Consciousness and arousal effects on emotional face processing as revealed by brain oscillations. A gamma band analysis

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International Journal of Psychophysiology 67 (2008) 41 – 46 www.elsevier.com/locate/ijpsycho

Consciousness and arousal effects on emotional face processing as revealed by brain oscillations. A gamma band analysis Michela Balconi a,⁎, Claudio Lucchiari b a

Laboratory of Cognitive Psychology, Department of Psychology, Catholic University of Milan, Largo Gemelli, 1 20123 Milan, Italy b Neurological National Hospital C. Besta, Milan, Italy Received 4 May 2005; received in revised form 29 August 2007; accepted 8 October 2007 Available online 13 October 2007

Abstract It remains an open question whether it is possible to assign a single brain operation or psychological function for facial emotion decoding to a certain type of oscillatory activity. Gamma band activity (GBA) offers an adequate tool for studying cortical activation patterns during emotional face information processing. In the present study brain oscillations were analyzed in response to facial expression of emotions. Specifically, GBA modulation was measured when twenty subjects looked at emotional (angry, fearful, happy, and sad faces) or neutral faces in two different conditions: supraliminal (10 ms) vs subliminal (150 ms) stimulation (100 target-mask pairs for each condition). The results showed that both consciousness and significance of the stimulus in terms of arousal can modulate the power synchronization (ERD decrease) during 150–350 time range: an early oscillatory event showed its peak at about 200 ms post-stimulus. GBA was enhanced by supraliminal more than subliminal elaboration, as well as more by high arousal (anger and fear) than low arousal (happiness and sadness) emotions. Finally a left-posterior dominance for conscious elaboration was found, whereas right hemisphere was discriminant in emotional processing of face in comparison with neutral face. © 2007 Elsevier B.V. All rights reserved. Keywords: Facial expression; EEG; Gamma band; Arousal; Consciousness

1. Introduction Correlates of affective face processing have been investigated using a variety of recording techniques. On one side, some authors studied ERP correlates associated with face comprehension. It has been argued that emotional face processing arises after 200 ms, and that differences between ERPs elicited by emotional faces and neutral faces were observable specifically between 250 and 550 ms after stimulus onset (Krolak-Salmon et al., 2001). An early negative deflection (N2) of higher amplitude was revealed for arousing facial stimuli (Balconi and Pozzoli, 2003; Sato et al., 2000; Streit et al., 2000) in comparison with neutral stimuli. Moreover, there is evidence that emotion processing is initiated and can proceed without conscious awareness (Bunce et al., 1999; LeDoux, 1998). An ⁎ Corresponding author. Tel.: +39 2 72342600; fax: +39 2 72342769. E-mail address: [email protected] (M. Balconi). 0167-8760/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2007.10.002

obvious and well-known example of unconscious perception of emotion is subliminal stimulation effect. This phenomenon was studied in a limited number of cases (Wong et al., 1994). Animal studies suggest that fear-related response are by a direct subcortical pathway from the thalamus direct to the amygdala, allowing emotional (and specifically threat) to be processed automatically and outside awareness. In humans, evidence for the unconscious perception of masked face has been revealed in terms of subjective reports (Esteves et al., 1994) autonomic reaction (Morris et al., 2001), brain imaging measures (Whalen et al., 1998), as well as ERPs (Kiefer and Spitzer, 2000). In addition, unconscious stimulation showed to be sensitive to the emotional content of the stimuli, as revealed by different behavioural and physiological measures (Lang et al., 1998). On the other side, brain oscillations were found to be a powerful tool to analyze the cognitive processes related to emotion comprehension in general (Başar et al., 1999; Krause, 2003), and, even if less studied, to unconscious perception

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(Summerfield et al., 2002). Few previous studies on ERD/ERS responses to emotion-related stimuli have examined the narrow frequency bands (Aftanas et al., 2001, 2002). Recent researches showed the event-related theta band power responds specifically to prolonged visual emotional stimulation (Krause et al., 2000), and a synchronization was revealed in case of coordinated response indicating readiness to process information (Başar, 1999). Thus, theta EEG power typically increases with increasing attentional demands and/or task difficulty. Also the effect of valence in affective picture processing was studied, showing that valence discrimination is associated with the early time-locked synchronized theta activity (Aftanas et al., 2001). Moreover, recent research have demonstrated that the modulation of gamma band activity (GBA) in time windows between 200 and 400 ms following the onset of a stimulus is associated with perception of coherent visual objects (Müller et al., 1996), and may be a signature of active memory. In parallel, GBA was found sensitive to emotional vs nonemotional stimuli and more specifically it was related to the arousal effect: early GBA was enhanced in response to aversive or highly arousing stimuli compared to neutral picture (Balconi and Pozzoli, 2007). This result was revealed in accordance with previous research that employed ERP measures for arousing pictures (Schupp et al., 2000) or emotional face (Balconi and Pozzoli, 2003; Sato et al., 2000), since these studies found a modulation of the increased arousal on ERP. Interestingly, previous research has found that gamma frequency band could also be considered a marker of degree of consciousness during elaboration of a stimulus: synchronous oscillations in the gamma frequency range may be necessary for the entry of information into conscious awareness (Crick and Koch, 1998). Specifically, Summerfield et al. (2002) have found that gamma activity increases after subjects had been made aware of the stimulus, and, therefore, synchronous gamma oscillations occurred in association with awareness processes. Therefore, gamma band is to be considered of main interest in exploring the effect of arousal as well as the consciousness in emotional face elaboration. The present study aims at studying the brain mechanisms underlying human emotional processing by measuring GBA changes in response to emotional faces presented visually in both supraliminal and subliminal stimulation. No previous study has widely explored the effect of consciousness on the processing of emotional faces, in conjunction with different types of stimulus (low or high arousing faces). Actually, although brain oscillations have been investigated in various sensory modalities, their role for brain functioning for emotion elaboration remains unclear. Secondly, it remains an open question whether it is possible to assign a single brain operation or psychological function for emotion decoding to a certain type of oscillatory activity. Thus, we intend to explore functional correlates of brain oscillations with regard to emotional face processing in supraliminal and subliminal condition and emphasize the importance of distributed oscillatory networks in gamma frequency band. We attended that emotional content may be indexed by oscillatory activity of the brain that was directly related to awareness or unawareness of the stimulus. Specifically, we hypothesized that

conscious elaboration of emotional stimuli will be indexed by GBA synchronization, whereas unconscious condition will be related to a decreased power intensity of this frequency band. Secondly, we expected that affective significance of a facial stimulus may result in changes of subjects' EEG responses (Lang et al., 1993). Emotion evaluated as highly arousing should be indexed by an enhanced power of gamma band in conscious condition. Finally, brain lateralization was found significant for emotional elaboration. As previously shown, right dominance was revealed for emotional stimuli compared to neutral ones, and specifically for face. On the contrary, left hemisphere was found to be more activated by conscious elaboration than unconscious. The present experiment based on ERD measure examined whether emotions would be associated with band modulation as regard as interhemispheric asymmetries in the right direction, whereas left hemisphere is expected to be discriminant for conscious processing if compared to unconscious. 2. Method 2.1. Subjects Twenty healthy volunteers took part in the study (eleven women, age range19–25, mean = 23.37, SD = 2.13). They were all right-handed and with normal or corrected-to-normal visual acuity. Exclusion criteria were history of psychopathology for the subjects or immediate family. They gave informed written consent for participating in the study. 2.2. Stimulus material Stimulus materials were taken from the set of pictures of Ekman and Friesen (1976). They were black and white pictures of male and female actors, presenting respectively a happy, sad, angry, fearful, or neutral face. 2.3. Supraliminal/subliminal stimulation A previous study was conducted in which the duration of target facial stimulus was varied in order to establish threshold condition (Liddell et al., 2004). In the current study we employed both an objective threshold, defined as the stimulus duration where the stimulus is perceived by the subject in 50% of the cases (Merikle et al., 2001); and a subjective threshold, defined as the overt lacking of discrimination of the stimulus and its emotional content. The pre-experimental study and posthoc briefing confirmed that subjects were unable to detect target stimulus in the subliminal condition. During the experiment we used a masking procedure. Each facial stimulus (target) was presented for either 10 (subliminal) or 150 (supraliminal) ms, followed by a neutral face presented for 150 ms (interstimulus interval 1.5 s) (Bernat et al., 2001; Brázdil et al., 1998; Liddell et al., 2004). The short stimulus presentation in subliminal condition prevents the subjects to have a clear cognition of the stimulus, but it allows for a semantic elaboration of the emotional faces. No target and mask pair

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depicted the same individual. In total there were 100 target-mask pairs in each threshold condition (each expression type was presented twenty times for condition). The condition was not counterbalanced across subjects (Bernat et al., 2001). 2.4. Procedure Subjects were seated comfortably in a moderately lighted room with the monitor screen positioned approximately 100 cm in front of their eyes. Pictures were presented in a randomised order in the center of a computer monitor, with a horizontal angle of 4° and a vertical angle of 6° (STIM 4.2 software). During the examination, they were requested to continuously focus their eyes on the small fixation point and to minimize blinking. Participants were required to observe the stimulus during ERP recording (passive task). In the subliminal condition it was emphasized that sometimes the target face would be difficult to see, but to concentrate as best they could on this stimulus, and that they would be asked question about these stimuli after the ERP recording. An explicit response to the emotional features of the stimulus was not required. This was done for three main reasons: to assure a real passive task (implicit elaboration of emotions); to not cause them to be more attentive to the emotional stimuli than the neutral ones; to not introduce an unequal condition between subliminal and supraliminal stimulation. In addition, the absence of an explicit response avoids confounding motor potentials in addition to brain potentials. Prior to recording ERPs, the subject was familiarized with the overall procedure (training session), where every subject saw in a random order all the emotional stimuli presented in the successive experimental session (a block of 10 trials, each expression type repeated twice). 2.5. EEG recording The EEG was recorded with a 62-channel DC amplifer (SYNAMPS system) and acquisition software (NEUROSCAN 4.2). An ElectroCap with Ag/AgCl electrodes were used to record EEG from active scalp sites referred to earlobe (10/20 system of electrode placement). Additionally two EOG electrodes were sited on the outer side of the eyes. The data were recorded using sampling rate of 256 Hz, with a frequency band of 0.1 to 60 Hz. The impedance of recording electrodes was monitored for each subject prior to data collection and it was always below 5 kΩ. After EOG correction and visual inspection only artefact-free trials were considered. Only fourteen electrodes were used for the successive statistical analysis (four central, Fz, Cz, Pz, Oz; ten lateral, F3, F4, C3, C4, T3, T4, P3, P4, O1, O2). 2.6. ERD/ERS data reduction The digital EEG data were bandpass filtered in the gamma frequency band (30–60 Hz). To obtain a signal proportion to the power of the EEG frequency band, the filtered signal samples were squared (Pfurtscheller, 1992). Successively, the data were epoched, triggered each second, using four different time windows of 100 ms (50–150; 150–250; 250–350; 350– 450 ms). An average absolute power value for each electrode

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for each condition (five expression types) was calculated. An average of the pre-experimental absolute power was used to determine the individual power during no stimulation. From this reference power value individual power changes during face viewing were determined as the relative stimulus-related decrease (desynchronization). In fact, according to ERD/ERS method, changes in band power were defined as the percentage of a decrease (ERD) in band power during a test interval (here 900 ms post-stimulus) as compared to a reference interval (here 1500 ms before picture onset). For each subject, after band-pass filtering ERD was calculated within the four time intervals. The average ERD values across the respective electrode sites were calculated for each condition, time interval, and emotional category. 2.7. Data analysis The data were entered into repeated measures analysis of variance (ANOVA) with four repeated factors: condition (2, supraliminal and subliminal), time (four time intervals, 4), stimulus type (emotion type, 5), and electrode sites (cortical sites, 14). Secondly, in order to analyze widely the cortical distribution of band modulation, the data were averaged over anterior (F3, Fz, F4), central (C3, Cz, C4), and posterior (P3, Pz, P4) electrode location, and secondly over left (F3, C3, T3, P3, O1) and right (F4, C4, T4, P4, O2) sides. These new values were entered in two distinct statistical analyses. For all the ANOVAs, degrees of freedom were Greenhouse–Geisser corrected where appropriate. 3. Results 3.1. Behavioral data The subjects were asked to analyze the stimuli viewed after the experimental section. Firstly, they evaluated the emotional significance of each expression by a categorization task. The five emotional categories were correctly recognized (for happy 96%, sad 94%, angry 97%, fearful 97% and neutral 95% faces). Successively, in order to distinguish the effect of arousal for emotional face the subjects evaluated on a Likert scale (5 points) their responses as a function of the arousing power of each stimulus (“how do you evaluate the arousing power of this stimulus for you?”). Fear (M = 4.78), anger (M = 4.51), happiness (M = 3.17), sadness (M = 2.76) and neutral (M = 2.20) faces differed in terms of their arousing power. Specifically, ANOVA showed significant differences between the emotion (F(4, 19) = 12.36, P b 0.001), and post-hoc comparisons (Tukey) revealed that anger and fear were considered more emotionally arousing than happiness (respectively F(1, 19)= 10.16, P b 0.001; F(1, 19)= 9.74, P b 0.001) and sadness (F(1, 19) = 11.69, P = 0.001; F(1, 19)= 12.36, P b 0.001), as well as than neutral stimuli (F(1, 19)= 14.03, P b 0.001; F(1, 19)= 15.41, P b 0.001). 3.2. ERD/ERS data GBA showed sensitivity to Condition (F(1,19)= 7.07, P = 0.001), Type (F(4,19) =10.12, P b 0.001), Time (F(3,19)= 8.55, P b 0.001) and Electrodes (F(13,19)= 13.09, P b 0.001), as well as

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Fig. 1. ERD % for Emotion × Time interaction in gamma band. (a) Supraliminal; (b) Subliminal.

for Condition × Type, Condition × Time (F(3,19) = 10.98, P b 0.001), Time ×Electrodes (F(39,19)= 14.89, P b 0.001), and Type× Time (F(12,19) =11.22, P b 0.001). As shown in Fig. 1, GBA increases in supraliminal condition compared with subliminal. In addition post-hoc comparison (contrast analysis) applied to the main effect of Time and Type revealed that GBA was maximum in 150–250 and 250–350 time interval compared with 50–150 ms (respectively F(1,19) = 19,03, P b 0.001), (F(1,19) = 8.70, P b 0.001) and 350–450 ms (F(1,19)= 11.24, P b 0.001), (F(1,19)= 9.93, P b 0.001). Moreover, high arousal emotions have an increased GBA than low arousal emotions (fear vs happiness F(1,19)= 12.96, P b 0.001; vs sadness F (1,19)= 14.51, P b 0.001; vs neutral F(1,19)= 18.73, P b 0.001; anger vs happiness F(1,19)= 13.08, P b 0.001; vs sadness F (1,19)=14.11, P b 0.001; vs neutral F(1,19) = 18.16, P b 0.001). By analyzing interaction effects, high arousal stimuli showed increased power GBA in conscious condition than in unconscious condition (for fear F(1,19) = 10.99, P b 0.001; for anger F(1,19) = 14.04, P b 0.001). Secondly, larger synchronization was found for anger and fear in 150–250 and 250–350 poststimulus than 50–150 (F(1,19) = 12.16, P b 0.001; F(1,19) = 15.05, P b 0.001) and 350–450 ms (F(1,19) = 9.07, P b 0.001; F (1,19) = 10.91, P b 0.001). Finally, enhanced brain gamma oscillations were observed for conscious condition in second and third time intervals than unconscious condition (respectively F(1,19) = 8.83, P b 0.001; F(1,19) = 8.03, P b 0.001). No other post-hoc comparison was statistically significant. We can summarize these results pointing out that 150–350 ms post-

stimulus was significant in distinguishing GBA modulation, and that it was during this time that types of emotion (high/low arousing) and condition (conscious/unconscious) differences emerge. The second order of analysis took into account Laterality (2) and Location (3) effects. The analysis revealed differences for Laterality × Condition (F(1,19) = 7.78, P = 0.001), as well as Type × Laterality (F(4,19) = 10.99, P b 0.001). The second ANOVA revealed a significant Location × Condition (F(2,19) = 9.15, P b 0.001) and Location × Type ( F(8,19) = 11.34, P b 0.001) interaction effects. Specifically, as revealed by the contrast analysis, GBA synchronizes mainly in the left hemisphere than in the right hemisphere in supraliminal condition (F(1,19) = 6.85, P = 0.002). Moreover, emotional faces (both high and low arousing) elicited a dominance in power synchronization of right hemisphere than neutral faces (F (1,19) = 9.06, P b 0.001). Finally, as shown in Fig. 2, post-hoc comparisons showed that supraliminal stimuli induced an increased GBA in posterior than in the anterior (F(1,19) = 5.09, P = 0.002) or central (F(1,19) = 6.73, P = 0.002) sites. In parallel, all the emotional faces differed from the neutral faces in terms of local distribution on the scalp of GBA: emotional stimuli were more posterior (Pz) distributed than neutral stimuli. 4. Discussion The first main result of the study was that GBA was increased by presentation of a supraliminal emotional face in

Fig. 2. Supraliminal/subliminal comparison (ERD decreasing) as a function of: (a) right/left hemisphere; (b) anterior/central/posterior site.

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comparison with a subliminal presentation. Indeed for each type of emotions we revealed that increasing in gamma band synchronization was significantly higher for conscious emotional stimuli than for unconscious. Moreover, we observed an enhanced activity of gamma band during 150–350 ms poststimulus onset, such as an early oscillatory event that showed its peak at about 200 ms post-stimulus. This time range was found to be of main importance in emotional face processing, since it was found to be discriminant in distinguishing between types of emotion (low or high arousing power). Therefore, we can suppose that GABA modulation could represent conscious processing of the subjects for the emotional face during this early time (Keil et al., 2001). Secondly, in both supraliminal and subliminal condition we found that GBA modulation increased linearly as a function of the degree of arousal that subjects experienced for each facial stimulus. Indeed, we noticed a similar increasing of GBA for anger and fear in comparison with happiness, sadness and neutral stimuli despite the subthreshold or suprathreshold stimulation, and this increasing was more pronounced between 250–350 ms. We can hypothesize that GBA could be considered not only a marker of conscious elaboration of emotional expression but even an index of an enhanced activation (high level of perceived arousal) of the subject in elaborating significant stimuli, even if they prevent to reach the level of awareness. Moreover, this emotional-effect is observable mainly in the early time of stimulus elaboration. This suggestion is supported by ERP studies on emotion, and taken together these results demonstrate that difference in affective significance of a stimulus influences the brain activity during 150–350 time range (Balconi and Pozzoli, 2003; Sato et al., 2000). A related and interesting point is that information presented to subjects under subliminal condition may be processed on a high level even if the subject is not aware of this information. This is in line with studies that have examined psychophysiological responses to unconscious emotional stimuli: they were effective both in capturing attention and in eliciting autonomic response. Subliminal process appears to have a preattentive origin, because it can be observed to stimuli that are prevented from reaching conscious recognition. This fast processing has adaptive value because it allows an immediate response to a relevant and potentially threatening stimulus, and this system can operate even prior to the conscious appraisal of the stimulus. With regard of the lateralization effect, we found that the left hemisphere more than the right can mediate conscious elaboration, since a clear dominance of left side was found in the supraliminal condition. This result is in line with previous research, that underlined a left-conscious/right-unconscious dichotomy. Moreover, supraliminal faces were mainly elaborated in posterior sites if compared to subliminal faces. Clearly defined synchronization increase over posterior cortical sites in response to affective stimuli presented supraliminally could be attributed to specific function of posterior sites for conscious stimulation (Summerfield et al., 2002). To summarize, a leftposterior localization is supposed for consciousness. A second interesting result on cortical distribution of GBA is that both types of emotions (high or low arousing) induced greater

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synchronization over right-posterior regions of the scalp than neutral stimuli, and this is the case of both supra- and subliminal condition. This result may elucidate a different role of the two hemispheres in comprehending the emotional significance of a facial stimulus. As it was underlined, whereas anterior brain regions may be important for the modulation of the valence (pleasant/unpleasant), posterior regions of the right hemisphere may be involved in the modulation of arousal dimension. Indeed emotional (and more arousing stimuli) are preferentially elaborated in the posterior (and right) side than neutral (nonemotional) stimuli: for example Aftanas et al. (2002) pointed out a more posterior emotional vs nonemotional distribution of gamma oscillations, even it was observed specifically for the narrow bands (theta). In sum, gamma band can be represented as a marker of consciousness as well as of the subject's evaluation of the arousing power of emotional stimuli. In fact it is not only increased by an aware processing but it appears to differentiate high from lowarousing emotional faces. This effect was found in both supraliminal and subliminal condition. Moreover, GBA resulted more right-posterior distributed for emotional vs nonemotional stimuli, and more left-posterior localized in case of conscious elaboration in comparison with unconscious. More generally posterior sites appear to be discriminant for emotions, independently from the type of facial expression. Finally, methodologically the present results indicate that gamma frequency band analysis offers a powerful tool for studying cortical activation patterns during emotional information processing. References Aftanas, L.I., Varlamon, A.A., Pavlov, S.V., Makhnev, V.P., Reva, N.V., 2001. Affective picture processing: event-related synchronization within individually defined human theta band is modulated by valence dimension. Neurosci. Lett. 303, 115–118. Aftanas, L.I., Varlamon, A.A., Pavlov, S.V., Makhnev, V.P., Reva, N.V., 2002. Time-dependent cortical asymmetries induced by emotional arousal: EEG analysis of event-related synchronization and desynchronization in individually defined frequency bands. Int. J. Psychophysiol. 44, 67–82. Balconi, M., Pozzoli, U., 2003. Face-selective processing and the effect of pleasant and unpleasant emotional expressions on ERP correlates. Int. J. Psychophysiol. 49, 67–74. Balconi, M., Pozzoli, U., 2007. Event-related oscillations (EROs) and eventrelated potentials (ERPs) comparison in facial expression recognition. J. Neuropsychology 1, 283–294. Başar, E., 1999. Brain function and oscillations. II. Integrative brain function. Neurophysiology and cognitive processes. Springer, Heidelberg. Başar, E., Başar-Eroğlu, C., Karakaş, S., Schürman, M., 1999. Are cognitive processes manifested in event-related gamma, alpha, theta and delta oscillations in the EEG? Neurosci. Lett. 259, 165–168. Bernat, E., Bunce, S., Shevrin, H., 2001. Event-related brain potentials differentiate positive and negative mood adjectives during both supraliminal and subliminal visual processing. Int. J. Psychophysiol. 42, 11–34. Brázdil, M., Rektor, I., Dufek, M., Jurák, P., Pavel, D., 1998. Effect of subthreshold target stimuli on event-related potentials. Electroencephalogr. Clin. Neurophysiol. 107, 64–68. Bunce, S.C., Bernat, E., Wong, P.S., Shevrin, H., 1999. Further evidence for unconscious learning: preliminary support for the conditioning of facial EMG to subliminal stimuli. J. Psychiat. Res. 33, 341–347. Crick, F., Koch, C., 1998. Consciousness and neuroscience. Cereb. Cortex 8, 97–107.

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