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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 investigat-
ed using a variety of recording techniques. On one side, some
authors studied ERP correlates associated with face compre-
hension. 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
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
A
vailable online at www.sciencedirect.com
International Journal of Psychophysiology 67 (2008) 41 –46
www.elsevier.com/locate/ijpsycho
⁎Corresponding author. Tel.: +39 2 72342600; fax: +39 2 72342769.
E-mail address: michela.balconi@unicatt.it (M. Balconi).
0167-8760/$ - see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.ijpsycho.2007.10.002
(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 specifi-
cally to prolonged visual emotional stimulation (Krause et al.,
2000), and a synchronization was revealed in case of
coordinated response indicating readiness to process informa-
tion (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 modula-
tion 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 stimu-
lation. 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 distrib-
uted 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 asymme-
tries 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 post-
hoc 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
42 M. Balconi, C. Lucchiari / International Journal of Psychophysiology 67 (2008) 41–46
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
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,
Pb0.001), and post-hoc comparisons (Tukey) revealed that anger
and fear were considered more emotionally arousing than hap-
piness (respectively F(1, 19)= 10.16, Pb0.001; F(1, 19)= 9.74,
Pb0.001) and sadness (F(1, 19)= 11.69, P=0.001; F(1, 19)=
12.36, Pb0.001), as well as than neutral stimuli (F(1, 19)= 14.03,
Pb0.001; F(1, 19) = 15.41, Pb0.001).
3.2. ERD/ERS data
GBA showed sensitivity to Condition (F(1,19)= 7.07, P=
0.001), Type (F(4,19)= 10.12, Pb0.001), Time (F(3,19)= 8.55,
Pb0.001) and Electrodes (F(13,19)=13.09, Pb0.001), as well as
43M. Balconi, C. Lucchiari / International Journal of Psychophysiology 67 (2008) 41–46
for Condition× Type, Condition× Time (F(3,19)= 10.98,
Pb0.001), Time×Electrodes (F(39,19) = 14.89, Pb0.001), and
Typ e × Tim e ( F(12,19)= 11.22, Pb0.001).
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,
Pb0.001), (F(1,19)= 8.70, Pb0.001) and 350–450 ms (F(1,19)=
11.24, Pb0.001), (F(1,19)= 9.93, Pb0.001). Moreover, high
arousal emotions have an increased GBA than low arousal emo-
tions (fear vs happiness F(1,19)= 12.96, Pb0.001; vs sadness F
(1,19)= 14.51, Pb0.001; vs neutral F(1,19)=18.73, Pb0.001;
anger vs happiness F(1,19) = 13.08, Pb0.001; vs sadness F
(1,19)=14.11, Pb0.001; vs neutral F(1,19)= 18.16, Pb0.001).
By analyzing interaction effects, high arousal stimuli showed
increased power GBA in conscious condition than in uncon-
scious condition (for fear F(1,19) = 10.99, Pb0.001; for anger
F(1,19)= 14.04, Pb0.001). Secondly, larger synchronization
was found for anger and fear in 150–250 and 250–350 post-
stimulus than 50–150 (F(1,19) = 12.16, Pb0.001; F(1,19)=
15.05, Pb0.001) and 350–450 ms (F(1,19) = 9.07, Pb0.001; F
(1,19)= 10.91, Pb0.001). Finally, enhanced brain gamma
oscillations were observed for conscious condition in second
and third time intervals than unconscious condition (respec-
tively F(1,19)= 8.83, Pb0.001; F(1,19)= 8.03, Pb0.001). 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, Pb0.001). The second
ANOVA revealed a significant Location ×Condition (F(2,19) =
9.15, Pb0.001) and Location× Type (F(8,19) =11.34,
Pb0.001) 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, Pb0.001). 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. 1. ERD % for Emotion × Time interaction in gamma band. (a) Supraliminal; (b) Subliminal.
Fig. 2. Supraliminal/subliminal comparison (ERD decreasing) as a function of: (a) right/left hemisphere; (b) anterior/central/posterior site.
44 M. Balconi, C. Lucchiari / International Journal of Psychophysiology 67 (2008) 41–46
comparison with a subliminal presentation. Indeed for each type
of emotions we revealed that increasing in gamma band
synchronization was significantly higher for conscious emo-
tional stimuli than for unconscious. Moreover, we observed an
enhanced activity of gamma band during 150–350 ms post-
stimulus 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 ona 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 elabo-
rated 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 left-
posterior 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
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 low-
arousing 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, indepen-
dently from the type of facial expression. Finally, methodologi-
cally the present results indicate that gamma frequency band
analysis offers a powerful tool for studying cortical activation
patterns during emotional information processing.
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