Incongruence effects in crossmodal emotional integration
Veronika I. Müllera,b,c,⁎, Ute Habela,c, Birgit Derntla,f, Frank Schneidera,c, Karl Zillesb,c,d,
Bruce I. Turetskye, Simon B. Eickhoffa,b,c
aDepartment of Psychiatry und Psychotherapy, RWTH Aachen University, Germany
bDepartment of Neuroscience und Medicine, INM-2, Research Centre Jülich, Germany
cJARA-BRAIN Translational Brain Medicine, Jülich/Aachen, Germany
dC. and O. Vogt Brain Research Institute, University of Düsseldorf, Germany
eNeuropsychiatry Division, Department of Psychiatry, University of Pennsylvania School of Medicine, Philadelphia, PA, USA
fInstitute for Clinical, Biological and Differential Psychology, Faculty of Psychology, University of Vienna, Austria
a b s t r a c t a r t i c l ei n f o
Received 23 July 2010
Revised 11 October 2010
Accepted 13 October 2010
Available online 23 October 2010
Emotions are often encountered in a multimodal fashion. Consequently, contextual framing by other
modalities can alter the way that an emotional facial expression is perceived and lead to emotional conflict.
Whole brain fMRI data was collected when 35 healthy subjects judged emotional expressions in faces while
concurrently being exposed to emotional (scream, laughter) or neutral (yawning) sounds. The behavioral
results showed that subjects rated fearful and neutral faces as being more fearful when accompanied by
screams than compared to yawns (and laughs for fearful faces). Moreover, the imaging data revealed that
incongruence of emotional valence between faces and sounds led to increased activation in the middle
cingulate cortex, right superior frontal cortex, right supplementary motor area as well as the right
temporoparietal junction. Against expectations no incongruence effects could be found in the amygdala.
Further analyses revealed that, independent of emotional valence congruency, the left amygdala was
consistently activated when the information from both modalities was emotional. If a neutral stimulus was
present in one modality and emotional in the other, activation in the left amygdala was significantly
attenuated. These results indicate that incongruence of emotional valence in audiovisual integration activates
a cingulate-fronto-parietal network involved in conflict monitoring and resolution. Furthermore in
audiovisual pairing amygdala responses seem to signal also the absence of any neutral feature rather than
only the presence of an emotionally charged one.
© 2010 Elsevier Inc. All rights reserved.
Affect processing and the ability to recognize emotions in facial
expressions is a crucial part of social cognition and inter-personal
relationships. In everyday life, however, the evaluation of facial
emotions is rarely based on the expression of a face alone. Rather,
most of the time a face is perceived in a particular context, for
instance, we see a face in a specific scene or accompanied by a
particular sound. Thus, facial affect recognition usually involves the
interpretation of a face in a specific context, even if the latter is not
processed consciously. Importantly, this context may not always be
congruent with the emotional expressiondisplayed by the face, which
implies that concurrently receiving two or more different emotional
inputs can lead to emotional conflict.
Non-emotional conflict has been studied extensively using
behavioural and neuroimaging experiments (Botvinick et al., 2004;
Carter et al., 1998; Carter and van Veen, 2007; Durston et al., 2003;
Egner and Hirsch, 2005; Kerns et al., 2004; MacDonald et al., 2000;
Ochsner et al., 2009; Weissman et al., 2004). The results of these
studies have led to the conflict monitoring hypothesis, which suggests
that conflict is detected by the dorsal anterior cingulate cortex (ACC),
which in turn recruits prefrontal regions to increase cognitive control
(Botvinick et al., 2004; Carter and van Veen, 2007; Kerns et al., 2004).
In contrast, rather few studies have focused on the effects of
affective conflict, reporting increased reaction times (Collignon et al.,
2008; de Gelder and Vroomen, 2000; Dolan et al., 2001; Haas et al.,
2006; Ochsner et al., 2009; Wittfoth et al., 2010) in incongruent
compared to congruent conditions for both unimodal and crossmodal
On the neurobiological level affective conflict has been linked to
activation in ACC for (within-modality) conflicts in the visual and
auditory domain (Haas et al., 2006; Ochsner et al., 2009; Wittfoth
et al., 2010), as well as right dorsolateral prefrontal cortex (DLPFC)
and bilateral posterior medial frontal cortex for visual (Ochsner et al.,
NeuroImage 54 (2011) 2257–2266
⁎ Corresponding author. Department of Psychiatry and Psychotherapy, RWTH
Aachen University, Pauwelsstraße 30, D-52074 Aachen, Germany. Fax: +49 241 80
E-mail address: firstname.lastname@example.org (V.I. Müller).
1053-8119/$ – see front matter © 2010 Elsevier Inc. All rights reserved.
Contents lists available at ScienceDirect
journal homepage: www.elsevier.com/locate/ynimg
2009) and superior temporal gyrus (STG) for auditory conflict
processing (Wittfoth et al., 2010).
As outlined above emotional conflicts may arise not only from
incompatible information encountered in the same modality but in
channels, such as when we see a frightened face and concurrently hear
laughter. In spite of their behavioral relevance, however, the neurobi-
ology of multi-modal emotional conflicts has rarely been studied.
Studies focusing on the neural correlates of audiovisual integration
independent of a potential conflict, consistently report increased
activation of posterior superior temporal sulcus (pSTS) (Beauchamp,
2005; Kreifelts et al., 2007; Pourtois et al., 2005; Robins et al., 2009), for
both emotional and non-emotional integration. Furthermore Dolan et
al. (2001) contrasted emotional congruent to emotional incongruent
conditions in an audiovisual paradigm and found greater activation of
the left amygdala and right fusiform gyrus (FFG) in congruent as
compared to incongruent conditions, but did not report a significant
effect of the reverse contrast. Nevertheless studies which focus on the
neural correlates of audiovisual emotional incongruence processing are
still sparse. Furthermore, most of the existing studies investigating
emotional incongruence effects either did not use neutral stimuli or did
not differentiate between different ways how incongruence could arise
in such settings. In particular, it may be argued that two different types
of incongruence can occur in audiovisual pairing when, in addition to
emotional, neutral stimuli are also presented. These two types may be
presence. On one hand, incongruenceof emotional valence arises when
in both modalities an emotional stimulus is presented but these two
stimuli differ in emotional valence (i.e. happy face paired with scream).
That is, the information from the two sensory channels disagrees in the
nature or valence of the portrayed emotion. On the other hand
incongruence of emotion-presence is characterized by pairing a neutral
In other words, an emotional stimulus may be present in one modality
but absentin the other (because a neutral stimulus is presented). Given
that emotion processing is supposed to be centered about filtering
behaviorally relevant information, in this case a conflict arises between
the two sensory channels, with one indicating a (potentially) salient
event, while the other is not.
Finally, clinical studies in patients with depression show that this
disorder goes along with a negativity bias (Drevets et al., 2008) and
problems inhibiting negative information (Goeleven et al., 2006;
Joormann, 2010). These problems have repeatedly been linked to dys-
et al., 2007; Drevets, 2000; Fales et al., 2008). Furthermore symptom
severity of depression correlates with amygdala activation in emotion
during a cognitive inhibition task (Matthews et al., 2009). Lastly, Abler
et al. (2010) demonstrated that activation in the amygdala does even
correlate with subclinical depression scores. Whether a similar correla-
tion of depressivity scores with regional brain activation can also be
found in crossmodal emotionalintegration is yet not clarified. Moreover,
revealing and understanding the relationship between subclinical traits
about neurobiological vulnerability markers for depression.
Given the open questions outlined above, the primary goal of the
current study is to investigate the influence of emotional sounds on
facial affect perception and the underlying neural substrates involved
in the mediation of both types of audiovisual (in-) congruence effects.
We hypothesize that behaviorally, emotional sounds influence the
perception of facial expressions while incongruence effects should
elicit increased activation in dACC and prefrontal regions. In contrast,
based on previous work, we would assume that emotional congru-
ence enhances activation in amygdala and FFG.
As a secondary aim the correlation of (subclinical) depressive
traits as quantified by the Beck Depression Inventory (BDI) with the
neural correlates of audiovisual inhibition processes is investigated.
Given previous reports in depressed patients (Abler et al., 2007;
Drevets, 2000; Fales et al., 2008), we would hypothesize that activity
in the amygdala, ACC and DLPFC over all task conditions relative to
baseline correlates with BDI scores.
In total 40 healthy subjects were examined. Five subjects were
excluded from the analysis due to BDI or alexithymia scores exceeding
the cut-off for clinically relevant depression (N15) and alexithymia
(N60), respectively, or excessive movement during scanning. Hence, 35
healthy right-handed volunteers (20 females; mean age 29.4±
8.1 years, mean education 14.1±3.2, 15 males; mean age 34.0±13.3,
mean education 14.5±3.2) were included in the analysis. Men and
women did not significantly differ in age (t33=1.29, ns.) or education
(t33=0.34, ns.). All participants had normal or corrected-to-normal
vision and were right handed as confirmed by the Edinburgh Inventory
(Oldfield, 1971). The structured clinical interview of DSM IV (SCID;
Wittchen et al., 1997) was used to screen the subjects revealing no
history of neurological or psychiatric disorders including substance
committee of the School of Medicine of the RWTH Aachen University.
The visual stimuli, obtained from the FEBA inventory (Gur et al.,
2002a), consisted of color pictures of male and female faces, showing
either a happy, neutral or fearful expression. In total 10 (5 males and 5
females) faces of different actors each showing every expression
(happy, neutral, fear) were used. To optimize the design, a behavioral
pre-study with 48 subjects was conducted where different versions of
the paradigm and varying presentation times were tested. These
results indicated that emotional faces were too clear to allow any
consistent context framing effects. As a consequence, happy and
fearful faces were degraded in emotionality in order to make them
more ambiguous. This was done by merging every emotional facial
image with the neutral mouths of the same actor.
Furthermore, as a longer auditory and a shorter visual stimulus
had to be combined, each trial also employed (visual) masks. This was
necessary because a long auditory presentation is needed to contain
clear emotional information, whereas a short visual presentation is
important to allow context effects. As visual input should be held
constant for the whole trial 10 different neutral faces blurred with a
mosaic filter were included as masks.
The auditory stimuli were either neutral (yawning) or socio-
emotional salient sounds like laughing (happy) or screaming (fear).
210 different sounds were obtained from various sound libraries and
equalized with respect to length and volume. In a pre-experiment,
these were then rated by a different sample of 10 subjects for
validation and selection of the stimuli used in the experiment. In total
10 laughs, 10 yawns and 10 screams (5 males and 5 females in each
case) were selected.
In the experiment a total of 180 stimulus pairs, each consisting of a
visual and an auditory stimulus were presented. Every face condition
(happy, fear, neutral) was combined with every sound condition
(happy, fear, neutral) resulting in a 3×3 design with nine different
conditions and 20 audiovisual pairs per condition. The pairing was
pseudo-random and matched with regard to gender, so that a male
face was always paired with a male voice and vice versa.
V.I. Müller et al. / NeuroImage 54 (2011) 2257–2266
Audiovisual stimulus pairs were presented for 1500 ms with a
jittered inter-stimulus-interval between 4000 and 6000 ms during
which a blank black screen was shown (see Fig. 1). Every trial started
with the presentation of a sound to establish a context. Concurrently
with the sound a blurred neutral face was shown. After 1000 ms the
blurred face was displaced by the target stimulus (neutral or emotional
face) and presented with the continuing sound for another 500 ms. The
subjects were asked toignore thesound and to rate asfast and accurate
from extremely fearful to extremely happy. Subjects were instructed
thatthe study focuses on attention processes in order toavoid effects of
presented with the software Presentation 14.2 (http://www.neurobs.
MR-compatible response pad (from extremely fearful—left little finger
(1) to extremely happy—right little finger (8)).
Additional tests and questionnaires
After the scanning session participants rated the valence and
arousal of sounds and pictures individually on a nine-point valence
scale ranging from very fearful to very happy and not at all arousing to
very arousing, respectively. Contrary to the rating in the scanner
where subjects had to make a forced choice on the emotional content
due to the absence of a “neutral” response, the rating of faces and
sounds after scanning included a neutral category. Moreover the TAS-
D (Bagby et al., 1994) was carried out to control for alexithymia and
the Beck Depression Inventory (BDI-II; Hautzinger et al., 2006) to
check for subclinical depressive symptoms.
fMRI data acquisition
Images were acquired on a Siemens Trio 3 T whole-body scanner
(Erlangen, Germany) in the Research Center Jülich using blood-
oxygen-level-dependent (BOLD) contrast (Gradient-echo EPI pulse
sequence, TR=2.2 s, in plane resolution=3.1×3.1 mm, 36 axial
slices (3.1 mm thickness)) covering the entire brain. Image acquisi-
tion was preceded by 4 dummy images allowing for magnetic field
saturation. These were discharged prior to further processing. Images
were analysed using SPM5 (www.fil.ion.ucl.ac.uk/spm). First, the EPI
a two-pass procedure, by which images were initially realigned to the
first image and subsequently to the mean of the realigned images.
After realignment, the mean EPI image for each subject was spatially
normalized to the MNI single subject template using the “unified
segmentation” approach (Ashburner and Friston, 2005). The resulting
parameters of a discrete cosine transform, which define the
deformation field necessary to move the subjects data into the
space of the MNI tissue probability maps, were then combined with
the deformation field transforming between the latter and the MNI
single subject template. The ensuing deformation was subsequently
applied to the individual EPI volumes that were hereby transformed
into the MNI single subject space and resampled at 2×2×2 mm3
voxel size. The normalized images were spatially smoothed using an
8 mm FWHM Gaussian kernel to meet the statistical requirements of
the General Linear Model and to compensate for residual macro-
anatomical variations across subjects.
Behavioral datawereanalyzedoff-line usingSPSS 18.0.0(SPSSInc.,
Chicago, IL). All data were confirmed to be normally distributed and
MANOVAs / ANOVAs were calculated. Violations of sphericity were
corrected by the Greenhouse–Geisser or Huynh–Feldt correction.
Post-hoc analyses, corrected for multiple comparisons, were calcu-
lated for significant main effects and interactions.
The imaging data were analyzed using a General Linear Model as
implemented in SPM5. Each experimental condition (fearful face/
scream, fearful face/yawn, fearful face/laugh, neutral face/scream,
neutral face/yawn, neutral face/laugh, happy face/scream, happy face/
yawn, happy face/laugh) as well as the response event were
separately modelled by a boxcar reference vector convolved with a
canonical hemodynamic response function and its first-order tempo-
ral derivative. Additionally, low-frequency signal drifts were filtered
using a cutoff period of 128 s. Parameter estimates were subsequently
calculated for each voxel using weighted least squares to provide
maximum likelihood estimators based on the temporal autocorrela-
tion of the data (Kiebel et al., 2003). No global scaling was applied. For
each subject, simple main effects for each of the nine experimental
conditions and the response were computed by applying appropriate
baseline contrasts. These individual first-level contrasts were then fed
to a second-level group-analysis using an ANOVA (factor: condition,
blocking factor subject) employing a random-effects model. In the
modelling of variance components, violations of sphericity have been
allowed by modelling non-independence across images from the
same subject and allowing unequal variances between conditions and
subjects using the standard implementation in SPM 5.
In the ANOVA mean (weighted by non-sphericity correction)
parameter estimates over all subjects were calculated for every
condition (fearful face/scream, fearful face/yawn, fearful face/laugh,
neutral face/scream, neutral face/yawn, neutral face/laugh, happy
face/scream, happy face/yawn, happy face/laugh). Based on these
estimates of the second level analysis, separate t-contrasts were
calculated for every differential effect (effect of fearful faces, effect of
happy faces, effect of fearful sounds, effect of happy sounds,
incongruence effects of emotional valence, incongruence effects of
emotion-presence) by applying the respective contrast to the 2nd
level parameter estimates. In other words, the ANOVA was used to
calculate the group level parameter estimates for each condition
whereast-contraststo theparameterestimates were employed totest
Fig. 1. Experimental procedure: Every trial started with the presentation of a sound concurrently with a blurred neutral face. After 1000 ms the blurred face was displaced by an
emotional or neutral face and presented with the continuing sound for another 500 ms.
V.I. Müller et al. / NeuroImage 54 (2011) 2257–2266
for differential effects between these. The resulting SPM (T) maps
were then thresholded at pb0.05, correcting for multiple comparisons
by controlling the family-wise error (FWE) rate according to the
theory of Gaussian random fields (Worsley et al., 1996). FWE corrects
for accumulation of type I error in multiple testing with non-compact
support, i.e., correlated statistics. By regarding the statistical image as
a lattice representation of a random Gaussian field (whose smooth-
nessisestimatedusing theresidualfield ofthe statisticalanalysis),the
probability that one or more false positive voxels are found in the
entire search volume can be estimated for each threshold applied to
thestatistic.The threshold is thenchosenas tocontrolthefamily-wise
error rate at pb0.05, i.e., in only one of twenty analyses of random
fields of the same type, size and smoothness one would expect to find
a single voxel above the chosen threshold.
Additionally, another model was estimated where the nine
conditionsand responses and BDI-scores as a covariate weremodeled.
Ensuing activations were anatomically localised using version 1.6b
of the SPM Anatomy toolbox (Eickhoff et al., 2005, 2006, 2007; www.
Valence and arousal of faces and sounds in the off-line rating
An one-factorial MANOVA with the factor emotion (fear/neutral/
happy) and the dependent variables “off-line valence rating of faces”
and “off-line valence rating of sounds” was conducted revealing a
significant main effect of emotion (F2,4=318.11, p b 0.05). This effect
was significant for both dependent variables, faces (Greenhouse–
Geisser corrected: F2,66=271.2; ε=0.74, p b 0.05) and sounds
(Greenhouse–Geisser corrected: F2,66=983.42, ε=0.76, p b 0.05).
Fearful stimuli got the lowest ratings, followed by neutral faces and
sounds, while the most positive ratings were given for happy stimuli
(all post-hoc comparisons were significant at p b 0.05, cf. Table 1).
An additional MANOVA with ratings of arousal also led to a
significant main effect of emotion (F2,4=53.14, pb0.05), significant
for both stimulus modalities (faces: F2,68=13.72; pb0.05; sounds:
F2,68=95.95; pb0.05). Neutral faces and sounds were rated as least
arousing, followed by happy stimuli, whereas fearful stimuli were
perceived as most arousing (all post-hoc comparisons were signifi-
cant at pb0.05 except for comparison of happy to neutral faces which
revealed a tendency towards significance, cf. Table 1).
On-line behavioral data
An ANOVA with the factors face (fear/neutral/happy) and sound
(scream/yawn/laugh) and the dependent variable “rating obtained in
the scanner” revealed significant main effects of face (Huynh–Feldt
corrected: F2,68=253.96, ε=0.66, pb0.01) and sound (F2,68=7.96,
pb0.01), as well as a significant interaction between face x sound
Post-hoc analyses of the main effect face showed the same pattern
as observed in the off-line rating, with lowest ratings for fearful,
highest for happy and intermediate values for neutral faces (all post-
hoc comparisons were significant at pb0.05).
As the task was to ignore the sound and to rate the face, the main
effect of sound reflects the influence of a sound on a face. Post-hoc
analyses of this effect did show that screams led, independently of
facial expression, to a more fearful rating of the faces compared to
yawns and laughs (post-hoc comparisons were significant at pb0.05),
whereas subjects did not rate faces differently when exposed to
laughs compared to yawns.
faces as being more fearful when accompanied by screams compared to
yawns or laughs. Neutral faces were also perceived as more fearful when
paired with screams compared to yawns but not to laughs (Fig. 2). No
context effect could be found for happy faces (Tukey's HSD=0.096).
To identify emotion specific areas all happy and fearful faces were
separately contrasted to neutral faces. For happy relative to neutral
faces, this contrast revealed increased activation in bilateral calcarine
sulcus, left middle occipital gyrus, left inferior parietal cortex, left
supplementary motor area, primary motor and postcentral gyrus as
well as left insula and right thalamus (pb0.05, FWE corrected,
Table 2). In contrast, there was no significant greater activation for
Mean ratings (standard deviation) of emotion and arousal of fearful, neutral and happy faces and sounds obtained outside the scanner.
Fig. 2. Mean ratings of fearful, neutral and happy faces while distracted with screams,
yawns or laughs (0—very fearful, 8—very happy). Screams led significantly to a more
fearful rating of fearful and neutral faces compared to yawns (and compared to laughs
in case of fearful faces).
Activation happy versus neutral faces.
Left middle occipital
Left inferior parietal
Left postcentral gyrus
Left primary motor
motor area (SMA)
−12 54 5.4899
Coordinates are in MNI space; mapping of cytoarchitectonic areas: 17,18—(Amunts et
al., 2000); PFm, PFt—(Caspers et al., 2006); 4a—(Geyer et al., 1996; Geyer, 2004).
V.I. Müller et al. / NeuroImage 54 (2011) 2257–2266
fearful compared to neutral faces at the corrected level. Comparison of
screams and laughs, respectively, to yawns showed activation in
bilateral STG for either emotional sound. Furthermore screams
compared to yawns activated bilateral inferior parietal cortex (IPC),
right supplementary motor area (SMA) and left middle cingulate
cortex (pb0.05, FWE corrected, Table 3).
Incongruence effects of emotional valence
To identify brain regions involved in detecting and processing
emotional conflict of valence, emotionally incongruent conditions
(fearful face paired with laugh and happy face paired with scream)
were contrasted to emotionally congruent conditions (fearful face
paired with scream and happy face paired with laugh). Significant
incongruence effects could be found in the middle cingulate cortex,
the right superior frontal gyrus, the right SMA and the right
temporoparietal junction (TPJ) (pb0.05, FWE corrected, Table 4,
In contrast, congruent compared to incongruent conditions did not
evoke significantly increased activation in any brain region. As neither
incongruence nor congruence effects were found in the amygdala, a
small volume correction (based on the coordinates by Dolan et al.,
2001; x=−20, y=−8, z=−14 Talairach coordinates converted into
MNI space x=−20, y=−8, z=−17; search volume 6 mm) was
carried out for both congruence and incongruence effects. Again, no
significant effect was detected, neither FWE corrected, nor
Incongruence effects of emotion-presence
To elucidate the neural correlates of incongruence concerning the
presence and absence of emotion, we compared pure emotional
conditions (fearful face with laugh or scream, happy face with laugh
or scream) with conditions where a neutral stimulus was presented in
one of the two modalities and an emotional one in the other (fearful
or happy face with yawn, neutral face with scream or laugh).
This contrast revealed significant activation (cluster peak at x=
−20, y=−3, z=−21, pb0.05, FWE corrected, Fig. 4) of the left
laterobasal/superficial nuclei of the amygdala (LB/SF; Amunts et al.,
2005). The overlap of the activated cluster with LB was 15.2%, while
78.6 % of its volume was allocated to SF; the maximum probabilities
were 60 % and 70 %, respectively.
Furthermore this contrast led to significant greater bilateral
occipital and temporal activation (Table 5).
Activation scream versus yawn and laugh versus yawn.
Scream vs. yawn
Left middle cingulate
1964 Left superior temporal
Laugh vs. Yawn
Coordinates are in MNI space; mapping of cytoarchitectonic areas: PF, PFcm—(Caspers
et al., 2006); 6—(Geyer, 2004); Id1—(Kurth et al., 2010).
Regions showing incongruence effects of emotional valence.
Middle cingulate cortex
Right superior frontal gyrus
Coordinates are in MNI space; mapping of cytoarchitectonic areas: PFm—(Caspers et al.,
2006); 6—(Geyer, 2004).
Fig. 3. Activation in (A) middle cingulate cortex (MCC), (B) right superior frontal gyrus (SFG), (C) right supplementary motor area (SMA) and (D) right temporoparietal junction
(TPJ) in emotional incongruent compared to congruent conditions. Dark grey brain regions represent regions that, until now, have not been mapped using observer-independent
cytoarchitectonic analysis (Schleicher et al., 2005).
V.I. Müller et al. / NeuroImage 54 (2011) 2257–2266
Correlation with BDI-scores
As it is known that depression goes along with impairments in
emotional processing, we were interested if even subclinical depres-
sive symptoms correlate with neural activation in an emotion-related
An analysis with BDI-Scores as covariate revealed a negative
correlation of BDI with activation (across all conditions) bilaterally in
middle occipital gyrus (x=−38; y=−86; z=9 and x=33; y=
−89; z=8) and in right pSTS (x=45; y=−44; z=8) and FFG
(x=29; y=−60; z=−9, all cluster-level corrected pb0.05) (Fig. 5).
There was no significant interaction between BDI and condition.
By using fMRI we investigated the influence of emotional sounds
on the perception of facial expressions and the neural correlates of
incongruence processing. The results revealed an influence of screams
ontheperception offearful andneutralfaces andincongruenceeffects
of emotional valence were found in middle cingulate cortex, right
superior frontal gyrus, right supplementary motor area (SMA) and
right temporoparietal junction (TPJ). Furthermore activation in the
left amygdala was attenuated when an emotional stimulus was paired
with a neutral one compared to when in both modalities the stimulus
Off-line rating of faces and sounds and neural correlates of face and
The off-line rating of faces and sounds showed that both, faces and
sounds were recognized correctly by the subjects with lowest ratings
for fearful faces and sounds, followed by neutral stimuli and the
highest (happiest) ratings for happy faces and sounds. Additionally
the rating of faces reflect that the perceived emotion was more
intense in happy as compared to fearful faces, evident by a larger
difference to the neutral category.
This pattern is reflected in the imaging data. While happy com-
pared to neutral faces activate a widespread cortical network, no
significantly (at the corrected level) increased activity was observed
for fearful as compared to neutral faces. Increased activation in
occipital areas (Britton et al., 2006), insula (Britton et al., 2006; Chen
et al., 2009) and thalamus (Dolan et al., 1996) for happy faces are well
in accordance with previous results.
In contrast, on the FWE correction level, fearful faces did not
recruit more activation in any areas compared to neutral faces. This
reflects the relative moderate expression of fear in the fearful face
condition and goes along with the less intense rating of these faces
Comparing laughs and screams to yawns activated bilateral
superior temporal gyrus (STG), which is in line with previous findings
on emotional vs. neutral vocalizations (Fecteau et al., 2007; Meyer
et al., 2005; Phillips et al., 1998). As Fecteau et al. (2007) pointed out
this activation may either reflectdifferences in acoustic characteristics
or indicate that the STG plays a role in extracting emotional
information from socially relevant sounds. Moreover, screams
compared to yawns led to greater activation in bilateral inferior
parietal cortex (IPC), right SMA and left middle cingulate cortex. This
pattern may reflect that the higher arousal evoked by the screams (as
reflected by the off-line ratings) has led to activation of parietal areas
to augment attention (Corbetta and Shulman, 2002), cingulate cortex
for monitoring (Botvinick et al., 2004) and SMA for increased motor
control (for review see Nachev et al., 2008).
Context effects on ratings of facial affect
Only two studies (de Gelder and Vroomen, 2000; Ethofer et al.,
2006) previously investigated how emotional sounds influence the
perception of (emotional) facial expressions. Our behavioral data
obtained in the scanner demonstrated that context, established by
concurrent social–emotional sounds, influences the perception of
facial expressions. Fearful and neutral faces were perceived more
fearful when accompanied by screams compared to yawns (or laughs
Fig. 4. Amygdala activation when conditions where in both modalities an emotional stimulus was presented (fearful/scream, fearful/laugh, happy/scream, happy/laugh) were
compared to conditions with a neutral stimulus in one and an emotional stimulus in the other modality (fearful/yawn, neutral/scream, neutral/laugh, happy/yawn). LB laterobasal,
SF superficial, CM centromedial nucleus of the amygdala (Amunts et al., 2005).
Additional regions showing incongruence effects of emotion-presence.
Left lingual gyrus
Left middle temporal
Coordinates are in MNI space; mapping of cytoarchitectonic areas: 17—(Amunts et al.,
Fig. 5. Negative correlation of BDI-scores with activation in left and right middle
occipital gyrus (MOG) and right fusiform gyrus (FFG) and posterior superior temporal
V.I. Müller et al. / NeuroImage 54 (2011) 2257–2266
in case of fearful faces). In contrast, these context effects were not
found for happy faces. This is in line with the results of Ethofer et al.
(2006) who also report context effects for fearful and neutral but not
for happy faces. One explanation for the lack of effect on happy faces
may be differences in ambiguity, as indicated by the off-line ratings.
This difference occurred even though happy and fearful faces were
matched in intensity based on the classification of Gur et al. (2002a),
were degraded by the neutral mouth and showed equally clear
separation from neutral faces in a prestudy conducted in a different
sample of 18 subjects. These results thus support earlier notions that
happiness is the easiest and fear one of the hardest recognizable
emotions in faces (Gur et al., 2002a; Montagne et al., 2007).
Compared to yawns only screams, not laughs led to a significantly
more emotional rating, potentially relating to the higher arousal
evoked by these sounds which makes them much harder to ignore.
This higher saliency fits well with the biological perspective that
screams, as threat signals, are far more important for survival than
laughs (Calder et al., 2001; Green and Phillips, 2004) and is further-
morereflected by the more widespread activation evoked by these (as
Neuronal effects of incongruence of emotional valence
Emotional incongruence or conflict (pairing of fearful faces with
laughs and happy faces with screams) evoked greater activation in
middle cingulate cortex, right superior frontal gyrus, right SMA and
right TPJ compared to emotional congruent trials. Crossmodal
emotional conflict thus recruits a network similar to those previously
described to be involved in unimodal emotional and cognitive conflict
and attentional control (Botvinick et al., 2004; Corbetta et al., 2008;
Ochsner et al., 2009; Wittfoth et al., 2010).
The (anterior) cingulate cortex (ACC) has repeatedly been linked
to conflict monitoring (Botvinick et al.,2004;Carter et al.,1998;Carter
and van Veen, 2007) and has been found by Ochsner et al. (2009) and
Egner et al. (2008) for cognitive and affective conflict in the visual
should be noted, that the location of these findings, although reported
as “ACC” corresponds well to the increased activation observed in the
middle cingulate cortex in our study. This discrepancy should be
attributable to the still widespread use of the outdated two-region
classification of the cingulate cortex introduced by Brodmann in spite
of convincing evidence for at least four major regions of this structure
(Palomero-Gallagher et al., 2009; Vogt et al., 2004). As this region has
already been demonstrated to respond to unimodal (Egner et al.,
2008; Ochsner et al., 2009; Wittfoth et al., 2010) and non-emotional
audiovisual (Weissman et al., 2004) conflict, current findings in
emotional audiovisual conflict provide further evidence for a
generalized role of the dorsal middle cingulate cortex in conflict
monitoring and attentional control, irrespectively of modality,
integration demands or affective content. Similarly, several studies
have already linked the superior frontal / dorsolateral prefrontal
cortices to the resolution of (non-emotional) conflict (Corbetta and
Shulman, 2002; Durston et al., 2003; Egner and Hirsch, 2005;
MacDonald et al., 2000) mainly by top-down control of attentional
resources. Again, our results extend these previous findings to
emotional conflict, pointing to an overlapping neuronal framework.
The SMA plays a major role in voluntary action, cognitive control
and initiation/inhibition of motor responses (Grefkes et al., 2008;
Kasess et al., 2008; Nachev et al., 2008; Sumner et al., 2007). SMA
activation was also found for emotional conflict in the study of
Ochsneretal. (2009)in an affective flankertask.Likethese authorswe
would conclude that higher SMA activity may reflect increased
executive control needed to select an adequate response in the
presence of conflicting (emotional) stimuli.
The TPJ, finally, has been implicated in predictive coding (Jakobs
et al., 2009), attentional reorienting, theory of mind and perspective
taking tasks (Corbetta et al., 2008; Derntl et al., 2010; Mitchell, 2008).
In our current data, we would side with the idea of predictive coding
postulating that the brain predicts upcoming events based on
previous information in order to reduce computational load and to
deal with ambiguous information (Creutzig and Sprekeler, 2008). The
auditory stimulus, starting 1000 ms before the face, could have
induced expectation of a visual stimulus congruent with the emotion
expressed in the sound. The presentation of an emotionally in-
congruentface shouldthen haveled toviolation ofthese expectations.
Consequently, if the TPJ integrates sensory signals and against the
expectations on these, the prediction error between bottom-up facial
information and expectation built on the sound may underlie the
greater TPJ activation in the incongruent condition.
of a cingulate-fronto-parietal network previously shown to be involved
in conflict monitoring and resolution (Botvinick et al., 2004; Carter
et al., 1998; Ochsner et al., 2009; Weissman et al., 2004; Wittfoth et al.,
2010). Conflict caused by the convergence of two incongruent
information streams is detected by the dACC/MCC (Botvinick et al.,
2004; Carter et al., 1998; Carter and van Veen, 2007; Kerns et al., 2004),
which recruits the dorsal prefrontal cortex and the SMA to increase
attentional and motor control to enable selection of an adequate
response. The current results expand this conflict monitoring hypoth-
esis in two ways. Firstly, we would argue for a role of the TPJ in
processing temporally asynchronous conflicting information by inte-
grating predictions and incoming stimuli (Jakobs et al., 2009). Second,
our results indicate that the same conflict monitoring and resolution
involved in emotional conflict processing.
This suggestion is in line with the biased competition model of
attention introduced by Desimone and Duncan (1995), postulating
that competition for neural representation occurs when two or more
stimuli with different task relevance are presented. This competition
can in turn be modulated (biased) in two different ways, namely
either based on bottom-up (salience) or by top-down (cognitive
control) influences. The increased activity of cingulate, frontal and
parietal areas in incongruent compared to congruent emotional
conditions observed in our study may reflect such top-down
mechanisms. In particular, given that subjects were instructed to
attend to and rate the faces rather than the sounds, these regions may
be the origin of top-down signals biasing competition towards the
task relevant stimuli (faces) in incongruent conditions where
competition and attentional demands are higher. In line with this
suggestion, other studies also demonstrate greater activity in ACC
(Bishop et al., 2004a) and parietal and frontal (Mitchell et al., 2007)
areas going along with higher attentional demands when a cognitive
task is distracted by emotional stimuli. Furthermore it is reported that
attention towards a non-emotional task suppresses activity in the
amygdala (Amting et al., 2009; Bishop et al., 2004b; Mitchell et al.,
2008; Pessoa et al., 2005). The absence of a (valence) congruency
effect in the amygdala could therefore just be the result of biased
competition, as the salience of emotional sounds is likewise
suppressed in favor of the (attended) face.
Role of the amygdala
In contrast to the finding of Dolan et al. (2001) we did not observe
any (in-) congruence effects of emotional valence in the amygdala
when explicitly testing for these. However, the testing of incongru-
ence effects with respect to the presence and absence of emotional
stimuli (incongruence of emotion-presence) revealed a significant
effect in the left basolateral/superficial amygdala complex.
Itshouldbenotedthatourresultshould beinterpreted withcaution
given the current resolutionof fMRI and the susceptibility of the medial
temporal lobe to imaging artifacts. Nevertheless, the applied histolog-
ical atlas allows anatomical allocation in a probabilistic fashion, hereby
V.I. Müller et al. / NeuroImage 54 (2011) 2257–2266
accommodating some of the uncertainty in establishment of structure–
function relationships (cf. Amunts et al., 2005; Eickhoff et al., 2005).
Moreover, this approach has already been repeatedly shown to allow
the attribution of functional activation to specific parts of the amygdala
(Ball et al., 2007; Goossens et al., 2009; Roy et al., 2009).
smoothing kernel as previous studies which targeted particularly at
amygdala responses (Ball et al., 2007; Goossens et al., 2009; Roy et al.,
2009). In this context, however, it is important to note, that while
smoothing blurs the data, it should per se not affect localisation
accuracy (Fox et al., 2001). Rather spatial uncertaintyin neuroimaging
results mainly derives from inter-individual variability and impreci-
the individual subjects’ mean EPI image directly as the source image
for spatial normalisation rather than co-registering T1. This approach
has the advantage of avoiding influences of non-linear distortions
between EPI and T1 images and yields a precise registration of the
functional data into MNI space (see supplementary Fig. 1).
Though, our result indicates that in audiovisual pairing the left
amygdala is active independent of crossmodal valence congruency
when emotional information is not accompanied by concurrent neutral
information. Conversely, it may be hypothesized, that a neutral
stimulus in onesensory channel may counteract the emotional saliency
provided by the stimulus in the other modality by attenuating
amygdala responses. In other words, in audiovisual integration it is
not only the presence of an emotional stimulus but rather the absence
of a concurrent, mitigating neutral stimulus that may be crucial for left
amygdala responses. Could this effect be related to priming, so that the
presentation of a neutral stimulus influences amygdala response to the
subsequent facial stimulus? Importantly this is not the case, as the
pattern of activation is the same independently of whether the neutral
stimulus (yawn) was presented first or as a neutral face 1000 ms after
the onset of an (emotional) sound.
The current findings thus place a new twist on the current views
about the function and role of the left amygdala. It has previously been
demonstrated that this structure is activated by attended and
unattended emotional stimuli in the visual or auditory modality (Belin
et al., 2004; Fecteau et al., 2007; Gur et al., 2002b; Habel et al., 2007;
Phillips et al., 1998; Sander and Scheich, 2001). We could show that the
left laterobasal/superficial amygdala nuclei also integrate neutral
stimuli across modalities, which probably leads to an “all-clear” signal.
From studies in macaque monkeys it is known that the laterobasal
amygdala receives direct input from auditory and visual cortices
(McDonald, 1998; Yukie, 2002). Moreover feedback projections from
the basal nucleus of the amygdala to sensory-associative areas have
pattern in combination with the observed response pattern may be
interpreted as follows. The left amygdala receives socially salient
information from all sensory domains which are then integrated and
evaluated. Information processing in visual and auditory areas is then
modulated via the feedback projections from the laterobasal amygdala
to early sensory cortices providing a route for enhancing behaviourally
relevant and suppressing less important information. Ultimately,
integrating a neutral stimulus into the evaluation by the amygdala
should then lead to top-down inhibition in associative visual and
down facilitation by the amygdala as evident from significantly higher
activation in the purely emotional conditions in lingual gyrus, calcarine
sulcus, STG and middle temporal gyrus (MTG).
Correlation with BDI
BDI scores were negatively correlated with activation in left and
right occipital gyrus as well as right FFG and STS, i.e., regions
contributing to the neural system for facial perception (Haxby et al.,
2000). Moreover, the posterior superior temporal sulcus plays also a
crucial role in audiovisual integration (Beauchamp, 2005; Campanella
and Belin, 2007). As we only investigated healthy subjects with BDI
scores in the normal range, these scores may be regarded as
subclinical depressive symptoms or traits which nevertheless were
shown to correlate with neuronal activation in an emotion-related
task. The observed correlation in sensory cortices may point to a
dysregulation of neuronal activity by depressive traits spreading
beyond areas involved in emotion regulation (for a review on findings
in depression see Leppanen, 2006) to early stages of face processing.
Alternatively, the negative correlation of BDI scores and activity in STS
could indicate decreased crossmodal integration associated with
higher depressivity, which has yet to be tested in patients with major
depression. In particular, it remains to be seen, how evaluation in the
amygdala and integration in the STS may be differentially affected in
Our audiovisual integration paradigm demonstrated that cross-
modal emotional conflict recruits a cingulate-fronto-parietal network
previously shown for cognitive, motor and (unimodal) emotional
conflict monitoring and resolution. We propose that emotional
conflict is detected by the TPJ integrating bottom-up input and
expectation while the middle cingulate cortex recruits the dorsal
prefrontal cortex and SMA to increase cognitive and motor control for
selecting the adequate response.
Additionally, our results reveal that irrespective of congruency the
left laterobasal/superficial amygdala is attenuated as soon as one
sensory channel carries neutral but ecologically valid information.
This indicates that crossmodal evaluation in the amygdala integrates
emotional as well as neutral information with the latter providing a
“clear-off” for implicit arousal regulation.
At last, BDI scores correlated negatively with activation in occipital
even subclinical traits into account when investigating emotional
This study was supported by the Deutsche Forschungsge-
meinschaft (DFG, IRTG 1328), by the Human Brain Project (R01-
MH074457-01A1), and the Helmholtz Initiative on systems biology
(The Human Brain Model).
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