. SERGENT, J. Theoretical and methodological consequences of variations in exposure duration in visual laterality studies. Perception and Psychophysics, 5: 451-461, 1982.
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STRAUSS, E., and MoscOVITCH, M. Perception of facial expression. Brain and Language, 13: 308-332, 1981. SUBER!, M., and McKEEVER, W.F. Differential right hemisphere memory storage of emotional and non-emotional faces. Neuropsychologia; 5: 757-768, 1977. THOMPSON, J.K. Right brain, left brain, left face, right face: Hemispherity and the expression of facial emotion. Cortex, 21: 281-299, 1985. TuCKER, D.M., STENSLIE, C.E., RoTH, R.S., and SHEARER, S.L. Right frontal lobe acti..: vation and right hemisphere performance. Archives ofGeneral Psychiatry; 38: 169-174, 1981. Jennifer McLaren, Department of Psychology, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4Jl.
Attention has focused recently on whether the perception of facial emotion is mediated asymmetrically by the human brain. Most investi gators (e.g., Buchtel, Campari, DeRisio and Rota, 1978; McKeever and Dixon, 1981; Safer, 1981) report a left visual field - right hemisphere (LVF-RH) advantage for the processing of all emotional expressions, with some (Ley and Bryden, 1979; Suberi and McKeever, 1977) claiming that this effect is independent of the well established LVF-RH superiority for face recognition. To date, it remains to be determined whether such findings reflect factors other than the emotion per se. Most studies of perceived emotion have used tasks involving memory (e.g., some variant of a delayed match ing task), higher-order visual processing (as required when categorizing or labelling emotion) and/or short stimulus exposures (e.g., 150 msecs). In related work (see Moscovitch, Scullion and Christie, 1976; Sergent, 1982), each of these has been shown to favour right as opposed to left hemisphere processes. Thus, it is possible that any or all of these factors contribute to, or even account for the previously reported LVF-RH advantage for the perception of emotional expressions. Additional support for this possibility comes from the work of Reuter Lorenz and her colleagues (Reuter-Lorenz and Davidson, 1981; Reuter Lorenz, Givis and Moscovitch, 1983). In their task, the demands on memory and visual analysis were minimized, and relatively long stimulus exposures were used ( -250 msecs). Subjects simply responded to the more emotional of two faces (happy and neutral or sad and neutral) presented simultaneously, one to each visual field. Rather than producing on overall 1 The data presented here were drawn from an M.A. thesis submitted by the first author. A version of this paper was presented at the annual meeting of the Canadian Psychological Asso ciation, Ottawa, June, 1984. This work was supported by grant A-8234 from The Natural Sciences and Engineering Research Council of Canada to S.E. Bryson.
Cortex (1987) 23, 645-654
646
Jennifer McLaren and Susan E. Bryson
LVF-RH superiority, responses were faster to sad faces in the LVF and faster to happy faces in the right visual field (RVF). Such findings have been taken as support for the claim that the two cerebral hemispheres are differentially specialized for the processing of positive and negative emo tion. Evidence from studies using physiological measures (e.g., Dimond and Farrington, 1977) or clinical populations (see Sackheim, Greenberg, Wieman, Gur, Hungerbuhler and Geschwind, 1982, for a review) appear to suggest the same, although in the latter the focus is on the production rather than the perception of facial emotion. An alternative interpretation of the Reuter-Lorenz et al. (1981, 1983) pattern of results is that subjects were simply using different strategies to process positive and negative emotion. Let us assume, for example, that subjects were simply looking for the face whose features were not in repose. Work in our laboratory (McLaren, 1984) suggests that an analytic (or left hemisphere) strategy (Bradshaw and Nettleton, 1981) might be employed to detect single features such as the mouth in happy faces. On the other hand, detection of sad faces might be facilitated by a holistic (or right hemisphere) strategy, since their features more closely resemble those of the neutral faces. These strategies, if employed, would give little information about the perception of emotion per se. The present experiment was designed to explore the possibility that factors other than emotion (e.g., memory, short stimulus exposures) might contribute to the overall LVF-RH advantage generally reported for per ceived emotion. To this end, we followed the methodology of Reuter Lorenz et al. (1981, 1983) by presenting two faces (of the same poser) simultaneously, one to each visual field, for a relatively long period of time. One face showed an emotional expression and the other was neutral; the only difference between the stimuli in each visual field was the emo tional expression. Thus, any visual field asymmetry must be due to the emotion. Rather than responding to the more emotional face, as in the Reuter-Lorenz et al. studies, subjects responded to the face that made them feel better or worse. The intent here was to focus attention on the emotion and not merely 6n particular facial features. Our task has the added advantage of requiring responses to neutral as well as to emotional faces (e.g., to the neutral of neutral-sad and to the happy of neutral-happy, in the "feel-better" condition). Unlike Reuter-Lorenz et al. and, to our knowledge, other investigators of hemispheric asymmetries in perceived emotion, we presented the faces in both their normal and mirror-image orientations. This was to ensure that any perceptual asymmetries did not merely reflect differences in the side of the face that was most expressive (e.g., Campbell, 1978; Heller and Levy, 1981; Sackheim and Gur, 1981). Such controls may be particularly important when using posed emotion (see Thompson, 1985, for a review
Asymmetry in the perception of emotion
647
of the literature on asymmetries of posed vs. spontaneous expressions of emotion). Because depression has been shown to interfere with right hemisphere functioning (Tucker, Stenslie, Roth and Shearer, 1981), we also screened our subjects for current mood. The main question of interest was whether, under conditions com parable to those of Reuter-Lorenz et al., these methodological changes would yield an overall LVF-RH superiority, or differential asymmetries for positive and negative emotion. While minimizing the possible role of factors such as memory, higher-order visual analysis and/or short expo sure durations, there was also an opportunity to evaluate the relative effects of responses to neutral versus emotional expressions. Finally, given the preponderance of sex differences in this (e.g., McKeever and Dixon, 1981; Safer, 1981) and related work (see McGlone, 1980, for a review), we examined the effects of subjects' sex on the perception of laterally presented facial expressions.
MATERIALS AND METHOD
Subjects
Twenty-four students (12 males, 12 females) received credit points toward an introductory psychology course for participating in the experiment. The subjects ranged in age from 17 to 23 years and averaged 18.8 years. Each reported a right foot preference and was strongly right-handed as assessed by Bryden's (1977) handedness questionnaire. All had normal vision and did not require corrective lenses. None scored above 12 on Beck's Depression Inventory (B.D.I.; Beck, Ward, Mendelson, Mock and Erbaugh, 1961), which has been shown to be a valid measure of depression in a university population (Bumberry, Oliver and McClure, 1978).
Stimuli
Slides of faces were from Ekman and Friesen's (1975) pictures of facial affect. A total of eight posers were used. Four of the posers (three male, one female) presented with neutral, sad, open mouth happy (OMH)., and closed mouth happy (CMH) expressions, and the otherfour posers (one male, three female) presented with only neutral, sad, and OMH expressions. The posers and emotional expres sions were essentially the same as those used by Reuter-Lorenz et al. (1983). The faces were photographed in both their normal and mirror-image orien tations. Each emotional face was paired with a neutral face from the same poser. Every possible combination of normal and mirror-image emotional and neutral faces was presented, such that each emotional face appeared four times on each side. Thus, there were 160 slides in all. The slides from two of the posers (one male, one female) with sad and open mouth happy expressions paired with neutral faces were used in practice block of 32 trials.
648
Jennifer McLaren and Susan E. Bryson
The remaining 128 slides were presented in two experimental blocks, each consisting of 64 trials. Each block contained a different random ordering of the slides. The only constraint on randomness was that the emotional face did not appear in the same visual field on more than four consecutive trials. Apparatus and Procedure
The slides were rear projected on to a 50 by 40 em Elmo translucent screen by means of a Kodak carousel projector (Model 860H) and Gerbrand's shutter (Model G-1165). The projected image of each face was 5 by 6.5 em, which subtended 4.1 deg. horizontally when viewed from 70 em. A PDP-11/03 com puter regulated the presentation of stimuli, and recorded latency and accuracy of responses. A photo-electric corneal reflection device was used to monitor eye movements during stimulus presentations. The system was recalibrated before the practice block and each of the experimental blocks. Eye movements which deviated from the fixation point by 0.5 deg. caused a brief tone to sound, providing feedback to the subjects. Trials associated with eye movements were excluded from the analysis. Subjects were seated at a table, opposite the viewing screen in a dimly lit room (luminance 5.5 lux), and were asked to place their chin in a chin rest. They initiated each trial by pressing a foot pedal, while fixating a small central dot on the screen. Following a 250 msecs, warning interval, the slides were presented for 250 msecs such that one face was projected to LVF-RH and the other face to the RVF-LH. Two response keys were positioned side by-side on the table in front of the subject. Subjects attended two separate experimental sessions, one week apart, each lasting approximately one hour. They responded in one session, to the face that made them feel better, and in the other session, to the face that made th~m feel worse (i.e., the sad of sad-neutral and the neutral of neutral-happy). The order of the tasks was counterbalanced. Half the subjects of each sex responded with the middle and index fingers of their right hand; the other half used their left hand. They indicated their choice by pressing the appropriate key with the finger corresponding to the side of the selected stimuli. Subjects were encouraged to respond as quickly but as accurately as possible, and were given 32 practice trials before each of the experimentals sessions. RESULTS
In this experiment subjects responded to faces which made them feel better or worse. In both cases, responses were made to neutral as well as to emotional faces (e.g., in the "worse" condition, to the sad of neutral-sad and to the neutral of neutral-happy). In order to compare responses to neutral and emotional faces, mean reaction time and accuracy scores to all neutral and to all emotional faces in each visual field were computed for each subject. A four-way analysis of variance was then carried out on both reaction time and accuracy data. Sex and response hand were between
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subject variables, and stimulus-type (emotional or neutral) and visual field of target stimulus (i.e., the "correct" stimuli for the given task) were repeated measures. Overall, responses were faster to emotional faces (783 msecs) than to neutral ones (852 msecs), F = 24.61; d.f. = 1, 20; p < .001. There was also amain effect ofvisualfieldin both reaction time(F = 7.84; d.f. = 1, 20; p <.05) and accuracy (F = 5.71; d.f. = 1, 20; p <.01). Performance was better when the target face was presented to the LVF (805 msecs, 85%, vs. 831 msecs, 81%, for the RVF). In addition, each analysis showed a sig nificant interaction between stimulus-type and visual field (F = 23.65; d.f. = 1, 20; p <.001; and F = 22.84; d.f. = 1, 20; p <.001 for reaction time and accuracy, respectively). Responses were both faster and more accurate to emotional faces presented in the LVF (738 msecs, 90%; RVF = 828 msecs, 78%) and to neutral faces presented in the RVF (834 msecs, 85%; LVF = 871 msecs, 80%). Data from responses to emotional faces were then analyzed separately from those to neutral faces. The purpose was to clarify the interaction of stimulus-type by visual field, and to examine the effects of positive versus negative emotion. Figure 1 shows
-LVF
~RVF
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Responses to emotional faces
~ SAO
Fig. 1 - Mean reaction times and accuracy of res· ponses to sad, open mouth happy (OMH) and closed mouth happy (CMH) faces by visual field, and to neutral faces by emotional compari son and visualfield. (Note that the sad, neutral (OMH), and neutral (CMH) data were generated by the ''feel worse" condition and the OMH, CMH, and neutral (sad) data by the ''feel better" condi tion.)
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Responses to neutral faces
NEUTRAL (SAO)
NEUTRAL (OMH)
NEUTRAL (CMH)
REACTION TIMES AND ACCURACY
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the mean reaction time and accuracy scores for each emotional compar ison (i.e. the type of emotional expression paired with the neutral face) and visual field. Separate five-way analyses of variance were performed on these data, with sex, order of task and response hand as between subject variables, and emotional comparison and visual field as repeated measures. Tukey's tests were used for post-hoc analysis of all significant interactions. Responses to Emotional Faces
A main effect of visual field was found for both reaction time (F = 37.60; d.f. = 1, 20; p<.Ol) and accuracy (F = 24.61; d.f, = 1, 20; p <.01). Responses to emotional faces in the LVF were faster (738 msecs) and more accurate (90.3%) than to those in the RVF (828 msecs, 77.5%) This finding obtained for all emotions except OMH, for which there appears to be a ceiling effect. As with previous work (Strauss and Mos covitch, 1981; Reuter-Lorenzetal., 1983; DudaandBrown, 1984),0MH faces were recognized faster and more accurately than the other expres sions, and thus seemed to be easier to distinguish. Responses to sad faces were less accurate than those to CMH faces, indicating that sad faces were the most difficult to discriminate from neutral ones. Overall then, res ponses to emotional faces showed no evidence of differential asymmetries for happy and sad expressions. Both were processed better in the LVF. Further support for this is provided by the only other test which reached significance. Analysis of reaction time to emotional faces rev ealed an interaction between response hand and visual field (F = 4.52; d.f. = 1, 20; p <.05). These scores (excluding left hand responding males who showed no visual field asymmetry), in order from fastest to slowest, were LVF-left hand response (721 msecs), LVF-right hand response (755 msecs), RVF-left hand response (780 msecs), and RVF-right hand res ponse (875 msecs). Suberi and McKeever's (1977) model predicts this ordering when all stimuli are processed by the RH and responses are primarily controlled by either the right or left hemisphere. For example, stimuli presented to the LVF are projected to and processed by the RH, which in tum initiates left hand responses; under these same conditions, right hand responses would require a subsequent transfer to the LH, and thus more processing time. To summarize the main findings, responses were both faster and more accurate to emotional faces in the LVF. This effect obtained for both positive (happy) and negative (sad) expressions, and for both male and female subjects. The data also suggest that independent of the responding hand, all emotional stimuli were selectively processed by the RH.
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Responses to Neutral Faces
Analysis of neutral face responses yielded a main effect of visual field in reaction time (F = 4.49; d.f. = 1, 20; p < .05). Responses to neutral faces in the RVF (834 msecs) were faster than to those in the LVF (870 msecs). The accuracy data also showed a non-significant trend (F = 3.95; d.f. = 1, 20; p < .1) toward superior responding to the RVF (84.7%, LVF = 80%). These findings are consistent with those for emotional faces, in that responses were superior when the emotional stimuli were presented to the LVF, although in this case subjects were not responding to the emotional expressions. In addition, and also consistent with the data for emotional faces, a main effect of emotional comparison for reaction time (F = 24.96; d.f. = 2, 40; p < .01) and for accuracy (F = 45.34; d.f. = 2, 40; p <.01) revealed that responses to neutral faces paired with OMH faces were superior to those paired with either CMH or sad faces. DISCUSSION
This study was designed to investigate further the hemispheric asym metries reported for the perception of facial emotion. The main question of interest was whether the LVF-RH superiority commonly found reflects the emotion per se, or other factors known to favour RH processes (Moscovitch, Scullion and Christie, 1976; Sergent, 1982). To this end, our task had no memory component, and relatively long stimulus exposure durations were used (250 msecs). Two faces (happy or sad paired with neutral) were presented simultaneously, one to each visual field, and subjects simply responded to the one that made them feel either better or worse. This task not only encourages attention to the emotion itself (rather than merely to particular facial features), but has the added advantage of requiring responses to neutral as well as to emotional faces. The main finding was that a LVF-RH advantage obtained for emo tional faces regardless of the type of emotion expressed, and in both the "better" and "worse" conditions. Furthermore, there was a systematic ordering of visual field and response hand latencies, with LVF-left hand being fastest and RVF-right hand being slowest. This constitutes strong evidence for the conclusion that all emotional stimuli were being pro cessed by the RH (Suberi and McKeever, 1977). The present findings extend earlier reports of a LVF-RH superiority for perceived emotion (e.g., Buchtel, Campari, DeRisio and Rota, 1978; Hirshman and Safer, 1982; Ley and Bryden, 1979; Suberi and McKeever, 1977) by showing that this effect persists despite the use of a methodology less favourable to
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the RH. In addition, the finding of a RVF advantage for neutral faces indicates that the LVF effect for emotional faces is due to the emotional expressions and not merely to the faces themselves. In fact, the RVF superiority for neutral faces may be a product of the LVF advantage for emotional faces (when there was a neutral face in the RVF there was an emotional face in the LVF). This interpretation is consistent with previous reports that emotional faces produce a stronger LVF advantage than neutral faces (Ley and Bryden, 1979; Suberi and McKeever, 1977). Additional support for this comes from our finding that responses to neutral faces were slower than those to emotional faces. This suggests that subjects first find the emotional face, and are faster when it satisfies the response criterion (e.g., happy face when responding to what makes them feel better) than when they must switch and respond to the neutral face (paired with sad when responding to what makes them feel better). Despite the similarity in methodology, we did not replicate the Reuter Lorenz et al. (1981, 1983) finding of differential VF asymmetries for positive and negative emotion (i.e., RVF for happy faces and LVF for sad faces). Our methodology differed from theirs in only two respects. Sub jects responded to the face that made them feel better or worse (rather than to the more emotional face), and we used mirror-image as well as normally oriented stimuli. Current work in our laboratory indicates that it is essential to include mirror-image faces to control for asymmetries in the expression of emotion. Indeed, VF asymmetries which have been attri buted to hemispheric differences may actually reflect asymmetries in the stimuli (Bryson, McLaren, Wadden and MacLean, in preparation). In summary, the results of this experiment provide strong support for the conclusion that all emotional expressions are processed better by the RH. Despite the use of a methodology less biased toward RH functioning, a LVF-RH advantage obtained for the perception of both positive and negative emotions, and regardless of whether subjects were looking for what made them feel bett~r or worse. ABSTRACf
This study was designed to investigate hemispheric asymmetries in the per ception of both positive and negative emotion, while minimizing extraneous factors known to favour right hemisphere processes. Pairs of faces (happy-neutral or sad-neutral) were presented, one to each visual field, and subjects responded to the face that made them feel either better or worse. Performance was superior when th~ emotional faces were presented to the left visual field- right hemisphere. This occurred in both the better and the worse conditions, and for both sexes. Indeed, the data indicate that all emotional stimuli were being processed by the right hemisphere, and that the effect for emotional faces is due to the expressions and not merely the faces themselves.
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STRAUSS, E., and MoscOVITCH, M. Perception of facial expression. Brain and Language, 13: 308-332, 1981. SUBER!, M., and McKEEVER, W.F. Differential right hemisphere memory storage of emotional and non-emotional faces. Neuropsychologia; 5: 757-768, 1977. THOMPSON, J.K. Right brain, left brain, left face, right face: Hemispherity and the expression of facial emotion. Cortex, 21: 281-299, 1985. TuCKER, D.M., STENSLIE, C.E., RoTH, R.S., and SHEARER, S.L. Right frontal lobe acti..: vation and right hemisphere performance. Archives ofGeneral Psychiatry; 38: 169-174, 1981. Jennifer McLaren, Department of Psychology, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4Jl.