Brain and Cognition 91 (2014) 108–112
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The influence of emotional faces on the spatial allocation of attention Sheyan J. Armaghani, Gregory P. Crucian, Kenneth M. Heilman ⇑ Department of Neurology and Center for Neuropsychological Studies, University of Florida College of Medicine, Gainesville, FL, USA Malcom Randall Veterans Affairs Medical Center, Gainesville, FL, USA
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Article history: Accepted 19 September 2014
Keywords: Emotional faces Line bisection Pseudoneglect Spatial attention
a b s t r a c t Background objectives: Studies suggest that the right hemisphere is dominant for emotional facial recognition. In addition, whereas some studies suggest the right hemisphere mediates the processing of all emotions (dominance hypothesis), other studies suggest that the left hemisphere mediates positive emotions the right mediates negative emotions (valence hypothesis). Since each hemisphere primarily attends to contralateral space, the goals of this study was to learn if emotional faces would induce a leftward deviation of attention and if the valence of facial emotional stimuli can influence the normal viewer’s spatial direction of attention. Methods: Seventeen normal right handed participants were asked to bisect horizontal lines that had all combinations of sad, happy or neutral faces at ends of these lines. During this task the subjects were never requested to look at these faces and there were no task demands that depended on viewing these faces. Results: Presentation of emotional faces induced a greater leftward deviation compared to neutral faces, independent of where (spatial position) these faces were presented. However, faces portraying negative emotions tended to induce a greater leftward bias than positive emotions. Conclusions: Independent of location, the presence of emotional faces influenced the spatial allocation of attention, such that normal subjects shift the direction of their attention toward left hemispace and this attentional shift appears to be greater for negative (sad) than positive faces (happy). Published by Elsevier Inc.
1. Introduction The brain has a limited capacity to process simultaneous information and there is more sensory information coming into the brain than the brain can fully process. In addition, even in the absence of stimuli, the human brain has the ability to activate sensory–perceptual and semantic–conceptual representations, and attending to these internal representations can further reduce the capacity to fully process incoming stimuli. Thus, the brain requires a means by which it can triage afferent input so that stimuli that are important to the person are fully processed and those that are not important (noise) do not undergo full processing. The triage processing system used by the brain is called attention. A person can decide, based on motivational states and long term goals or intentions, the stimuli to which s/he should attend. This is called ‘top down’ or intentional attention. Alternatively, in the absence of an intentional goal, some stimuli, such as novel stimuli, will automatically draw a person’s attention. Because of their saliency, emotional faces can capture attention more readily than
⇑ Corresponding author at: Department of Neurology, University of Florida College of Medicine, Gainesville, FL 32610, USA. E-mail address: [email protected]fl.edu (K.M. Heilman). http://dx.doi.org/10.1016/j.bandc.2014.09.006 0278-2626/Published by Elsevier Inc.
other objects (Vuilleumier & Schwartz, 2001; Mack & Rock, 1998; Palermo & Rhodes, 2007). It is unclear, however, if faces displaying emotional expressions, shown in either right or left hemispace (to the right or left of the body’s midsagittal plane) are more likely to capture a person’s attention than emotional faces displayed in the opposite hemispace. It is also unclear if, independent of the location of the face, the presentation of certain specific forms of emotional facial expressions (e.g., positive emotions such as a happy face versus negative emotions such as a sad face) might induce spatial (right versus left) attentional biases. There are several neuropsychological hypotheses that can be used in an attempt to predict the side of space to which people would attend when viewing emotional faces. The dominance hypothesis predicts that the perception and processing of emotional faces is mediated by the right hemisphere (Heilman, Watson, & Valenstein, 2003). Multiple studies have shown that independent of the valence of the emotion displayed on a face, patients with right hemisphere damage are more likely to be impaired at discriminating–comprehending emotional facial expressions than are those with left hemisphere damage (DeKosky, Heilman, Bowers, & Valenstein, 1980; Bowers, Bauer, Coslett, & Heilman, 1985). Functional imaging has provided converging evidence for this facial emotional dominance hypothesis
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(Ishai, Schmidt, & Boesiger, 2005). In addition, a tachistoscopic study of normal subjects showed that the emotional expression of faces on cartoons were more accurately recognized in the left visual field (right hemisphere) than the right visual field (Ley & Bryden, 1979) and Munte et al. (1998) showed that there is greater evoked response potential (ERP) activity in the right than left hemisphere during emotional face processing. Thus, based on these studies it might be more likely for emotional faces that are presented in either side of space to induce right hemispheric activation, but this activation may be even greater for those faces presented in left (versus right) viewer-centered hemispace. An alternative theory, the valence hypothesis, posits that the right hemisphere mediates negative emotions such as sadness and the left hemisphere mediates positive emotions such as happiness (Borod et al., 1998; Silberman & Weingartner, 1986). This association was observed in studies of brain impaired subjects (Starkstein, Robinson, & Price, 1987) as well as physiological activation studies (Davidson, Mednick, Moss, Saron, & Schaffer, 1987). In a facial emotion recognition study that used tachistoscopic presentations (Reuter-Lorenz, Givis, & Moscovitch, 1983), right-handed subjects were shown emotional faces in one hemifield (right versus left) while a neutral face was shown in the opposite hemifield. These investigators found that recognition reaction times were faster when happy faces were presented in the right hemifield and sad faces in the left hemifield. These results support the valence hypothesis since the happy faces in the right hemifield should be processed by the left hemisphere and vice versa for the sad faces. In a similar study, normal subjects were shown cartoon images of faces expressing emotions ranging from extremely positive to extremely negative and these images were placed in either the right or left visual field (Van Strien & Van Beek, 2000). The participants were asked to rate the faces as either positive or negative. Compared to men, women rated faces more positively, especially in response to right visual field presentations. Women rated neutral and mildly positive faces more positively in the right than in the left visual field, whereas men rated these faces consistently across visual fields. Thus, the results of this study were mixed as women performed according to the valence hypothesis but the men did not. In a review of over 20 emotional perception laterality studies (Mandal & Ambady, 2004) provide additional evidence in support of the valence hypothesis. Thus, it is possible that when presented with happy faces, it would be more likely for normal subjects to attend to these faces when they are presented in right than left hemispace. And when presented with sad faces, they would be more likely to attend in the opposite direction. It is also possible that there might be an interaction between this dominance and valence hypotheses. Independent of the side of presentation, seeing a meaningful stimulus such as an emotional face might also induce asymmetrical alterations in brain function, such that the areas that process these faces become more activated than areas not involved in this process. Each hemisphere primarily attends to contralateral hemispace (Kinsbourne, 1970), and thus when there is asymmetrical hemispheric activation, a person might be more likely to attend to stimuli or to portions of stimuli that are contralateral to this more activated hemisphere. Therefore, according to the valence hypothesis mentioned above, independent of the side of presentation, faces that display a negative emotion (sad) might activate the right hemisphere more than the left and bias attention toward left hemispace and faces that display a positive emotion (happy) might bias attention more to the right. In contrast, according to the dominance hypothesis, independent of the side of presentation, when seeing either a face expressing a negative emotion (e.g., sad) or a positive emotion (e.g., happy) attention would be directed toward left hemispace. There is also the possibility that there can be an interaction between these effects predicted by these two
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hypotheses such that independent of the emotion expressed on a face, facial emotional will induce right hemisphere activation and a leftward attentional bias, but this bias will be even greater for those faces that express a negative than positive emotion. When people direct their attention to an object, they perceive that object’s magnitude as being greater than the magnitude of an identical object to which they are devoting less attention (Chatterjee, Mennemeier, & Heilman, 1992). Thus, measuring estimates of magnitude in different portions of viewer-centered space is technically one of the best means of assessing the spatial allocation of directed attention. The line bisection task (Liepmann, 1900) has been used to assess attentional asymmetries in patients with hemispheric lesions. In general, when patients with hemispheric injury attempt to perform line bisections they deviate toward the lesioned hemisphere (Heilman et al., 2003). These results suggest that these patients’ attention is biased to the ipsilesional part of space and this attentional bias toward the segment of the line that is ipsilateral to the lesion makes this part of the line appear relatively larger than an equal segment that is in the less attended portion of space which is contralateral to lesioned hemisphere. Since hemispatial alteration of attention can be measured by the line bisection task, if the presence of faces expressing emotions alters the allocation of attention, then the line bisection task might be an ideal means of testing the valence versus dominance emotional face-spatial attention hypotheses. Thus, in this study the line bisection task was used to assess how emotional faces placed on the sides of lines influence normal subjects’ allocation of spatial attention. 2. Methods 2.1. Participants Twenty participants (10 women and 10 men) with an average age of 21.61 years and 13.8 years of education volunteered for testing. Potential subjects were screened with a questionnaire and exclusionary criteria included history of head injuries, alcohol or drug abuse, learning disabilities, neurological diseases, seizures, or psychological–psychiatric disorders. Three participants revealed a history of psychological issues (treatment was sought) and therefore, were subsequently excluded from the study, resulting in the data of 17 participants being included in these analyses. The participants all had normal or corrected to normal vision at the time of testing and all were right-handed by self-report. All participants provided written informed consent approved by the Institutional Review Board of the University of Florida. 2.2. Apparatus We used 9 different types of test stimuli, each consisting of a black line (253 2 mm) placed centrally on legal size paper (216 355 mm). Black-and-white photographs of one actress were taken from the Florida Affect Battery (Bowers, Blonder, & Heilman, 1992) depicting a happy (H), sad (S), or neutral (N) face as illustrated in Fig. 1. To avoid perceptual biases induced by the presentation of asymmetrical arrays, faces were always presented on both sides of the line test stimuli. These photographs were presented bilaterally 10 mm to the right and left ends of the horizontal lines (the intersection of two spatial planes that are anterior but parallel to the subjects’ coronal and transverse planes). The test stimuli were arranged utilizing a similar coding method as that used by Tamietto, Corazzini, de Gelder, and Geminiani (2006). The unilateral emotional face condition (UEC) contained an emotional (H or S) face on either the left or right side of the line paired with an unemotional or neutral (N) face on the other side. The
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Fig. 1. Face stimuli. The facial stimuli which served as stimuli on the line bisection task are presented above. The facial stimuli were paired in every combination and presented bilaterally on a horizontal line. The same actress depicts a happy (a), neutral (b), and sad (c) face.
bilateral-congruent emotional face condition (BCEC) consisted of an emotional face on one side paired with a face expressing the same emotion on the other side. In the bilateral-incongruent emotional condition (BIEC), there was a happy face on one side and sad face on the other side. Stimuli with bilateral congruent emotional faces were included to provide methodological balance for the other stimuli. In all the incongruent conditions, the right– left placements of the specific emotional (H, S) or neutral (N) face were right–left counter-balanced. Thus, the test battery for this study consisted of 27 stimuli (3 of each unique stimulus including: HN, NH, SN, NS, NN, HH, SS, HS, SH). The order of presentation of these emotional face – line stimuli was randomized but each participant was tested using the same order. 2.3. Procedures The seated subjects were instructed to bisect each presented line stimulus as close to the center as possible by making a vertical mark through the line with a pencil. These instructions did not contain any instructions regarding the facial cues, allowing the faces to be ignored or viewed if chosen so by the subject. These line stimuli were placed 12 in. in front of the subjects such that the subjects’ mid-sagittal plane, which was perpendicular to the line, bisected each line. Each stimulus array was presented one at a time by the examiner and removed after the subject attempted to bisect the line. The examiner then provided the next stimulus until each subject completed the 27 line bisections. The line bisection tests were self-paced and no participant had difficulty with this task. After the subjects completed the testing, all attempted bisections were measured to the nearest millimeter from the true center of the horizontal line. Bisections to the left of center were assigned negative values and bisections to the right of center were assigned positive values.
stated that when bilateral congruent stimuli are simultaneously presented there is a ‘‘redundant target effect’’ with neural summation and inter-hemispheric cooperation. This inter-hemispheric cooperation would be likely to induce bilateral hemispheric activation. Since the main goal of this study was to examine hemispheric asymmetries induced by positive and negative emotions, as well as the laterality of presentation, the comparison between the bilateral emotional face conditions would confound our results. Thus, in our analyses the experimental stimuli were only those stimuli that contained unilateral sad or happy emotional faces and the control stimuli were lines with only the neutral faces on both sides of the line. The right hemisphere dominance hypothesis for emotional face recognition and activation was assessed with planned comparisons after collapsing results from the UEC conditions (both side and valence) and comparing the bias induced by lateral emotional faces to the bilateral neutral (non-emotional face) control condition to determine if emotional faces independent of valence and side of presentation induced the posited left sided bias. The valence hypothesis was assessed with planned comparisons after collapsing the conditions in which unilateral positive stimuli were combined with a unilateral neutral stimulus (HN and NH) and compared to the bilateral neutral condition. In addition, unilateral negative stimuli were combined with unilateral neutral stimuli (SN and NS) and also compared to the bilateral neutral condition to assess the valence hypothesis. The influence of spatial position of emotional faces on spatial biases: We found in the UEC condition when emotional faces (S or H) were presented on the left (M = 3.863, SD = 4.159) there was no significantly greater absolute deviation than when in the UEC faces were presented on the right (M = 3.676, SD = 4.397) (t(16) = 0.314, p = 0.757). In addition, in the UEC condition, when the emotional (H and S) faces were presented on the left side and the neutral face on the right side, the deviation to the left with the sad face (M = 3.980, SD = 4.352) was not significantly greater than the deviation associated with the happy face (M = 3.745, SD = 4.361) (t(16) = 0.374, p = 0.713). In the UEC condition, when the emotional faces (H and S) were presented on the right side, with the neutral face on the left side, there was no significantly greater leftward deviation with the happy face (M = 3.118, SD = 5.346) than sad faces (M = 4.235, SD = 3.942) (t(16) = 1.395, p = 0.182). Influence of emotion on spatial biases: The difference between the bisection errors (deviation from midline) of all the emotional stimuli versus the control neutral stimuli condition (NN) are shown in Fig. 2. A comparison of the differences in line bisection errors made in the all the UEC stimulus conditions (HN, SN, NS, NH) (M = 3.770 mm, SD = 4.101 mm) versus the control (bilateral neutral faces) condition (M = 2.6, SD = 4.561) revealed that participants bisected lines more leftward when presented UEC stimuli
Unilateral Emotional Cue M = -3.792 SE = 0.966
3. Analysis and results In this study we were not only interested in the influence of the presence of faces expressing positive (happy) and negative (sad) emotions on spatial attention, but also on the side (right versus left) on which these emotional faces were presented. Thus, the stimuli with bilateral congruent emotional faces were included to provide a comparison for the other stimuli where emotional faces were presented on the left versus the right side of the lines. In addition, Zaidel and Rayman (1994) have suggested that redundant bilateral presentations of the same stimuli may induce a confound they termed the ‘‘bilateral gain theory’’. This confound induces alterations of inter-hemispheric control which may influence asymmetries of hemispheric activation. In addition, Tamietto et al. (2006)
p = 0.017
Control M = -2.608 SE = 1.106
-6
-5
-4
-3
-2
-1
0
1
2
3
Deviation (mm) Fig. 2. Bisection deviation by face stimulus condition. Average deviation (mm) from center in the line bisection task by type of face (emotional versus neutral) stimulus. Deviations to the right of true center are positive while those to the left of center are negative. Error bars indicate standard error of measurement.
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on either the right or left side, than when bisecting lines that contained only neutral faces, t(16) = 2.660, p = 0.017. However, it appears that even when these normal participants attempted to bisect lines with bilateral neutral faces their was a significant leftward deviation (t(16) = 2.357, p = 0.031 (2-tailed), see also Fig. 2). Independent of the location (right versus left) of sad faces in the UEC condition, the attempted bisections of lines that contained the sad faces at one end (R and L) deviated more to the left (M = 4.108, SD = 4.004) than the bisections of the control lines that had neutral facial stimuli on both sides (M = 2.608, SD = 4.561), (t(16) = 2.829, p = 0.012). The line stimuli containing a happy face on either the left or right side (M = 3.431, SD = 4.416) tended to be bisected more to the left of midline that the control stimuli (M = 2.608, SD = 4.561), t(16) = 1.791, p = 0.092. 4. Discussion When normal young participants attempt to bisect lines, they often deviate their bisections to the left of actual midline (Bowers & Heilman, 1980; Jewell & McCourt, 2000). This phenomenon is called pseudoneglect (Bowers & Heilman, 1980). When presented with neutral faces on both sides of a line, our participants’ attempted bisections were significantly deviated to the left of center with no subject demonstrating an overall rightward deviation. Although this leftward deviation with neutral faces might be related to the pseudoneglect phenomenon, the analysis of faces, independent of emotions, is primarily mediated by the right hemisphere (Benton, 1990) and the presentation of faces might have induced activation of the right hemisphere. Since we did not have a ‘‘no faces’’ condition and thus with our data we could not perform an analyses comparing the pseudoneglect phenomena on lines that contained no faces versus lines that contain neutral faces on both sides. Fortunately, however, we can assess the influence of these bilateral neutral facial stimuli on the pseudoneglect phenomenon by comparing our data with the meta-analysis results of Jewell and McCourt (2000). Review of Jewell and McCourt’s (2000) meta-analysis data indicates that young adults significantly deviate to the left on line bisection tasks without bilateral cues, with an average magnitude of deviation of approximately 0.60 and a range of 0.20–1.0, thus reliably demonstrating ‘‘pseudoneglect’’. In the presence of simultaneous cues at both ends of the test stimulus, Jewell and McCourt reported a significant rightward bias, with a magnitude of deviation of approximately 0.80 and a range between 0.20 and 1.40. In contrast, as indicated in Table 1, the results of this study reflect an average magnitude of deviation to the left of midline that is, at the very minimum, approximately twice that found by Jewell and McCourt in young adults using lines without lateral stimuli, and nearly 2.5 times that using simultaneous bilateral cues. The Jewell and McCourt meta-analysis had a
Table 1 Bisection performance by condition. Descriptive statistics of test conditions used in analysis of emotional asymmetries. Test condition
Mean
Std. deviation
d
Control UEC UPC Combined UPC Left UPC Right UNC Combined UNC Left UNC Right
2.608 3.770 3.431 3.745 3.118 4.108 3.980 4.235
4.561 4.101 4.416 4.361 5.346 4.004 4.352 3.942
1.179 1.895 1.602 1.771 1.202 2.115 1.886 2.215
Abbreviations: UEC = unilateral emotional cues (HN, NH, SN, & NS); UPC = unilateral positive cue (HN & NH); UNC = unilateral negative cue (SN & NS). Control = no emotional cue (NN presented bilaterally). d = magnitude of difference from zero p (2t/ df) (Jewell & McCourt, 2000).
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small sample size with large variability and our study had similar characteristics. Thus, while the results of this study do suggest that the presence of faces on both sides of the line, does augment the pseudoneglect bias, additional research should be performed to validate these results. One explanation of this enhanced leftward bias with neutral faces might be related to the right hemispheric dominance of mediating facial recognition (Benton, 1990); however, there is an alternative explanation. Although there were no task demands for subjects to discriminate between neutral and emotional faces, emotional discrimination might be ‘‘automatic’’ or ‘‘bottom up’’ and similar to bottom up attention given to novel stimuli. Thus, the leftward deviation in the bilateral neutral face condition might be related to increased activation of the right hemisphere that is required to discriminate between neutral and emotional facial expressions. In this study, in all line bisections conditions, facial stimuli (both emotional and unemotional) were presented on both sides of the lines. The bilateral presentations of these facial stimuli minimize the possible influence of an asymmetrical perceptual bias induced by the unilateral presentation of stimuli. In addition, to learn if emotional stimuli induced alterations in the allocation of attention, we compared emotional faces to neutral faces. We also used the same actress and thus doubt that the differences in these neutral versus emotional face conditions could be related to perceptual asymmetries induced by attributes of different faces. A weakness in the current study is that there are some differences in the lighting and these stimulus artifacts might have been a confounding element. Prior studies have revealed that emotional faces are often processed more rapidly than other objects (Vuilleumier & Schwartz, 2001) and these emotional faces can draw attention without conscious awareness (de Gelder, Vroomen, Pourtois, & Weiskrantz, 1999; Vuilleumier, Armony, Driver, & Dolan, 2001). In this study, we did not attempt to learn how aware our subjects were of these lateral emotional facial stimuli because we were concerned that assessing awareness after each trial might have influenced how our participants in subsequent trials might develop ‘‘top down’’ or intentional attention that was directed to these emotional faces. Thus, when these laterally placed emotional faces influenced line bisection performance, they did so because of ‘‘bottom up’’ attention. Prior studies have also revealed that the presentation of emotional faces can even influence patients with attentional biases. For example, Tamietto et al. (2005) studied unilateral emotional cues on the line bisection in patients who exhibited hemispatial neglect and found that the presence of these emotional faces, even in the neglected hemispace, attracted these patients’ attention and altered their performance on the line bisection task. Our results support the postulate that when compared to nonemotional faces the presence of emotional faces, independent of their right–left locations in viewer centered space, induce an overall leftward attentional bias. In addition, we also wanted to learn if the attentional bias induced by the presence of emotional faces, can be better explained by the right hemisphere global emotional facial dominance hypothesis or the bi-hemispheric positive–negative emotional valence hypothesis. Whereas the global right hemisphere facial emotional dominance hypothesis predicts that, independent of the valence of an emotional facial expression (happy-positive or sad-negative), the perception of this emotionally expressive face is primarily mediated by the right hemisphere. Thus, the viewing of these emotional faces would cause activation of the right hemisphere and this increase of right hemisphere activation, during the line bisection, would cause an increase of normal subjects’ leftward spatial bias. In contrast, the bi-hemispheric emotional hypothesis would predict that whereas with sad faces there would be a left sided deviation with happy faces the attempted line
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bisections would deviate rightward. In this study emotional faces, independent of valence of these faces and independent of the side of presentation, when compared to the neutral face condition did induce a significant leftward shift in attempted line bisections. Thus, this result supports the right hemisphere emotional facial dominance hypothesis. Further support for the global right hemisphere dominance hypothesis comes from the studies of Ley and Bryden (1979) who demonstrated that emotional faces were more accurately recognized in the left visual field independent of their valence. In a similar, but more recent study, Tamietto et al. (2006) presented an emotional faces for 200 ms in either the left or right visual field and participants were asked to respond when the face conveyed a target expression. Reaction times were significantly faster for emotional faces, independent of the valence of the emotion expressed by these faces, presented in the left visual field compared to the right. In contrast to the dominance hypothesis, as mentioned, the bihemispheric valence hypothesis posits that the processing of emotions takes place in both the right and left hemisphere, with the right hemisphere being more specialized for the processing of negative emotions and the left hemisphere being more specialized for positive emotions. While overall the viewing of faces that are expressing an emotion, independent of their valence, does induce a leftward attentional bias, supporting the right hemispheric dominance postulate, there appears be a superimposed hemispheric valence asymmetry, such that the right hemisphere is relatively more activated by faces expressing emotions with negative (versus positive) valence and/or the left hemispheric more activated by faces expressing a positive emotion such that the presence of positive emotional faces reduced the leftward bias on the line bisection task. Our finding that there appears to be only a superimposed facial hemispheric valence asymmetry is in conflict with the report of Reuter-Lorenz et al. (1983) who found that normal participants recognized happy facial expressions faster when presented in the right than left visual field, and found the opposite field asymmetry with faces expressing negative emotions. Although speed of recognition might be related to spatial allocation of attention, there are other factors that influence the speed of recognition and our study more directly assessed the spatial allocation of attention induced by the presence of emotional faces. However, our mixed support for the valence hypothesis is similar to a study by Asthana and Mandal (2001) where a right hemisphere advantage was seen in sad emotions, but the left hemisphere did not have an advantage in positive emotions. Our results are also consistent with the results of several studies which reveal that negative emotions are more strongly lateralized than positive emotions (Asthana & Mandal, 2001; Adolphs, Jansari, & Tranel, 2001). Although our results suggest that the presence of emotional faces may bias attention toward left hemispace and this change in bias is especially true when negative (sad) faces versus positive (happy) faces were presented, additional studies are need to better learn the influence of emotional valence on the allocation of spatial attention as well as attempting to learn if these findings generalize to other positive and negative emotional stimuli. Further studies are needed to better understand what brain processes (e.g., perception–categorization versus mood induction) are inducing this spatial attentional bias. Finally, this study has several limitations that future studies need to address, including other measures of spatial attention such as eye movements, measurements of hemispheric activation, such as functional imaging and electroencephalography, as well as measures of the subjects’ emotional responses and mood.
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Brain and Cognition journal homepage: www.elsevier.com/locate/b&c
The influence of emotional faces on the spatial allocation of attention Sheyan J. Armaghani, Gregory P. Crucian, Kenneth M. Heilman ⇑ Department of Neurology and Center for Neuropsychological Studies, University of Florida College of Medicine, Gainesville, FL, USA Malcom Randall Veterans Affairs Medical Center, Gainesville, FL, USA
a r t i c l e
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Article history: Accepted 19 September 2014
Keywords: Emotional faces Line bisection Pseudoneglect Spatial attention
a b s t r a c t Background objectives: Studies suggest that the right hemisphere is dominant for emotional facial recognition. In addition, whereas some studies suggest the right hemisphere mediates the processing of all emotions (dominance hypothesis), other studies suggest that the left hemisphere mediates positive emotions the right mediates negative emotions (valence hypothesis). Since each hemisphere primarily attends to contralateral space, the goals of this study was to learn if emotional faces would induce a leftward deviation of attention and if the valence of facial emotional stimuli can influence the normal viewer’s spatial direction of attention. Methods: Seventeen normal right handed participants were asked to bisect horizontal lines that had all combinations of sad, happy or neutral faces at ends of these lines. During this task the subjects were never requested to look at these faces and there were no task demands that depended on viewing these faces. Results: Presentation of emotional faces induced a greater leftward deviation compared to neutral faces, independent of where (spatial position) these faces were presented. However, faces portraying negative emotions tended to induce a greater leftward bias than positive emotions. Conclusions: Independent of location, the presence of emotional faces influenced the spatial allocation of attention, such that normal subjects shift the direction of their attention toward left hemispace and this attentional shift appears to be greater for negative (sad) than positive faces (happy). Published by Elsevier Inc.
1. Introduction The brain has a limited capacity to process simultaneous information and there is more sensory information coming into the brain than the brain can fully process. In addition, even in the absence of stimuli, the human brain has the ability to activate sensory–perceptual and semantic–conceptual representations, and attending to these internal representations can further reduce the capacity to fully process incoming stimuli. Thus, the brain requires a means by which it can triage afferent input so that stimuli that are important to the person are fully processed and those that are not important (noise) do not undergo full processing. The triage processing system used by the brain is called attention. A person can decide, based on motivational states and long term goals or intentions, the stimuli to which s/he should attend. This is called ‘top down’ or intentional attention. Alternatively, in the absence of an intentional goal, some stimuli, such as novel stimuli, will automatically draw a person’s attention. Because of their saliency, emotional faces can capture attention more readily than
⇑ Corresponding author at: Department of Neurology, University of Florida College of Medicine, Gainesville, FL 32610, USA. E-mail address: [email protected]fl.edu (K.M. Heilman). http://dx.doi.org/10.1016/j.bandc.2014.09.006 0278-2626/Published by Elsevier Inc.
other objects (Vuilleumier & Schwartz, 2001; Mack & Rock, 1998; Palermo & Rhodes, 2007). It is unclear, however, if faces displaying emotional expressions, shown in either right or left hemispace (to the right or left of the body’s midsagittal plane) are more likely to capture a person’s attention than emotional faces displayed in the opposite hemispace. It is also unclear if, independent of the location of the face, the presentation of certain specific forms of emotional facial expressions (e.g., positive emotions such as a happy face versus negative emotions such as a sad face) might induce spatial (right versus left) attentional biases. There are several neuropsychological hypotheses that can be used in an attempt to predict the side of space to which people would attend when viewing emotional faces. The dominance hypothesis predicts that the perception and processing of emotional faces is mediated by the right hemisphere (Heilman, Watson, & Valenstein, 2003). Multiple studies have shown that independent of the valence of the emotion displayed on a face, patients with right hemisphere damage are more likely to be impaired at discriminating–comprehending emotional facial expressions than are those with left hemisphere damage (DeKosky, Heilman, Bowers, & Valenstein, 1980; Bowers, Bauer, Coslett, & Heilman, 1985). Functional imaging has provided converging evidence for this facial emotional dominance hypothesis
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(Ishai, Schmidt, & Boesiger, 2005). In addition, a tachistoscopic study of normal subjects showed that the emotional expression of faces on cartoons were more accurately recognized in the left visual field (right hemisphere) than the right visual field (Ley & Bryden, 1979) and Munte et al. (1998) showed that there is greater evoked response potential (ERP) activity in the right than left hemisphere during emotional face processing. Thus, based on these studies it might be more likely for emotional faces that are presented in either side of space to induce right hemispheric activation, but this activation may be even greater for those faces presented in left (versus right) viewer-centered hemispace. An alternative theory, the valence hypothesis, posits that the right hemisphere mediates negative emotions such as sadness and the left hemisphere mediates positive emotions such as happiness (Borod et al., 1998; Silberman & Weingartner, 1986). This association was observed in studies of brain impaired subjects (Starkstein, Robinson, & Price, 1987) as well as physiological activation studies (Davidson, Mednick, Moss, Saron, & Schaffer, 1987). In a facial emotion recognition study that used tachistoscopic presentations (Reuter-Lorenz, Givis, & Moscovitch, 1983), right-handed subjects were shown emotional faces in one hemifield (right versus left) while a neutral face was shown in the opposite hemifield. These investigators found that recognition reaction times were faster when happy faces were presented in the right hemifield and sad faces in the left hemifield. These results support the valence hypothesis since the happy faces in the right hemifield should be processed by the left hemisphere and vice versa for the sad faces. In a similar study, normal subjects were shown cartoon images of faces expressing emotions ranging from extremely positive to extremely negative and these images were placed in either the right or left visual field (Van Strien & Van Beek, 2000). The participants were asked to rate the faces as either positive or negative. Compared to men, women rated faces more positively, especially in response to right visual field presentations. Women rated neutral and mildly positive faces more positively in the right than in the left visual field, whereas men rated these faces consistently across visual fields. Thus, the results of this study were mixed as women performed according to the valence hypothesis but the men did not. In a review of over 20 emotional perception laterality studies (Mandal & Ambady, 2004) provide additional evidence in support of the valence hypothesis. Thus, it is possible that when presented with happy faces, it would be more likely for normal subjects to attend to these faces when they are presented in right than left hemispace. And when presented with sad faces, they would be more likely to attend in the opposite direction. It is also possible that there might be an interaction between this dominance and valence hypotheses. Independent of the side of presentation, seeing a meaningful stimulus such as an emotional face might also induce asymmetrical alterations in brain function, such that the areas that process these faces become more activated than areas not involved in this process. Each hemisphere primarily attends to contralateral hemispace (Kinsbourne, 1970), and thus when there is asymmetrical hemispheric activation, a person might be more likely to attend to stimuli or to portions of stimuli that are contralateral to this more activated hemisphere. Therefore, according to the valence hypothesis mentioned above, independent of the side of presentation, faces that display a negative emotion (sad) might activate the right hemisphere more than the left and bias attention toward left hemispace and faces that display a positive emotion (happy) might bias attention more to the right. In contrast, according to the dominance hypothesis, independent of the side of presentation, when seeing either a face expressing a negative emotion (e.g., sad) or a positive emotion (e.g., happy) attention would be directed toward left hemispace. There is also the possibility that there can be an interaction between these effects predicted by these two
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hypotheses such that independent of the emotion expressed on a face, facial emotional will induce right hemisphere activation and a leftward attentional bias, but this bias will be even greater for those faces that express a negative than positive emotion. When people direct their attention to an object, they perceive that object’s magnitude as being greater than the magnitude of an identical object to which they are devoting less attention (Chatterjee, Mennemeier, & Heilman, 1992). Thus, measuring estimates of magnitude in different portions of viewer-centered space is technically one of the best means of assessing the spatial allocation of directed attention. The line bisection task (Liepmann, 1900) has been used to assess attentional asymmetries in patients with hemispheric lesions. In general, when patients with hemispheric injury attempt to perform line bisections they deviate toward the lesioned hemisphere (Heilman et al., 2003). These results suggest that these patients’ attention is biased to the ipsilesional part of space and this attentional bias toward the segment of the line that is ipsilateral to the lesion makes this part of the line appear relatively larger than an equal segment that is in the less attended portion of space which is contralateral to lesioned hemisphere. Since hemispatial alteration of attention can be measured by the line bisection task, if the presence of faces expressing emotions alters the allocation of attention, then the line bisection task might be an ideal means of testing the valence versus dominance emotional face-spatial attention hypotheses. Thus, in this study the line bisection task was used to assess how emotional faces placed on the sides of lines influence normal subjects’ allocation of spatial attention. 2. Methods 2.1. Participants Twenty participants (10 women and 10 men) with an average age of 21.61 years and 13.8 years of education volunteered for testing. Potential subjects were screened with a questionnaire and exclusionary criteria included history of head injuries, alcohol or drug abuse, learning disabilities, neurological diseases, seizures, or psychological–psychiatric disorders. Three participants revealed a history of psychological issues (treatment was sought) and therefore, were subsequently excluded from the study, resulting in the data of 17 participants being included in these analyses. The participants all had normal or corrected to normal vision at the time of testing and all were right-handed by self-report. All participants provided written informed consent approved by the Institutional Review Board of the University of Florida. 2.2. Apparatus We used 9 different types of test stimuli, each consisting of a black line (253 2 mm) placed centrally on legal size paper (216 355 mm). Black-and-white photographs of one actress were taken from the Florida Affect Battery (Bowers, Blonder, & Heilman, 1992) depicting a happy (H), sad (S), or neutral (N) face as illustrated in Fig. 1. To avoid perceptual biases induced by the presentation of asymmetrical arrays, faces were always presented on both sides of the line test stimuli. These photographs were presented bilaterally 10 mm to the right and left ends of the horizontal lines (the intersection of two spatial planes that are anterior but parallel to the subjects’ coronal and transverse planes). The test stimuli were arranged utilizing a similar coding method as that used by Tamietto, Corazzini, de Gelder, and Geminiani (2006). The unilateral emotional face condition (UEC) contained an emotional (H or S) face on either the left or right side of the line paired with an unemotional or neutral (N) face on the other side. The
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Fig. 1. Face stimuli. The facial stimuli which served as stimuli on the line bisection task are presented above. The facial stimuli were paired in every combination and presented bilaterally on a horizontal line. The same actress depicts a happy (a), neutral (b), and sad (c) face.
bilateral-congruent emotional face condition (BCEC) consisted of an emotional face on one side paired with a face expressing the same emotion on the other side. In the bilateral-incongruent emotional condition (BIEC), there was a happy face on one side and sad face on the other side. Stimuli with bilateral congruent emotional faces were included to provide methodological balance for the other stimuli. In all the incongruent conditions, the right– left placements of the specific emotional (H, S) or neutral (N) face were right–left counter-balanced. Thus, the test battery for this study consisted of 27 stimuli (3 of each unique stimulus including: HN, NH, SN, NS, NN, HH, SS, HS, SH). The order of presentation of these emotional face – line stimuli was randomized but each participant was tested using the same order. 2.3. Procedures The seated subjects were instructed to bisect each presented line stimulus as close to the center as possible by making a vertical mark through the line with a pencil. These instructions did not contain any instructions regarding the facial cues, allowing the faces to be ignored or viewed if chosen so by the subject. These line stimuli were placed 12 in. in front of the subjects such that the subjects’ mid-sagittal plane, which was perpendicular to the line, bisected each line. Each stimulus array was presented one at a time by the examiner and removed after the subject attempted to bisect the line. The examiner then provided the next stimulus until each subject completed the 27 line bisections. The line bisection tests were self-paced and no participant had difficulty with this task. After the subjects completed the testing, all attempted bisections were measured to the nearest millimeter from the true center of the horizontal line. Bisections to the left of center were assigned negative values and bisections to the right of center were assigned positive values.
stated that when bilateral congruent stimuli are simultaneously presented there is a ‘‘redundant target effect’’ with neural summation and inter-hemispheric cooperation. This inter-hemispheric cooperation would be likely to induce bilateral hemispheric activation. Since the main goal of this study was to examine hemispheric asymmetries induced by positive and negative emotions, as well as the laterality of presentation, the comparison between the bilateral emotional face conditions would confound our results. Thus, in our analyses the experimental stimuli were only those stimuli that contained unilateral sad or happy emotional faces and the control stimuli were lines with only the neutral faces on both sides of the line. The right hemisphere dominance hypothesis for emotional face recognition and activation was assessed with planned comparisons after collapsing results from the UEC conditions (both side and valence) and comparing the bias induced by lateral emotional faces to the bilateral neutral (non-emotional face) control condition to determine if emotional faces independent of valence and side of presentation induced the posited left sided bias. The valence hypothesis was assessed with planned comparisons after collapsing the conditions in which unilateral positive stimuli were combined with a unilateral neutral stimulus (HN and NH) and compared to the bilateral neutral condition. In addition, unilateral negative stimuli were combined with unilateral neutral stimuli (SN and NS) and also compared to the bilateral neutral condition to assess the valence hypothesis. The influence of spatial position of emotional faces on spatial biases: We found in the UEC condition when emotional faces (S or H) were presented on the left (M = 3.863, SD = 4.159) there was no significantly greater absolute deviation than when in the UEC faces were presented on the right (M = 3.676, SD = 4.397) (t(16) = 0.314, p = 0.757). In addition, in the UEC condition, when the emotional (H and S) faces were presented on the left side and the neutral face on the right side, the deviation to the left with the sad face (M = 3.980, SD = 4.352) was not significantly greater than the deviation associated with the happy face (M = 3.745, SD = 4.361) (t(16) = 0.374, p = 0.713). In the UEC condition, when the emotional faces (H and S) were presented on the right side, with the neutral face on the left side, there was no significantly greater leftward deviation with the happy face (M = 3.118, SD = 5.346) than sad faces (M = 4.235, SD = 3.942) (t(16) = 1.395, p = 0.182). Influence of emotion on spatial biases: The difference between the bisection errors (deviation from midline) of all the emotional stimuli versus the control neutral stimuli condition (NN) are shown in Fig. 2. A comparison of the differences in line bisection errors made in the all the UEC stimulus conditions (HN, SN, NS, NH) (M = 3.770 mm, SD = 4.101 mm) versus the control (bilateral neutral faces) condition (M = 2.6, SD = 4.561) revealed that participants bisected lines more leftward when presented UEC stimuli
Unilateral Emotional Cue M = -3.792 SE = 0.966
3. Analysis and results In this study we were not only interested in the influence of the presence of faces expressing positive (happy) and negative (sad) emotions on spatial attention, but also on the side (right versus left) on which these emotional faces were presented. Thus, the stimuli with bilateral congruent emotional faces were included to provide a comparison for the other stimuli where emotional faces were presented on the left versus the right side of the lines. In addition, Zaidel and Rayman (1994) have suggested that redundant bilateral presentations of the same stimuli may induce a confound they termed the ‘‘bilateral gain theory’’. This confound induces alterations of inter-hemispheric control which may influence asymmetries of hemispheric activation. In addition, Tamietto et al. (2006)
p = 0.017
Control M = -2.608 SE = 1.106
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-1
0
1
2
3
Deviation (mm) Fig. 2. Bisection deviation by face stimulus condition. Average deviation (mm) from center in the line bisection task by type of face (emotional versus neutral) stimulus. Deviations to the right of true center are positive while those to the left of center are negative. Error bars indicate standard error of measurement.
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on either the right or left side, than when bisecting lines that contained only neutral faces, t(16) = 2.660, p = 0.017. However, it appears that even when these normal participants attempted to bisect lines with bilateral neutral faces their was a significant leftward deviation (t(16) = 2.357, p = 0.031 (2-tailed), see also Fig. 2). Independent of the location (right versus left) of sad faces in the UEC condition, the attempted bisections of lines that contained the sad faces at one end (R and L) deviated more to the left (M = 4.108, SD = 4.004) than the bisections of the control lines that had neutral facial stimuli on both sides (M = 2.608, SD = 4.561), (t(16) = 2.829, p = 0.012). The line stimuli containing a happy face on either the left or right side (M = 3.431, SD = 4.416) tended to be bisected more to the left of midline that the control stimuli (M = 2.608, SD = 4.561), t(16) = 1.791, p = 0.092. 4. Discussion When normal young participants attempt to bisect lines, they often deviate their bisections to the left of actual midline (Bowers & Heilman, 1980; Jewell & McCourt, 2000). This phenomenon is called pseudoneglect (Bowers & Heilman, 1980). When presented with neutral faces on both sides of a line, our participants’ attempted bisections were significantly deviated to the left of center with no subject demonstrating an overall rightward deviation. Although this leftward deviation with neutral faces might be related to the pseudoneglect phenomenon, the analysis of faces, independent of emotions, is primarily mediated by the right hemisphere (Benton, 1990) and the presentation of faces might have induced activation of the right hemisphere. Since we did not have a ‘‘no faces’’ condition and thus with our data we could not perform an analyses comparing the pseudoneglect phenomena on lines that contained no faces versus lines that contain neutral faces on both sides. Fortunately, however, we can assess the influence of these bilateral neutral facial stimuli on the pseudoneglect phenomenon by comparing our data with the meta-analysis results of Jewell and McCourt (2000). Review of Jewell and McCourt’s (2000) meta-analysis data indicates that young adults significantly deviate to the left on line bisection tasks without bilateral cues, with an average magnitude of deviation of approximately 0.60 and a range of 0.20–1.0, thus reliably demonstrating ‘‘pseudoneglect’’. In the presence of simultaneous cues at both ends of the test stimulus, Jewell and McCourt reported a significant rightward bias, with a magnitude of deviation of approximately 0.80 and a range between 0.20 and 1.40. In contrast, as indicated in Table 1, the results of this study reflect an average magnitude of deviation to the left of midline that is, at the very minimum, approximately twice that found by Jewell and McCourt in young adults using lines without lateral stimuli, and nearly 2.5 times that using simultaneous bilateral cues. The Jewell and McCourt meta-analysis had a
Table 1 Bisection performance by condition. Descriptive statistics of test conditions used in analysis of emotional asymmetries. Test condition
Mean
Std. deviation
d
Control UEC UPC Combined UPC Left UPC Right UNC Combined UNC Left UNC Right
2.608 3.770 3.431 3.745 3.118 4.108 3.980 4.235
4.561 4.101 4.416 4.361 5.346 4.004 4.352 3.942
1.179 1.895 1.602 1.771 1.202 2.115 1.886 2.215
Abbreviations: UEC = unilateral emotional cues (HN, NH, SN, & NS); UPC = unilateral positive cue (HN & NH); UNC = unilateral negative cue (SN & NS). Control = no emotional cue (NN presented bilaterally). d = magnitude of difference from zero p (2t/ df) (Jewell & McCourt, 2000).
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small sample size with large variability and our study had similar characteristics. Thus, while the results of this study do suggest that the presence of faces on both sides of the line, does augment the pseudoneglect bias, additional research should be performed to validate these results. One explanation of this enhanced leftward bias with neutral faces might be related to the right hemispheric dominance of mediating facial recognition (Benton, 1990); however, there is an alternative explanation. Although there were no task demands for subjects to discriminate between neutral and emotional faces, emotional discrimination might be ‘‘automatic’’ or ‘‘bottom up’’ and similar to bottom up attention given to novel stimuli. Thus, the leftward deviation in the bilateral neutral face condition might be related to increased activation of the right hemisphere that is required to discriminate between neutral and emotional facial expressions. In this study, in all line bisections conditions, facial stimuli (both emotional and unemotional) were presented on both sides of the lines. The bilateral presentations of these facial stimuli minimize the possible influence of an asymmetrical perceptual bias induced by the unilateral presentation of stimuli. In addition, to learn if emotional stimuli induced alterations in the allocation of attention, we compared emotional faces to neutral faces. We also used the same actress and thus doubt that the differences in these neutral versus emotional face conditions could be related to perceptual asymmetries induced by attributes of different faces. A weakness in the current study is that there are some differences in the lighting and these stimulus artifacts might have been a confounding element. Prior studies have revealed that emotional faces are often processed more rapidly than other objects (Vuilleumier & Schwartz, 2001) and these emotional faces can draw attention without conscious awareness (de Gelder, Vroomen, Pourtois, & Weiskrantz, 1999; Vuilleumier, Armony, Driver, & Dolan, 2001). In this study, we did not attempt to learn how aware our subjects were of these lateral emotional facial stimuli because we were concerned that assessing awareness after each trial might have influenced how our participants in subsequent trials might develop ‘‘top down’’ or intentional attention that was directed to these emotional faces. Thus, when these laterally placed emotional faces influenced line bisection performance, they did so because of ‘‘bottom up’’ attention. Prior studies have also revealed that the presentation of emotional faces can even influence patients with attentional biases. For example, Tamietto et al. (2005) studied unilateral emotional cues on the line bisection in patients who exhibited hemispatial neglect and found that the presence of these emotional faces, even in the neglected hemispace, attracted these patients’ attention and altered their performance on the line bisection task. Our results support the postulate that when compared to nonemotional faces the presence of emotional faces, independent of their right–left locations in viewer centered space, induce an overall leftward attentional bias. In addition, we also wanted to learn if the attentional bias induced by the presence of emotional faces, can be better explained by the right hemisphere global emotional facial dominance hypothesis or the bi-hemispheric positive–negative emotional valence hypothesis. Whereas the global right hemisphere facial emotional dominance hypothesis predicts that, independent of the valence of an emotional facial expression (happy-positive or sad-negative), the perception of this emotionally expressive face is primarily mediated by the right hemisphere. Thus, the viewing of these emotional faces would cause activation of the right hemisphere and this increase of right hemisphere activation, during the line bisection, would cause an increase of normal subjects’ leftward spatial bias. In contrast, the bi-hemispheric emotional hypothesis would predict that whereas with sad faces there would be a left sided deviation with happy faces the attempted line
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bisections would deviate rightward. In this study emotional faces, independent of valence of these faces and independent of the side of presentation, when compared to the neutral face condition did induce a significant leftward shift in attempted line bisections. Thus, this result supports the right hemisphere emotional facial dominance hypothesis. Further support for the global right hemisphere dominance hypothesis comes from the studies of Ley and Bryden (1979) who demonstrated that emotional faces were more accurately recognized in the left visual field independent of their valence. In a similar, but more recent study, Tamietto et al. (2006) presented an emotional faces for 200 ms in either the left or right visual field and participants were asked to respond when the face conveyed a target expression. Reaction times were significantly faster for emotional faces, independent of the valence of the emotion expressed by these faces, presented in the left visual field compared to the right. In contrast to the dominance hypothesis, as mentioned, the bihemispheric valence hypothesis posits that the processing of emotions takes place in both the right and left hemisphere, with the right hemisphere being more specialized for the processing of negative emotions and the left hemisphere being more specialized for positive emotions. While overall the viewing of faces that are expressing an emotion, independent of their valence, does induce a leftward attentional bias, supporting the right hemispheric dominance postulate, there appears be a superimposed hemispheric valence asymmetry, such that the right hemisphere is relatively more activated by faces expressing emotions with negative (versus positive) valence and/or the left hemispheric more activated by faces expressing a positive emotion such that the presence of positive emotional faces reduced the leftward bias on the line bisection task. Our finding that there appears to be only a superimposed facial hemispheric valence asymmetry is in conflict with the report of Reuter-Lorenz et al. (1983) who found that normal participants recognized happy facial expressions faster when presented in the right than left visual field, and found the opposite field asymmetry with faces expressing negative emotions. Although speed of recognition might be related to spatial allocation of attention, there are other factors that influence the speed of recognition and our study more directly assessed the spatial allocation of attention induced by the presence of emotional faces. However, our mixed support for the valence hypothesis is similar to a study by Asthana and Mandal (2001) where a right hemisphere advantage was seen in sad emotions, but the left hemisphere did not have an advantage in positive emotions. Our results are also consistent with the results of several studies which reveal that negative emotions are more strongly lateralized than positive emotions (Asthana & Mandal, 2001; Adolphs, Jansari, & Tranel, 2001). Although our results suggest that the presence of emotional faces may bias attention toward left hemispace and this change in bias is especially true when negative (sad) faces versus positive (happy) faces were presented, additional studies are need to better learn the influence of emotional valence on the allocation of spatial attention as well as attempting to learn if these findings generalize to other positive and negative emotional stimuli. Further studies are needed to better understand what brain processes (e.g., perception–categorization versus mood induction) are inducing this spatial attentional bias. Finally, this study has several limitations that future studies need to address, including other measures of spatial attention such as eye movements, measurements of hemispheric activation, such as functional imaging and electroencephalography, as well as measures of the subjects’ emotional responses and mood.
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