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Laterality: Asymmetries of Body,

Brain and Cognition
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Lateralisation effect in
comprehension of emotional
facial expression: A comparison
between EEG alpha band power
and behavioural inhibition (BIS)
and activation (BAS) systems
a a
Michela Balconi & Guido Mazza
a
Catholic University of Milan , Italy
Published online: 17 Jun 2009.

To cite this article: Michela Balconi & Guido Mazza (2010) Lateralisation effect
in comprehension of emotional facial expression: A comparison between EEG
alpha band power and behavioural inhibition (BIS) and activation (BAS) systems,
Laterality: Asymmetries of Body, Brain and Cognition, 15:3, 361-384, DOI:
10.1080/13576500902886056

To link to this article: http://dx.doi.org/10.1080/13576500902886056

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 LATERALITY, 2010, 15 (3), 361
384

Lateralisation effect in comprehension of emotional

facial expression: A comparison between EEG alpha
band power and behavioural inhibition (BIS) and
activation (BAS) systems
Downloaded by [University of Tennessee, Knoxville] at 11:15 24 December 2014

Michela Balconi and Guido Mazza

Catholic University of Milan, Italy

Asymmetry in comprehension of facial expression of emotions was explored in the

present study by analysing alpha band variation within the right and left cortical
sides. Second, the behavioural activation system (BAS) and behavioural inhibition
system (BIS) were considered as an explicative factor to verify the effect of a
motivational/emotional variable on alpha activity. A total of 19 participants looked
at an ample range of facial expressions of emotions (anger, fear, surprise, disgust,
happiness, sadness, and neutral) in random order. The results demonstrated that
anterior frontal sites were more active than central and parietal sites in response to
facial stimuli. Moreover, right and left side responses varied as a function of
emotional types, with an increased right frontal activity for negative, aversive
emotions vs an increased left response for positive emotion. Finally, whereas higher
BIS participants generated more right hemisphere activation for some negative
emotions (such as fear, anger, surprise, and disgust), BAS participants were more
responsive to positive emotion (happiness) within the left hemisphere. Motivational
significance of facial expressions was considered to elucidate cortical differences in
participants’ responses to emotional types.

Keywords: EEG; Emotion; Face; Frequency band analysis; Hemispheric

differences.

Brain asymmetry in response to emotional stimuli has been investigated in

a several studies. Recent research demonstrated differences between the two
hemispheres as a function of the emotional content for linguistic content
(words) (Borod, Tabert, Santschi, & Strauss, 2000), movies (Hagemann,
Hewig, Naumann, Seifert, & Bartussek, 2005), and facial expressions of
emotions (Münte et al., 1998; Narumoto, Okada, Sadato, Fukui, &
Yonekura, 2001). The right hemisphere model supposes that the right side is

Address correspondence to: Michela Balconi, Department of Psychology, Catholic University

of Milan, Largo Gemelli, 1, Milan 20123, Italy. E-mail: michela.balconi@unicatt.it
# 2009 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business
http://www.psypress.com/laterality DOI: 10.1080/13576500902886056
 362 BALCONI AND MAZZA

specialised for the perception, expression, and experience of emotion,

regardless of the valence (positive or negative) of the emotional content
(Davidson & Schwartz, 1976; Heilman & Bowers, 1990). Some research
found that the left side of the face, controlled by the contralateral
hemisphere, is more active than the right side during emotional expression
(Borod, 1993; Borod, Haywood, & Koff, 1997; Williamson, Harrison,
Shenal, Rhodes, & Demaree, 2003). Regarding the perception of emotion,
recent studies on faces have demonstrated left visual field (right hemisphere)
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superiority for discriminating emotional faces (Adolphs, Damasio, Tranel, &

Damasio, 1996; Borod et al., 1998). Moreover, the specific response by the
right hemisphere was observed in the case of affective experience. In
addition, many studies have found evidence of increased right-sided cortical
activity for more anxious participants (for reviews see Heller, 1993; Nitschke,
Heller, & Miller, 2000).

ASYMMETRY IN FACIAL EXPRESSION OF EMOTIONS

With regard to facial expressions, affect discrimination has shown right
hemisphere superiority for discriminating emotional faces (Root, Wong, &
Kinsbourne, 2006). Brain-damage studies have confirmed this effect,
showing that patients with right hemisphere lesions performed worse than
patients with left hemisphere lesions in recognising facial expressions
(Adolphs et al., 1996; Ahern, Schomer, Kleefield, & Blume, 1991). More-
over, ERP and fMRI studies supported the hypothesis of right hemisphere
specialisation for the processing of facial emotions (Narumoto et al., 2001;
Sato, Kochiyama, Yoshikawa, Naito, & Matsumura, 2004; Vanderploeg,
Brown, & Marsh, 1987). With regard to the expression of emotions a facial
asymmetry was found, with a more expressive left side (right controlled)
during emotion expression (Borod et al., 1997; Gainotti, 1972). Also
identified was a reduced ability for facial emotional expression in the case
of right hemisphere damage.
Nevertheless, alternative hypotheses were recently formulated on the
lateralisation effect, which offered different explanations of hemispheric
differences. The valence model, as opposed to the right hemisphere hypoth-
esis, supposes that cortical differences between the two hemispheres are
attributable to positive vs negative valence of emotions (Everhart, Carpenter,
Carmona, Ethridge, & Demaree, 2003; Silberman & Weingartner, 1986). In
general, this model was tested for expression and perception of emotions, as
well as for emotional experience. Based on this model, the right hemisphere is
specialised for negative emotions and the left hemisphere for positive
emotions. A study found that reaction times were shorter for happy faces
presented to the right visual field (left hemisphere) (Reuter-Lorenz, Givis, &
 LATERALITY AND EMOTIONAL FACIAL EXPRESSION 363

Moscovitch, 1983) and, on the contrary, negative affective faces were

identified more rapidly when presented within the right visual field (Everhart
& Harrison, 2000). Generally, right hemisphere injury prevents the patient
from processing more negative vs positive expressions (Borod et al., 1998).
Some EEG research has supported the valence hypothesis: relative increase
of left hemisphere activity was found with positive emotional states
(Davidson & Henriques, 2000; Waldstein et al., 2000), although other EEG
studies have also found some opposite results (for example, Schellberg,
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Besthorn, Pfleger, & Gasser, 1993).

More recently, the approach-withdrawal model of emotion regulation
posits that emotional behaviours are associated with a balance of activity in
left and right frontal brain areas that can be explained in an asymmetry
measurement (Davidson, 1995; Harmon-Jones & Allen, 1997; Sutton &
Davidson, 1997). Resting frontal EEG asymmetry has been hypothesised to
relate to appetitive (approach-related) and aversive (withdrawal-related)
motivation and emotion, with heightened approach tendencies reflected in
left frontal activity and heightened withdrawal tendencies reflected in relative
right frontal activity (Davidson, 1992). Participants with relatively less left
than right frontal activity exhibit larger negative affective responses to
negative aversive emotions and smaller positive affective responses to
positive approach emotions (Wheeler, Davidson, & Tomarken, 1993).
Some interesting results were collected in response to specific emotional
patterns. In particular, sadness was correlated positively with right alpha
power and negatively with left alpha power, whereas happiness was mainly
related to left-side activation (Davidson & Fox, 1982). For other emotions,
such as anger, results were more heterogeneous. More generally, lateralised
electrophysiological parameters (decreased alpha power EEG), measured
during the recollection of events associated with anger, increased within the
right hemisphere (Waldstein et al., 2000). However, contrasting results have
been collected in some studies (Coan, Allen, & Harmon-Jones, 2001).
Increased left frontal cortical activity was associated with anger (Harmon-
Jones & Sigelman, 2001). In addition, increased left frontal activity and
decreased right frontal activity were associated with trait anger (Harmon-
Jones & Allen, 1998) and state anger (Harmon-Jones & Sigelman, 2001).
These two models make different previsions on the lateralisation of the
emotion of anger. The approach
withdrawal model predicts that anger will
be associated with relatively greater left frontal activity, whereas the valence
model would predict more right frontal activity. This is due to the fact that,
in line with the approach
withdrawal model, anger is considered an
approach motivational tendency with a negative valence (Harmon-Jones &
Sigelman, 2001; Harmon-Jones, Sigelman, Bohlig & Harmon-Jones, 2003;
Lazarus, 1991) and not a negative emotion per se, and that approach
motivation would be correlated to increased left frontal cortical activity
 364 BALCONI AND MAZZA

regardless of the valence of the emotional cue. These heterogeneous trends

need a deeper analysis in order to explain the contrasting results observed.

EMOTIONAL TYPE EFFECT

As shown by previous studies, lateralisation effect in facial expression
perception may be explained by the right-side, the valence, or the approach

withdrawal models, and many data have been furnished in support of these
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different hypotheses. Nevertheless some contrasting results remain to be

explained, mainly about the real significance of each emotion with respect to
its functional value. According to this assumption, the ‘‘functional model’’
of emotional expression supposes that people adopt a behaviour that is
functional to their coping activity (Frijda, 1994; Frijda, Kuipers, &
Terschure, 1989). Coping activity determines the significance of the
emotional situation, since it is able to orient the participant’s behaviour as
a function of the individual expectancies about successfully acting to alter
the situation/external context. In fact, whereas some negative emotional
expressions, such as anger and sadness, are generated by negative, aversive
situations, the coping potential may introduce some differences in subjective
response as a function of how people appraise their ability to cope with the
aversive situation (Frijda, 1993; Hewig, Hagemann, Seifert, Naumann, &
Bartussek, 2004; Lazarus, 1991). From this perspective, anger may be
appraised as a negative but also an active emotion that arouses approach
motivation.
In this view, facial expressions are an important key to explaining the
emotional situation and, consequently, they can produce different reactions
in a viewer. As a whole, the significance of emotional expressions for the
participant (in terms of their high/low averseness, valence, and coping
potential related to the corresponding emotion) should influence both the
physiological and cognitive level, with interesting correspondence on EEG
modulation. It was assumed that emotional expressions are distributed
along a continuum as a function of the motivational significance of the
emotional cue in terms of averseness (from higher to lower) and hedonic
value (from negative to positive) and coping potential (Balconi & Lucchiari,
2007; Sato, Kochiyama, Yoshikawa, & Matsumura, 2001; Streit, Wolwer,
Brinkmeyer, Ihl, & Gaebel, 2000).

BIS/BAS SYSTEMS AND BEHAVIOURAL RESPONSE TO

EMOTIONAL CUES
Another main factor affecting participants’ response to facial expressions of
emotions was the subjective sensitivity to the environmental emotional cues
 LATERALITY AND EMOTIONAL FACIAL EXPRESSION 365

(Allen & Kline, 2004). The role that temperament plays in influenc-
ing cortical responses was confirmed by several empirical studies, in both
normal and pathological samples. For example, it was shown that high
anxiety trait is directly related to increased accuracy for negative facial
expressions presented to the left visual field (right hemisphere) in compar-
ison with low anxiety trait (Everhart & Harrison, 2000; Heller, 1993).
Two main models were adopted to explain asymmetries in brain activity
within the frontal areas: the dispositional model of frontal affective style,
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which postulates that people possess a general tendency to respond pre-

dominantly with either an approach or a withdrawal behaviour despite the
situational differences (Davidson, 1998); and the situational model, such as the
capability model, which postulates that individual differences are better
represented as interactions between the emotional demands of specific
situations and the emotion-monitoring abilities individuals use to respond
to those situations (Coan, Allen, & McKnight, 2006; Lilienfeld, Wood, &
Garb, 2000; Wallace, 1966). Nevertheless, few studies have investigated the
relationship between comprehension of facial expressions and subjective
predisposition to respond to emotions. Second, the impact of these predis-
positions on cortical lateralisation has been underestimated.
Gray has attempted to explain behavioural motivational responses in
general and, second, the generation of emotions that are relevant to approach
and withdrawal behaviour (Gray, 1981; Gray & McNaughton, 2000). Gray’s
model supposes that two anatomical pathways underlying emotional/
motivational systems are the behavioural activation (or facilitation, BAS)
and behavioural inhibition (BIS) systems. The BAS appears to activate
behaviour in response to conditioned, rewarding stimuli and in relieving
nonpunishment. This system is putatively responsible for both approach and
active behaviours, and emotions associated with these behaviours generally
induce the participant to approach the event/object that generated the
emotional response. Animal research suggests that the BAS is mediated by
mostly dopaminergic pathways emanating from the ventral tegmental area to
the nucleus accumbens and ventral striatum (Fowles, 1994; Nöthen,
Erdmann, Körner, & Lanczik, 1992). The BIS, conversely, inhibits behaviour
in response to stimuli that are novel, innately feared, and conditioned to be
aversive. The aversive motivational system is responsive to nonreward,
preventing the participant from experiencing negative or painful outcomes.
Gray also held that BIS functioning is responsible for the experience of
negative feelings such as fear and anxiety in response to these cues (Gray,
1987, 1994). Thus, each of two motivational systems is presumed to be
uniquely related to one broad affective quality, the BAS to positive-approach
affect and the BIS to negative-withdrawal affect, and to be unrelated to the
alternative affect.
 366 BALCONI AND MAZZA

Empirical data suggest the left and right frontal activity may reflect the
strength of BAS and BIS activity respectively. Previous studies have found
that resting frontal EEG asymmetry is related to measures of BAS sensitivity.
Carver and White (1994) formulated a psychometric response to Gray’s
construct by ideating the BIS/BAS Scales. These measures allow quantifica-
tion of the prevalence of behavioural inhibition or behavioural activation
based on four subscales (Jorm et al., 1999). Specifically, individuals with
relatively greater left frontal activity (less alpha) should possess greater levels
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of BAS sensitivity (approach motivation) (Coan & Allen, 2003; Harmon-

Jones & Allen, 1997; Sutton & Davidson, 1997), whereas participants with
higher BIS scores should have greater right frontal activation (Sutton &
Davidson, 1997). This result was interpreted considering that BAS and
frontal EEG asymmetry are part of the same approach motivation system.
BAS participants may respond in great measure to positive, approach-related
emotions, such as the expression of happiness and positive affect, that allow
the participant to have a favourable behaviour towards the environment
(Davidson, Ekman, Saron, Senulis, & Friesen, 1990; Tomarken, Davidson,
Wheeler, & Kinney, 1992). Nevertheless, it is also possible that BAS may be
responsible for negative affective responses when these responses are
associated with behavioural approach. Since the primary function of the
BAS is approach motivation, and approach motivation may be associated
with negative affect, some negative emotional faces, like anger, may also be
associated with an increased BAS profile (Harmon-Jones & Sigelman, 2001).
Consistent with this idea, Corr (2002) found that high levels of BAS were
associated with higher expectancies for rewards, which should cause higher
levels of frustration upon termination or reduction of the magnitude of
reward.

OBJECTIVES AND HYPOTHESES

The present study analysed cortical activation, taking into account the
subjective motivational attitude using BIS/BAS measures. Although we did
not directly explore the effect produced in the viewer by the facial
expressions in terms of valence and approach
withdrawal significance by a
self-report measure, a specific analysis was conducted on the cortical
response to each emotional pattern, in order to test the relationship among
motivational systems, alpha modulation, and emotional cues. Currently, no
specific study has explored the relationship among comprehension of an
ample range of facial expressions of emotion, BAS/BIS motivational system
effect, and asymmetrical responses in brain activity. Since asymmetrical
electroencephalogram (EEG) alpha activity over anterior regions of the
 LATERALITY AND EMOTIONAL FACIAL EXPRESSION 367

scalp predicts a variety of measures of interest to emotion research

(Cacioppo, 2004), in the present work we intend to analyse the following:

1. First, the relationship between facial expression of emotions and

cortical responses by measuring EEG activity (alpha power). Our goal
was to analyse the lateralisation effect of EEG as a function of the
different emotional type. An ample range of emotions was used in this
study, in order to test the subjective response to different facial
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expressions, valenced as positive or negative, and more or less aversive

with regard to their content. We expected that, varying along the level
of averseness and valence, each facial expression would induce different
responses in the left and right hemispheres. In particular, frontal
responses tend to be modulated by emotional type, with a left
prevalence for positive approach expressions vs negative withdrawal
faces (an ampler response for happiness than anger and fear) and vice
versa for the right hemisphere.
2. The relationship between EEG alpha modulation and BAS/BIS
sensitivity. The second goal was to show the prevalence in responding
to approach emotional cues by high-BAS participants and, conversely,
to negative aversive cues by high-BIS participants. In particular, BIS
participants may be more attentive to some types of emotional
expressions, such as emotions that represent a potential threat and
that are potentially aversive for the person. For this reason, relatively
greater right than left frontal activity is expected for BIS participants in
response to particular aversive stimuli: their EEG response should
result in a greater synchronisation for negative emotions that produce a
potential avoidance by the person (mainly fear and disgust). Some
contrasting expectations are related to anger, which was found to
generate different responses in the participants. Specifically, the facial
expression of anger may induce an aversive response by the person,
presumably a fear response, thus being associated with a more right
than left side response. On the other hand, BAS participants may be
more responsive to positive, approach emotions, and their left more
than right frontal cortical activity would be related to heightened
approach-related dispositional tendencies in response to emotions like
happiness.
3. The lateralisation effect as a function of both BAS/BIS construct and
the significance of emotions. The third goal considered whether BAS
participants were more responsive to positive, approach facial expres-
sion, with an increased left lateralisation activity (alpha reduction).
A contrasting response, increased for negative and aversive emotions in
right cortical side, was expected for BIS participants.
 368 BALCONI AND MAZZA

METHOD
Participants
A total of 19 healthy volunteers took part in the study (11 women, age range
19
25, mean23.37, SD2.13). They were all right-handed and with
normal or corrected-to-normal visual acuity. Exclusion criteria were history
of psychopathology for the participant or immediate family. They gave
informed written consent for participating in the study.
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Stimulus materials
Stimulus materials were taken from the set of pictures of Ekman and Friesen
(1976). They were black and white pictures of a male actor, presenting
respectively a happy, sad, angry, fearful, surprised, disgusted, or neutral face.

Procedure
Participants 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 randomised order in the centre of the computer
monitor, with a horizontal angle of 48 and a vertical angle of 68 (STIM 4.2
software). Each expression was presented 20 times, resulting in a total of 140
stimuli. The stimulus was presented for 200 ms, with an inter-stimulus
interval of 200 ms.
During the examination, the participants were requested to minimise
blinking. Participants were required to observe the stimulus during EEG
recording (passive task). An explicit response to the emotional features of
the stimulus was not required. This was done for three main reasons: to
assure the task was passive (implicit elaboration of emotions); to avoid
causing participants to be more attentive to the emotional stimuli than the
neutral ones; and to reduce motor potentials. Prior to recording EEG, the
participant was familiarised with the overall procedure. During the training
session every participant saw, in random order, all the emotional stimuli
presented in the successive experimental session (a block of 14 trials, each
expression type repeated twice).
A post-experimental phase allowed evaluation of the accuracy with which
participants categorised each emotional expression. After completing the
experimental trials, the participant was asked to identify the emotion viewed
using a free choice response. The participants correctly recognised the
emotional value of the facial stimuli. Specifically, a correct identification and
a high judgement agreement was found for happiness (86.96%; on a five-point
 LATERALITY AND EMOTIONAL FACIAL EXPRESSION 369

Likert scale: M4.32; SD.56), surprise (86.97%; M4.27; SD.76),

anger (73.91%; M3.95; SD.72), fear (91.30%; M4.41; SD.79),
disgust (91.30%, M3.95; SD.89), and sadness (78.26%; M3.82; SD
.18).

BIS/BAS scores
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BIS and BAS scores were calculated for each participant taking into account
the Italian version of the Carver and White questionnaire (Leone, Pierro, &
Mannetti, 2002). The questionnaire was administered to the participants
after completing the experimental phase. Based on these measures, two total
scores (BIS and BAS total) and three BAS subscale scores (Reward, Drive,
and Fun Seeking) were calculated. The mean values and standard deviations
for each scale were 19.45 (3.45) for BIS, 39.56 (4.83) for BAS; 15.29 (1.89) for
Reward, 11.20 (2.87) for Drive, and 12.76 (3.65) for Fun Seeking. Finally,
Cronbach’s alpha was calculated for BIS (0.81) and BAS (0.74) and
separately for each BAS subscale (Reward 0.72; Drive 0.69, and Fun
Seeking 0.75).

EEG data reduction

The EEG was recorded with a 32-channel DC amplifier (SYNAMPS
system) and acquisition software (NEUROSCAN 4.2). An ElectroCap with
Ag/AgCl electrodes was used to record EEG from active scalp sites referred
to linked earlobes (10/20 system of electrode placement). Additionally two
EOG electrodes were sited on the outer side of the eyes. The data were
recorded using an amplified sampling rate of 256 Hz, with a frequency band
of 0.1 to 60 Hz (60-Hz notch filter enabled). The impedance of recording
electrodes was monitored for each participant prior to data collection, and it
was always below 5 kv. After EOG correction and visual inspection, only
artefact-free trials were considered. Only 14 electrodes were used for the
subsequent statistical analysis (4 central, Fz, Cz, Pz, Oz; 10 lateral, F3, F4,
C3, C4, T3, T4, P3, P4, O1, O2). Specifically, EEG signals were visually
scored on a high-resolution computer monitor and data contaminated by
eye movements or muscle artefacts were removed (rejected epochs 10.4%).
Subsequently, the digital EEG data were bandpass filtered in alpha
frequency bands (8
12 Hz) (Cooper, Croft, Dominey, Burgess, & Gruzelier,
2003). To obtain a signal proportional to the power of the EEG frequency
band, the filtered signal samples were squared (Pfurtscheller, 1992). Then the
data were epoched, using a time window of 400 ms (0
400 ms). The power
spectra were derived by means of the fast Fourier transform method (FFT)
 370 BALCONI AND MAZZA

for each epoch and then averaged across epochs within each emotion type.
An average of about 20 epochs comprised the data for each emotion.

RESULTS
Phase 1
The dependent variable of alpha power was entered into two three-way
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ANOVAs using the following repeated factors: emotion (7)site (3: frontal/
central/parietal)side (2: right/left). BIS and BAS (z-standardised) were
used as covariates in the ANOVA design. To assess lateralisation, a lateral
electrode factor (left: F4, C4, P4, vs right: F3, C3, P3) was created. At the
same time, frontal (F4 and F3), central (C4 and C3), and parietal (P4 and
P3) sites were calculated. Type I errors associated with inhomogeneity of
variance were controlled by decreasing the degrees of freedom using the
Greenhouse-Geiser epsilon. Tables 1 and 2 report the mean power of alpha
for each emotion as a function of cortical sites (frontal, central, and parietal)
and side (right and left), and the F values of first ANOVA for the statistically
significant effects.
Planned contrasts applied to main effect of emotion showed differences
between anger and sadness, F(1, 18)8.12, p.001, h2 .38, and fear and
sadness, F(1, 18)8.01, p.001, h2 .36, with a decreased alpha power
(increased activity) for anger and fear respectively. Moreover, neutral
stimulus differed from the other emotions, respectively compared with anger
F(1, 18)10.11, p.001, h2 .39, fear F(1, 18)13.01, p.001, h2 .38,
surprise F(1, 18)9.15, p.001, h2 .39, disgust F(1, 18)5.67, p.001,
h2 .43, happiness F(1, 18)9.10, p.001, h2 .33, and sadness F(1, 18)
9.96, p.001, h2 .39. Second, as shown by contrast analysis, frontal sites
were more activated than central, F(1, 18)13.22, p.001, h2 .40, and
parietal, F(1, 18)8.98, p.001, h2 .32, ones. Simple effects applied to
emotionsite interaction showed an increased frontal activity in comparison
to central and parietal sites respectively for anger F(1, 18)12.76, p.001,
h2 .35; F(1, 18)15.66, p.001, h2 .40, fear F(1, 18)14.32, p .001,
h2 .40; F(1, 18)15.40, p.001, h2 .43, happiness F(1, 18)10.03, p
.001, h2 .30; F(1, 18)10.09, p.001, h2 .36, surprise F(1, 18)11.13,
p.001, h2 .35; F(1, 18)14.55, p.001, h2 .43, and disgust F(1, 18)
13.04, p.001, h2 .37; F(1, 18)12.21, p.001, h2 .36. In addition, as
shown in Figure 1a, simple effects (emotionside) revealed an increased
activity in frontal right cortical side for anger as compared to happiness F(1,
18)10.10, p.001, h2 .38, sadness F(1, 18)22.51, p.001, h2 .50,
and neutral faces F(1, 18)24.33, p.001, h2 .55; fear compared to
happiness F(1, 18)14.18, p.001, h2 .42), sadness F(1, 18)12.76, p
.001, h2 .46, and neutral faces F(1, 18)24.26, p.001, h2 .50; surprise
 LATERALITY AND EMOTIONAL FACIAL EXPRESSION 371
TABLE 1
Mean absolute power of alpha band EEG for emotion, side, and site

Frontal Central Parietal Right Left

M (SD) M (SD) M (SD) M (SD) M (SD)

Anger 6.78a 1.23 9.80 1.11 11.26 0.83 8.96 1.05 9.65 1.16
Fear 7.32 1.34 9.05 0.94 9.87 0.94 7.60 1.27 8.98 1.09
Disgust 6.89 1.65 8.45 0.88 8.11 1.16 6.74 0.75 8.20 0.78
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Surprise 7.90 1.09 9.32 1.43 10.06 1.32 9.18 0.83 10.01 0.87
Happiness 8.43 1.87 10.65 1.12 11.22 1.27 13.45 1.06 6.77 1.15
Sadness 11.87 0.78 11.24 0.82 11.76 1.10 11.55 1.38 11.79 1.23
Neutral 12.33 1.03 12.98 0.92 11.65 1.04 12.73 1.15 12.01 0.98

a
 measured in mVolt2.

compared with sadness F(1, 18)19.65, p.001, h2 .48, and neutral faces
F(1, 18)13.18, p.001, h2 .40. Moreover, an increased activity was
found in the left frontal area for happiness compared with anger, F(1, 18)
21.12, p.001, h2 .52, and fear F(1, 18)16.54, p.001, h2 .49.

TABLE 2
Repeated measure ANOVA with emotion, site, and side as within-factors and
BIS/BAS as covariate

Source df F

BIS
Emotion 6 18.22
Site 2 11.32
Emotion BIS 6 12.33
Emotion Side 6 20.54
Emotion Site 12 15.42
Emotion Site Side 12 10.04
Emotion Side BIS 6 19.56
Emotion Site BIS 12 17.09
Emotion Site Side BIS 12 18.56
BAS
Emotion 6 19.00
Site 2 11.53
Emotion BAS 6 14.68
Emotion Side 6 21.52
Emotion Site 12 15.56
Emotion Site Side 12 13.05
Emotion Side BAS 6 15.67
Emotion Site BAS 12 19.80
Emotion Site Side BAS 12 14.34

p 5 .001
 372 BALCONI AND MAZZA
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Figure 1. Absolute power of alpha (mVolt2) for right and left frontal site.
 LATERALITY AND EMOTIONAL FACIAL EXPRESSION 373

Simple effects applied to emotionBIS, emotionsiteBIS and

emotionsideBIS interactions showed an increased cortical activity for
anger, fear, and disgust in higher BIS participants, in comparison with the
other emotions*anger vs sadness F(1, 18)13.45, p.001, h2 .41, and
happiness F(1, 18)15.12, p.001, h2 .45; fear vs sadness F(1, 18)15.66,
p.001, h2 .47, and happiness F(1, 18)16.12, p.001, h2 .43; disgust
vs sadness F(1, 18)16.56, p.001, h2 .49, and happiness F(1, 18)15.55,
p.001, h2 .46. Neutral face differed from all the other emotions. More-
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over, anger, fear, surprise, and disgust produced an increased response for BIS
within the frontal compared to central*respectively F(1, 18)13.44, p
.001, h2 .43, F(1, 18)17.76, p.001, h2 .46, F(1, 18)16.09, p.001,
h2 .43, F(1, 18)21.10, p.001, h2 .52*and parietal sites*respectively
F(1, 18)16.90, p.001, h2 .44, F(1, 18)17.90, p.001, h2 .47, F(1,
18)29.23, p.001, h2 .52, F(1, 18)15.02, p.001, h2 .42. Right
hemisphere was more active than left hemisphere for BIS in response to anger
F(1, 18)13.33, p.001, h2 .37, fear F(1, 18)20.15, p.001, h2 .45,
surprise F(1, 18)15.32, p.001, h2 .38, and disgust F(1, 18)19.04, p
0.001, h2 .49. Finally a significant right frontal activation was found for
anger and fear, more than left frontal*respectively F(1, 18)14.89, p.001,
h2 .38, F(1, 18)13.20, p.001, h2 .33*and the other central and
parietal sites.
For the second ANOVA, planned contrasts applied to main effect of
emotion showed differences between anger and sadness F(1, 18)7.45, p
.001, h2 .34, fear and sadness F(1, 18)8.90, p.001, h2 .35, and fear
and happiness F(1, 18)6.13, p.001, h2 .32, with a decreased alpha
power (increased activity) for anger and fear respectively.
Moreover, neutral stimulus differed from the other emotions, respectively
compared with anger F(1, 18)8.15, p.001, h2 .37, fear F(1, 18)10.11,
p.001, h2 .34, surprise F(1, 18)10.03, p.001, h2 .38, disgust F(1,
18)12.67, p.001, h2 .38, happiness F(1, 18)9.60, p.001, h2 .30,
and sadness F(1, 18)8.03, p.001, h2 .33.
Frontal sites were more activated than central, F(1, 18)10.07, p.001,
h2 .31, and parietal sites, F(1, 18)8.42, p.001, h2 .28. Simple effects
applied to emotionsite interaction showed an increased frontal activity in
comparison to central and parietal sites respectively for anger F(1, 18)
16.98, p.001, h2 .40; F(1, 18)10.65, p.001, h2 .36, fear F(1, 18)
13.24, p.001, h2 .39; F(1, 18)18.06, p.001, h2 .48, and surprise
F(1, 18)9.15, p.001, h2 .36; F(1, 18)16.05, p.001, h2 .43.
Simple effects applied to emotionside revealed an increased activity in
frontal right cortical side for anger compared to happiness F(1, 18)12.14,
p.001, h2 .40, and neutral faces F(1, 18)23.87, p.001, h2 .52; fear
compared to happiness F(1, 18)14.21, p.001, h2 .43), sadness F(1,
18)23.78, p.001, h2 .57, and neutral faces F(1, 18)27.77, p.001,
 374 BALCONI AND MAZZA

h2 .55. Moreover, an increased activity was found within the left frontal
area for happiness compared with anger F(1, 18)24.89, p.001, h2 .55,
fear F(1, 18)15.66, p.001, h2 .52, disgust F(1, 18)21.67, p.001,
h2 .52, and surprise F(1, 18)17.89, p.001, h2 .47.
Simple effects calculated for emotionBAS, emotionsideBAS and
emotionsiteBAS interactions showed a decreased alpha (increased
activity) for happiness in higher BAS participants, in comparison with the
other emotions*respectively sadness F(1, 18)20.87, p.001, h2 .52, fear
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F(1, 18)18.16, p.001, h2 .49, anger F(1, 18)21.13, p.001, h2 .50,

disgust F(1, 18)16.78, p.001, h2 .48, surprise F(1, 18)15.09, p.001,
h2 .43, and neutral F(1, 18)13.43, p.001, h2 .36. Second, happiness
produced an increased response for BAS within the frontal than central, F(1,
18)21.45, p.001, h2 .53, and parietal sites, F(1, 18)19.58, p0.001,
h2 .49. In addition, left hemisphere was more active than right hemisphere
in response to happiness, F(1, 18)21.05, p.001, h2 .52. Finally a
significant left frontal activation was found for happiness than right frontal,
F(1, 18)12.49, p.001, h2 .31, and the other central and parietal sites.

Phase 2
Pearson’s correlation was applied to EEG measures and BIS/BAS scores for
each emotion in the six cortical sites considered separately.

BIS measure. Table 3 reports the Pearson’s coefficients for each total
score of BIS and BAS related to each emotion. With respect to fear, Pearson
correlation between BIS and frontal sites showed significant effects. As can
be seen, a significant negative correlation was found between BIS and alpha
activity. Specifically, decreased alpha power (increased cortical activity) is
correlated to higher BIS measures in the right frontal (F4) site. Conversely,
the left frontal site (F3) was not related to BIS score. An inverse correlation
was also revealed between F3/F4. The same statistical trend was found for
anger: higher BIS participants showed more right frontal activation and no
significant correlation with the left hemisphere. Right and left frontal sites
(F3/F4) were negatively correlated with each other.
Surprise showed a significantly increased activity for BIS participants in
both right and left frontal sites, whereas no other comparison was statistically
significant. Also, an asymmetrical frontal activation was found between F3
and F4. Disgust showed an alpha reduction (cortical activation) for BIS
participants in the right frontal site and an activity reduction in the left side.
Conversely, no significant correlation was revealed for BIS in response to
happiness. Finally, sadness and neutral faces were not significantly correlated
with left/right alpha activation for BIS.
 LATERALITY AND EMOTIONAL FACIAL EXPRESSION 375
TABLE 3
Correlation matrix (Pearson’s correlation) for alpha power and BIS/BAS

Anger Fear Surprise Disgust Happiness Sadness Neutral

BIS
F3 .10 .15 .40** .46** .11 .16 18
F4 .48** .53** .40** .38** .16 .17 .20
C3 .16 .16 .26** .26** .16 .16 .11
C4 .18** .18** .18** .18** .18** .18** .16
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P3 .11** .11** .16** .16** .13** .16** .16**

P4 .12* .20** .22** .20** .20** .20** .17
BAS
F3 .16 .18 .12 .18 .53** .18 15
F4 .13 .15 .29* .10 .13 .11 .15
C3 .18 .16 .20 .16 .12 .22 .11
C4 .18** .11** .18** .18** .20** .18** .17
P3 .10** .11** .15** .11 .13** .14** .10**
P4 .17* .20** .22** .20** .10** .17** .17

BAS measure. BAS showed an absence of significant correlation with

alpha power for fear in the right and left sides (see Table 3). Similar results
were found for anger and disgust, with no significant correlational index in
the right and left side for BAS participants. Surprise showed a significant
activity reduction for high BAS in the right side. Conversely, happiness
revealed a higher cortical response by the left frontal side for BAS (alpha
decreasing). Finally, sadness and neutral faces were not significantly
correlated with left/right alpha activation for BAS participants.

DISCUSSION
Three main points can synthesise the results found by the present research:

1. First, a clear frontal cortical activity was revealed in response to

emotional faces, specifically for the emotions of fear, anger, surprise,
disgust, and happiness. On the other hand, brain sites were not
differentiated as a function of sadness and neutral faces, since cortical
activation was equally distributed on frontal, central, and parietal sites.
2. Second, the right frontal area was differentially activated by facial
expression types: the right anterior side was mainly responsive to the
emotions of anger, fear, and surprise as compared to sadness or positive
(happiness) emotions and neutral stimuli. On the contrary, happiness
activated the left more than the right cortical side.
 376 BALCONI AND MAZZA

3. Third, BIS and BAS were significant measures in distinguishing the

participants’ responses to facial expressions. Specifically, the contribu-
tion of motivational responses to alpha modulation was identified, with
an increased sensitivity of BIS participants to negative and aversive
emotions (mainly anger, fear, disgust, and surprise) and of BAS to the
positive emotion of happiness.

We discuss these three points in detail. First, the findings from EEG alpha
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activity lend support to increased frontal, more than central or posterior,

cortical activity in response to facial expressions of emotions. Previous
studies have underlined the significance of frontal sites for face perception:
a general frontal facilitation effect was found for facial stimulus process-
ing than posterior or temporal areas (Kanwisher, 2000; Liu, Harris, &
Kanwisher, 2002). Nevertheless, other results appear to be partly in contrast
with the frontal specialisation for emotional face comprehension, since they
showed that broad regions of the occipital and temporal cortices, particularly
within the right hemisphere, evidenced increased activity during the viewing
of facial expressions (Sato et al., 2004). This apparent divergence could be
due to the fact that some research was based on dynamic facial stimuli instead
of static faces, such as those used in the present research.
Second, greater right than left side activation was found for some negative
emotions and a reverse tendency (left more than right side) was found for the
positive emotion of happiness. In addition, the absence of a significant left
side activation in response to negative faces and, conversely, of right side to
positive faces reinforced these results. Thus, negative emotional stimuli are
able to induce a more intense response by the right hemisphere, whereas
positive ones are responsible for a more accentuated left response. A possible
explanation for this finding may be that the right hemisphere selectively
attends more to negative facial stimuli and, conversely, the left hemisphere
shows increased attention towards positive faces. In fact, studies applied to
normal or clinical samples have found hemispheric differences as a function
of positive vs negative emotions; differences that are attributable to the
facility of the two hemispheres to identify specific emotional types (Adolphs
et al., 1996; Borod et al., 1998; Everhart et al., 2003). For example, it was
found that reaction times were shorter for happy faces shown within the
right visual field (left hemisphere) and sad faces presented within the left
visual field (right hemisphere) (Reuter-Lorenz et al., 1983).
Nevertheless, a main critical point to be discussed in the present
contribution is the fact that the right frontal prevalence was found for all
the negative emotional faces but not for sadness. This result contrasted with
the previous right side negative hypothesis, and it is unexplained by other
empirical investigations (see for example, Reuter-Lorenz et al., 1983).
Nevertheless, it should be noted that some EEG researchers, investigating
 LATERALITY AND EMOTIONAL FACIAL EXPRESSION 377

the positive
negative distinction, have also found opposite patterns of

activation (Cole & Ray, 1985; Tucker & Dawson, 1984). Based on these data,
a more exhaustive paradigm of analysis may be adopted in order to explain
our results, taking into account both the valence (positive vs negative) and
degree of averseness of the emotional stimuli (high vs low). The circumflex
model is able to explain the right frontal facilitation for some emotional
types*that is, the negative, high-arousal, aversive emotional expressions*
and the right frontal inhibition for those emotions that have a less-arousing
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power, with a concomitantly reduced significance in producing a lateralisa-

tion effect (Russell, 2003; Russell & Bullock, 1985). Although we did not
directly test the arousing power and averseness of each emotional face,
previous studies have underlined the differential impact of anger, fear, and
disgust on facial expressions in comparison to sadness (Balconi & Pozzoli,
2003; Junghöfer, Bradley, Elbert, & Lang, 2001; Morita, Morita, Yama-
moto, Waseda, & Maeda, 2001).
The circumflex model predicts that the structure of emotional expression
and comprehension is related to a roughly circular order in a two-dimensional
space, the axes of which could be interpreted as pleasure
displeasure and
arousal
sleepiness. In particular, the two orthogonal axes allow for a clear
categorisation of emotion perception, subdividing the entire emotional
universe as a function of arousal response produced by emotional patterns
in addition to the negative/positive value they have. In general, it is possible
that the higher aversive and arousing stimuli (fear, anger, disgust, and surprise)
may have induced a clear cortical lateralisation within the right side, whereas
sadness generates a less significant response by the participants. Moreover,
a particular effect was related to anger, which was found to induce increasing
right more than left cortical activity. Previous studies on anger experience
have also found an opposite pattern, with more left than right hemi-
sphere activation (Harmon-Jones et al., 2003). This result is consistent with
the position that anger is an approach motivational tendency with negative
emotional valence (Berkowitz, 1999; Harmon-Jones et al., 2003) and, more
generally, left frontal activity is associated with approach motivation,
regardless of the valence (positive vs negative) of the emotion. In the present
investigation the right cortical activation could be explained by taking into
account that, in most cases, an angry face generates a fear response in the
viewer and, for this reason, it is possible that the anger profile could be similar
to fear.
The third main point is related to the subjective response to the emotional
cues, as a function of behavioural activation (BAS) and inhibition (BIS)
systems, that may have an effect on the hemispheric differences. Previous
research has found that, generally, persons with higher BAS scores have an
increased left frontal activation (Coan & Allen, 2003; Harmon-Jones &
Allen, 1997), whereas individuals with higher BIS scores have greater right
 378 BALCONI AND MAZZA

frontal activation (Sutton & Davidson, 1997). Moreover, persons with high
BAS and BIS scores experience more positive and negative affect,
respectively, during everyday experiences (Gable, Reis, & Elliot, 2000), and
they have more sensitivity to positive (BAS) or negative (BIS) cues (Sutton &
Davidson, 2000). These findings are consistent with data suggesting that
greater left and right frontal activity is associated with a more positive and
negative evaluation of equivalent stimuli. The results of the present
investigation on facial expression of emotions support findings from
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previous studies. Indeed, BIS participants were revealed to be more

responsive to negative faces in the right frontal side. Moreover, they did
not have an increased response to happiness in the left side, showing a
substantial equivalence of left/right side in elaborating positive facial
expressions. Conversely, BAS participants appeared to be more responsive
to the positive facial expression of happiness, with an increased activity in
the left frontal area. Nevertheless, an interesting and unexpected result was
related to surprise. In fact, in addition to a more right side response, we
found an analogous left side increased activity for BIS participants. This
effect should be explained taking into account the emotional valence of
surprise, which could be perceived as a negative as well as a positive
expression. On the other hand, in the present research the fact that higher
BAS participants did not show a preferred response for surprise, in analogy
with happiness, suggests a mainly negative than positive valence attribution
to this facial pattern.
The main general conclusion on this issue may be in favour of a broad
significance of BIS/BAS construct in affecting the participants’ cortical
responses as a function of the significance of emotional faces. Nevertheless,
the present study has shown another interesting result related to the effect of
emotion type. Indeed, the valence (positive vs negative) of faces is not
sufficient to explain what we have found in response to the emotional
categories. In fact, between the negatively valenced emotions, sadness did not
produce an increased response in the right side in BIS participants; rather it
showed an analogous contribution by the two hemispheres. This interesting
effect allows us to integrate Gray’s model. Sadness, in fact, generated an
undifferentiated response by the BIS/BAS participants, and both the cortical
sides were implicated in response to this expression. It could make prominent
a different significance of this expression, and the related emotion in general,
within the functional model of emotion perception (Frijda, 1994; Hamm,
Schupp, & Weike, 2003; Keil et al., 2003; Lang, Greenwald, Bradley, &
Hamm, 1993). Sadness may be a less-prominent emotion, since it does not
imply a direct and immediate threat to the individual’s safety. It may be
represented as a ‘‘secondary’’ emotion, which is acquired later in develop-
ment (Russell, 2003). In other words, the effect of aversive and negative
emotional cues could be greater for unpleasant threatening stimuli, which are
 LATERALITY AND EMOTIONAL FACIAL EXPRESSION 379

generally considered as slightly more arousing than less-prominent stimuli for

human safety (Polich & Kok, 1995; Wild, Erb, & Bartels, 2001).
This fact highlights the subjective lateralised cortical findings related to
the motivational significance of the emotional stimulus, not uniquely
determined by the positive vs negative valence of a face. Specifically negative
faces, perceived as aversive and potentially threatening (those that express
anger, fear, or surprise, for example), produce a more intense response by BIS
people in the right hemisphere, whereas BAS people’s responses are more
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sensitive to the positive expression of happiness on the left side, potentially

representing a reinforcing, favourable emotional cue.
Moreover, taking into account the general significance of Gray’s model of
subjective behavioural response to emotional stimuli, we could hypothesise
that an alerting response is another factor that may be included to explain the
different participants’ reactions to positive vs negative aversive facial
expressions. BIS activation is associated with negative hedonic experience
like fear or anxiety. In other words, high anxiety trait participants generally
correlated to higher BIS measures, and therefore would experience increased
accuracy for negative affective faces that may be potentially threatening to
individual safety (Everhart & Harrison, 2000). Conversely, higher BAS
participants may be more attentive to stimuli that produce a positive
experience and that reinforce the behaviours that are generally positive in
nature. That said, as we have previously discussed, BIS/BAS measures have
an important function in evaluating human predispositions towards positive
(potentially rewarding) and negative (potentially threatening) conditions.
In conclusion, we may state the importance of EEG, and specifically of
alpha modulation, to exploring the participants’ responses to facial expres-
sions. In general the EEG measures showed a broad sensitivity to the
motivational significance of faces, varying as a function of the degree of
negativity/positivity and averseness power (high/low) of the emotional cues
(Balconi & Lucchiari, 2005). From this perspective, the significance of
emotions offers a valid explanatory hypothesis to the hemispheric differences
as revealed in the present study. Left and right side activation was also
demonstrated in response to positive and negative faces respectively, even if it
was mediated by the emotional significance of facial expressions in terms of
their motivational value. A third main conclusion points out the relevance of
the BIS/BAS construct to testing the effect of behavioural systems on
emotional face comprehension. A clear dichotomy was observed between two
emotional/motivational systems, which responded mainly to negative and
aversive stimuli (BIS system) in one case, and mainly to positive and
favourable stimuli in the other (BAS system).
Nevertheless, in the future more detailed studies should explore the
significance of BIS/BAS constructs in relation not only to facial expression
perception but also to emotional face production. That is, the equivalence of
 380 BALCONI AND MAZZA

cortical asymmetry of alpha in producing an emotional face should be

verified taking into account the two inhibition/activation systems. Moreover,
a more direct manipulation check on the subjective evaluation of their
emotional response to facial expression should be included in future, in
order to evaluate the contribution of the valence vs the motivational model
for the lateralisation of face comprehension.
Manuscript received 8 February 2008
Revised manuscript received 10 March 2009
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First published online 17 June 2009

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