Brain and Cognition 92 (2014) 92100

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Brain and Cognition

journal homepage: www.elsevier.com/locate/b&c

Atypical crossmodal emotional integration in patients with gliomas

Viviane Luherne-du Boullay a,, Monique Plaza b, Annabelle Perrault a, Laurent Capelle d,
Laurence Chaby b,c
a

Universit Paris 8 Vincennes Saint Denis, Saint-Denis, France

Institut des Systmes Intelligents et Robotique, ISIR, CNRS UMR 7222, Paris, France
c
Universit Paris Descartes, Sorbonne Paris Cit, Institut de Psychologie, Boulogne-Billancourt, France
d
Neurochirurgie, Hpital Piti-Salptrire, AP-HP, 47-83, boulevard de lHpital, 75651 Paris cedex 13, France
b

a r t i c l e

i n f o

Article history:
Accepted 6 October 2014

Keywords:
Gliomas
Facial emotion
Vocal emotion
Multisensory integration
Hodotopic model

a b s t r a c t
The relevance of emotional perception in interpersonal relationships and social cognition has been well
documented. Although brain diseases might impair emotional processing, studies concerning emotional
recognition in patients with brain tumours are relatively rare. The aim of this study was to explore emotional recognition in patients with gliomas in three conditions (visual, auditory and crossmodal) and to
analyse how tumour-related variables (notably, tumour localisation) and patient-related variables inuence emotion recognition. Twenty six patients with gliomas and 26 matched healthy controls were
instructed to identify 5 basic emotions and a neutral expression, which were displayed through visual,
auditory and crossmodal stimuli. Relative to the controls, recognition was weakly impaired in the patient
group under both visual and auditory conditions, but the performances were comparable in the crossmodal condition. Additional analyses using the race model suggest differences in multisensory emotional
integration abilities across the groups, which were potentially correlated with the executive disorders
observed in the patients. These observations support the view of compensatory mechanisms in the case
of gliomas that might preserve the quality of life and help maintain the normal social and professional
lives often observed in these patients.
2014 Elsevier Inc. All rights reserved.

1. Introduction
Gliomas are invasive brain tumours occurring more frequently in
young people and most commonly discovered after sudden epileptic seizures (Capelle et al., 2013; Pallud et al., 2013). Astrocytomas,
oligodendrogliomas, and mixed gliomas often concern frontal and
temporal lobes (Correa et al., 2007) in cortical and subcortical structures (Duffau, Gatignol, Mandonnet, Capelle, & Taillandier, 2008).
According to World Health Organization (WHO), a grading system
leads to separate low-grade (II) gliomas (LGG) and high-grade (III
and IV) gliomas (HGG) (Figarella-Branger et al., 2008). LGG show a
continuous, constant growth (about 4 mms/year) in local, white
matter and systematically evolve toward HGG (Bonnetblanc,
Desmurget, & Duffau, 2006), with a median of around 78 years
for anaplastic transformation and a median survival around
10 years without treatment (Duffau, 2005). Due to their slow development and inltrating characteristics, gliomas efciently activate

Corresponding author at: Universit Paris 8 Vincennes Saint Denis, 2 rue de la

Libert, 93526 Saint-Denis cedex, France.
E-mail address: viviane.du.boullay@gmail.com (V. Luherne-du Boullay).
http://dx.doi.org/10.1016/j.bandc.2014.10.003
0278-2626/ 2014 Elsevier Inc. All rights reserved.

brain plasticity and connectivity (Duffau, Capelle, & Denvil, 2003;

Szalisznyo, Silverstein, Duffau, & Smits, 2013).
Because cognitive disorders inuence social status and quality
of life (Correa et al., 2008), early diagnosis in patients with gliomas
attached particularly emphasis to neuropsychological functioning
in last decade. The patients often present a quasi normal neuropsychological prole when assessed with classical tests, which
were created to assess the impairments that can follow sudden
strokes or neurodegenerative diseases (De Angelis, 2001;
Desmurget, Bonnetblanc, & Duffau, 2007; Duffau, 2005; Duffau
et al., 2008; Meyers & Brown, 2006; Plaza, du Boullay, Perrault,
Chaby, & Capelle, 2013). By contrast, ne-grained neuropsychological assessments have shown discrete cognitive impairments, particularly in language, working memory, verbal memory, attention
and executive function (Archibald et al., 1994; Le Rhun,
Delbeuck, Devosc, Pasquier, & Dubois, 2009; Plaza, Capelle,
Maigret, & Chaby, 2012; Plaza et al., 2013; Reijneveld, Sitskoorn,
Klein, Nuyen, & Taphoorn, 2001; Satoer et al., 2014; Teixidor
et al., 2007; Wu et al., 2011). Subtle impairments in emotion recognition have also been described in a group of eleven patients with
left frontal glioma (Mu et al., 2012) and in our previous study

V. Luherne-du Boullay et al. / Brain and Cognition 92 (2014) 92100

concerning a group of seven patients with LGG (Du Boullay, Plaza,

Capelle, & Chaby, 2013).
The ability to identify the emotional states of other individuals
is a fundamental aspect of interpersonal interaction and social cognition (Gallese, Keysers, & Rizzolatti, 2004) and inuences the
quality of life (Correa et al., 2008). It includes the ability to accurately interpret linguistic and non-linguistic (e.g., facial and vocal
expressions) emotional signals that play a crucial role in the perception of emotion and behavioral intentions (Hawk, van Kleef,
Fischer, & van der Schalk, 2009). Identifying emotions requires
the rapid interpretation of subtle changes in facial features and
voice tones; thus, it involves executive capacities and speed of
information processing. The fact that executive functions and the
speed of information processing are frequently impaired in cases
of gliomas could contribute to the observed patients difculties
in emotion recognition (Luherne-du Boullay, Chaby, & Plaza,
2013; Mu et al., 2012).
Emotion recognition has been previously explored in various
brain diseases, such as traumatic and vascular brain injuries (e.g.,
Adolphs, Baron-Cohen, & Tranel, 2002; Hornak et al., 2003;
Williams & Wood, 2010), neurodegenerative diseases (e.g., Chaby
& Narme, 2009; Narme, Bonnet, Dubois, & Chaby, 2011) and psychiatric troubles (e.g., Green & Leitman, 2008; Petresco David, Soeirode-Souza, Moreno, & Soares Bio, 2014; Simpson, Pinkham, Kelsven,
& Sasson, 2013). These studies most often concerned the recognition of emotional expression in a single sensory modality, although
in natural situations, emotions are processed through different sensory modalities. It is of note that congruent emotional information
processed via multisensory channels optimises behavioral reactions, which results in faster response times and increased accuracy
(de Gelder & Vroomen, 2000; Klasen, Kenworthy, Mathiak, Kircher,
& Mathiak, 2011; Kreifelts, Ethofer, Grodd, Erb, & Wildgruber,
2007). This effect was observed in our previous exploratory study
with a group of seven LGG patients before tumour resection (du
Boullay et al., 2013). Compared with the control group, the patient
group had (non-signicant) lower and slower performances in
auditory and visual conditions but similar crossmodal performances. This global preservation of capacities could be attributed
to the plasticity and connectivity mechanisms used by the brain
to compensate for the progressive tumour inltration.
According to the hodotopical model (De Benedictis & Duffau,
2011), the anatomical and functional organization of the brain is
based on synchronous and often redundant interactions of the
entire network. Due to intra- and inter-territorial connections,
brain lesions could result in alterations of both local cortical
regions and white matter connecting pathways far from the lesion
site (Catani & Ffytche, 2005) with or without functional impairments. Notably, brain gliomas can be associated with spared abilities, or specic impairments (e.g., mutism) or a disconnection
syndrome (Catani & Ffychte, 2005; Duffau, 2013), which could
modify the nature of the crossmodal integration.
Although each basic emotion is characterized by both consistent and discriminable neural correlates across studies (Vytal &
Hamann, 2010), many brains regions are implicated in emotion
recognition in visual and auditory conditions. Neural basis of emotion recognition are founded on a broad cortico-subcortical interconnected network (Di Bitonto et al., 2011). Furthermore, neural
bases of emotional face/voice integration may involve the bilateral
superior temporal sulcus (STS) (Kreifelts et al., 2007), the middle
temporal gyrus (MTG) (Pourtois, de Gelder, Bol, & Crommelinck,
2005) and the medial prefrontal cortex (MPF) (Peelen et al.,
2010). Moreover, the posterior temporal sulcus (pSTS) is identied
as a key region in integration of emotional information and may
exert modulator inuence on unisensory cortices and their forward
connections (Mller, Cieslik, Turetsky, & Eickhoff, 2012). An
increase in connectivity between fusiform gyrus, and superior tem-

93

poral gyrus with ipsilateral pSTS in bimodal compared to unimodal

conditions has also been described par Kreifelts et al. (2007).
In the present study of a group of 26 patients with gliomas, we
aimed to (a) determine their visual, auditory and crossmodal emotional recognition abilities, (b) thorough the nature of the crossmodal integration in the patient group compared with the control
group using the race model methodology; (c) analyse whether
emotion recognition is correlated with language and executive
functions and (d) determine how tumour-related variables (notably, tumour localisation) and patient-related variables inuence
emotion recognition.
2. Methods
2.1. Participants
Twenty-six patients with gliomas undergoing surgery at our
institution were included in this study (Table 1). The pre-surgical
radiological imagery and clinical presentation suggested for all
patients a diagnosis of low-grade gliomas. After tumour resection,
pathological examination revealed that most tumours were lowgrade gliomas (18/26) and about one-third (8/26) presented an
early anaplastic transformation and was considered as high-grade
gliomas. This series included 15 men and 11 women, ranging in age
from 22 to 61 years (mean age = 40.27 9.18). A neurosurgeon (LC)
and a psychologist (VL, AP or MP) administered neurological and
neuropsychological examinations, respectively. Seizures occurred
as the presenting symptoms in 77% of the cases. Pharmacologically
resistant epilepsy was present in 22 patients and epileptic seizures
were controlled for all patients. None received a previous oncological treatment. The Karnosky Performance Status (KPS) was 90%
(able to work despite a mild decit and/or chronic seizures) or
100% in 18 patients. The topography of the tumour was accurately
demonstrated in preoperative Magnetic Resonance Images (T1weighted and spoiled-gradient images obtained before and after
Gd enhancement in the three orthogonal planes, T2-weighted axial
images and FLAIR-weighted axial images). Clinical data are presented in Table 1.
The control group (CTRL) was comprised of 26 healthy subjects
(15 men and 11 women, ranging in age from 23 to 63 years (mean
age = 39.62 10.88) with no history of neurological or psychiatric
illness. None of these individuals reported any hearing impairment, and all had normal or corrected-to-normal vision. The two
groups were matched for age and gender.
The exclusion criteria for all subjects included habitual drug or
alcohol abuse, secondary neurological disorders (e.g., dementia), a
history of previous head trauma or neurological disorders and
other psychiatric or personality disorders. All participants were uent in French.
All subjects provided informed consent to participate in the
study. The demographic information are summarised in Table 2.
2.2. Emotional recognition task
2.2.1. Stimuli
The visual stimuli consisted of a set of photographs of human
emotional faces obtained from the Karolinska Directed Emotional
Faces Database (Lundqvist, Flykt, & Ohman, 1998). Ten full frontal
view pictures (5 males and 5 females) conveying happiness, sadness, disgust, anger, fear and a neutral face were presented in slide
form on a screen for 60 trials. The faces were clipped and smoothed
using Adobe Photoshop and saved on a black background.
The auditory stimuli was comprised of a set of 60 affect vocalisations (5 males and 5 females) conveying happiness, sadness, disgust, anger, fear and a neutral vocalisation, obtained from The
Montral Affective Voices, a standardised set of emotional vocal

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V. Luherne-du Boullay et al. / Brain and Cognition 92 (2014) 92100

Table 1
Clinical data.
Patient

Tumour

Anti-epileptic drug

Case

Age

Sex

KPS score

Location

Type

Grade

Volume (3D/SEGM)

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26

52
42
41
40
44
37
40
42
29
36
39
50
33
61
37
51
49
44
36
23
27
44
36
22
52
40

F
F
F
H
H
F
H
F
H
H
F
H
F
H
H
F
H
F
H
H
H
H
H
H
F
F

80
100
70
100
100
100
85
100
100
100
80
80
75
90
100
100
90
100
90
90
100
80
100
100
80
90

L
R
L
L
L
L
L
R
L
L
L
L
BI
R
L
L
L
L
L
L
R
L
L
R
R
L

Oligodendroglioma
Mixed glioma
Oligodendroglioma
Mixed glioma
Mixed glioma
Mixed glioma
Mixed glioma
Astrocytoma
Oligodendroglioma
Mixed glioma
Astrocytoma
Gliobastoma
Mixed glioma
Oligodendroglioma
Oligodendroglioma
Mixed glioma
Gliobastoma
Mixed glioma
Mixed glioma
Mixed glioma
Mixed glioma
Mixed glioma
Mixed glioma
Mixed glioma
Oligodendroglioma
Oligodendroglioma

III
II
II
II
II
II
II
II
II
II
II
IV
III
II
II
III
IV
III
II
II
II
III
IV
II
II
II

29.6
33.8
16.2
3.9
24.3
43.3
64.9
47.7
15.6
58.5
135.5
46.1
211.4
26.5
17.2
30
11.4
26.1
119.8
78.6
23.8
175.6
35.2
8.4
53.3
35.2

Temporal
Insular
Frontal
Frontal
Frontal
Fronto-temporo-insular
Insular
Parietal
Frontal
Cingular
Fronto-temporo-insular
Temporal
Frontal
Frontal
Temporal
Frontal
Temporal
Cingular
Temporo-insular
Temporo-insular
Insular
Fronto-insular
Frontal
Temporal
Temporo-insular
Frontal

USA) was used to control the visual and auditory stimulus delivery
and record the response times and the accuracy for each subject.

Table 2
Demographic characteristics of study participants.

Age, years; mean (SD)

Sex, M/F
Education, years of schooling; mean (SD)

Yes
Yes
Yes
No
Yes
Yes
Yes
Yes
No
Yes
Yes
Yes
No
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
No

Patients
(n = 26)

Controls
(n = 26)

40.27 (9.18)
15/11
13.81 (2.73)

39.62 (10.88)
15/11
16 (1.2)

expressions designed for research on auditory affective processing

with the avoidance of potential confounds from linguistic content
(Belin, Fillion-Bilodeau, & Gosselin, 2008). The average duration
of the stimuli was 1199 s.
The crossmodal stimuli were comprised of a set of the same 60
emotional faces and voices congruently and simultaneously
presented.

2.2.2. Procedure
All stimuli were presented on a 17 in. monitor (resolution set to
1200  800 pixels). Each participant performed 180 trials, which
were divided into 3 blocks (visual, auditory, and crossmodality).
Two sets of 60 items in pseudo random order were constructed
for each block. The visual and auditory conditions were randomly
presented and the crossmodal condition was always presented
last. Each trial was initiated with the presentation of a xation
cross for 300 ms, followed by the stimulus presentation. An intertrial interval of 500 ms announced the next trial. In the three emotion recognition tasks, the participants were instructed to carefully
consider all six alternatives before responding. The verbal labels for
the six emotion expressions were printed under each picture on
the computer screen throughout the test, and the subjects were
asked to select the word that best described the emotion presented
in each slide. The responses were recorded from mouse clicks.
There was no time limit for analyzing each stimulus or for responding. The patients were not given feedback on their performance.
Ten additional practice trials were conducted prior to each block.
E-prime software (Physiology Software Tools, Pittsburgh, PA,

2.3. Cognitive tests

Before completing the emotional task, the LGG group underwent a battery of standardised neuropsychological tests as part
of a routine clinical assessment. Some tests were selected in order
to investigate the relationship between the measures of emotional
recognition and cognition. Because attention, executive function,
language and short-term memory might impact emotion task performance, we administered the Trail Making Test (TMT: part A and
B; Reitan, Wolfson, 1985; adaptation Tombaugh, T. 2004), the
Frontal Assessment Battery (FAB; Dubois, B., Slachevesky, A., Litvan, I., & Pillon, B. 2000), the STROOP (J.R. Stroop, 1935, adaptation
Chatelois, 1993), the forward and backward digit span from the
Wechsler Adult Intelligence Scale3rd Edition (WAIS-III; Wechsler,
1997) and a visual naming test (Denomination 70: DO 70; created
and previously used by our group for the evaluation of lexical performance, Plaza et al., 2012). To facilitate the statistical analyses,
all raw scores (except digit span) were converted into z-scores
for each patient in reference to the mean and standard deviation
of his/her control group matched in age, gender, and the level of
education. We also administered the Beck Depression Inventory
(BDI II; Beck, Steer & Brown, 1996) to evaluate the mood state.
Neuropsychological data are presented in Table 3.
2.4. Statistical analysis
All statistical analyses were performed using Statistica 8 software (StatSoft, Inc. Tulsa, USA). To determine whether emotion
recognition performance differed across groups and across modalities and emotions, a 2  3  6 mixed ANOVA was performed with
one between-group factor (group: gliomas, CTRL) and two within
group factors (task: visual, auditory, and crossmodal; emotions:
neutral, happiness, anger, fear, sadness and disgust) for the accuracy score (%) and the response times (ms), respectively. When nec-

V. Luherne-du Boullay et al. / Brain and Cognition 92 (2014) 92100

Table 3
Neuropsychological data.
Patients (n = 26)

Mean (SD)

FAB/18
DO70/70

16.52(1.6)
67.81(2.4)

TMT
Part A, time, s
Part B, time, s
Part B score /13
Forward span/backward span

32.27(12.3)
85.96(34.4)
13.04(2.1)
5.21(1.1)/3.88(1.2)

STROOP test
Inhibition, time, s
Flexibility, time, s
Flexibility, corrected errors

100.54(32.4)
114.42(28.3)
1.17(1.9)

essary, Greenhouse-Geisser corrections were employed to adjust

for the violation of the sphericity assumption in testing repeated
measures effects. To provide clarity, the uncorrected degrees of
freedom are reported, with the p value associated with the Greenhouse-Geisser adjustment. The magnitude of the signicant differences was interpreted by calculating a partial eta squared (g2p).
Using the criteria proposed by Cohen (1988), g2p values 6.01, P.06,
P.14 indicate small, moderate and large effects, respectively. Planned
comparisons were used to compare the gliomas and CTRL groups, and
the Bonferroni correction was used for multiple comparisons.
Multisensory integration was tested using the race model of
inequality. This model provided by Miller (1982) tests whether
the redundant target effect (faster response times in the crossmodal
condition) reects a multisensory integrative process. This method
facilitates the comparison of the multisensory condition with the
joint probability of the unisensory conditions ((pAuditory + pVisual)
(pAuditory  pVisual)). If the probability of a response to the multisensory stimulus is signicantly greater than that predicted by the
summed probability of the unisensory stimuli, then this probability
is considered to violate the race model. Analyses of the violation of
the race model inequality were performed using the RMItest software and implemented the algorithm described in Ulrich, Miller,
and Schrter (2007). This algorithm estimates the cumulative probability distributions of the RT under the two unimodal conditions
and the crossmodal condition and examines whether redundanttarget response times (the bimodal condition) are signicantly faster than predicted by the race model (with t-tests).
A correlation matrix was conducted to determine the associations between the emotion recognition score and the neuropsychological data (i.e., executive tasks). We then investigated the
potential relationships between the emotion recognition scores
and the tumour-related and patient-related variables. A correlation
matrix was conducted to determine the associations between the
emotion recognition score and patients variables. Due to the small
size and non-normal distribution of the subgroups, we used KruskalWallis and MannWhitney U tests when necessary to evaluate
tumors relative variables.
Finally, we determined four subgroups of patients depending on
the tumour localisation (frontal, temporo-insular, fronto-temporoinsular, or parietal) and calculated the z-score for each patient in
the three modalities to determine the number of patients impaired
(z < 1.65) in each subgroup.

95

(91.18 5.60% vs 93.78 2.70%). We observed a signicant interaction between Group and Modality (F(2, 100) = 3.76, p = .027, e = .94,
g2p = .07). Planned comparisons revealed that the patient group performed more poorly than the CTRL group, in the visual modality
(87.82% vs 91.73%, F(1, 50) = 4.69, p = .04, g2p = .09) and the auditory
modality (87.95% vs 91.47%), F(1, 50) = 4.76, p = .03, g2p = .09). By contrast, the scores did not signicantly differ between the two groups
(F < 1) in the crossmodal condition (Fig. 1).
A signicant effect of Emotion was observed (F(5, 250) = 42.31,
p < .001, e = .77, g2p = .45). The participants recognized happiness
(97.82%) and neutral (98.8%) more accurately than the other emotions, particularly anger, which was recognized less accurately
(82.98%). There was a signicant interaction between Emotion and
Modality (F(10, 500) = 37.27, p < .001, e = .51, g2p = .43), and also
between Group and Emotion (F(10, 250) = 1.02, p = .41, e = .77,
g2p = .02).
Importantly, a signicant effect of Modality was observed
(F(2, 100) = 90.27, p < .001, e = .94, g2p = 0.64). Planned comparisons
revealed that the participants recognized the emotion more accurately in the crossmodal condition than in the visual and auditory
modalities (F(1, 50) = 194.67, p < .001, g2p = .80). No signicant differences were observed between the visual and auditory modalities
(F < 1).
For the response times, the results were slightly different. We
rst observed a main effect of the Group (F(1, 50) = 15.65,
p < .001, g2p = .24). Indeed, the LGG group was consistently slower
than the CTRL group (2994 972 ms vs 2213 424 ms). A signicant
interaction failed to reach signicance between the Group and
Modality (F(2, 100) = .92, e = .74, p = .40). A signicant effect of Emotion was observed (F(5, 250) = 46.35, p < .001, e = .68, g2p = .48). Participants responded more quickly to happiness and neutral, and
fear was the slowest to be recognized (see Table 2). There was a signicant interaction between Emotion and Modality (F(10, 500) =
13.42, p < 0.001, e = .52, g2p = .21) and a signicant interaction
between Emotion and Group (F(5, 250) = 5.15, p < .001, e = .68,
g2p = .09). A Bonferroni post hoc analysis revealed that happiness
and neutrality were always recognized faster (all p < .001), and the
differences between these two emotions and the other emotions
(i.e., negatives emotions) were more important in the patient group
compared than in with the CTRL group.
Finally, we observed a signicant effect of Modality
(F(2, 100) = 59.83, p < .001, e = .74, g2p = 0.54). Planned comparisons
revealed faster responses in the crossmodal condition than in unimodal (visual and auditory) conditions (F(1, 50) = 105.25, p < .001,
g2p = .68). The auditory modality was faster than the visual modality
(F (1,50) = 17.43, p < .001, g2p = 0.26).
3.2. Multisensory integration

3. Results

To determine the nature of the crossmodal advantage over unimodal integration in each group, we used the race model of
inequality. If the response times obtained in the crossmodal condition are better than predicted by the race model, this provides evidence that the information from the visual and auditory modalities
interacted to produce the RT facilitation, suggesting the likely neural integration of the two unisensory inputs. As expected, we
observed a violation of the race model prediction for the CTRL
group over the 5, 25 and 35 percentiles of the RT distribution
(p < .05). By contrast, in the patient group, the race model was
not violated on any percentile of the distribution (Fig. 2).

3.1. Visual, auditory and crossmodal emotion recognition

3.3. Correlation analyses with neuropsychological data

For the accuracy scores, we observed an effect of Group

(F(1, 50) = 4.56, p = .038, g2p = .08) on emotion recognition, with the
patient group performing more poorly than the CTRL group

On the premise that neuropsychological functioning might contribute to emotion recognition difculties following gliomas, notably in crossmodal integration, we investigated whether a

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V. Luherne-du Boullay et al. / Brain and Cognition 92 (2014) 92100

100

4000
GLIOMAS
CTRL

GLIOMAS
CTRL

3500

Response times (ms)

Accuracy score (%)

90

80

70

60

3000

2500

2000

50

1500
Visual

Auditory

Crossmodal

Visual

Auditory

Crossmodal

Fig. 1. Mean score (%) and response times (in milliseconds) for each modality (visual, auditory, crossmodal) and for each emotion, for the two groups (GLIOMAS, CTRL).

signicant relationship exists between the executive tasks and

emotion recognition. Above all, and in accordance with literature,
neuropsychological data indicated that most patients were not or
only slightly impaired in cognitive tasks. 12 presented no impairment, 13 were impaired in 14 tasks, 1 presented 6 tasks impaired
and no one had more than 6 tasks impaired. We then analyzed the
correlations of emotion recognition with the FAB, the TMT (A & B),
the SPAN (forward & backward) and the STROOP (inhibition, exibility). We observed signicant correlations between the total
score of emotion recognition and the FAB (p = .05), the forward
SPAN (p = .05) the backward SPAN (p = .01), the STROOP inhibition
(p = .05) and exibility (p = .01), and no correlations with the TMT.
We also observed signicant correlations between the crossmodal
score of emotion recognition and the FAB (p = .01), the forward
SPAN (p = .01) and the STROOP inhibition (p = .05) and exibility
(p = .05).
Furthermore, no correlations were found between BDI score and
emotion recognition (p = .21).
3.4. Inuence of tumor-related and patient-related variables on
emotion recognition

ognition score (p > .19). Additional analysis showed that the emotion recognition score (ranging from 72.78% to 97.22%) correlated
with the KPS score (p = .01) and not with age (p > .05).
When tumor-related variables were investigated, we found that
tumor volume did not inuence emotion recognition score
(p > .05). U-MannWhitney tests revealed none effect of tumor
malignity (LGG vs HGG) on emotion recognition score in visual,
auditory and crossmodal modalities (all p > .24). An effect of laterality was found in auditory modality (p = .05), with patients with
left glioma better performing than those with right gliomas. None
effect of laterality was found in visual and crossmodal modality (all
p > .06). KruskalWallis tests revealed none effect of histology (all
p > .25) or localization (divided in four groups) (all p > .10). Concerning the tumor localization, slight differences were found
between the four subgroups (see Table 4). MannWhitney U Test
revealed a signicant difference between the frontal and the temporo-insular group in visual modality (p = .04), with the frontal
group responding worse than the temporo-insular group (84.09
vs 91.39%). None signicant difference was found in auditory
modality or crossmodal condition (p > .14).
4. Discussion

As antiepileptic therapy has been frequently associated with

more pronounced cognitive dysfunction (Correa et al., 2007;
Pallud et al., 2013), we rst compared performances between
patients with and without antiepileptic therapy. MannWhitney
U tests revealed none effect of antiepileptic drugs on emotion rec-

In the present study, we investigated the ability of a group of

patients with gliomas to recognize emotions from both facial
expressions and emotional prosody. Although several studies have
demonstrated that patients with traumatic and vascular brain

CTRL

0,8

0,8

Cumulative probability

Cumulative probability

GLIOMAS

0,6

0,4

Visual
Auditory
Crossmodal
Predicted

0,2

0
1000

2000

3000

4000

5000

Responses Time (ms)

6000

0,6

0,4

Visual
Auditory
Crossmodal
Predicted

0,2

7000

0
1000

2000

3000

4000

5000

6000

Responses Time (ms)

Fig. 2. The cumulative probability distributions for discrimination response times to visual (black dots), auditory (black squares), and multisensory stimuli (white dots). The
summed probability for the visual and auditory responses is depicted by the race model curve (red stars). (For interpretation of the references to color in this gure legend,
the reader is referred to the web version of this article.)

V. Luherne-du Boullay et al. / Brain and Cognition 92 (2014) 92100

Table 4
Number of patients with z-scores below
subgroups.
Localization (number of patients)
Frontal (n = 11)

Temporo-insular (n = 12)
Fronto-temporo-insular (n = 2)
Parietal (n = 1)

L(n = 9)
R(n = 1)
B(n = 1)
L(n = 8)
R(n = 4)
L(n = 2)
R(n = 0)
L(n = 0)
R(n = 1)

1.65 for each modality in the four

Visual

Auditory

Crossmodal

2
1
0
1
1
1
0
0
0

2
1
1
1
2
1
0
0
1

3
1
0
0
0
1
0
0
0

injury are impaired in recognizing facial and prosodic emotions,

little is known about emotion recognition in patients with cerebral
tumors. We also examined the relationship between emotion recognition performance and cognitive skills and clinical variables.
The present data rened our previous results concerning a small
group, and showed that patients with gliomas have slight but signicant difculty in recognizing emotion. Compared with the CTRL
group, they performed lower in the visual and auditory modalities
and were slower under all conditions, which is consistent with previous studies concerning emotion processing in patients with cerebral diseases (Bonora et al., 2011; Williams & Wood, 2010; Willis,
Palermo, Darren, Mc Grillend, & Miller, 2010). However, the decits
observed were minor (mean accuracy of 87.82% for faces and
87.95% for voices), suggesting the involvement of efcient compensatory mechanisms during tumor development. Patients with
gliomas inltrating eloquent areas often display quite normal preoperative language and neuropsychological testing. For example,
language may be preserved despite a tumor in Brocas area
(Plaza, Gatignol, Leroy, & Duffau, 2009), the striatum (Duffau,
Taillandier, Gatignol, & Capelle, 2006; Gil Robles, Gatignol,
Capelle, Mitchell, & Duffau, 2005) or the prefrontal dorsolateral
cortex (Plaza, Gatignol, Cohen, Berger, & Duffau, 2008). As gliomas
slowly inltrate brain areas, they permit increased plasticity and
better functional reshaping. To exert efcient compensatory mechanisms, the neural networks are activated along the vertical (corticalsubcortical) and horizontal (cross-cortical) axes. The brain
progressively recruits intra- or large peri-tumoral regions in the
ipsi-lateral hemisphere and regions in the contra-lateral hemisphere (Bonnetblanc et al., 2006), reecting the frequent induction
of weak cognitive impairments in gliomas (Duffau et al., 2003;
Plaza et al., 2008). The results of the present study suggest that
emotion processing, which concerns a wide neural cortico-subcortical network (Berthoz, Blair, Le Clech, & Martinot, 2002; Sabatinelli
et al., 2010) with specic brain structures in fronto-temporal cortices (Vytal & Hamann, 2010), also benets from compensatory
mechanisms.
Moreover, a hodological system at cortical and subcortical level
sustains mentalizing, which is another brain function supporting
social cognition. Mentalizing is the ability to understand the mental states and emotions of others on the basis of perceptual properties. Both low (dedicated to the identication of mental states) and
high (dedicated to the attribution of mental states) aspects of mentalizing would involve the arcuate fasciculus and the right cingulum as two parallel distinct but functionally interdependent
networks. Indeed, lesions in cortical epicenters or frontoparietal
disconnection in subcortical white matter are correlated with poor
mentalizing performance (Herbet et al., 2014).
In addition to minor difculties observed in visual and auditory
modalities, patients with gliomas were signicantly slower than the
CTRL group to recognize emotion in all conditions. This slowness
was observed in previous studies. Moritz-Gasser, Herbet, Lima
Maldonado, and Duffau (2012) found that after tumor resection,

97

there was no correlation between picture naming accuracy scores

and return to previous professional activity. Conversely, there was
a correlation between slow naming speed and efcient return to
work. Patients were tested pre-and post operatively and were t
to return to work when they recovered exactly the same level of
naming speed recorded during the pre-operative test. The present
study reinforces the general concept that a LGG brain works well
but slowly, and this could impact patients quality of life.
Interestingly, although slower response times were observed
under all conditions, the performances of patients with gliomas
were signicantly lower in the visual and auditory modalities,
but comparable in the crossmodal condition. Consistent with previous studies (Collignon et al., 2008; Collignon et al., 2010; de
Gelder & Vroomen, 2000; Klasen et al., 2011; Kreifelts et al.,
2007; Laurienti, Burdette, Maldjian, & Wallace, 2006), the crossmodal condition provided a redundancy gain for the patient and CTRL
groups, indicated by improved scores and reduced response times.
However, in the crossmodal condition, the RT trials were not faster
than those predicted using the race model estimation. This nding
suggests that signal integration has occurred in the CTRL group, but
not in the patient group. In the CTRL group, the information from
the visual and auditory sensory modalities interacted to mediate
the RT facilitation. In contrast, the patient group exhibited at once
general difculties in the recognition of emotions and a reduced
ability to integrate separate sensory representations of the emotional expressions. In the patient group, the redundancy gain
would occur because the multisensory condition contains redundant stimulus components rather than through an integrative
effect. In accordance with a disconnection syndrome, one hypothesis is that inltrating tumors reduce communication between
functionally specialized brain areas and do not permit the integration of the different sensory areas. Using magneto encephalography, alterations in functional connectivity were recently
described in patients with gliomas (Bosma et al., 2008). Moreover,
increasing evidences suggests the participation of white matter
tracts in emotion recognition. Notably, the inferior longitudinal
fasciculus and the inferior fronto-occipital fasciculus would participate in the visual recognition of the facial expression of emotion
(Catani et al., 2012; Crespi et al., 2014; Philippi, Mehta,
Grabowski, Adolphs, & Rudrauf, 2009). Some evidences appear
for crossmodal integration too. Whereas many studies reported
the activation of amygdala in emotional unimodal channels
(Belin, Fecteau, & Bdard, 2004; Fecteau, Belin, Joanette, &
Armony, 2007; Sabatinelli et al., 2010) and greater activation in
audiovisual congruent presentation (Dolan, Morris, & de Gelder,
2001; Klasen et al., 2011), Mller et al., 2012), using dynamic causal modelling emphasized the effective connectivity in audiovisual
integration. They found feed-forward connections between the
pSTS and the visual (FFG) and auditory (STG) regions, revealing
multimodal integration, but they also emphasized the inuence
of pSTS on connectivity between the amygdala and the FFG.
Therefore, an alteration of white-matter integrity due to the
inltrating characteristic of gliomas might decrease crossmodal
integration.
The second hypothesis concerns the participation of the frontal
region in the facevoice integration (Peelen et al., 2010; Pourtois,
de Gelder, Bol, & Crommelink, 2002). Notably, frontal areas might
be recruited when the associations between crossmodal cues are
essentially arbitrary (Calvert, Hansen, Iversen, & Brammer, 2001).
In the protocol used in the present study, the participants had to
recognize one emotion from emotional faces and emotional prosody simultaneously and congruently presented. In case of conicts
between the two modalities, executive functioning is needed to
apply a decision-making process between the two modalities and
the voluntary control of interference of the wrong choice. We can
hypothesize that the automatic and early cross-modal processes

98

V. Luherne-du Boullay et al. / Brain and Cognition 92 (2014) 92100

sustained by the STS (Calvert et al., 2001; Pourtois et al., 2002)

were preserved in the patient group, providing a redundancy gain.
In contrast, the executive functioning sustained by the frontal
areas (Godefroy, Spagnolo, Roussel, & Boucart, 2010; Heekeren,
Marrett, Bandettini, & Ungerleider, 2004), which is greatly affected
by gliomas (Correa et al., 2007; Mu et al., 2012), was disturbed and
did not permit efcient crossmodal integration, resulting in slower
response times.
Notably, correlations between the cognitive tests requiring
executive functioning (FAB, EMPANS and STROOP) and the total
emotional recognition and the under crossmodal condition score
were observed in the patient group. These results support the
hypothesis of a link between executive functioning and crossmodal
integration. Surprisingly, no correlations were observed with the
TMT part B. However, this task is less sensitive than the STROOP
task and a maximum performance obtained for most of our
patients could prevent any correlation.
Concerning the impact of tumor-related variables on emotion
recognition, we observed none effect of histology, volume or
tumor grade. There were no signicant differences between LGG
(grade II) and HGG (grade III and IV). The precise contribution of
tumor grade in cognitive decits is uncertain to determine.
Miotto et al. (2011) reported that HGG have greater cognitive
impairments than LGG, but both groups were below average and
their total IQs were comparable. Surgical removal of HGG has been
reported to induce cognitive impairments in some studies
(Taphoorn et al., 1994) and not in others (Satoer et al., 2012) inasmuch as the effects of oncologic treatments could combine with
those induced by the tumor. Although some studies observed that
the tumor itself primarily contributed to cognitive dysfunction
(Taphoorn & Klein, 2004), others reported that the tumor type or
volume did not predict cognitive performance (Kayl & Meyers,
2003; Reijneveld et al., 2001; Satoer et al., 2014). If the tumor itself
is the main cause of cognitive decits, treatments, in particular
radiotherapy with high fraction doses (Douw et al., 2009; Klein
et al., 2002) or chemotherapy (Correa, 2010; Correa et al., 2007;
Correa et al., 2008; Scheibel, Meyers, & Levin, 1996) induce additional long-term cognitive disability. A previous study analyzing
multimodal skills in a group of patients with gliomas did not show
correlations between performances and tumor localization and
type (Plaza et al., 2012). In the present study, HGG patients presented radiological and clinical history of LGG, did not receive
oncologic treatment and were pre-operative assessed. HGG was
diagnosed after histopathology examination. Thus, it is no totally
surprising that the patients performance in emotional recognition
did not differ from those with LGG.
If we did not observe general correlations between emotion recognition and tumor localization, we noted that in each modality,
the largest number of impaired patients was found in the frontal
subgroup and that the difference between the two groups was signicant in visual modality. It should be noted that 88% of patients
of the frontal group harbored a left glioma. This nding is in accordance with Mus data (2012), which recruited a group of patients
with left frontal gliomas who were impaired in recognizing facial
expression of Anger. Frontal areas have been previously linked to
recognition of negative emotional faces (Baird et al., 2006;
Hornak et al., 2003) and happiness (Vytal & Hamann, 2010). In
addition, the right frontal cortex, especially its inferolateral and
dorsomesial parts, is frequently presented as a core system in
the two aspects of mentalizing. Nevertheless, extensive resection
of the right prefrontal cortex does not induce long-term worsening
of the mentalizing process in LGG patients, suggesting that these
areas are not crucial for mentalizing (Herbet, Lafargue,
Bonnetblanc, Moritz-Gasser, & Duffau, 2013). In this study, only
one patient presented a right frontal lesion; although he was
impaired in the three modalities, we cannot generalize in favor

of the contribution of the right frontal cortex to emotion

recognition.
A laterality effect was found only in auditory modality, the six
patients with right gliomas performing worse than the twenty
with left gliomas. Four of them suffered from a temporo-insular
lesion. As the right temporal lobe is involved in auditory treatment
(Pourtois et al., 2005) and as our prosodic material does not require
lexical-semantic competences, the decit of right temporal
patients in emotional voices recognition is not surprising. This further emphasizes the importance of using non-verbal stimuli in
emotional auditory tasks. However, these results must be taken
with caution, because of the small number of right lesions in our
population (6/26).
Considering that a higher percentage of our patients received
antiepileptic therapy following the diagnosis, it was difcult to discern the specic effects of seizure therapy on cognitive functions.
Both epileptic seizure and antiepileptic drugs predispose patients
to cognitive impairments (Pallud et al., 2013). The treatment might
disrupt or alter some cognitive processes, notably psychomotor or
attentional and executive skills (Klein et al., 2002). Correa et al.
(2007) reported that patients who did not experience seizures
within at least one month prior to the evaluation obtained normal
scores in all cognitive domains. In the present study, all patients
had controlled seizures the month before the neuropsychological
assessment. Moreover, we did not observe any differences between
the patients with and without treatment, which suggests that the
epileptic treatment did not signicantly inuence emotional
recognition.
Finally, KPS score correlated with the score in emotion recognition. The KPS index facilitates the classication of functional
impairment, and a good preoperative KPS typically predicts a good
survival. As this global performance status provides information
about the capacity to perform normal activity and do work, cognitive impairments might impact this parameter. In the present
study, the patients KPS scores were globally homogeneous but
nonetheless slightly different; only two subjects cared for themselves but were unable to do active work (KPF score <80%), and
24 subjects had KPS scores greater than 80%, indicating that they
were able to perform normal activities and work, but half of them
presented signs or symptoms of the disease. This observation suggests that despite an excellent performance status for more than
half of the patients, in addition to the cognitive decits, the functional performance status could be affected through the impairments in emotion recognition. The difculties in emotion
recognition might play a role beyond the ability to engage in the
activities of daily living and continuing work. Thus, this impairment might have an adverse effect on the quality of life. Although
the KPS scores were relatively homogeneous and thus could have
affected the statistical power of the results, the links between emotion recognition and capacity to perform normal activity and do
work merits attention.
Several possible limitations of the present study should be
noted. First, psychological burden with resultant anxiety, depression and uncertainty regarding the diagnosis are likely to inuence
cognitive performance (Gehring, Sitskoorn, Aaronson, & Taphoorn,
2008). Nevertheless, no correlations were observed between the
emotion recognition score and the BDI score (p = .12). Second, if
the identication of facial and vocal emotional expression is an
important factor contributing to the regulation of social interactions (Milders, Fuchs, & Crawford, 2003; Williams & Wood,
2010), the impact of emotion recognition on social cognition is
unknown. Some studies (Hornak et al., 2003) have shown that
the recognition of basic emotions is consistently associated with
a decit in social behavior. Moreover, Petroni et al. (2013) observed
that emotional inference (which is the more basic process of Theory of Mind) is supported, at least in part, by early brain activity

V. Luherne-du Boullay et al. / Brain and Cognition 92 (2014) 92100

that is sensitive to facial emotional valence; this suggests an association between the cortical markers of facial processing and the
performance on tasks of social cognition. The present study did
not include a measure of real-life social behavior, but the results
indicated that the recognition of emotional faces and voices serves
as an important mediator to investigate the activities of daily living
and continuing to work in patients with gliomas. These data also
highlighted the need to use social cognition scales, which mediate
the relationship between emotion recognition and daily life functioning. Importantly, although the present study provides information about characteristics of emotion recognition and emotional
crossmodal integration in patients with gliomas, future studies
should investigate more precisely the neural basis of emotional
crossmodal integration and focus attention on the relation
between decits in particular emotions and tumor localization
using intraoperative direct electrical stimulation during awake
brain surgery in gliomas population.
In conclusion, the results of the present study suggest that
patients harboring a glioma present a mild impairment in emotion
recognition despite a normal clinical examination and a normal
score according to the patients functional status (e.g., KPS). These
results support the notion of effective compensatory mechanisms
in patients with gliomas, for emotional processes as well as in
other cognitive domains. They also conrm the efcacy of congruent multisensory presentation in normal and pathological subjects
when identifying emotions. Nevertheless, unlike the control group,
the crossmodality gain obtained in the LGG group might reect a
redundancy presentation of the visual and auditory modalities
rather than a real multisensory integrative process. Indeed, in addition to the general difculties in the recognition of emotions, the
patient group exhibited a reduced integration of the separate sensory representations of the emotional expressions, which was
associated with executive weakness. However, the crossmodality
gain might improve the emotional abilities in daily life and help
maintain the quality of social interactions. Continued effort is
required to include more systematic emotion recognition measures and introduce response times in the neuropsychological
assessment of patients with cerebral disease, notably, LGG.
Acknowledgments
We are grateful to the patients and healthy volunteers who participate in this study. The authors wish to thank Nicolas Bodeau for
help in statistical analyses. The authors have no nancial relationships or conicts of interest to disclose.
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