Biological Psychology 157 (2020) 107973

Contents lists available at ScienceDirect

Biological Psychology
journal homepage: www.elsevier.com/locate/biopsycho

Sex differences in behavioral and brain responses to incongruity in

emotional speech controlling for autistic traits
Ming Lui a, *, 1, Xiaojing Li b, d, f, 1, Werner Sommer c, Andrea Hildebrandt d, e, Gilbert Ka-Bo Lau a,
Changsong Zhou b, *
a
Department of Education Studies, Centre for Learning Sciences, Hong Kong Baptist University, Hong Kong, China
b
Department of Physics, Centre for Nonlinear Studies and Beijing-Hong Kong-Singapore Joint Centre for Nonlinear and Complex Systems (Hong Kong), Institute of
Computational and Theoretical Studies, Hong Kong Baptist University, Hong Kong, China
c
Institut für Psychologie, Humboldt-Universität zu Berlin, Germany
d
Department of Psychology, Carl von Ossietzky Universität Oldenburg, Germany
e
Research Center Neurosensory Science, Carl von Ossietzky Universität Oldenburg, Germany
f
Chinese Academy of Disability Data Sciences, Nanjing Normal University of Special Education, Nanjing, China

A R T I C L E I N F O A B S T R A C T

Keywords: Accurate interpretation of speech requires the integration of verbal and nonverbal signals. This study investi­
Speech comprehension gated sex differences in behavior and neural activities associated with the integration of semantic content and
Emotional prosody emotional speech prosody, while the level of autistic traits was controlled for. Adults listened to Cantonese words
Semantic processing
spoken with happy and sad prosody, and made judgments on semantic valence while event-related potentials
Sex differences
Autistic traits
(ERP) were recorded. Behaviorally, men were slower than women in making semantic valence judgments. At the
Event-related potentials neural level, men had a greater congruity effect in the N400 component, whereas women had a greater congruity
Individual differences effect in the 1150–1300 ms time window for happy prosodies. There was no effect of sex in case of sad prosodies.
Our study reveals novel findings on sex differences in the timing of the integration between verbal and non-
verbal signals that cannot be explained by differences in autistic traits.

1. Introduction
Speech is a major channel through which individuals communicate
and understand the thoughts of others. Accurate interpretation of speech
often requires the integration of multi-channel information, including
both verbal and non-verbal cues. Previous reports indicate that men
exhibit less multi-channel integration during speech processing as
compared with women (Schirmer et al., 2006; Schirmer, Kotz, & Frie­
derici, 2002; Schirmer, Zysset, Kotz, & von Cramon, 2004). Since men
also tend to score higher on autistic trait measures (Baron-Cohen,
Wheelwright, Skinner, Martin, & Clubley, 2001), which are known to be
related to social and communication problems, the present study aims to
investigate whether men and women differ in multi-channel integration
given that sex differences in autistic traits are controlled for.
In previous studies, cross-cultural and individual differences on
multi-channel integration were investigated. Cross-cultural studies have
compared Asians and Westerners with respect to their integration of
emotional signals. Kitayama and Ishii (2002) and Ishii, Reyes, and
Kitayama (2003) required participants to judge the semantic valence of
words while ignoring the emotional prosody, or vice versa. The results
revealed that Japanese more automaticly integrated contextual
emotional prosody when processing the meaning of speech as compared
to Americans (Kitayama & Ishii, 2002; Ishii et al., 2003). Tanaka et al.
(2010) also found differences between Japanese and Dutch participants
in integrating emotional signals expressed via faces and voices. Their
results indicated that Japanese more automatically integrate vocal
emotions than Dutch, while Dutch more automatically integrate facial
expression than Japanese. Consistently, Liu, Rigoulot, and Pell (2015)
also found that North Americans more automatically attend to
task-irrelevant faces when judging vocal emotions as compared to
Chinese.
Apart from culture, there are individual differences variables apart
from autistic traits which were shown to be associated with the inte­
gration of multi-channel information during communication. Such

* Corresponding authors.
E-mail addresses: m-lui@u.northwestern.edu (M. Lui), cszhou@hkbu.edu.hk (C. Zhou).
1
Equal contribution.

https://doi.org/10.1016/j.biopsycho.2020.107973
Received 28 February 2020; Received in revised form 12 October 2020; Accepted 13 October 2020
Available online 19 October 2020
0301-0511/© 2020 Elsevier B.V. All rights reserved.
M. Lui et al.
variables are empathy and trait anxiety. For example, Jiang and Pell
(2016a) found that trait empathy was positively related to the integra­
tion of lexical contents and vocal cues of speaker confidence, while trait
anxiety mediated the effect of sex on processing speaker confidence.
Also, van den Brink et al. (2012) reported that highly empathetic adults
integrated voice-based speaker identity information with the contents of
speech to a larger extent than less empathetic adults.
The current study focuses on sex as a grouping variable consistently
linked to individual differences in multi-channel integration during
speech perception. Previous behavioral studies showed that women
exhibit a higher tendency to integrate task-irrelevant vocal cues as
compared to men while processing verbal contents. Jiang and Pell
(2016b) demonstrated larger difference in women than men with
respect to their confidence ratings of sentences spoken with congruous
and incongruous vocal tones. This was taken to indicate a stronger
tendency to integrate vocal tones among women. Consistently, Schirmer
et al. (2002) found a significant reaction time (RT) difference between
congruous and incongruous conditions among women but not men
when they judged semantic valence while ignoring emotional prosody.
Apart from behavioral findings, there is neural evidence showing sig­
nificant sex differences in multi-channels integration during speech
perception. For example, women had larger amplitudes in the N400 and
late negativity components of event-related brain potentials (ERPs) than
men when they processed words spoken with incongruous emotional
prosody, compared to congruous emotional prosody (Ishii, Kobayashi, &
Kitayama, 2010; Schirmer et al., 2002; Schirmer et al., 2004; Schirmer
et al., 2006). These findings support a larger degree of integration of
prosodic and semantic cues among women than men.
As argued above, level of autistic traits – which is itself more pro­
nounced in males – is another variable inducing individual differences in
multi-channel information processing. Autism is a clinical condition
involving social communication impairments, repetitive behaviors, and
restricted interests (American Psychiatric Association, 2013). However,
there is evidence that autistic traits are distributed across the entire
population seen as a continuum, including non-clinical individuals (e.g.
Baron-Cohen et al., 2001). Since at the population level, men on average
have higher level of autistic traits than women (e.g., Baron-Cohen et al.,
2001), and given that autism is linked to impairments in multi-channel
integration of sensory signals (e.g. Brandwein et al., 2012; Stevenson
et al., 2014), it is possible that sex differences in multi-channel inte­
gration reported in previous studies are partially driven by higher levels
of autistic traits in men compared with women. There is, however, a lack
of evidence on this hypothesis because previous sex differences studies
did not control for the level of autistic traits. Moreover, most previous
studies on autistic traits required participants to process social infor­
mation in a single modality only (Canal et al., 2019; Lassalle & Itier,
2015; Peled-Avron & Shamay-Tsoory, 2017). It is still largely unknown
whether autistic traits in the non-clinical population are linked to the
integration of multi-channel social signals. It needs to be additionally
mentioned that many of the past studies dichotomized the spectrum of
autistic traits and solely employed group comparisons between high vs.
low autistic trait individuals. Relatively few studies (Gayle, Gal, &
Kieffaber, 2012; Halliday, MacDonald, Sherf, & Tanaka, 2014; Pele­
d-Avron & Shamay-Tsoory, 2017) have considered level of autistic traits
as a continuum within the subclinical population and assessed its rela­
tionship with behaviours. It is however arguably more fruitful to
consider individual differences variables on a continuum and exploit the
information in the data more extensively. The present study aimed to
filling these research gaps.
1.1. Aims of the present study
The current study aimed to examine sex differences in the integration
of emotional prosody and semantic content in speech, while level of
autistic traits was controlled for. Participants’ degree of autistic traits
were measured using the Autism Spectrum Quotient (AQ; Baron-Cohen
2
Biological Psychology 157 (2020) 107973
et al., 2001), a self-administered instrument. Sex differences were
investigated after aligning the mean level of AQ for female and male per
recruitment design. Participants were involved in a social cognition task
that required them to listen to auditory words spoken with emotional
prosody, matching or mismatching in valence with the semantic word
meaning.
Behaviorally, we expected sex differences in reaction times of se­
mantic judgments. On the neural level, we hypothesized that sex would
be significantly related to the ERP congruity effect (amplitude differ­
ences between incongruous and congruous conditions) in the time
windows: 350–650 ms (N400), 750–900 ms, and 1150–1300 ms. The
time windows were selected based on two previous studies applying
similar stimuli and tasks (Schirmer & Kotz, 2003; Schirmer et al., 2006).
The N400 is a negative-going ERP component peaking around 400 ms
after stimulus onset at central-parietal electrodes. Its amplitude in­
creases with the degree of semantic incongruity (Kutas & Federmeier,
2011). The other time windows lie within the time frames of late com­
ponents, which can be late positivity or late negativity, depending on
polarity. In the literature, the late negativity starts between 600− 800 ms
and may last for 2000 ms, peaking at central and parietal sites (Herron,
2007). It implies action monitoring triggered by response conflict and
memory retrieval (Herron, 2007; Johansson & Mecklinger, 2003). The
late positivity starts around 500 ms and lasts for several hundred mil­
liseconds with peaks mostly found at central-parietal sites (Friederici,
2002). This component is related to subjective stimulus probability that
may be triggered by syntactic and semantic incongruity (Coulson, King,
& Kutas, 1998; Hahne & Friederici, 2002; Kutas & Hillyard, 1980). We
hypothesize sex differences in ERP differences between incongruous and
congruous conditions (i.e., ERP congruity effect) in the three time
windows, after level of autistic traits was controlled for by design.
Women are expected to show a larger ERP congruity effect than men. As
the pattern of results may differ in different prosodic conditions, we
conducted the analyses separately for happy and sad prosody conditions.
2. Methods
2.1. Participants
We invited college students via posters on campus and mass emails to
fill in an online AQ questionnaire (Baron-Cohen et al., 2001). In
response, we received 1059 valid data from young adults (mean age =
20.75, SD = 2.47). Their mean AQ score was 21.58 (SD = 5.96) out of a
possible score ranging from 0 to 50. For comparison, in a previous study
of 6934 subclinical participants, the mean AQ was 16.94 (95 % C.I. 11.6,
20.0; Ruzich et al., 2015). Among the 1059 online respondents, 601
indicated their interest in participating in an EEG study. Since we
intended to match the average AQ of female and male participants,
specific questionnaire respondents were invited for the EEG study based
on the selection criteria and measured AQ scores. The selection criteria
were: Cantonese speaker, aged between 18 and 30 years, no hearing
impairment, no psychiatric and neurological disorder, no metal inside
the body, and no prescribed medication for skin problems. Twenty-three
female and 23 male participants’ data with matched age and AQ were
included for the present study (Table 1). None of the participants re­
ported a formal diagnosis of autism spectrum disorder (ASD). Data of 14,
out of the 23 male participants were reported in a previous study (Lui,
So, & Tsang, 2018) which examined group difference between high and
low AQ participants among men. In addition to AQ, participants also
completed the Empathy Quotient questionnaire (EQ; Baron-Cohen &
Wheelwright, 2004) and a 30-minute speeded version of Raven’s
Advanced Progressive Matrices Test (Raven, Raven, & Court, 1998) to
assess non-verbal IQ. EQ was highly correlated with AQ. To avoid
multicollinearity, EQ was not included in the analyses involving AQ.
Comparisons of AQ, IQ, and EQ between female and male participants
were conducted to ensure that these variables were well matched be­
tween the two groups. The study was carried out in accordance with the
M. Lui et al. Biological Psychology 157 (2020) 107973

Table 1 emotional prosody. The stimuli were presented, and button-press re­
Descriptive statistics of age, AQ, EQ, and nonverbal IQ among women and men. sponses were recorded using Eprime© 2.0 software (PST, Inc.). In each
Sex N Statistics Age AQ EQ IQ trial, a fixation cross was presented on the screen for 2700 ms; 500 ms
after its onset, an auditory word started, requiring a button press. After
23 M 20.0 18.43 40.13 19.61
Women
SD 1.48 8.56 10.41 4.51 the offset of the fixation cross, a feedback (indicating “correct”,
Range 18 – 23 10 – 37 22 – 65 11 – 26 “incorrect”, or “too slow”) appeared. Absence of response within 2200
Men
23 M 20.78 19.61 37.26 22.18 ms after word onset prompted the feedback screen of “too slow”. Par­
SD 1.17 7.20 12.24 5.88 ticipants were instructed to blink, if necessary, during this feedback
Range 19 – 22 11 – 36 13 – 58 12 – 33
t − 1.99 − .50 .86 − 1.45
period. To minimize anticipation effects, stimulus onset asynchronies
p .052 .62 .40 .16 (SOA) were equally distributed across values of 3300 ms, 3400 ms, 3500
− 1.57 – − 5.87 – − 3.88 – − 6.16 – ms, or 3600 ms, implemented by showing the feedback screen for du­
C.I.
.008 3.53 9.62 1.03 rations of 600–900 ms. Each participant completed all 240 trials. The
Note. AQ – Autism Spectrum Quotient ; EQ – Empathy Quotient; IQ – Raven’s trials were presented in four blocks, separated by three breaks for rest.
Advanced Progressive Matrices Test Score. The order of the stimulus presentation was pseudo-randomized, such
that the first and second appearances of the same word spoken with a
recommendations of the Research Ethics Committee of Hong Kong different prosody occurred in different blocks, one in the first half and
Baptist University. All subjects gave written informed consent and were the other in the second half of the trials. To familiarize the participants
reimbursed HKD $100 (about USD 13) per hour. with the task, they were given eight practice trials with similar stimuli
and difficulty as the test trials. Participants who showed many incorrect
trials during practice, were given instructions again about the task re­
2.2. Stimuli quirements and went through one more round of practice. All partici­
pants responded correctly in the first or second round of practice trials.
The stimuli consisted of 240 auditory words containing 120 different
two-syllable Chinese words spoken in either happy or sad prosody. Half
2.4. EEG recording and data processing
of the 120 words were positive and half were negative in their semantic
meaning. All words were Cantonese produced by a female native
The EEG was sampled at a rate of 500 Hz from 64 Ag/AgCl electrodes
speaker with drama experience, and none of the words were homo­ mounted in an electrode cap (Waveguard™ original) connected to an
phones. The words were considered verbs in daily life usage by over 70
amplifier (eego™ mylab, ANT Neuro); initial common reference was
% of the raters in Schirmer et al. (2006). In the current study 30 college CPz. Electrode impedances were kept below 10 kOhms. Offline pro­
students (15 men) were recruited to rate the word stimuli in terms of
cessing, including re-referencing, filtering, epoching, artifact removal,
semantic valence and emotional prosody. The raters did not participate and averaging, was performed using the EEGLAB toolbox (Delorme &
in the current EEG experiment. Both semantic valence and emotional
Makeig, 2004) and in-house MATLAB scripts. Offline, EEG was
prosody were rated on a 7-point scale (1= very negative; 2 = negative; 3 re-referenced to average mastoid. After filtering at a 0.05–40 Hz
= slightly negative; 4 = neutral; 5 = slightly positive; 6 = positive; 7 = band-pass, the continuous EEG data were epoched with a 200 ms
very positive). pre-stimulus baseline and a 2000 ms post-stimulus window. Artifacts
For semantic valence, positive words (M = 5.53; SD = .43) were resulting from eye and body movement or muscle contraction were
rated significantly more positive than negative words (M = 2.17; SD = removed by an ICA algorithm using the EEGLAB toolbox. Visual in­
.36; t (118) = 46.38, p < .001). For emotional prosody, happily spoken spection was performed to remove any residual atypical artifacts. The
words (M = 4.97) were rated significantly more positive in prosody than preprocessed ERP trials were subjected to RIDE (see below).
sadly spoken words (M = 2.01; t (119) = 85.18, p < .001). Positive and
negative words did not differ in word frequency (Cai & Brysbaert, 2010)
2.5. Electrophysiological data analyses
(t (117) = 1.46, p = .15).
The four stimulus types were classified as either congruous in se­
A methodological novelty achieved by the current study is the
mantic valence and emotional prosody, that is, happily spoken positive
application of an advanced method to analyze ERP data, the Residual
words and sadly spoken negative words, or incongruous, that is, happily
Iteration Decomposition (RIDE; Ouyang, Herzmann, Zhou, & Sommer,
spoken negative words and sadly spoken positive words. The sound in­
2011; Ouyang, Sommer, & Zhou, 2015). RIDE allows to cope with the
tensity levels of congruous and incongruous stimuli did not differ (t
well-known, but rarely addressed trial-by-trial latency jitter. In the
(238) = -0.79, p = .43), nor did the mean durations of positive and
present study, the stimuli were spoken Cantonese words with two syl­
negative words (t (238) = .21, p = .83); however, happily spoken words
lables. As a nature of Cantonese two-syllable words, the time at which
(M =877 ms) were significantly shorter in duration than sadly spoken
the semantic meaning is accessible (recognition point) varies from word
words (M =1240 ms; t (119) = -27.91, p < .001).
to word (Marslen-Wilson, 1987). For some words, semantic meaning is
Note that the stimuli did not include neutral words because the
ambiguous at the first syllable and only becomes fully clear at the second
current study does not aim to compare the differences between
syllable. For other words, semantic valence is obvious already when the
emotional and neutral stimuli. Our research question is related to the
first syllable is pronounced. Therefore, the ERP latencies in response to
integration between emotional prosody and semantic valence of words
the processing of these stimuli vary substantially from stimulus to
in speech processing. Therefore, the targeted comparison is between
stimulus. Conventional ERPs are computed by averaging multiple single
congruous and incongruous conditions, with the latter involving a
trials in each stimulus condition. The inter-trial variability in ERP la­
conflict between the valence of semantic meaning and emotional
tency often blurs ERP waveforms and smears condition effects in aver­
prosody.
aged ERP amplitudes (Ouyang et al., 2015). To deal with the ERP
latency jitter caused by the large variation in the timing of semantic
2.3. Procedure meaning conveyed by Cantonese two-syllable words, RIDE was applied
to the trials in each of the four conditions of each participant.
The data collection procedure was in line with Lui et al. (2018). With RIDE, the latency variability in single trial ERPs can be taken
Participants listened to auditory words through air-tube earphones and into account, mitigating the smearing problem by reconstructing the
were instructed to judge the semantic valence (positive vs. negative) of ERP after correcting the latency jitter. When applying RIDE, all ERPs are
each word as accurately and as quickly as possible while ignoring decomposed into three component clusters: the S cluster time-locked to

3
M. Lui et al.
the stimulus, the R cluster time-locked to the response, and the C
(central) cluster neither time-locked to the stimulus nor the response.
Under conventional circumstances the three clusters capture the sub-
processes in the ERP involved in stimulus processing (S), response
preparation and execution (R), and central cognitive processes such as
stimulus classification, response selection, or decision-making (Ouyang
et al., 2011).
The RIDE procedure consists of a decomposition module and a C
latency estimation module, applied to each electrode in each partici­
pant. In the decomposition module, the single-trial ERPs are decom­
posed into a stimulus-locked component cluster S, a response-locked
component cluster R, and an intermediate component cluster C without
explicit time marker, starting from initial latencies LS , LR and a rough
initial estimation of latency LC from the original data. In order to esti­
mate S, RIDE subtracts the C and R components from each single trial
and aligns the residual waveforms of all trials to LS to obtain the median
waveform across trials. The same procedures are applied to C and R. In
the C latency estimation module, RIDE calculates the cross-correlation
between a predefined C template based on the original data and the
residual single trials after removing the S and R components. The cross-
correlation curves for all electrodes are averaged to identify a common C
latency for the topography. The two procedures are iterated, namely, the
C latency estimation uses an updated C template from the last iteration
of decomposition, and the next decomposition will use the updated C
latency, until convergence of both – the components S, R, and C and the
C latency. Thus, single-trial latencies and amplitudes of the C cluster are
made available by applying RIDE. More details can be found in Ouyang
et al. (2015) and in the toolbox manual at: http://cns.hkbu.edu.hk
/RIDE.htm.
Next, the new ERPs are reconstructed by summing up the RIDE
estimated components S, R, and C each synchronized at their respective
latencies. In the present study the ERPs of each participant was recon­
structed with RIDE for each of the four stimulus conditions: happy-
positive (congruous), happy-negative (incongruous), sad-positive
(incongruous) and sad-negative (congruous). In statistical analyses,
ERP differences between congruous and incongruous conditions were
calculated in each of the prosodic stimulus conditions (happy prosody
vs. sad prosody), after applying RIDE.
Nine central-parietal electrode sites (Cz, C1, C2, C3, C4, CP1, CP2,
CP3, and CP4) were averaged as region-of-interest (ROI) for analysis.
Past studies found that those sites typically show the largest semantic
congruity effect on the N400 (Besson, Kutas & Van Petten, 1992; Kutas &
Federmeier, 2000) and late ERP components (e.g., Herring, Taylor,
White, & Crites, 2011). Moreover, several studies on semantic violations
in Cantonese word processing consistently found maximal congruity
effects at central and parietal sites (Lui et al., 2018; Schirmer et al.,
2006; Schirmer, Tang, Penney, Gunter, & Chen, 2005). Analyses were
conducted for average amplitudes with three time windows: 350–650
ms, 750–900 ms, and 1150–1300 ms. The 350–650 ms time window was
used in many previous N400 studies (e.g., Liu, Wang, & Jin, 2010;
Schirmer & Kotz, 2003). The late time windows, 750–900 ms, and
1150–1300 ms, were selected based on Schirmer and Kotz (2003) and
Schirmer et al. (2006) respectively, who used similar stimuli and tasks as
the current study. The latter study revealed an interaction of congruity
and sex in the 1150–1300 ms time window in a Cantonese sample. A late
ERP component effect was also reported previously when vocal cues
were in conflict with the context of speech (e.g., Besson, Kutas & Van
Petten, 1992). This was suggested to be linked to the pragmatic infer­
ence processes required for deriving contextually appropriate meaning
due to the conflict (e.g., Jiang & Pell, 2016b).
Sex and AQ were independent variables in regression analyses.
Dependent variables included reaction time (RT), accuracy, and ERP
differences between incongruous and congruous conditions (i.e., ERP
congruity effect).
4
Biological Psychology 157 (2020) 107973
3. Results
3.1. Behavioral data
The descriptive statistics with respect to age, AQ, EQ, and nonverbal
IQ among women and men are provided in Table 1. We conducted in­
dependent samples t-tests with sex as independent variable, and with
AQ, EQ, nonverbal IQ, and age as dependent variables. There were no
significant differences between men and women on AQ, EQ, IQ, and age
(see Table 1 for statistics).
The average RTs and the accuracies of the four stimulus conditions
are displayed in Table 2. Women’s and men’s RTs were on average
1232.65 ms and 1302.32 ms, respectively. Please note that the auditory
stimuli had an average duration of 1059 ms (happy prosodic words: 877
ms; sad prosodic words: 1240 ms), which could be the reason of these
long RTs.
Two separate sets of analyses were performed to investigate different
aspects of the behavioral data. First, three-way mixed-design repeated
measures ANCOVAs were conducted to examine the congruity effect and
its interactions with prosody, sex, and AQ. Second, multiple regression
analyses were performed to examine individual differences, asking
whether sex and AQ alone predict congruity effects in RT and accuracy
(i.e., differences between incongruous and congruous conditions).
A three-way mixed-design repeated measures ANCOVA was con­
ducted to investigate sex differences (women vs. men), prosody effects
(happy vs. sad tone), and congruity effects (congruous vs. incongruous)
on RT, with AQ as a covariate. The results showed a main effect of sex:
men responded more slowly to stimuli than women (F (1, 43) = 5.75, p =
0.021, partial η2 = .12). The main effect of prosody was also significant:
participants responded more slowly to stimuli spoken in sad tone, as
compared to happy tone (F (1, 43) = 386.80, p < 0.001, partial η2 = .90).
Furthermore, there was a main effect of congruity: participants
responded more slowly to incongruous than congruous stimuli (F (1, 43)
= 4.47, p = 0.04, partial η2 = 0.09). With respect to interactions, our
analyses revealed a significant interaction between prosody and con­
gruity (F (1, 43) = 9.02, p = 0.004, partial η2 = 0.17), indicating the
effect of congruity to be larger in happy tone stimuli (M = 38.53) as
compared with sad tone stimuli (M = 11.07). No other interaction ef­
fects were significant (ps > .05).
To investigate the effects of the same factors on accuracy, a three-
way mixed-design repeated measures ANCOVA was conducted with
sex (women vs. men), prosody (happy vs. sad tone), and congruity
(congruous vs. incongruous) as factors, and AQ as a covariate. No sig­
nificant main effects or interaction effects were observed. We should,
however, note that results regarding the effects on accuracy are limited
by the range restriction of accuracy scores in this task.
Multiple regression analyses were conducted with sex and AQ as
predictors, and RT difference (between incongruous and congruous
conditions) as the dependent variable. There were no significant effects
for both happy prosodic and sad prosodic conditions. The same analyses
were performed on accuracy data. Similarly, no significant effects
resulted. Note however that accuracy effects are limited by range re­
striction of accuracy scores in this task.
There was a significant negative correlation between RTs of specific
prosodic condition and the congruity effect (RT of incongruous minus
RT of congruous condition) in the corresponding prosodic condition (r =
-0.31, p = .003). Fig. 1 illustrates the negative association between RTs
and congruity effect for all participants, such that females and males are
specifically coded. Conditions with longer RTs tended to reveal smaller
congruity effect. Correlations amounted -0.31 (p = .036) and -.29 (p =
.052) for females and males respectively.
3.2. ERP data
The grand average RIDE-corrected ERPs of women and men for the
four stimulus conditions at a representative site, Cz, are provided in
M. Lui et al. Biological Psychology 157 (2020) 107973

Table 2
Women’s and men’s reaction times (RT) and accuracies (ACC) in the four stimulus conditions.
Measure Sex Statis Happy congruous Happy incongruous Sad congruous Sad incongruous Congruity effect Congruity effect Average
-tics for Happy condition for Sad condition

M 1084.92 1125.26 1352.61 1367.81 40.33 15.20 1232.65

Women
SD 70.97 70.45 72.99 73.43
RT
M 1155.61 1192.33 1427.21 1434.14 36.72 6.93 1302.32
Men
SD 119.30 122.74 120.01 112.71
M .96 .96 .96 .94 0 − .02 .96
Women
SD .04 .02 .04 .05
ACC
M .95 .93 .95 .92 − .02 − .03 .94
Men
SD .04 .07 .04 .05

Note: Congruity effect is calculated by incongruous minus congruous condition.

Fig. 1. Negative correlation between mean reaction time (Mean RT) across congruous and incongruous conditions but separated for the different prosodic condition
and the RT congruity effect (RT of incongruous condition minus RT of congruous condition) in the corresponding prosodic condition.

Figs. 2a and 2b, respectively. Fig. 3 show te bar plots of the ERP con­
gruity effect in happy and sad prosodic condition at Cz electrode in the
time windows of 350–650 ms, 750–900 ms, and 1150–1300 ms. Fig. 4
illustrates the topographical plots of ERP congruity effects (incongruous
minus congruous condition) in happy (A) and sad (B) prosodic condition
in the time windows 350–650 ms, 750–900 ms and 1150–1300 ms for
females vs. males.
Multiple regression analyses were performed with the ERP amplitude
differences between incongruous and congruous condition (i.e., ERP
congruity effect) as the dependent variables, and sex and AQ as pre­
dictors. Separate regressions were computed on data in three time
windows, and for happy and sad prosodic stimulus conditions (see
Table 3 for a summary of the statistics).
Time window 350 – 650 ms (N400).
In the happy prosodic condition, there was a significant sex differ­
ence in the N400 congruity effect (between incongruous and congruous
conditions) (b = 0.34, t = 2.43, p = .01). Men had a larger N400 con­
gruity effect than women. The effect of AQ was not significant (b = 0.13,
t = 0.93, p > .1). Sex and AQ together explained 13 % of the variance of
the N400 difference (R2 = 0.13, F (2, 43) = 3.38, p = 0.04). There were
no significant effects for the sad prosodic condition (see Table 3 for the
estimates).
Time window 750 – 900 ms.
No significant effects of sex (happy: p > .1; sad: p = 0.09) or AQ (ps >
0.1) occurred, for both happy and sad prosodic conditions (see Table 3).
Time window 1150 – 1300 ms.
For happy prosodic stimuli, sex was significantly related with the
congruity effect at 1150 – 1300 ms (b = 0.30, t = 2.04, p = .048). Women
had larger ERP differences than men in this time window. There was no
significant association between AQ and sad prosodic stimuli processing
(see Table 3).
4. Discussion
This study aimed to examine sex differences while controlling for
autistic traits regarding two aspects of communication processes: 1)
efficiency of emotional speech processing and; 2) multi-channel inte­
gration of emotional prosody and semantic valence. Regarding effi­
ciency of processing, we found a significant sex difference in reaction
time but not accuracy. The absence of sex differences in accuracy is not
surprising because the task was designed to be very easy, as shown by
the ceiling effect of accuracy rates among female and male participants
alike. However, men responded more slowly than women when making
semantic judgments about emotionally spoken words, suggesting lower
efficiency in the processing of emotional speech in men. It is plausible
that these differences are not due to differences in general cognitive
processing speed as sex differences were not revealed by the speeded
version of the applied non-verbal IQ test. Our results showed that sex
differences in reaction times were highly significant even with AQ
controlled, that is, women and men differed in task performance even
though on average they had similar AQ. Therefore, our results refute the
hypothesis that sex differences in semantic valence processing are driven
by the generally higher average AQ of men as compared to women in the
population. Instead, our findings are consistent with previous studies

5
M. Lui et al. Biological Psychology 157 (2020) 107973

Fig. 2. 2a & 2b. Grand ERP averages of females vs. males in congruous and incongruous conditions for happy prosodic stimuli (top panel) and sad prosodic stimuli
(bottom panel) at Cz electrode.

Fig. 3. Bar plots illustrating ERP congruity effects (incongruous minus congruous condition) in happy and sad prosodic conditions at Cz electrode in the time
windows 350 – 650 ms, 750 – 900 ms and 1150 – 1300 ms.

6
M. Lui et al. Biological Psychology 157 (2020) 107973

Fig. 4. Topographical plots of ERP congruity effects (incongruous minus congruous condition) in happy (A) and sad (B) prosodic condition in the time windows 350
– 650 ms, 750 – 900 ms and 1150 – 1300 ms for females vs. males.

Table 3
Regression analysis results with Sex and AQ as predictors of ERP amplitude differences between incongruous and congruous condition for happy and sad prosody and
three different time windows (350 – 650 ms, 750 – 900 ms, and 1150 – 1300 ms).
Prosody Time window (ms) R2 F p bsex tsex psex bAQ tAQ pAQ

Happy 350–650 .13* 3.38 .04 .34 2.43 .01* .13 .93 .35
750–900 .03 .75 .47 .15 1.02 .31 .10 .67 .50
1150–1300 .09 2.15 .13 .30 2.04 .048* .06 .39 .69
Sad 350–650 .03 .67 .51 − .02 − .11 .91 − .17 − 1.15 .25
750–900 .07 1.79 .17 − .24 − 1.68 .09 − .12 − .88 .38
1150–1300 .01 .31 .73 − .12 − .76 .45 − .03 − .21 .83

Note: *p < .05; ** p < .01. The regression weights (b) are standardized estimates.

showing women’s superior performance in processing emotional sig­
nals, such as higher accuracy in identifying facial emotions (Collignon
et al., 2010; Montagne, Kessels, Frigerio, de Haan, & Perrett, 2005) and
vocal emotions (Schirmer et al., 2004). Note that the semantic judgment
is an easy task while participants were required to respond as fast as
possible. Thus, the superior performance of women was reflected by
shorter reaction times instead of higher accuracy rates.
4.1. Integration between emotional prosody and semantic valence
Apart from efficiency in processing emotional signals, we aimed to
demonstrate sex differences in the automatic integration between

7
M. Lui et al.
semantic valence and emotional prosody with both behavioral and
neural measures, when AQ is controlled for. The integration was indi­
cated by differences between incongruous and congruous conditions in
reaction times, accuracy, and ERP amplitudes (congruity effects). In
incongruous conditions where prosody and semantic valence mis­
matched (e.g., negative meaning words spoken in happy prosody),
conflicts in perception and response generation are expected. A larger
difference between congruous and incongruous conditions (congruity
effect) indicates more automatic (involuntary) integration between
prosody and semantic valence, given that emotional prosody was irrel­
evant to the task of judging semantic valence.
The main effect of congruity on reaction time indicates that the
participants did automatically integrate emotional prosody when pro­
cessing semantic valence. This replicates the findings of Schirmer et al.
(2006) that revealed a main effect of congruity. Our finding indicating
no sex difference in multi-channel integration of emotional prosody and
semantic valence is however at variance to other studies demonstrating
women’s superior performance in processing emotional signals from
multiple modalities. For example, Collignon et al. (2010) found that
woman had a larger bimodal facilitation than men, supporting that
women integrate vocal and facial emotional expressions to a larger
extent than men. In another study, Hall, Witelson, Szechtman, and
Nahmias (2004) found women to be more accurate in matching sad
prosodic and visual stimuli than men. Importantly, that study also
showed that women and men differ in their neural patterns of responses
when processing multi-modal emotional stimuli. Women showed
stronger activation of the limbic system (e.g., anterior cingulate and
thalamus) while men recruited more frontal areas (e.g., left interior
frontal gyrus). The authors suggested that women may treat emotional
cues of multi-modal stimuli as unconditional innate stimuli, whereas
men may allocate more resources to regulatory and inhibitory processes
for emotional responses. In our study, although no sex differences
occurred regarding the congruity effects in reaction times, it is possible
that the timing of the neurocognitive integration processes of emotional
prosody and semantic valence of spoken words differs between women
and men. This is indicated in the ERP results to be discussed next.
Interestingly, in several time segments of ERPs there were sex dif­
ferences in congruity effects: for happy prosodic stimuli, men exhibited a
greater ERP difference than women in the N400 component (350 – 650
ms), while women had a greater ERP difference than men in the late
positive component (1150 – 1300 ms). These ERP results show that both
sexes integrate emotional prosody and semantic valence, while their
timing differs. This is a novel finding as previous studies have not yet
examined sex differences in integrating emotional prosody and semantic
valence for specific types of emotions. Although past studies showed
women’s advantage in recognizing emotions, many of them were emo­
tions in a single channel such as faces and voices alone, instead of
integrating multi-channel information (e.g., Hall & Matsumoto, 2004;
Montagne et al., 2005; Thayer & Johnsen, 2000). Our findings add to the
literature by showing that men and women differ in the timing of neu­
rocognitive integration of happy prosody with valence of semantic
meaning and that this cannot be accounted for by differences in autistic
traits. While men had larger ERP congruity effect than women in the
N400 time window, which corresponds to the incongruity detection
stage (Kutas & Federmeier, 2011), women had larger ERP congruity
effect than men in the later time window (1150 – 1300 ms), which
corresponds to the evaluation process of stimulus probability. In previ­
ous language studies, the late component was found to be larger when a
word is in discordant with semantic or syntactic constraints (Hahne &
Friederici, 2002; Van den Brink, Brown, & Hagoort, 2001). Our finding
suggest that men allocate more neural resources in detecting incongruity
than women, while women dedicate more neural resources in evaluating
the stimulus probability (Coulson et al., 1998), even if sex differences in
autistic traits are controlled for. Future studies are needed to further test
the robustness of this interpretation.
Another major finding is the missing sex difference in the integration
8
Biological Psychology 157 (2020) 107973
between sad prosody and semantic valence when controlling for autistic
traits. This is in contrast to previous behavioral studies which showed
women’s higher sensitivity towards sad stimuli (e.g., Eugène et al.,
2003; Fujisawa & Shinohara, 2011; Orozco & Ehlers, 1998; Rotter &
Rotter, 1988) and neuroimaging studies which demonstrated that
women recruited a more extensive and less lateralized neural network
during induced sadness (Schneider, Habel, Kessler, Salloum, & Posse,
2000). One possibility is that sex differences in processing sad stimuli
are alleviated when both sexes have similar level of autistic traits.
Autistic traits are highly and negatively correlated with empathy and a
past study revealed that adolescents with autism were less able to
empathize with other people’s negative emotions than with positive
emotions (Mazza et al., 2014). Controlling the levels of autistic traits
between men and women may therefore reduce differences in process­
ing sad stimuli as shown by the lack of sex differences in ERPs for sad
prosodic stimuli.
Another possibility could be that the applied sad stimuli were quite
long in duration (sad prosodic words =1240 ms versus happy prosodic
words =877 ms). Long stimuli may have granted participants prolonged
periods of time to process and respond, as shown by the longer reaction
time to sad stimuli (1387 ms) than to happy stimuli (1145 ms). The long
duration of sad stimuli might have diminished the cognitive demands
required to handle the conflicting information between prosody and
semantic valence, which is supported by our finding that the congruity
effect on reaction times was negatively correlated with reaction times.
The lack of sex differences in ERP congruity effect in the sad prosodic
condition could be due to the overall diminished congruity effect.
A third possibility to explain the lack of sex difference in the sad
stimulus condition is the nature of the stimuli used in our study. The
emotional prosodies, happy and sad, were discrete emotions while the
semantic valence were categorized more broadly as positive and nega­
tive valence. It is generally agreed that there are multiple negative
emotions (e.g., fear, anger, disgust, and embarrassment) as compared
with positive emotions (e.g., happiness, elation, calmness). In our
stimuli, while happy prosody generally matches with positive meaning
of words, sad prosody only matches exactly with the meanings of around
20 (out of 60) negative words included in our study. It is therefore
possible that some of the sadly spoken negative words are not exactly
congruous, which may explain why the congruity effect was smaller in
sad stimuli than in happy stimuli. Future studies may consider matching
the emotional prosody with specific word meaning instead of a broad
valence.
4.2. Limitations
The current study recorded participants’ responses to the congruity
between emotional prosody and semantic content in speech. It is
possible that the observed congruity effects are not only specific to
emotional stimuli, but also non-emotional information from multiple
channels such as in Stroop tasks (e.g., Zahedi, Abdel-Rahman, Stürmer,
& Sommer, 2019). Further studies may include a non-emotional conflict
processing task as a control condition. Regarding participant selection,
our study included neurotypical participants with different levels of
autistic traits. Future studies are needed to investigate the relationship
between autistic traits and emotional prosody processing by including
participants diagnosed with ASD, in order to examine the targeted ef­
fects across the whole autism spectrum. In terms of stimulus charac­
teristics, auditory words were produced by a single female speaker in
this study. Future studies will need to include stimuli produced by both
female and male speakers, and by multiple speakers to be able to
generalize across specific stimuli.
4.3. Conclusion
This study indicates that women process emotional speech more
efficiently than men, while no behavioral sex differences were found in
M. Lui et al.
multi-channel integration processes for prosody and semantic meaning
when the level of autistic traits was controlled for. At the neural level,
sex differences emerged in the timing of integration between prosody
and semantic valence when processing happily spoken words. Men
showed integration effects in earlier neurocognitive processes than
women. Our study provides novel findings on sex differences in
emotional speech processing that are not due to autistic traits. This
contributes to a better understanding of individual differences in
prosody-semantic integration during human communication, and it
helps disentangling differences between individuals in higher order so­
cial cognition.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
This work was supported by the Hong Kong Baptist University
Research Committee Interdisciplinary Research Matching Scheme [RC-
IRMS/16-17/04]; Hong Kong Baptist University Interdisciplinary
Research Clusters 2018/19 [RC-IRCMs/18-19/SCI/01]; and the General
Research Fund of Research Grants Committee, Hong Kong [Ref No.
12604418]. The work was also supported by Hong Kong University
Grants Committee, Germany-Hong Kong Joint Research Scheme
[G_HKBU/201/17] awarded to Changsong Zhou and Xiaojing Li, and [ID
57391438] awarded to Werner Sommer and Andrea Hildebrandt. The
author Xiaojing Li is thankful to the Hanse-Wissenschaftskolleg Institute
for Advanced Study, Delmenhorst, Germany for the fellowship support.
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