Motiv Emot (2009) 33:106–112 DOI 10.1007/s11031-009-9121-9
ORIGINAL PAPER
Influence of emotional expression on the processing of gaze direction Reginald B. Adams Jr. Æ Robert G. Franklin Jr.
Published online: 20 February 2009 Ó Springer Science+Business Media, LLC 2009
Abstract Research demonstrates an influence of gaze direction in emotion recognition. Here we examined whether facial affect similarly influences recognition of gaze direction. Across two studies we found that averted relative to direct gaze was processed more quickly and accurately when coupled with fear, and direct relative to averted gaze with anger. Also evident was that slower overall gaze processing was associated with increased interaction effects between emotion and gaze. Examining individual differences, therefore, enabled us to extend previous research examining speed of processing as a moderator of the interaction effect, while holding constant task demands and stimulus features. Unexpectedly, a main effect emerged such that averted relative to direct gaze was found to be processed more quickly and accurately overall. This effect was not moderated by processing speed and is discussed as a potential stimulus-driven effect that may help explain discrepant findings in the literature. Keywords Eye gaze Emotional expression Individual differences Interdependence
Folklore would have it that ‘‘the eyes are the windows to the soul.’’ Scientists seem to agree, finding that the processing of eye gaze information plays a pivotal role in the development of Theory of Mind (Baron-Cohen 1995), and more recently an important role in the processing and decoding of basic emotional displays (e.g., Adams and Kleck 2003, 2005; Ganel et al. 2005; Graham and LaBar R. B. Adams Jr. (&) R. G. Franklin Jr. The Pennsylvania State University, 438 Moore Building, University Park, PA 16802, USA e-mail:
[email protected]
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2007; Hess et al. 2007; Sander et al. 2007). Surprisingly, little research has examined the role of perceived emotional expression on the detection and processing of gaze direction. The human attraction to the eyes is arguably innately prepared (Argyle 1967; Baron-Cohen 1995). The eyes capture significantly more attention than other areas of the face in both adults (Janik et al. 1978) and infants (Farroni et al. 2002). The region around the eyes is associated with complex musculature changes during the expression of emotion, including upper and lower eyelid and eyebrow position (Ekman and Friesen 1975). Not surprisingly then, emotions can be accurately decoded from just the eye region of the face alone (Baron-Cohen 1995; Nummenmaa 1964). Although the work cited above indicates that the eyes may ‘‘have it’’ with regard to emotion recognition, until recently little work actually examined the influence of eye behavior in the communication of emotion. In addition to the facial musculature around the eyes, the eyes can yield tear secretion, pupil dilation, and eyeball movements, all of which may play an integral role in the expression of emotion. Given our natural attraction to the eyes, it stands to reason that even slight changes in the behavior of the eyes might exert a powerful impact on how we process and perceive facial emotion. Indeed, despite mere millimeter shifts in irises indicating visual attention, eye gaze behavior is a highly salient and informative social signal, and by far the most studied behavior of the eyes in social perception.
Shared signal hypothesis Recent evidence demonstrates a meaningful impact of eye gaze on decoding emotional expressions. Both emotion and eye gaze behaviors are associated with underlying
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motivational orientations to approach or avoid. This insight gave rise to the ‘‘shared signal hypothesis’’ (Adams and Kleck 2003, 2005; Adams et al. 2006), which predicts that when paired, social cues that share a congruent signal value should be processed more efficiently. Research has corroborated this hypothesis in terms of the role of gaze on emotion processing. Using speeded reaction time tasks and self-reported perception of emotional intensity, Adams and Kleck (2003, 2005) found that direct gaze facilitated processing and increased the perceived intensity of facially communicated approach-oriented emotions (e.g., anger and joy). Likewise, averted gaze facilitated facially communicated avoidance-oriented emotions (e.g., fear and sadness). These effects were recently replicated by Sander et al. (2007) using dynamic threat displays. Similarly, Hess et al. (2007) found that direct relative to averted anger expressions and averted relative to direct fear expressions elicited more reported negative psychological responses in observers. In general, mounting evidence supports interdependency in the processing of eye gaze and emotion, using psychophysical, self-report ratings, and neuroimaging paradigms (e.g., Ganel et al. 2005; Graham and LaBar 2007; Hadjikhani et al. 2008; Holmes et al. 2006; Hori et al. 2005; Mathews et al. 2003; Putman et al. 2006; Sato et al. 2004; Tipples 2006), and demonstrates compound cue interactions (Fox et al. 2007; Graham and LaBar 2007; Sander et al. 2007; Klucharev and Sams 2004; Sato et al. 2004; Yoshikawa and Sato 2000). One other theoretical explanation predicts this same pattern, namely attentional appraisal. Direct eye gaze along with other environmental cues can serve to alert the perceiver to potential aggression, mate interest, and affiliation, whereas averted eye gaze might alert him or her to potential hidden danger in the environment. The level of danger immediately apparent in the environment is arguably detectable only through the joint effects of expression recognition and gaze direction (see Adams et al. 2003; Hess et al. 2007; Sander et al. 2007). For example, seeing someone looking fearfully at some point in the environment is particularly informative with regard to detecting immediate danger. Likewise, if someone looks at you with an angry expression, you are particularly likely to sense immediate danger to yourself, as the threat is coming from the sender and is directed at you. This perspective is consistent with the shared signal hypothesis of emotion and gaze processing in that shared signals would mutually inform the behavioral relevance of these combined cues.
A role for facial affect in gaze perception Although to this point the emphasis has been on the effects of gaze on emotion perception, it is important to note that
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the shared signal hypothesis also predicts a similar impact of facial affect on perceiving gaze direction. Gaze researchers have contemplated a role for facial affect in the social interpretation of gaze. For instance, Ellsworth and Ross (1975) suggested that because eye gaze does not carry a specific ‘‘sign-referent’’ meaning, its interpretation must be considered dependent on context. Thus the meaning of direct eye gaze can be interpreted as friendly or threatening depending on the context within which it takes place, such as in a crowded bar versus alone on the street (Argyle and Cook 1976; Ellsworth and Ross 1975; Kendon 1967; Rubin 1973; Schneider et al. 1979). Emotional expression conveyed by a face offers a minimal context; joy and anger expressions indicate affiliative versus threatening information, respectively. The shared signal value of eye gaze and emotion, however, rests on the even more fundamental distinction of approach and avoidance motivation associated with both gaze and emotion. Given the demonstrated role of gaze in emotion processing, it stands to reason that emotional expression would similarly influence the perception of gaze. Indeed, recent research efforts have shown that emotions differentially influence reflexive orienting and attention capture induced by averted and direct eye gaze respectively (e.g., Mathews et al. 2003; Putman et al. 2006), and in a manner consistent with the shared signal hypothesis (see Fox et al. 2007). Further, two recent studies reveal mutual interdependency of gaze and emotion (Ganel et al. 2005; Graham and LaBar 2007). Given that Adams and Kleck (2003) found that direct relative to averted gaze facilitated the processing of anger and averted relative to direct gaze facilitated fear, the current investigation sought to examine the possibility of a similar influence of emotional expression on gaze discrimination. To accomplish this we utilized the same stimuli from Adams and Kleck (2003). The first aim of the current work, therefore, was to examine interaction effects driven by the influence of emotional expression on gaze processing. Importantly, recent work has also demonstrated that speed of processing based on manipulated stimulus features serve as a moderator of the gaze by emotion interdependency (Ganel et al. 2005; Graham and LaBar 2007). Ganel et al. found greater interdependent processing between gaze and emotion when making eye gaze direction slower to recognize by varying the angle of aversion. In their study, gaze was initially processed significantly faster than emotion, and they predicted that if the processing of gaze and emotion were equally discriminable, then integration of gaze and emotion may be more likely to occur, which it was. Graham and LaBar similarly demonstrated speed of responding on the stimulus level. In their study, emotion was initially processed significantly faster than gaze, and they found more interdependent processing when making emotional displays slower
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to discriminate by morphing high intense expressions with their corresponding neutral displays. Thus, the second aim of the current work was to extend these efforts by examining this important moderator (speed of processing) at the level of individual differences, thereby keeping stimulus features and task demands constant.
whether each face displayed direct or averted eye gaze. Stimulus trials were presented in Superlab ProTM (see Haxby et al. 1993). Each trial began with a 500 ms fixation, replaced by a 50 ms blank screen before face onset. The face remained until a response was made. Participants were asked to label each face as quickly and accurately as possible.
Study 1
Results
To recap, Adams and Kleck (2003) found direct eye gaze facilitated the decoding of anger versus fear and averted eye gaze facilitated fear versus anger. The aim of the current study, therefore, was to examine whether facial affect exerts a similar influence on gaze perception. Predictions follow from the shared signal hypothesis. For these reasons we predicted that anger would facilitate the processing of direct relative to averted eye gaze, whereas fear would facilitate the processing averted relative to direct eye gaze, matching the pattern found previously for the role of gaze on emotion processing.
Prior to data analysis, data were log-transformed. Incorrect responses were removed (6.4%). Additionally, responses more than three standard deviations above or below the mean were also removed (0.9%). For ease of interpretation, we converted data back into milliseconds for reporting the means and standard errors. To test the influence of emotion on gaze processing, we conducted a 2 (emotion: anger versus fear) 9 2 (gaze direction: direct versus averted) repeated measures ANOVA, first on reaction times. A main effect of gaze emerged such that averted eye gaze (M = 746.1 ms, SE = 36.6) was processed more quickly than direct eye gaze (M = 798.4 ms, SE = 33.2), F(1, 21) = 4.89, p \ .05, g2p = .189. No main effect of emotion was apparent. Critically, the predicted interaction was also significant, F(1, 21) = 6.64, p \ .05, g2p = .240. Inspection of the means confirmed the pattern of anger facilitating the processing of direct relative to averted gaze and fear facilitating the processing of the averted relative to direct gaze (see Table 1). Direct contrasts revealed that averted gaze was more quickly identified when presented on a fear than an anger display t(21) = 2.87, p \ .01, r = .531. Conversely, direct gaze was more quickly identified when presented on anger than fear expressions; this latter finding reached marginal significance, t(21) = -1.74, p \ .1, r = .355. Although accuracies were very high and therefore subject to ceiling effects, we also examined error rates. These revealed a very similar pattern to that found reported above for reaction times, thereby ruling out the existence of potential speed-accuracy trade-offs. There was a marginally significant main effect of gaze, F(1, 21) = 3.54, p \ .08, g2p = .144, such that direct eye gaze led to more
Method Participants Twelve female, nine male, and one gender undisclosed undergraduates were recruited in exchange for partial course credit. Students arrived to the laboratory and were run individually. Apparatus and stimuli Thirty actors, half female, were selected from the Pictures of Facial Affect (Ekman and Friesen 1978), a set developed by Kirouac and Dore´ (1984), the Montreal Set of Facial Displays of Emotion (Beaupre´ et al. 2000), and a set developed by us (Adams and Kleck 2001). These same stimuli were used in Adams and Kleck (2003), except that we did not incorporate the anger/fear blended expression in the current study. All stimulus persons were of European descent. Eye gaze was digitally manipulated in these images to create averted right and left gaze stimuli. Since each face was shown with left and right gaze, it was also shown with direct gaze twice, yielding a total of 240 trials. Expressions were digitized and cropped to expose only the head and neck region and presented in black and white at an approximate size of 4 9 3 in.
Table 1 Reaction times (ms), standard error (SE), and error rates (% incorrect) as a function of gaze direction and emotional expression (Study 1) Expression/gaze
Procedure Participants were seated 24 in. from a 15 in. monitor. Participants indicated with a right or left mouse click
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RTs (ms)
SE
Errors (%)
Anger
Fear
Anger
Fear
Anger
Fear
Direct
779.2
817.5
32.9
37.1
5.8
10.4
Averted
752.6
739.6
35.4
36.8
5.3
4.1
Motiv Emot (2009) 33:106–112
errors (M = .047, SE = .010) than averted gaze (M = .081, SE = .012). A main effect of emotion was also apparent, F(1, 21) = 6.60, p \ .02, g2p = .239, revealing reduced error rates for fear (M = .055, SE = .007) than anger (M = .072, SE = .007) gaze. Notably these main effects were again qualified by the predicted interaction, F(1, 21) = 26.76, p \ .0001, g2p = .560. Differences in error rates for direct eye gaze were significantly lower in anger than fear faces, t(21) = 5.27, p \ .001, r = .754, whereas no difference was found for averted gaze as a function of emotional display, though the pattern was in the predicted direction. Study 1 offers preliminary evidence for interaction effects driven by the influence of emotion on gaze discrimination, with the patterns of effects consistent with that previously reported for the influence of gaze on emotion reported by Adams and Kleck (2003). A significant main effect of gaze also emerged, such that averted gaze was processed faster and with fewer errors.
Study 2 The aim of this study was to replicate and extend Study 1 by examining the potential moderating effects of processing speed on the interaction of emotion and gaze (see Ganel et al. 2005; Graham and LaBar 2007), this time at the level of individual differences. Examining individual variation in the interactivity of gaze and emotion necessarily holds stimulus features and task demands constant across participants. Because mean response times reported in Study 1 appear faster than those previously reported for emotion recognition using the same paradigm and stimuli [i.e., Adams and Kleck (2003), Study 1: approximately 130 ms discrepancy], we predicted that individuals who process gaze more slowly would yield greater interactivity effects, thereby replicating and extending that found previously for speed of processing without employing stimulus manipulation. Method
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(PST, Pittsburgh, PA). Participants were seated 24 in. from a 17 in. monitor. Procedure The same procedure was used as in Study 1. Results Data were log-transformed and pre-processed as described in Study 1. Incorrect responses (5.5%) and outliers (1.7%) were removed. The central hypothesis was tested by computing a 2 (emotion: anger versus fear) 9 2 (gaze direction: direct or averted gaze) mixed analysis of variance. As in Study 1, a main effect of gaze emerged, F(1, 44) = 5.42, p \ .05, g2p = .105. Responses to averted gaze (M = 620.9, SE = 7.66) were faster than direct gaze (M = 641.2, SE = 8.43). No main effects for emotion were evident. In addition the predicted interaction of emotion and gaze direction was significant, F(1, 44) = 7.41, p \ .01, g2p = .139 (see Table 2). Averted gaze was more quickly decoded on fearful expressions than angry expressions, t(46) = 2.65, p \ .02, r = .364. Conversely, direct gaze was more quickly decoded on angry expressions though not reaching significance, t(46) = -1.58, p \ .13, r = .227. In order to examine the influence of overall speed of processing on these effects, correlations were then computed. To examine correlations with the interaction we computed an index of the interaction in the following manner: (averted anger ? direct fear) - (direct anger ? averted fear). Higher scores represent faster responses to congruent versus incongruent signals. To examine correlations with the main effect of gaze, we computed an index of the main effect in the following manner: (direct anger ? direct fear) - (averted anger ? averted fear). Higher scores here represent faster responses to averted gaze faces. Using these indices, we found a significant and positive correlation between overall speed of responding, r(47) = .295, p \ .05. The correlation between overall speed of responding and the main effect of gaze, however, did not reach significance, r(47) = -.215, p [ .14.
Participants Thirty-two female and 15 male undergraduates (Mean age = 18.8, SD = 1.61) were recruited in exchange for partial course credit. Apparatus and stimuli The same stimuli were used as in Study 1. Participants completed the experiment in individual running rooms on computers containing E-Prime experimental software
Table 2 Reaction times (ms), standard error (SE), and error rates (% incorrect) as a function of gaze direction, emotional expression, and individual differences in overall speed of processing (Study 2) Expression/gaze
RTs (ms)
SE
Errors (%)
Anger
Fear
Anger
Fear
Anger
Fear
Direct
647.9
658.8
15.8
18.6
4.3
8.7
Averted
636.6
622.0
14.9
14.2
4.5
4.5
123
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When examining error rates, a significant gaze effect emerged, F(1, 44) = 5.30, p \ .05, g2p = .103 such that averted gaze (M = .045, SE = .006) yielded a lower proportion of errors than direct gaze (M = .055, SE = .008). A significant emotion effect also emerged, F(1, 44) = 5.30, p \ .05, g2p = .268, as anger (M = .044, SE = .005) yielded lower errors than fear faces (M = .066, SE = .007). These main effects were again qualified by the predicted two-way interaction between eye gaze and emotion, F(1, 44) = 5.30, p \ .05, g2p = .200. Direct gaze was found to be more accurately labeled in anger than fear faces, t(46) = 4.13, p \ .001, r = .520, whereas no significant differences were observed for averted gaze between anger and fear t(46) \ 1. Notably, when computing indices of the interaction and mean effects as indicated above for error rates, the correlations with overall speed of response were nonsignificant (all ps [ .1), thereby further indicating no presence of speed-accuracy trade-off. Study 2 replicates the interactive influence of emotion in gaze processing found in Study 1. In addition, individual differences in speed of processing were related to this effect. Participants with slower processing speeds revealed greater gaze by emotion interaction effects. As in Study 1, a main effect of faster responding to averted than direct gaze also emerged, though this was not related to overall speed of responding.
General discussion Studies 1 and 2 revealed an interactive pattern of influence for emotion on the processing of gaze, one similar to that previously found for the processing of gaze on emotional expression in these same stimuli (i.e., Adams and Kleck 2003). In both Studies 1 and 2, direct comparisons revealed that averted gaze was processed more quickly for fear than anger faces. Although not reaching traditional levels of significance in either Study 1 or 2, direct gaze was conversely found to be processed more quickly for anger than fear faces. Notably, when aggregating across the studies, the combined effect for faster responding to direct gaze anger than fear did reach significance.1 Furthermore, despite the high accuracy rates and potential for ceiling effects, in both Study 1 and 2 the interaction was significant when comparing error rates. Significantly less errors were associated with direct anger relative direct fear faces, though for averted gaze the opposite trend did not reach significance. Taken together, these results support the 1 When aggregating across studies, the effect size (weighted by df) for the comparison of direct gaze anger versus direct gaze fear reached significance, r(62) = .328, p \ .01 (see Rosenthal and Rosnow 1991).
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conclusion that gaze and emotion mutually influence the processing of one another in a manner consistent with the shared signal hypothesis (Adams and Kleck 2003). We also found that individual differences in processing speed were associated with the interactive effects of facial affect on gaze direction discrimination (Study 2). Slower responders showed stronger interaction effects overall. This finding is consistent with previous work examining processing speed as a moderator of interactivity that was conducted at level of manipulated stimulus features (Ganel et al. 2005; Graham and LaBar 2007). We predicted that for those who process eye gaze more slowly, presumably more on par with emotion, we would find greater integration of emotion in gaze processing. By finding these effects at the level of individual differences we were able to demonstrate that speed of processing matters even when holding stimulus and task features constant. An alternate explanation for the influence of overall speed of responding includes obligatory responding to gaze direction, which tends to happen very early in the perceptual stream (i.e., direct gaze attention capture, Senju and Hasegawa 2005; reflexive orienting, Driver et al. 1999). Thus, attentional allocation effects may interfere with the perceptual integration of gaze and emotion, which could therefore allow for greater integration in slower responders. This conclusion is consistent with the work of both Ganel et al. (2005) and Graham and LaBar (2007). Graham and LaBar found that slowing responses to expression yielded greater integrality. This could be in part because a delay in processing speed allows for recovery from attentional shifts before integrative processing occurs. In Ganel and colleagues’ study, they reduced the angle of averted gaze, which not only slowed the time to process gaze direction, but arguably the extent to which reflexive orienting occurred in the first place, allowing unencumbered perceptual integration of gaze and emotion. In this case, those slower to process gaze may simply be less prone to reflexive orienting. However, given this account, we may have predicted integration to be most apparent in direct gaze faces. Another potential explanation for the role of overall speed in influencing interactivity comes from the appraisal account, which would argue that facial expressions and gaze are appraisal-driven responses to emotional events. From this view eye gaze and emotion interact because they convey increased behavioral relevance when processed in combination. Such an account suggests interactivity due to cognitive rather than perceptual influences, which might therefore be slower. That said, recently researchers using the same stimuli employed here in an emotion discrimination task found that when employing a four-choice task, thereby slowing responses considerably, no interaction effects were apparent, whereas when employing the same
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stimuli in a two-choice task, interaction effects were apparent (see Bindemann et al. 2008). Thus, such findings are not consistent with the slower cognitive-appraisal account. The specific nature of these interaction effects, cognitive, perceptual, or both, requires additional research efforts to clarify. Also apparent in both studies was that the highest error rates were apparent for direct gaze fear expressions, which appears to have driven the gaze by emotion interactions for these comparisons. Notably, researchers have recently found that when presenting faces of various head angles in relation to the observer (one direct, four averted) with observers reporting on whether each face is making eye contact or not, happiness and anger were more often labeled as making direct eye contact compared to neutral and fearful faces (Lobmaier et al. 2008). Perhaps our findings reveal the reverse effect, in this case that direct gaze is harder to interpret when coupled with fear. Future research will be necessary to corroborate this speculation. Overall averted gaze was responded to more quickly than direct gaze. This is surprising given evidence for an attention capture function of direct gaze (Senju and Hasegawa 2005) and attention shifting function of averted gaze (Driver et al. 1999). Notably, we previously found no main effects of gaze direction (i.e., Adams and Kleck 2003), whereas others have reported direct eye gaze effects (e.g., Graham and LaBar 2007) consistent with an attention allocation mechanism. That said, there have also been previous cases of faster responsivity to averted gaze faces (e.g., Vuilleumier et al. 2005). Such discrepancies suggest a possible stimulus-driven influence, a conclusion that can not be ruled out here given that individual differences in overall processing speed were not associated the main effect of gaze. The whites of the eyes are accentuated by averted eye gaze. Thus, they may offer an easy physical feature used to discriminate averted gaze from direct gaze. Critically, just the whites of the eyes have been found to be sufficient to trigger amygdala responsivity to fear, even when subliminally presented (Whalen et al. 2005). This finding suggests that the processing of the whites of eyes occurs at even the very earliest stages of visual processing, helping explain its contribution to fast detection of averted gaze faces in these studies. It is likely therefore that discrepancies across studies may be due to the degree to which gaze is averted, with more extreme aversion yielding faster averted than direct gaze processing. Such variation warrants additional empirical inquiry, and might help explain the puzzling discrepancies in the social perception literature. For instance, even though direct gaze has often been found to capture and hold social attention (Senju and Hasegawa 2005), some research has demonstrated the opposite effect. As a case in point, although Macrae et al. (2002) find
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compelling evidence that direct gaze facilitates gender discrimination of faces, Vuilleumier et al. (2005) were unable to replicate this effect using different stimuli, finding in fact the opposite effect, that averted gaze facilitated gender discrimination. The difference in these two studies may simply have been the degree to which gaze was averted. Better understanding such stimulus-based effects, therefore, may help explain these puzzling discrepancies. In sum, the current work found that the interactive influence of emotion on gaze direction parallels previous work for the influence of gaze direction on emotion. In addition, we found that this effect was associated with how quickly participants discriminated gaze direction, extending efforts in this domain to the realm of individual differences. Finally, we also found that the main effect of gaze was not associated with overall processing speed. Taken together with other work on gaze perception this may indicate a stimulus-based moderator of the effects of gaze on social perception that warrants future empirical investigation. Future work manipulating the extent of averted gaze (i.e., angle of aversion) may thus help resolve discrepancies in the literature, such as why some studies find faster social perception in response to faces with direct gaze, while others find faster responses to faces with averted gaze. The current work thus underscores the importance of continued examination into the perceptual determinants of social cognitive functions as well as the influence of individual differences on these effects.
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