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Encoding of emotional facial expressions in direct and incidental tasks: Two event-related potential studies*

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Emotional face encoding process was explored through electroencephalographic measures (event-related potentials [ERPs]). Previous studies have demonstrated an emotion-specific cognitive process in face comprehension. However, the effect of emotional significance of the stimuli (type of emotion) and task (direct or indirect task) on the ERP is uncertain. In Experiment 1 (indirect task) ERP correlates of 21 subjects were recorded when they viewed emotional (anger, sadness and happiness) or neutral facial stimuli. An emotion-specific cortical variation was found, a negative deflection at approximately 200 ms after simulus (N2 effect). This effect was sensitive to the emotional valence of faces, because it differentiated high arousal emotions (i.e., anger) from low arousal emotions (i.e., sadness). Moreover, a specific cortical site (posterior) was activated by emotional faces but not by neutral faces. In Experiment 2 (direct task), the authors investigated whether encoding for emotional faces relies on a single neural system irrespective of the task, or whether it is supported by multiple, task-specific systems. Differences in the cortical distribution (posterior for incidental task; central and posterior for direct task) and lateralisation (right-distribution for the negative emotions in direct task) of N2 on the scalp were observed in the different tasks. This indicates that distinct task-specific cortical responses to emotional focus can be detected with ERP methodology.
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Encoding of emotional facial expressions in direct and incidental tasks:
Two event-related potential studies
Michela Balconi
a
; Claudio Lucchiari
b
a
Department of Psychology, Catholic University of Milan,
b
Department of Neurology, Neurological
National Hospital “C. Besta”, Milan, Italy
To cite this Article Balconi, Michela and Lucchiari, Claudio(2007) 'Encoding of emotional facial expressions in direct and
incidental tasks: Two event-related potential studies ', Australian Journal of Psychology, 59: 1, 13 — 23
To link to this Article: DOI: 10.1080/00049530600941784
URL: http://dx.doi.org/10.1080/00049530600941784
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Encoding of emotional facial expressions in direct and incidental tasks:
Two event-related potential studies*
MICHELA BALCONI
1
& CLAUDIO LUCCHIARI
2
1
Department of Psychology, Catholic University of Milan and
2
Department of Neurology, Neurological National Hospital
‘‘C. Besta’’, Milan, Italy
Abstract
Emotional face encoding process was explored through electroencephalographic measures (event-related potentials [ERPs]).
Previous studies have demonstrated an emotion-specific cognitive process in face comprehension. However, the effect
of emotional significance of the stimuli (type of emotion) and task (direct or indirect task) on the ERP is uncertain.
In Experiment 1 (indirect task) ERP correlates of 21 subjects were recorded when they viewed emotional (anger, sadness and
happiness) or neutral facial stimuli. An emotion-specific cortical variation was found, a negative deflection at approximately
200 ms after simulus (N2 effect). This effect was sensitive to the emotional valence of faces, because it differentiated high
arousal emotions (i.e., anger) from low arousal emotions (i.e., sadness). Moreover, a specific cortical site (posterior) was
activated by emotional faces but not by neutral faces. In Experiment 2 (direct task), the authors investigated whether
encoding for emotional faces relies on a single neural system irrespective of the task, or whether it is supported by multiple,
task-specific systems. Differences in the cortical distribution (posterior for incidental task; central and posterior for direct
task) and lateralisation (right-distribution for the negative emotions in direct task) of N2 on the scalp were observed in the
different tasks. This indicates that distinct task-specific cortical responses to emotional focus can be detected with ERP
methodology.
Facial expressions of emotions are social and com-
municative tools. Because humans use facial expres-
sions to interpret the intentions of others, they play
an important role in daily interactions (Darwin,
1872). The existence of a specific process to encode
emotional features has been well documented by the
cognitive model of face processing proposed by
Bruce and Young (1986, 1998). This model
supposes that there are seven distinct types of
information that can be derived from the face, such
as structural, expression and identity information.
These types of information, which differ in terms of
the cognitive and functional subprocesses impli-
cated, are represented as ‘‘codes’’. In line with this
model, event-related potential (ERP) studies in
humans have provided evidence for the early
emergence of emotional encoding and its distinc-
tiveness from other cognitive processes.
The aim of the present study was to investigate
the encoding processes of emotional faces, taking
into consideration these main points: (a) an accurate
description of encoding process of emotional faces,
through ERP measures; and (b) exploring the effect
of a range of emotional expressions on ERPs, as a
function of their salience. There are three principal
ways in which electrophysiological measures can
inform the neural (hence cognitive) processes that
support operations of face comprehension. They can
provide information about the time course of cogni-
tive processes implicated; whether qualitatively dis-
tinct processes are engaged as a function of type of
stimulus (type of emotion); and the extent to which
such processes are engaged as a result of different
encoding procedures (Balconi, 2003; Rugg & Coles,
1995). From that perspective, evidence that emo-
tional faces elicit specific patterns of brain activity
could be construed as support for the claim that a
dedicated cognitive process exists.
An increasing range of research studies have analy-
sed the cognitive and neuropsychological features
Correspondence: Dr M. Balconi, Department of Psychology, Catholic University of Milan, L.go Gemelli, 1 20123 Milan, Italy.
E-mail: michela.balconi@unicatt.it
*Accepted under the previous Editorial Board.
Australian Journal of Psychology, Vol. 59, No. 1, May 2007, pp. 13 23.
ISSN 0004-9530 print/ISSN 1742-9536 online ª The Australian Psychological Society Ltd
Published by Taylor & Francis
DOI: 10.1080/00049530600941784
Downloaded By: [Ingenta Content Distribution TandF titles] At: 12:30 13 January 2010
of face comprehension (Posamentier & Abdi, 2003;
Russell, 1994). Although some studies have ex-
plored the later endogenous components (Holmes,
Vuilleumier, & Eimer, 2003; Streit, Wo¨ lwer,
Brinkmeyer, Ihl, & Gaebel, 2000), there is also
evidence that emotional processing can be differ-
entiated in earlier time windows. A very early positive
peak was observed at approximately 100 ms after
stimulus, the P1 effect, related to emotional valence
of the facial stimulus, which might demonstrate that
emotional perception of faces can take place pre-
attentively and automatically (Pizzagalli, Regard, &
Lehmann, 1999).
In addition, recent ERP studies found an early
posterior negativity (peaking at around 230 270 ms),
reflecting facilitated processing of emotional stimuli
(Schupp, Junghoper, Weiker, & Hamm, 2003). In
fact, it was demonstrated that emotional faces (fear
and happiness) elicited a larger negativity at approxi-
mately 270 ms than neutral faces over the posterior
temporal areas (Marinkovic & Halgren, 1998; Sato,
Takanori, Sakiko, & Michikazu, 2001; Vanderploeg,
Brown, & Marsh, 1987). Another study investigated
the influence of facial expressions and blurred faces on
ERP measures, without any differences between
conditions (emotional vs. blurred faces) at 120 and
170 ms after stimulus onset, but with significant
differences in amplitude between 180 and 300 ms
(Balconi & Lucchiari, 2005; Streit et al., 2000).
Nevertheless, in spite of these consistent results, other
studies found that N200 did not supply evidence in
favour of differential processing for facial expressions
(Carretie´ & Iglesias, 1995), and this ERP effect was
considered as independent from facial expression
analysis (Herrmann et al., 2002).
The first interpretation supposed that N2 could be
a cognitive marker of the complexity and relevance
of the facial stimulus (Carretie´ & Iglesias, 1995).
Nevertheless, some authors stated that this position
is in contrast with a large part of the experimental
evidence (Marinkovic & Halgren, 1998; Sato et al.,
2001). Consequently, a second hypothesis pointed
out the emotional specificity of N2, because it is
thought to be an index of the emotional encoding of
facial stimuli, and it may signal different semantic or
functional value of the emotional expressions
(Balconi & Pozzoli, 2003a; Posamentier & Abdi,
2003). Thus, some fundamental questions remain to
be answered.
First, the cognitive nature of this ERP variation
must be clarified, taking into consideration the
specificity of N200 for emotional facial expression
encoding. The comparison of facial expressions
with a neutral condition (neutral facial expression)
becomes crucial, in order to characterise the emo-
tional significance of this early peak variation.
Moreover, spatial localisation of the N200 effect is
unclear. Previous research found a more posterior
distribution of the peak, and specifically it was
localised in the temporo-occipital sites of the scalp
(Sato et al., 2001). Nevertheless, some studies have
found a different cortical distribution of the peak,
such as the central or anterior localisation. Therefore,
we chose to analyse ERP profile, in terms of brain
distribution of the N200.
A second main question of the current study
relates to the effect of type of emotions on ERP
correlates. Recent neuropsychological and neuro-
imaging data have been interpreted as indicating
that emotional perception, and specifically percep-
tion of facial expressions, is organised in a modular
fashion, with distinct neural circuitry subserving in-
dividual emotions (Adolphs, Tranel, & Damasio,
2003; Batty & Taylor, 2003; Calder, Keane, Manes,
Anton, & Young, 2000). However, few studies have
examined the range of basic emotions or distin-
guished possible differential cortical activation as a
function of the emotions. Some of them analysed
face-specific brain potentials but they did not explore
exhaustively the emotional content of faces and its
effect on ERPs (Eimer, 2000; Eimer & McCarthy,
1999). In some cases only a limited number of
emotions were considered, usually comparing one
positive and one negative emotion, such as sadness
and happiness (Herrmann et al., 2002).
Moreover, findings of previous research have noted
a modulation of late deflections of ERP as a func-
tion of ‘‘motivational significance’’ (Lang, Bradley, &
Cuthbert, 1997). Specifically, greater magnitude of
ERP deflection characterises the response to emo-
tionally salient stimuli (unpleasant compared to
neutral) (Palomba, Angrilli, & Mini, 1997; Schupp
et al., 2000). This effect has been theoretically related
to motivated attention, in which motivationally
relevant stimuli naturally arouse and direct atten-
tional resources (Hamm, Schupp, & Weike, 2003;
Keil et al., 2002; Lang et al., 1997). How can we
explain these effects of motivation and salience of
emotional facial expressions on ERPs? As suggested
by the functional model, each emotional expression
represents the subject’s response to a particular kind
of significant event a particular kind of harm or
benefit that drives coping activity (Frjida, 1994;
Hamm et al., 2003; Moffat & Frijda, 2000). Thus, an
important question of the present study is whether the
salience value of facial expressions could have an
effect on stimulus elaboration, and whether this could
be shown by ERP variations. We hypothesise that, if
the ERP variations are useful markers of cognitive
processes underlying emotion encoding, significant
differences should be found between the two cate-
gories of high/low arousal emotions. As suggested by
the functional model, we expected that subjects could
be more engaged by a high-threat negative expression
14 M. Balconi & C. Lucchiari
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(i.e., anger) than a low-threat positive emotion
(happiness), and that they might have a more intense
emotional reaction while viewing a negative high-
arousal (highly salient) than a negative low-arousal
emotion (Lang, Nelson, & Collins, 1990; Wild,
Erb, & Bartels, 2001).
Experiment 1
Method
Participants. Twenty-one subjects (11 male, age
range 21 25 years, M ¼ 23.32 years; SD ¼ 0.58
years), students of psychology at the Catholic
University of Milan, took part in the research. They
all were right-handed, with normal or corrected to
normal visual acuity and all denied any history of
neurological or mental abnormalities. They were
recruited for a cognitive task of stimulus encoding
but were not aware that the investigation of
emotional variables was the real purpose of the
experiment. The subjects gave their overt consent to
participate in the experiment (they were neither paid
nor did they receive course credits). The Ethics
Committee approved the study.
Materials and procedure. Stimulus materials were
taken from the set of pictures of Ekman and Friesen
(1976). They were black and white pictures
(11 6 15 cm) of a young male and female actor
(opportunely randomised across the emotions),
presenting respectively a happy, sad, angry, or
neutral face. The neutral faces did not present a
specific emotional expression. The items are iden-
tical in terms of lighting and angle. Pictures were
presented in a random order in the center of a
computer monitor placed approximately 80 cm from
the subject, with a visual horizontal angle of 48 and
a vertical angle of 68 (STIM 4.2 software). An
interstimulus fixation point was projected at the
center of the screen (a white point on a black
background). Each stimulus was presented for
500 ms on the monitor with an interstimulus interval
(ISI) of 1500 ms. Every type of emotional expression
was applied 20 times, resulting in a total of 80 trials.
After a brief introduction to the laboratory, the
subjects were seated in a sound-attenuated, electri-
cally shielded room and they were asked not to blink
during the task. The subject was told to observe the
stimuli carefully, but they were not asked to judge
the emotional content of faces. However, in this
experiment we used an incidental task (gender
decision task). A motor response (by stimpad) to
the features of the stimulus was required (button
response was counterbalanced). Prior to recording
ERPs, the subject was familiarised 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 16 trials, each type of expression repeated
four times).
Stimulus evaluation task. All the subjects were sub-
sequently asked (after the experimental phase) to
analyse the facial expressions and to express the
degree of their own emotional involvement for each
emotion. In order to rate the emotional valence of
face and the emotional reaction to a single ex-
pression, the subjects were asked to identify each
expression (categorisation of face), to evaluate its
pertinence (category pertinence), and to quantify the
strength of experienced emotions (Balconi & Pozzoli,
2003a; Lang, Greenwald, Bradley, & Hamm, 1993).
They correctly recognised the emotional valence
of the stimuli (correct identification 94.52%; for
neutral expression the definition was: ‘‘no emotion’’)
and they evaluated each expression as highly
pertinent with its emotional category (5-point Likert
scale; fear M ¼ 4.73, SD ¼ 0.60; happiness M ¼ 4.40,
SD ¼ 0.51, sadness M ¼ 4.25, SD ¼ 0.32; neutral
M ¼ 4.12, SD ¼ 0.83). Moreover, they evaluated on
a 5-point Likert-like scale as more emotionally
involving, the negative high-threat emotion (fear,
M ¼ 4.55, SD ¼ 0.62) than happiness (M ¼ 2.15,
SD ¼ 0.68), sadness (M ¼ 2.50, SD ¼ 0.37) and
neutral (M ¼ 1.01, SD ¼ 0.80). The statistical sig-
nificance of the difference between the four facial
expressions was tested on univariate analysis of
variance (ANOVA); for the main factor of emotion,
F(3,20) ¼ 13.52, p
¼ 0.001, Z
2
¼ .53. A post hoc
comparison (ANOVA for planned contrasts) showed
different responses between anger and happiness,
F(1,20) ¼ 9.52, p ¼ 0.001, Z
2
¼ .44, and sadness,
F(1,20) ¼ 7.73, p ¼ 0.001, Z
2
¼ .36. Finally, the three
expressions were rated more highly than the neutral
expression, anger F(1,20) ¼ 14.12, p ¼ 0.001, Z
2
¼ .50;
happiness F(1,20) ¼ 9.02, p ¼ 0.001, Z
2
¼ .40; and
sadness F(1,20) ¼ 10.51, p ¼ 0.001, Z
2
¼ .46. Type I
errors associated with inhomogeneity of variance were
controlled by decreasing the degrees of freedom using
the Greenhouse-Geiser epsilon.
Registration and ERP measures. The electroencepha-
logram (EEG) was recorded with a 64-channel DC
amplifer (SYNAMPS system) and acquisition soft-
ware (NEUROSCAN 4.2) at 32 electrode sites
(International 10-20 system, Jasper, 1958) with
reference electrodes at the mastoids, and mounted
in a stretch-lycra electrode cup (high-density regis-
tration). Electroculograms (EOG) were recorded
from electrodes lateral and superior to the left eye.
The signal (sampled at 256 Hz) was amplified and
processed on-line with a pass-band from .01 to
50 Hz and was recorded in continuous mode.
Encoding of emotional facial expression 15
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Impedance was controlled and maintained below
5KO. Twelve of the registered sites were considered
for the statistical analysis (four central: Fz, Cz, Pz,
Oz; eight lateral: F3, F4, T3, T4, P3, P4, O1, O2).
An averaged waveform (off-line) was obtained from
approximately 20 artefact-free (trials 450 mVin
amplitude were excluded from the averaging
process) individual target stimuli for each type of
emotion. The EEG signals were visually scored on a
high-resolution computer monitor and portions of
the data that contained eye movements, muscle
movements, or other sources of artefact were
removed. The percentage of the rejected epochs
was low (5%). Peak amplitude measurement was
quantified relative to 100 ms before stimulus (epoch
duration: –100/900 ms).
Results
Component windows were defined based on grand
average ERP waveforms across all type of emotion
and electrodes. To evaluate differences in ERP
response the data analysis was focused within the
time window 200 300 ms after stimulus. The time-
window reference is a common procedure that
allowed us to measure the average variation around
a peak (Rugg & Coles, 1995). In order to analyse
early ERP effects in face encoding, we focalised this
temporal range and we did not consider successive
peak variations. The morphological analysis of waves
confirmed the existence of a consistent ERP negative
deflection (N200) at this time, whereas some succes-
sive deflections (e.g., P300) were not consistently
present.
Two dependent variables, the peak value (calcu-
lated from baseline to peak amplitude) and the
latency of the peak (the time of emergence of the
peak), were entered into three-way repeated-measure
ANOVAs, using the following repeated factors:
type of stimuli (4) 6 site (4) 6 lateralisation (2).
To assess lateralisation, a lateral electrode factor
(F4, T4, P4, O2 vs. F3, T3, P3, O1) was created.
The site effect (anterior/central/parietal/occipital)
was analysed by means of four separate electrodes
(Fz vs. Cz vs. Pz vs. Oz).
The repeated-measure ANOVA applied to peak
amplitude showed a significant main effect for
type, F(3,20) ¼ 18.20, p ¼ 0.001, Z
2
¼ .54, and site,
F(3,20) ¼ 13.31, p ¼ 0.001, Z
2
¼ .50, but not for
lateralisation, F(1,20) ¼ 1.07, p ¼ 0.22, Z
2
¼ .16.
Table I shows the mean values for each emotion
and electrode site.
The two- and three-way interactions were not
statistically significant. As shown in Figure 1, a peak
at approximately 220 ms (223 ms) is observable for
all of the emotional expressions.
In order to compare different facial expressions, an
ANOVA for planned contrasts was applied for type of
expression. From the analysis it was observed that
happiness, sadness and neutral expressions had a
more positive peak than anger (anger/happiness
comparison: F(1,20) ¼ 9.02, p ¼ 0.001, Z
2
¼ .44;
anger/sadness: F(1,20) ¼ 10.12, p ¼ 0.001, Z
2
¼ .48;
anger/neutral: F(1,20) ¼ 13.53, p ¼ 0.001, Z
2
¼ .55).
In contrast, no differences were found between
happiness and sadness, but they both were differen-
tiated from the neutral face, as shown by the com-
parison happiness/neutral, F(1,20) ¼ 7.71, p ¼ 0.001,
Z
2
¼ .40, and sadness/neutral, F(1,20) ¼ 6.98,
p ¼ 0.001, Z
2
¼ .37. Second, the planned contrast
analysis applied to the simple effect of site showed
that the negative deflection was higher at the posterior
(Pz) than anterior (Fz), F(1,20) ¼ 10.34, p ¼ 0.001,
Z
2
¼ .48, and central (Cz) sites, F(1,20) ¼ 6.42,
p ¼ 0.001, Z
2
¼ .39. Figure 2 shows the cortical distri-
bution of N2 as a function of the four sites.
A second repeated measure ANOVA was applied
to the latency dependent measure. No main effect
was significant to the analysis (type: F(3,20) ¼ 0.92,
p ¼ 0.53, Z
2
¼ .10; site: F(2,20) ¼ 1.30, p ¼ 0.29,
Z
2
¼ .13; lateralisation: F(1,20) ¼ 1.02, p ¼ 0.26,
Z
2
¼ .11), nor were their two- and three-way inter-
actions. Therefore, the peak latency was quite similar
in each emotion and in all sites of the scalp.
Table I. Mean values of N2 ERP for each emotion and electrode site (incidental task)
Electrode sites
Fz Cz Pz Oz Right Left
Amplitude (volt)
MSDMSDMSDMSDMSDMSD
Happiness 2.28 .29 2.30 .64 2.28 .61 2.26 .48 2.18 .37 2.26 .44
Sadness 2.14 .37 2.39 .61 2.51 .80 2.40 .56 2.53 .47 2.10 .69
Anger 2.63 .49 2.50 .33 3.40 .55 2.89 .42 2.78 .22 2.42 .73
Neutral 2.04 .40 2.08 .34 2.23 .41 2.10 .69 2.05 .59 2.03 .44
Total mean 2.27 .38 2.31 .48 2.50 .58 2.41 .53 2.38 .41 2.20 .57
Notes. ERP ¼ event-related potential. The amplitude values reported are negative.
16 M. Balconi & C. Lucchiari
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Discussion
Our data support the view that emotion discrimina-
tion occurs at the first stage of stimulus processing,
with a latency of approximately 220 ms from stimulus
onset, and that the N2 deflection is affected by
emotional significance of faces (Streit et al., 2000).
First, because all of the emotional expressions were
differentiated from the neutral expression, N2 can
represent an ERP marker of emotional facial exp-
ressions, and not a generic cue of facial stimulus
elaboration. Thus, our data indicate that this compo-
nent reflects specific emotional processing. When the
emotional content of faces is varied (i.e., emotional or
neutral), N2 reacts more to the emotional valence of
the stimulus.
The second main and new result of this research is
that N2 is different among the four facial stimuli in
terms of peak amplitude variation. The different ERP
profiles found as a function of the emotional content
of the stimulus may indicate the sensitivity of this
negative-wave variation to the ‘‘semantic’’ value of
facial expressions (Jung et al., 2000). A more negative
peak is produced by anger than by happiness and
sadness. In contrast, very similar potentials, with
identical early latency and amplitude, were observed
for happy and sad expressions, differentiated from the
negative high-arousal emotion (anger). The results
allowed us to extend the range of emotions and to
explore in detail the functional value of ERPs applied
to facial expressions. Two main parameters seem to
affect the ERP profile: the high/low arousal of the
stimuli (related to their threatening significance) and
the type of emotional expression.
Specifically, negative emotions (such as anger) may
induce a stronger reaction than positive emotions
(such as happiness), with a more intense emotional
response, and emotional intensity may increase
Figure 2. Waveforms of grand-averaged event-related potential (ERP; all expressions) for the cortical sites
Figure 1. Waveforms of the grand-averaged event-related potential (ERP; all electrodes) for the facial stimuli
Encoding of emotional facial expression 17
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while viewing a negative high-threat emotion but
decrease while viewing a negative low-threat emotion
(Lang et al., 1990; Yee & Miller, 1987). This
assumption is strengthened by the finding of the
subject behavioral responses: anger elicited negative
intense feelings, whereas happiness and sadness were
less involving. This would suggest that effects due to
emotional arousal should be greater for unpleasant
salient stimuli, which were rated as slightly more
arousing than less relevant stimuli. Negative, relevant
emotions appear to be prominent as a human
safeguard (Lang et al., 1990). Specifically, they facili-
tate the survival of the species; and the immediate and
appropriate response to emotionally salient (threat-
related) stimuli confers an ‘‘adaptive’’ value on them
(Ellsworth & Scherer, 2003). For example, anger is
related to negative feeling and high attention. This
appraisal produces specific physiological and cogni-
tive reactions.
Experiment 2
The aim of the second experiment was to assess the
effect of an explicit judgement task on neural
responses to facial expressions when multiple emo-
tions were considered within a single experiment.
Previous studies have shown a consistent difference
in face-encoding process based on type of task
(direct vs. incidental task) (Critchley et al., 2000;
Gorno-Tempini, Pradelli, Serafini, Baraldi, & Porro,
2001; Rossion et al., 1999; Winston, O’Doherty, &
Dolan, 2003). Specifically, consistent variations were
observed between an explicit and an implicit task,
where the first includes the request of a direct
elaboration of a specific feature of the stimulus (i.e.,
emotion) and the second does not require a direct
encoding but only an incidental processing (Critchley
et al., 2000). A task effect was observed for words,
objects, and faces. In particular, a significant effect of
face encoding on several cortical and subcortical
regions was modulated by task type and by facial
expressions (Adolphs, 2002; Calder, Lawrence, &
Young, 2001). Nevertheless, the stimulus material
used included only a few emotions (normally
two emotional expressions) (Gorno-Tempini et al.,
2001).
We reasoned that, in contrast to the incidental
encoding condition examined in Experiment 1,
direct encoding would require participants to attend
more closely to emotional features of the stimuli, and
to engage in more evaluative operations in compre-
hending facial expressions. Second, different cortical
wave variations in terms of wave morphology or wave
distribution might indicate that there exists a
qualitative rather than a quantitative difference in
the neural activity underlying the ERP effects in the
two tasks.
Method
Participants. Twenty subjects (different from
Experiment 1), students of psychology at the Catholic
University of Milan, took part in the research. They
all were right-handed and with normal or corrected to
normal visual acuity (12 male, age range 21 25 years,
M ¼ 23.13 years; SD ¼ 0.34 years) and all denied any
history of neurological or mental abnormalities. They
gave informed consent and were neither paid nor did
they receive course credits. The Ethics Committee
approved the study.
Materials and procedure. The same procedure adop-
ted in Experiment 1 was used, as well as the stimulus
material. The main variation was the experimental
task. In order to assess the neural correlates of making
judgments concerning the emotional content of faces,
our design incorporated a direct task, in which
subjects made an emotional judgment concerning
each expression (expression recognition) (Winston
et al., 2003). Prior to recording ERPs, the subjects
were familiarised with the overall procedure, where
every subject saw in random order all the emotional
stimuli presented in the successive experimental
session (16 trials).
Stimulus evaluation task. All the subjects were
subsequently asked to analyse the facial expressions
in a post-experimental phase (for details see Experi-
ment 1). The subjects were asked to identify each
expression, to evaluate their pertinence, and to
quantify the strength of experienced emotions. They
correctly recognised the emotional valence of the
stimuli (correct identification 96.51%; and a judg-
ment of ‘‘no emotion’’ for neutral face,) and evalu-
ated each expression as pertinent (anger M ¼ 4.62
SD ¼ 0.98; happiness M ¼ 4.22 SD ¼ 0.83; sadness
M ¼ 4.17 SD ¼ 0.47; neutral M ¼ 4.16 SD ¼ 0.63).
Finally, they evaluated as more emotionally involving
and threatening, the negative emotion of anger
(M ¼ 4.63 SD ¼ 0.72) than happiness (M ¼ 2.30
SD ¼ 62), sadness (M ¼ 2.15 SD ¼ .83), and neutral
(M ¼ 1.77 SD ¼ 0.61). The repeated-measure
ANOVA showed a significant main effect for type of
emotion, F(3,19) ¼ 14.32, p
¼ 0.001, Z
2
¼ .53, and the
successive post hoc comparison (ANOVA for con-
trasts) found different responses between anger and the
other emotions (happiness F(1,19) ¼ 8.15, p ¼ 0.001,
Z
2
¼ .45; sadness F(1,19) ¼ 8.93, p ¼ 0.001, Z
2
¼ .43).
Neutral expression was differentiated from the other
three emotions (anger F(1,19) ¼ 16.70, p ¼ 0.001,
Z
2
¼ .47, happiness F(1,19) ¼ 15.32, p ¼ 0.01, Z
2
¼
.43, sadness F(1,19) ¼ 14.25, p ¼ 0.03, Z
2
¼ .42).
EEG registration parameters. EEG was recorded in
the same manner as Experiment 1 (32 electrodes in
18 M. Balconi & C. Lucchiari
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an electrocap, international 10-20 system) with
acquisition software NEUROSCAN 4.2. Only 4%
of the epochs was rejected due to artefacts.
Results
Component windows were defined based on grand
average ERP wave forms across all type of emotion
and electrodes. The time window 200 300 ms after
stimulus was used to analyse peak variations, because
morphological investigation of the wave profiles
showed a peak variation analogous to that observed
in Experiment 1, within the same time interval. The
variables were entered into three-way repeated
measure ANOVAs, using as repeated factors
Type of emotion (4) 6 Site (4) 6 Lateralisation (2).
Table II shows the mean values as a function of
emotion and electrode sites.
The type of emotion was significant in distinguish-
ing peak variation, F(3,19) ¼ 19.35, p ¼ 0.001,
Z
2
¼ .61, as well as site, F(3,19) ¼ 7.70, p ¼ 0.001,
Z
2
¼ .40, and there was a Type 6 Lateralisation
interaction, F(3,19) ¼ 8.93, p ¼ 0.001, Z
2
¼ .44.
The contrast analysis indicated differences between
anger and happiness, F(1,19) ¼ 13.29, p ¼ 0.001,
Z
2
¼ .47, and anger and sadness, F(1,19) ¼ 14.66,
p ¼ 0.001, Z
2
¼ .50. Moreover, all the emotions were
differentiated from the neutral face: anger F(1,19) ¼
12.45, p ¼ 0.001, Z
2
¼ .47; happiness F(1,19) ¼ 10.47,
p ¼ 0.001, Z
2
¼ .44; and sadness F(1,19) ¼ 9.53,
p ¼ 0.001, Z
2
¼ .42. The site main effect showed
a more central (Cz), F(1,19) ¼ 9.03, p ¼ 0.001,
Z
2
¼ .45, and posterior (Pz), F(1,19) ¼ 10.04,
p ¼ 0.001, Z
2
¼ .49, distribution of the peak than
anterior (Fz) position (Figure 3).
Finally, the post hoc comparison for Type 6
Lateralisation effect a more right distribution of the
peak for the negative expressions of anger,
F(1,19) ¼ 8.70, p ¼ 0.001, Z
2
¼ .42, and sadness,
F(1,19) ¼ 6.93, p ¼ 0.001, Z
2
¼ .36, compared with
happiness. The same trend was found for the negative
emotions of anger, F(1,19) ¼ 9.04, P ¼ 0.001,
Z
2
¼ .47, and sadness, F(1,19) ¼ 8.80, P ¼ 0.001,
Z
2
¼ .44, compared with neutral face. Figure 4
presents the topographical maps of the scalp for each
emotion.
Latency was entered as the dependent variable in a
successive repeated-measure ANOVA. The analysis
Table II. Mean values of N2 ERP for each emotion and electrode site (direct task)
Electrode sites
Fz Cz Pz Oz Right Left
Amplitude (volt)
MSDMSDMSDMSDMSDMSD
Happiness 2.08 .33 2.49 .69 2.53 .58 2.39 .40 2.24 .28 2.37 .66
Sadness 1.89 .28 2.70 .72 2.68 .53 2.65 .32 2.92 .43 2.45 .73
Anger 2.39 .41 2.90 .62 3.10 .28 2.93 .57 3.21 .23 2.83 .45
Neutral 2.03 .56 2.25 .91 2.25 .30 2.28 .48 2.15 .20 2.06 .39
Total mean 2.09 .39 2.58 .73 2.67 .42 2.56 .44 2.63 .28 2.42 .55
Notes. ERP ¼ event-related potential. The amplitude values reported are negative.
Figure 3. Waveforms of grand-averaged event-related potential (ERP; all expressions) for the cortical sites
Encoding of emotional facial expression 19
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did not find a significant main effect for either type,
site or lateralisation effects.
Direct/incidental task compa rison (Experim ent 1
and 2). A direct comparison between the two types
of task (direct and incidental) was conducted by a
mixed design ANOVA (Type 6 Site 6 Lateralisa-
tion 6 Task), applied to both peak and latency-
dependent measures. The first ANOVA showed a main
effect for type, F(3,39) ¼ 13.05, p ¼ 0.001, Z
2
¼ .48, and
site, F(3,39) ¼ 9.32, p ¼ 0.001, Z
2
¼ .42, but not for
task, F(1,39) ¼ 1.15, p ¼ 0.18, Z
2
¼ .12, or lateralisa-
tion, F(1,39) ¼ 1.17, p ¼ 0.23, Z
2
¼ .10. For the inter-
action effects, Task 6 Site was significant, F(6,39) ¼
9.03, p ¼ 0.001, Z
2
¼ .45, as well as Type 6 Task 6
Lateralisation, F(3,39) ¼ 9.14, p ¼ 0.001, Z
2
¼ .48.
Specifically, in addition to the type effect, the post
hoc comparisons showed a more posterior (Pz),
F(1,39) ¼ 5.23, p ¼ 0.02, Z
2
¼ .34, and central (Cz),
F(1,39) ¼ 14.24, p ¼ 0.001, Z
2
¼ .49, site of N2 for the
direct task than the incidental task. In contrast, N2 at
the frontal site was similar for the direct and incidental
tasks, F(1,39) ¼ 0.73, p ¼ 0.32, Z
2
¼ .09. Moreover, a
more right distribution of the N2 was found for anger
and sadness than for happiness: F(1,39) ¼ 10.32,
p ¼ 0.001, Z
2
¼ .46; F(1,39) ¼ 8.08, p ¼ 0.001, Z
2
¼
.42, respectively; and neutral faces: F(1,39) ¼ 14.67,
p ¼ 0.001, Z
2
¼ .52; F(1,39) ¼ 11.12, p ¼ 0.001,
Z
2
¼ .48; respectively) in direct task. In contrast, no
differences in N2 were found in the incidental task
condition between the left and right sides.
The latency measure was entered in a successive
mixed-design ANOVA. No specific main or interac-
tion effect was significant.
Discussion
The present experiment allowed us to identify some
main effects due to different types of task. First,
we can state the existence of a specific cortical
module devoted to emotional feature analysis, that
is, a specific module for emotional configuration.
Second, we can state that this cortical effect is
activated independently from type of task, because it
was observed in the same form for both the direct
and the indirect conditions. From a morphological
point of view, we showed that the direct task
produces an analogous peak variation to the inci-
dental task, represented by the N200 ERP effect.
We can explain this result by stating that the
emotional encoding is an automatic process, devoted
to extrapolate the emotional meaning from facial
expressions regardless of the type of task (Balconi &
Pozzoli, 2003b). This supposition is compatible with
a model in which simple perception of emotional
faces entailed activation of specific recognition
processes, indexed by the N2 ERP effect (Winston
et al., 2003). Nevertheless, consequent to a direct
comparison between the two types of task, some
consistent differences were found for N2 as a func-
tion of direct and incidental elaboration of the
stimulus, mainly related to the cortical distribution
of the negative deflection. Whereas in the incidental
task N2 was mainly posteriorly distributed, in the
direct elaboration of faces a central localisation was
observed in addition to the posterior (parietal) one.
These differences are in line with previous studies
that found a central larger effect for a direct semantic
task. We can explain this topographical difference by
supposing that encoding in the two tasks may have
engaged neurophysiologically equivalent activity in
differently located neural generators. Alternatively,
encoding in the two tasks may have engaged neuro-
physiologically distinct activity in a different set of
generator populations. While the present data do not
allow a selection between these two possibilities, they
do allow the conclusion that ERP encoding in a
direct task is not simply a stronger version of ERP
encoding in an incidental task, because our findings
suggest that emotional encoding is supported by
multiple neural systems.
A striking finding of this research was the effect of
the emotion category on N2. The peak amplitude
variations as a function of emotions follow the
same direction for the two tasks. The fact that
the motivational features of faces can affect both
Figure 4. Topography of event-related potential maps for each emotion (coronal section, left view)
20 M. Balconi & C. Lucchiari
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the implicit and explicit comprehension of emotions
allows us to suppose that an underlying main factor,
such as arousal, may act in emotion comprehension
and that this factor plays a major role in determining
the cognitive significance of the stimulus. Moreover,
the study indicates that subjects can discriminate
between types of facial emotions even when facial
emotion perception is not task relevant, concomitant
with the idea that facial expression is processed
automatically (Blair, Morris, Frith, Perrett, & Dolan,
1999; Dolan et al., 1996; Vuilleumier, Armony,
Driver, & Dolan, 2001).
Finally, an interesting effect was the lateralisation
observed as a function of type of emotional expres-
sion in the direct task. N200 peak amplitude was
higher to the right than the left side for the negative
expressions (anger and sadness) compared with the
positive emotion (happiness). This needs to be
explored further in the future, because N2 may turn
out to be a marker of the left right processing
dichotomy in relation to the type of emotion. In this
regard, future research must consider the lateralisa-
tion effect more closely, through a more direct
comparison between the processes of production
and recognition of facial expressions.
General discussion
In the present study we investigated the processes of
encoding of emotional facial stimuli in two different
conditions of elaboration: direct and incidental
tasks. The elaboration of emotional facial expres-
sions appears indexed by a specific ERP effect, the
N2 effect. The emotional specificity of N2 is
underlined by the major differences observed
between emotional and neutral stimuli. In line with
the Bruce and Young (1998) model, we postulate
that a specific neural mechanism could exist for the
processing of facial expressions of emotion. In
addition, N2 can be considered a marker of the
specific emotional content because it was observed
to vary in amplitude as a function of type of
emotion, and more specifically of motivational
significance for the subject. The peak increases as
the subject appears more emotionally aroused and
attentively involved by the stimulus. Recent re-
search emphasises that motivational relevance is a
primary determinant of selective attention: somatic,
autonomic, and cortical events associated with
orienting are automatically activated by more
emotionally arousing representations in a variety of
paradigms, independently from instructional direc-
tion and from task condition, because the relevance
of the stimulus is pre-task or ‘‘intrinsic’’ (Lang
et al., 1997). From this perspective, the significance
of emotional expression for the subject, in terms
of low/high-threat power and relevance, should
influence both the physiological (i.e., arousal) and
the cognitive level (mental processes and attentional
effort), and has an important effect on ERP
correlates (Balconi & Pozzoli, 2003a; Frijda, 1986;
Keil et al., 2002; Lang et al., 1993; Schorr, 2001;
Wild et al., 2001).
The absence of differences in the cortical distribu-
tion of the peak related to type of emotion is a fact
that must be considered here. Whereas the idea of
the right hemisphere advantage in facial identity
recognition has been extended to facial expression
processing, our study did not find a clear superiority
of one hemisphere in the encoding of emotional
faces. However, it should be noted that recent data
exist indicating that the right dominance in facial
expression recognition is modulated by variables
such as the task requirements, which can modify the
right-hemisphere advantage. Therefore, the laterali-
sation of ERP is a major aspect to be considered in
relation to task manipulation.
We can summarise the task effect for encoding
processing of face into two main points: the cortical
distribution of the N2 on the scalp and the
lateralisation of the peak deflection. We observed a
more posterior and central localisation of N2 for
direct compared to incidental conditions. It follows
that at least one aspect of the cognitive operations
associated with emotional encoding in the two tasks
could differ. Either the cognitive processes that
enable the encoding, the type of information the
processes act upon, or both, differ depending on the
type of task.
A second result related to task manipulation is a
right lateralisation effect observed for negative
emotions in comparison with positive and neutral
emotions for the direct task, but not for the
incidental task. A specific right lateralisation for
negative emotions was found when the subjects had
to be attentive to the emotional content of faces. A
considerable number of studies have investigated the
lateralisation of emotional processing. According to
the ‘‘right hemisphere hypothesis’’, the right hemis-
phere plays a superior role in emotional processing,
such as recognition of both positive and negative
emotions (Borod et al., 1998 ). An alternative view
(the ‘‘valence hypothesis’’) is that the right hemi-
sphere primarily mediates negative rather than
positive emotions. Our data seem to be better
explained by the valence model of lateralisation,
but it is not clear why this effect was found
exclusively in the direct task condition. It is possible
that this localisation effect is a consequence of
differences in attentional effort in processing the
stimuli. That is, in a direct task negative and positive
emotions may be more clearly distinct, with a related
activation of right side of the scalp only for the
emotional face evaluated as negative.
Encoding of emotional facial expression 21
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Encoding of emotional facial expression 23
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Chapter
There is a long tradition in emotion psychology of examining facial expressions as a visible indicator of unobservable emotional processes. On the one hand, cognitive research into facial expression has pointed out the cognitive role of processes underlying facial decoding and their specificity compared to other cognitive mechanisms. On the other hand, theoretical paradigms of the analysis of emotions have underlined the early emergence of this cognitive skill during ontogenesis, as well as the social significance of this acquisition.