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Chemosensory communication of aggression: women's fine-tuned neural processing of male aggression signals

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The current study is the first to examine the central nervous processing of aggression chemosignals within men and women by means of chemosensory event-related potential (CSERP) analysis. Axillary sweat was collected from 17 men and 17 women participating in a competitive computer game (aggression condition) and playing a construction game (control condition). Sweat samples were pooled with reference to donor gender and condition, and presented to 23 men and 25 women via a constant flow olfactometer. Ongoing electroencephalogram was recorded from 61 scalp locations, CSERPs (P2, P3-1, P3-2) were analysed and neuronal sources calculated (low-resolution electromagnetic tomography, LORETA). Women, especially, showed larger P3-1 and P3-2 amplitudes in response to male as compared with female aggression signals (all p values < 0.01). The peak activation of this effect was related to activity within the dorsomedial prefrontal cortex (Brodmann area 8). As male aggression commonly targets physical harm, the competence of the human brain to sensitively detect male aggression signals is considered to be highly adaptive. The detection of male aggression signals seems to be of higher importance for women than for men. It is suggested that the processing of male aggression signals in women induces an immediate response selection. This article is part of the Theo Murphy meeting issue ‘Olfactory communication in humans’.
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Research
Cite this article: Pause BM, Storch D, Lübke
KT. 2020 Chemosensory communication of
aggression: womens fine-tuned neural
processing of male aggression signals. Phil.
Trans. R. Soc. B 375: 20190270.
http://dx.doi.org/10.1098/rstb.2019.0270
Accepted: 23 October 2019
One contribution of 18 to a Theo Murphy
meeting issue Olfactory communication in
humans.
Subject Areas:
behaviour, cognition, neuroscience
Keywords:
aggression, body odours, chemosensory
communication, olfaction, sex differences
Author for correspondence:
Bettina M. Pause
e-mail: bettina.pause@hhu.de
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.4870215.
Chemosensory communication of
aggression: womens fine-tuned neural
processing of male aggression signals
Bettina M. Pause, Dunja Storch and Katrin T. Lübke
Department of Experimental Psychology, Heinrich-Heine-University Düsseldorf, D-40225 Düsseldorf, Germany
BMP, 0000-0003-0471-2550
The current study is the first to examine the central nervous processing of
aggression chemosignals within men and women by means of chemosensory
event-related potential (CSERP) analysis. Axillary sweat was collected from
17 men and 17 women participating in a competitive computer game (aggres-
sion condition) and playing a construction game (control condition). Sweat
samples were pooled with reference to donor gender and condition, and
presented to 23 men and 25 women via a constant flow olfactometer. Ongoing
electroencephalogram was recorded from 61 scalp locations, CSERPs (P2, P3-1,
P3-2) were analysed and neuronal sources calculated (low-resolution electro-
magnetic tomography, LORETA). Women, especially, showed larger P3-1
and P3-2 amplitudes in response to male as compared with female aggression
signals (all pvalues < 0.01). The peak activation of this effect was related to
activity within the dorsomedial prefrontal cortex (Brodmann area 8). As
male aggression commonly targets physical harm, the competence of the
human brain to sensitively detect male aggression signals is considered to
be highly adaptive. The detection of male aggression signals seems to be of
higher importance for women than for men. It is suggested that the processing
of male aggression signals in women induces an immediate response selection.
This article is part of the Theo Murphy meeting issue Olfactory
communication in humans.
1. Introduction
One core function of emotions in social animals is the communication of survi-
val-related behavioural adaptations between conspecifics through social signals
[1]. Most widely used signals across the metazoan species are chemosensory in
nature [2] and science has just started to uncover their relevance for human be-
haviour (see [3]). Chemosensory stress signals are ubiquitous in the animal
kingdom and seem to act contagiously, alerting group members to potential
threats, thereby preventing a direct exposure to the source of danger [4]. In
humans, the emotions fear and anxiety can be considered to be part of a
stress response [5]. Meanwhile numerous studies demonstrate a successful che-
mosensory transmission of fear and anxiety in humans (see [6,7]), which,
however, sometimes can only be demonstrated in female receivers and is
absent in males [810].
While intra-species aggression might have evolved in the context of defending
or obtaining resources [11], aggressive signals are considered to increase fitness by
evoking a defence response in order to avoid an escalated fight [1,12]. In many
animal species, scent marks alert conspecifics to the competitive ability or
dominance of the signal sender [13,14]. Whether or not the signal perceiver
reacts aggressively depends on its own social status and experience, and the con-
text of exposure [15,16]. First studies in humans investigated the communicative
properties of chemosignals derived from malessweat while being engaged in a
competitive badminton match [17] or in boxing [18]. Aggression-related
© 2020 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution
License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original
author and source are credited.
chemosignals activate physiological arousal [17], elicit an
anxiety-related attentional focus [18] and are processed
preferentially within the limbic system [19].
The current study aimed to investigate the central nervous
processing of aggression chemosignals. In order to examine
early, pre-attentive as well as late, evaluative processes, chemo-
sensory event-related potentials (CSERPs) were recorded [20].
So far, only maleschemosensory aggression signals have
been investigated or the related participant samples were too
small to investigate gender-related effects in the receivers
[1719]. However, as in humans, the communication of aggres-
sion strongly varies with the gender of the signal senderas well
as with the gender of the signal perceiver [21,22]; both genders
were investigated. It is hypothesized that CSERP responses to
human chemosensory aggression signals are indicative of
preferential processing.
2. Material and methods
(a) Participants
In total, 50 heterosexual (according to self-labelling) individuals
took part in the experiment; however, data of two individuals
had to be excluded from analysis owing to pronounced electro-
encephalogram (EEG) artefacts; see EEG data reduction. The
remaining 48 participants (23 males, 25 females) had a mean age
of 25.7 years (s.d. = 5.2 years; range = 1943 years, with age not
differing between genders, p= 0.266). Participants reported that
they were non-smokers, right-handed (Annett Handedness Ques-
tionnaire [23]) or both; participants and sweat donors reported that
they were of European descent (minimizing effects of culture,
ethnos and genetic background). None of the participants reported
receiving acute or chronic medication, or the use of drugs. In
addition, no participant suffered from any neurological, psychia-
tric, endocrine or immunological condition, or diseases related to
the upper respiratory system. Participating women had a regular
menstrual cycle and did not use oral contraceptives. None of
these participants acted as a sweat donor in the presentexperiment.
A brief olfactoryscreening test revealed no suspicion of general
hyposmia in any participant. The test required the participants
to detect phenylethyl alcohol (99%, 1: 100 (v/v) diluted in 1,2-
propanediol, 99%; both substances: Sigma-Aldrich, St Louis,
Missouri,USA), being present in oneof three bottles in two consecu-
tive trials, with the remaining two bottles containing the same
volume of solvent ( phenylethyl alcohol smells rose-like, and is
regularly used as a standard in olfactory sensitivity testing, [24]).
Participants gave their written informed consent and were
paid for their participation. The entire study, including the
sweat donation procedure, was approved by the ethics commit-
tee of the Faculty of Mathematics and Natural Sciences of the
Heinrich-Heine-University Düsseldorf (Germany).
(b) Sweat donation
Methods and results of the sweat donation are presentedin detail in
the electronic supplementary material (figures S1S3, tables S1
S3). In brief, axillary sweat was sampled on cotton pads from
both armpits of 17 women and 17 men. The donors first attended
the aggression induction session, and 116 days later, a non-
emotional control session. Within the aggression condition, partici-
pants were exposed to the Point Subtraction Aggression Paradigm
(PSAP, [25,26]). Within this game, the participantstask is to collect
as many points as possible via button presses, while a fictitious
opponent simultaneously is stealing these points. Participants can
choose betweenthree behavioural strategies, one of which is related
to overt aggressive behaviour against their opponent. In the control
session, the PSAP was replaced by a construction computer game.
Almost all donors (30 out of 34) showed overt aggressive be-
haviour during the PSAP game. In addition, donors reported a
stronger increase of anger during the aggression condition than
during the control condition ( p< 0.001; none of the other basic
emotions increased during the aggression condition). Accordingly,
their salivary testosterone levels rose during the aggression
condition ( p= 0.05). Donorsmean baseline-corrected heartrate
decreased during the control session ( p= 0.001), but did not
change during the aggression condition.
Following the completion of collection, all cotton pads carry-
ing the sweat samples were cut and pooled with respect to the
donors gender and the donation condition. Each of the final
four homogenized samples (male aggression, male control,
female aggression and female control) was divided into 100 por-
tions of 0.4 g cotton pad and stored at 20°C.
(c) Presentation of the sweat samples
For EEG recordings and stimulus ratings, the chemosensory
stimuli were presented by a constant flow (100 ml s
1
; stimulus
duration = 0.4 s) eight-channel olfactometer (latency of stimulus
onset after valve activation=40 ms; rise time =50 ms; OL023,
Burghart, Wedel, Germany). Both nostrils were stimulated
simultaneously, and both air streams were controlled by separate
mass flow meters. The temperature of the air flow at the exit
of the olfactometer was 37°C and the relative humidity was
set above 80%. White noise of 75 dB(A) was presented
binaurally via earplugs (Etymotic Research, ER3-14A), in order
to prevent the participants from hearing the switching valves
of the olfactometer. During EEG recordings and odour
ratings, participants performed the velopharyngeal closure
technique [27,28].
(d) Odour detection, odour ratings and emotional
ratings
Following each stimulus presentation during the EEG recording,
participants indicated whether they had perceived an odour (yes,
no), and afterwards (independent of their detection statement),
their opinion on whether the putative stimulus was obtained
from women or men. Participants indicated either answer by
ticking a box on a screen (yes/no or male/female) with a
mouse (forced choice). In order not to bias the participants and
to ensure attention, participants were told that body odours
would only be presented in some, but not all trials. In fact,
odours were presented during all trails and no blank trials
were included. For odour detection as well as for the assessment
of the donorsgender, a hit rate was calculated, defined as per-
centage of correct answers. Missing data within the detection
task were treated as not detected.
In order to obtain odour ratings, at the beginning of the
experiment, before EEG recording, each sample was presented
for 0.4 s for each of the three ratings. The order of odour presen-
tations was randomized. Participants rated the sweat samples
intensity on a pictographic scale ranging from 1 (not at all
intense) to 9 (extremely intense). In addition, participants
selected terms from a list of 147 verbal descriptors that best
described the sweat samplesodorous quality [29]. Here, partici-
pants were required to select at least one descriptor, but were free
to select as many descriptors as they deemed fitting. Participants
practised using the descriptor list for as long as they needed to by
describing the odour of phenylethyl alcohol, which was used in
the hyposmia screening.
In order to assess the donorsemotional experience during
donation, participants reported to what extent they thought
the donorsfelt each of three basic emotions (fear, anger
and happiness) on visual analogue scales (0 = not at allto 10 =
extremely).
royalsocietypublishing.org/journal/rstb Phil. Trans. R. Soc. B 375: 20190270
2
(e) Electroencephalogram procedure
The time course of the entire experimental session, including the
EEG procedure, is depicted in electronic supplementary material,
figure S4. During EEG recording, each of the four stimuli (male
aggression, male control, female aggression and female control)
was presented 25 times. The stimuli were presented in a pre-
viously randomized, fixed order (with the restriction that the
same emotion or the same donor gender was presented no
more than three times in a row). Participants were informed
that they would receive body odours; however, they knew
neither anything about the emotional state of the odour donors,
nor how many different odours they would receive. At the begin-
ning of each trial, a fixation cross was presented on a screen for
5.5 s, and sweat samples were presented randomly 23 s after
cross-onset (stimulus duration: 0.4 s). Subsequent to the fixation
cross, the screen turned grey for 23 s (randomized), followed by
the question Did you smell anything?appearing on the screen
for 3 s. Afterwards, the question Which was the donors
gender?appeared on the screen for 3 s. In order to ensure sus-
tained attention throughout EEG recording in spite of the
relatively long inter-stimulus intervals (ISIs), the participants
were further presented with a task during which they had to
assign a colour to the odour they just had perceived (3 s).
The trials ended with the presentation of a grey screen for 25s
(randomized). In total, the trialsduration was 18.5 to 22.5 s
(randomized), with a total recording duration of 34 min 10 s.
EEG recordings were subdivided into three blocks (33, 33 and 34
trials), separated by two individually adjusted resting periods.
On average, the EEG sessionsduration was 41 min (s.d. = 4 min).
(f) Data recording and reduction
Ongoing EEG was recorded from 61 scalp locations with Ag/AgCl
sintered electrodes (inner diameter 6 mm), using an electrode cap
(EasyCap, Herrsching, Germany). An additional electrode was
placed 1.5 cm below the right eye, outside the vertical pupil axis
to record the vertical eye movements. Fp2 was used to record the
horizontal eye movements. The ground electrode was placed at
position FT10. The electrodesimpedance was usually below 10
and always below 20 kΩ. Data were sampled at 500 Hz with an
averaged reference and low-pass filtered online at 135 Hz (Quick-
Amp-72 amplifier and BrainVision Recorder software, Brain
Products, Munich, Germany).
Offline, EEG signals were re-referenced to linked ear lobes,
low-pass filtered with 40 Hz (48 dB/octave) and high-pass fil-
tered with 0.05 Hz (48 dB/octave). Additionally, a 50 Hz notch
filter was applied. Each EEG was corrected for eye movements
[30] and baseline-corrected (5000 ms before stimulus onset).
Channels containing voltage bursts (75 µV maximum voltage
difference within 100 ms) were excluded from the analyses. In
cases where more than one-third of the channels forming one
electrode pool (see below) were contaminated with artefacts in
a given trial, trials were also excluded. In sum, two participants
were completely excluded from analysis (with fewer than 13 out
of 25 trials in at least one condition).
For peak detection, the artefact-reduced EEG was low-pass
filtered with 7 Hz, 48 dB/octave. The 61 scalp electrode positions
were subdivided into nine areas (pools), and a mean peak for
each pool was calculated by averaging adjacent electrodes in
anterior (a), central (c) and posterior (p) areas for the left (l) and
the right (r) hemisphere as well as for midline electrodes (resulting
electrode pools: al: AF7, AF3, F7, F5, F3; am: Fpz, AFz,F1, Fz, F2;
ar: AF4, AF8, F4, F6, F8; cl: FT7, FC5, FC3, T7, C5, C3, TP7, CP5,
CP3; cm: FC1, FCz, FC2, C1, Cz, C2, CP1, CPz, CP2; cr: FC4,
FC6, FT8, C4, C6, T8, CP4, CP6, TP8; pl: P7, P5, P3, PO7, PO3,
O1; pm: P1, Pz, P2, POz, Oz; pr: P4, P6, P8, PO4, PO8, O2). In
relation to the baseline period (5000 ms before stimulus onset),
four separate peaks were differentiated within predefined latency
windows (N1: 250600 ms, P2: 500700 ms, P3-1: 700900 ms,
P3-2: 900-1100 ms; [20]), and amplitudes and latencies of each
peak were calculated. As the N1 deflection within the present
data was almost absent (mean, M=0.4 µV, s.d. = 1.1), we
refrained from statistically analysing the N1.
(g) Data analysis
Detection rates, odour intensity and the attribution of the donors
gender were analysed by means of three-way mixed-factors
ANOVAs, including the within-subjects factors Emotion (EMO;
aggression sweat sample, control sweat sample), DonorsGender
(DG; male sweat sample, female sweat sample) and the between-
subjects factor ParticipantsGender: (PG; men, women). Detection
rates for each sweat sample (male aggression, male control, female
aggression and female control ) were also tested against chance
level by means of one-sample t-tests. In order to investigate
whether participants could identify the emotional content of the
sweat samples, the suspected emotions of the donors were ana-
lysed by means of a two-way mixed-factors ANOVA separately
for each sweat sample, including the within-subjects factor
Assessed Emotion (anger, fear and happiness) and the between-
subjects factor PG. All significant ANOVA results regarding the
detection rates and ratings are reported.
The amplitudes and latencies of the CSERP components were
subjected to a five-way mixed-factors ANOVA, including the
within-subjects factors EMO, DG, Sagittal (SAG; anterior,
central, posterior) and Transversal (TRANS; left, midline, right),
and the between-subjects factor PG. Significant interactions were
followed up by nested ANOVA effects analysis [31] and, in the
case of significant nested effects, simple comparisons (e.g. paired
t-tests). In all analyses, the alpha level was set to p< 0.05 (based
on HuynhFeldt corrected degrees of freedom). Within the main
article, all significant ANOVA and nested ANOVA effects includ-
ing the factors EMO, DG and PG are reported. Effects including
exclusively the factors SAG and TRANS are reported in the elec-
tronic supplementary material.
Current source density (CSD) maps were calculated using a
spherical spline model ([32], order of splines: m= 4, maximal
degree of Legendre polynominals = 20). Low-resolution electro-
magnetic tomography (LORETA) was used in order to localize
the source of brain activity [33]. The source space comprises 2394
voxels at 7 mm spatial resolution, covering the cortical grey
matter and the hippocampus [34], defined via a reference brain
from the Brain Imaging Center at the Montreal Neurological Insti-
tute (MNI, [35]). LORETA uses a three-shell spherical head model,
co-registered to the Talairach anatomical brain atlas [36].
3. Results
(a) Stimulus detection and assessment of donors
gender
During EEG recording, participants detected on average 52.3%
(s.d. = 26.7; range = 0.0100.0%) of the presented sweat samples,
not differing from chance in their overall detection performance
(t
47
= 0.60, p= 0.555). However, separating detection rates for
each stimulus, male aggression sweat was detected more
often than expected by chance (M=60.0%, s.d. = 30.0; t
47
=
2.31, p= 0.025). Odour detection rates did not change from the
first to the second 50 trials (t
47
=0.90, p=0.375).
In general, detection rates were higher for male (M= 56.0%,
s.d. = 27.2) than for female sweat (M= 48.5%, s.d. = 27.4; DG:
F
1,46
= 20.16, p< 0.001,
h
2
p¼0:31, power = 0.99), and women
responded more often to aggression sweat (M= 56.2%, s.d. =
28.2) than to control sweat (M= 46.4%, s.d. = 27.5; EMO × PG:
royalsocietypublishing.org/journal/rstb Phil. Trans. R. Soc. B 375: 20190270
3
F
1,46
= 6.86, p= 0.012,
h
2
p¼0:13 , power = 0.73; nested effects:
EMO within women: F
1,46
= 15.68, p< 0.001).
Participantscorrect assessment of the donorsgender did
not differ from chance ( p= 0.066). On average, participants
correctly assessed 51.6% (s.d.= 5.9) of the presented samples.
Neither participantsgender nor the chemosensory condition
affected the assessment (all pvalues > 0.089). All group mean
values regarding stimulus detection (table S4) and donors
gender assessment (table S5) are presented in the electronic
supplementary material.
(b) Odour ratings and descriptions
(i) Intensity
Across all samples, the body odoursintensity was judged as
relatively weak (M= 3.02, s.d. = 1.54), with male sweat (M=
3.33, s.d. = 1.76) being judged as slightly more intense than
female sweat (M= 2.70, s.d. = 1.59; DG: F
1,46
= 10.33, p= 0.002,
h
2
p¼0:18, power = 0.88). However, intensity ratings were
unaffected by the emotional condition or participantsgender
(all pvalues > 0.142; for all group mean values see electronic
supplementary material, table S6).
(ii) Suspicion of donorsemotional state
In general, any emotion the participants suspected the sweat
donors to have experienced during sweat donations was
rated as very low in intensity (M= 1.88, s.d. = 1.39). Participants
imagined the donors of male aggression sweat to have been
more anxious (M= 2.57, s.d. = 2.64) than happy (M= 1.28,
s.d. = 1.61; Assessed Emotion: F
2, 88
= 5.34, p= 0007,
h
2
p¼0:11, power = 0.82). Ratings did not differ in the context
of any other sweat sample and were not affected by the
ratersgender (all pvalues > 0.050; for all group mean values
see electronic supplementary material, table S7).
(iii) Verbal descriptors
Out of the 147 verbal descriptors the participants could
choose from, they selected the descriptor lightmost often,
and the descriptor warmsecond most often for characteriz-
ing each of the four sweat samples (for the frequency
distribution of selected verbal descriptors see electronic sup-
plementary material, figures S5 and S6).
(c) Chemosensory event-related potentials
The distribution of CERPs across the scalp, separated for
the experimental conditions, is depicted in figure 1. All
CSERP ANOVA effects are listed in electronic supplementary
material, tables S8 and S9. A detailed analysis of the CSERP
componentslocal distribution is included in the electronic
supplementary material.
(i) Amplitudes
P2-amplitude. When presented with aggression sweat,
participants display larger P2 amplitudes in response to male
(M= 2.30 µV, s.d. = 2.39) as compared with female sweat
samples (M= 1.49 µV, s.d. = 1.88; EMO × DG: F
1,46
= 4.41,
p= 0.041,
h
2
p¼0:09, power = 0.54; nested effects: DG within
aggression sweat: F
1,46
= 4.81, p= 0.033,
h
2
p¼0:09, power =
0.57).
P3-1 amplitude. The amplitude of the P3-1 component is
affected by the donorsemotion, the donorsgender and the
participantsgender: female participantsP3-1 amplitude is
larger in response to male aggression sweat than to male con-
trol sweat (EMO × DG × PG: F
1,46
= 6.14, p= 0.017,
h
2
p¼0:12,
power = 0.68; nested effects: EMO within male sweat within
women: F
1,46
= 9.82, p= 0.003,
h
2
p¼0:18, power = 0.87; male
aggression sweat: M= 4.26 µV, s.d. = 3.40; male control sweat:
M= 2.56 µV, s.d. = 2.06; restricting the first-order interaction
EMO × DG to female participants, and reducing the relevance
of the EMO × DG × TRANS interaction).
Furthermore, female participants show a larger P3-1 ampli-
tude in response to male aggression sweat than to female
aggression sweat (based on the same interaction EMO × DG ×
PG; nested effects: DG within female participants within
aggression sweat: F
1,46
= 12.15, p= 0.001;
h
2
p¼0:21, power =
0.93; male aggression sweat: M= 4.26 µV, s.d. = 3.40, female
aggression sweat: M= 2.41 µV, s.d. = 2.50; accordingly, the
main effect DG and the interaction EMO× DG are limited to
the significant second-order interaction).
Finally, female participants display larger P3-1 amplitudes
than male participants in response to female control sweat
(based on the same interaction EMO × DG × PG; nested
effects: PG within female sweat within neutral sweat: F
1,46
=
5.32, p= 0.026,
h
2
p¼0:10, power = 0.61; women: M=3.13 µV,
s.d. = 2.26, men: M= 1.55 µV, s.d. = 2.49; invalidating the
first-order interaction PG × TRANS).
P3-2 amplitude. Within theP3-2 latency range, female partici-
pants respond with a larger amplitude to male aggression as
compared with male control sweat (EMO × DG × PG: F
1,46
=
4.61, p= 0.037,
h
2
p¼0:09, power = 0.55; nested effects: EMO
within male sweat within women: F
1,46
=7.21, p=0.010,
h
2
p¼0:14, power = 0.75; male aggression sweat: M=4.0V,
s.d. = 3.34, male control sweat: M= 2.61 µV, s.d. = 2.30). Men,
on the other hand, show a significant emotion-specific P3-2
amplitude only in response to female sweat (EMO × DG × PG;
nested effects: EMO within female sweat within men: F
1,46
=
4.50, p=0.039,
h
2
p¼0:09, power= 0.55; female aggression
sweat: M=2.05 µV, s.d. = 1.62, female control sweat: M=
1.10 µV, s.d. = 2.46; invalidating a general implication of the
main effect EMO and the first-order interaction EMO × DG).
Moreover, in female participants, P3-2 amplitudes in
response to male aggression sweat are larger as compared
with P3-2 amplitudes in response to female aggression sweat
(EMO × DG × PG; nested effects: DG within women within
aggression sweat: F
1,46
=15.07, p< 0.001,
h
2
p¼0:25, power =
0.97; male aggression sweat: M= 4.08, µV, s.d. = 3.34, female
aggression sweat: M= 1.93 µV, s.d. = 2.49; accordingly, the
main effect DG and the interaction EMO × DG are limited to
the significant second-order interaction).
Indeed, similar to the P3-1, women generally display larger
P3-2 amplitudes than men in response to female control sweat
(EMO × DG × PG; nested effects: PG within female sweat
within neutral sweat: F
1,46
= 5.09, p= 0.029,
h
2
p¼0:10, power =
0.60; women: M= 2.72 µV, s.d. = 2.51, men: M= 1.10 µV, s.d. =
2.46; invalidating the first-order interaction PG × TRANS).
(ii) Latencies
The P2 latency is not affected by any experimental condition
(all pvalues > 0.057). However, both P3-1 and P3-2 latencies
vary with the sweat samplesemotional content as well as
the donorsgender.
The P3-1 latency is larger in response to male aggression
as compared with male control sweat at left electrode posi-
tions (EMO × DG × TRANS: F
2,92
= 8.43, p= 0.002,
h
2
p¼0:16,
royalsocietypublishing.org/journal/rstb Phil. Trans. R. Soc. B 375: 20190270
4
power = 0.96; nested effects: EMO within left pools within
male sweat: F
1,46
= 9.32, p= 0.004,
h
2
p¼0:17, power = 0.85;
aggression sweat: M= 825.76 ms, s.d. = 50.81, control sweat:
M= 796.44 ms, s.d. = 47.82). The P3-2 shows a similar pattern,
generally appearing with a longer latency upon presentation
of male aggression sweat (M= 1015.48 ms, s.d. = 46.77) as
compared with male control sweat (M= 989.47 ms, s.d. =
46.94; EMO × DG: F
1,46
= 15.70, p< 0.001,
h
2
p¼00:25, power =
0.97; nested effects: EMO within male sweat: F
1,46
= 10.48,
p= 0.002;
h
2
p¼0:19, power = 0.89).
In response to female sweat, however, the P3-2 latency
shows the reverse pattern, with a longer latency in response
to female control (M= 1012.59 ms, s.d. = 48.46) as compared
with female aggression sweat (M= 988.22 ms, s.d. = 49.34;
EMO × DG: F
1,46
=15.70, p<0.001,
h
2
p¼0:254, power= 0.972;
nested effects: EMO within female sweat: F
1,46
=5.27,
p= 0.026,
h
2
p¼0:10, power = 0.61).
Finally, after presentation of aggression sweat, the P3-2
latency in response to male sweat (M= 1015.48 ms, s.d. = 46.77)
is larger than in response to female sweat (M= 988.22 ms,
s.d.= 49.34), but the reverse is true in the case of control sweat
(male control sweat: M=989.47 ms, s.d.=46.94; female control
sweat: M= 1012.59 ms, s.d .= 48.46 ; EMO × DG: F
1,46
= 15.70,
p< 0.001,
h
2
p¼0:25, power= 0.97; nested effects: DG within
aggression sweat: F
1,46
=6.79, p= 0. 012,
h
2
p¼0:13, power=
0.72; DG within control sweat: F
1,46
=6.50, p= 0. 014,
h
2
p¼0:12,
power = 0.70).
(d) Current source density analyses
Within the P3-1 latency range, men respond to male aggres-
sion sweat with cortical activations along the midline,
strongest at frontopolar brain areas (figure 2a). In response
to male control sweat, a left-sided parieto-occipital activation
is dominant. Mens brain responses to female sweat in gen-
eral are weaker than to male sweat. In response to female
aggression sweat, parietal areas are bilaterally activated.
Neuronal responses to female control sweat appear extremely
weak and disperse.
Women show a pattern of cortical activation along the
midline, with distinct clusters of activation across frontocen-
tral and parietal areas in response to all sweat samples
Figure 1. Grand averages of the CSERP across male (left column) and female (right column) participants in response to male (upper row) and female (lower row)
sweat. Black lines indicate CSERPs for aggression sweat and dotted lines indicate CSERPs for control sweat. Time point 0 refers to the valve activation.
royalsocietypublishing.org/journal/rstb Phil. Trans. R. Soc. B 375: 20190270
5
(figure 2b). Simultaneously, inhibition is prominent bilaterally
across fronto-temporal areas. This pattern of activation is
most pronounced in response to male aggression sweat.
With regard to the CSERP results, an emotion-specific
differential brain response could be observed when males
were smelling female sweat and when females were smelling
male sweat. Accordingly, CSD difference maps (aggression
control) were calculated for the respective conditions (figure 3).
In males smelling females, aggression-specific activity seems to
be most prominent in right parietal brain areas. In females
smelling males, aggression-specific activity appears to be
most prominent above left frontal brain areas (CSD difference
maps for all experimental conditions are plotted in electronic
supplementary material, figure S7).
(e) Low-resolution electromagnetic tomography
LORETA analyses are limited to the conditions resembling
significant emotion-related effects (males smelling female
sweat and females smelling male sweat, figure 3). In males,
the peak activation in response to female aggression sweat (as
difference in relation to female control sweat) appears within
the right angular gyrus (Brodmann area, BA 39). In females,
the maximum activation in response to male aggression sweat
(as difference in relation to male control sweat) can be observed
in the dorsomedial frontal gyrus (BA 8, LORETA analyses for all
difference (aggressioncontrol) conditions are shown in the
electronic supplementary material, figure S8).
4. Discussion
The current study is the first to our knowledge to show
enhanced neural processing of human aggression sweat. It is
found that male aggression signals are more intensely pro-
cessed than female aggression signals and that especially
womens brains respond strongly to male aggression signals.
These effects seem unlikely to be consciously mediated, as
the sweat samples could hardly be recognized as odours.
The sweat was obtained from odour donors experiencing
a strong increase in anger during being frustrated by a ficti-
tious co-player. The increase of anger is a valid indicator of
reactive aggression [37] and occurred emotion-specifically
(no other emotion increased simultaneously). The anger
increase was accompanied by an increase of testosterone, as
typically associated with PSAP-induced aggressive behaviour
[26]. Accordingly, almost all sweat donors reacted with overt
aggressive behaviour towards their opponent.
Sweat samples from the aggression condition were rated
as equally low in intensity to the control sweat samples, and
both were described as predominantly light and warm. The
use of the descriptor warmmight refer to the air flow being
presented by the olfactometer at body temperature; the pre-
dominant use of lightseems to reflect a non-specific and
faint odour perception. Further, participants were not able to
assign the correct gender or emotion to the donors of the
sweat samples. However, across all participants, male aggres-
sion sweat was the only stimulus detected as an odour, while
detection rates of all other stimuli did not differ from chance.
Since the participants were aware of their constant connection
to an olfactometer, they might have expected to receive olfac-
tory stimuli at least in certain trails. Thus, we consider the
participants to probably have been biased towards reporting
smelling an odour, rather than reporting no odour perception.
Accordingly, the detection rates reported can be considered to
overestimate the true detection performance. It is concluded
that the stimuli were perceived at the level of the perceptual
threshold, not being associated with a specific odour quality
profile. Even though being processed as relevant information
in the human brain, human emotional chemosensory stimuli
have repeatedly been reported to be difficult to detect or to
recognize (e.g. [9,19]). However, in the present study, male
aggression sweat was the only stimulus recognized as odorous
more frequently than would be expected by chance.
–14 mV m–2 14 mV m–2
0 mV m–2 –14 mV m–2 14 mV m–2
0 mV m–2
(a)(b)
Figure 2. CSD maps (two-dimensional smoothing for a view across all electrodes) at the time of the total mean P3-1 peak latency (810 ms). (a) CSD maps of men
in response to male aggression sweat (upper left), male control sweat (upper right), female aggression sweat (lower left) and female control sweat (lower right).
(b) CSD maps of women in response to male aggression sweat (upper left), male control sweat (upper right), female aggression sweat (lower left) and female
control sweat (lower right). Red colours represent cortical activation (neuronal sources) and blue colours represent cortical deactivation (neuronal sinks).
royalsocietypublishing.org/journal/rstb Phil. Trans. R. Soc. B 375: 20190270
6
In accordance with the higher detection rates for male
aggression odour, the respective chemosensory signal evoked
a larger P2 amplitude and longer P3-1 and P3-2 latencies
than all other stimuli. As prior work on the chemosensory com-
munication of dominance or aggression relied on male
chemosignals only [1719], this is the first study to our knowl-
edge demonstrating the strong impact of male aggression
signals on the human brain. The chemosensory P2 amplitude
is an indicator of pre-attentive processes and is affected by
the stimulus intensity [38]; therefore, its increased amplitude
in response to male aggression signals might reflect the stron-
ger odour of male aggression signals and their capacity to
catch neuronal resources. The P3, on the other hand, reflects
late evaluative stimulus processing and is not related to
exogenous stimulus properties, but to the subjective stimulus
relevance [20]. As aggression signals do not automatically
induce a certain response, but might evoke fight or flight
responses depending on the perceiversown competencies,
response selection strategies need to be carefully balanced
[22]. Accordingly, a prolonged P3 latency has been described
to be due to effortful response selection strategies [39]. Male
aggression is most often expressed as physical aggression
[40] and thus can threaten physical health or can even be life
threatening. Successful survival depends on a sensitive detec-
tion of such signals.
In addition to the general effects of male aggression chemo-
signals on the P2-amplitude and P3-1 and P3-2 latencies in
male and female perceivers, the most pronounced effects on
the P3-1 and P3-2 amplitudes can be observed in female partici-
pants. Within the P3 latency range, women show larger
potentials (P3-1, P3-2) than men. They especially respond
to male aggression sweat with much larger potentials (P3-1,
P3-2) than to male control sweat or to female aggression
sweat. These findings are in line with a female processing
advantage of chemosensory anxietysignals [810], and suggest
a general superior processing of human emotion-related che-
mosignals in women. The CSERP effects are accompanied by
neuronal sources within medio-frontocentral brain regions
–14 mV m–2 14 mV m–2
5
6
(cm)
(cm)
–8
–6
–4
–2
0
2
4
6
8
–6
–4
–2
0
2
4
6
8
10
–6
–4
–2
0
2
4
6
8
10
–6
–4
–2
0
2
4
6
(cm)
(cm)
–8
–6
–4
–2
0
2
4
6
8
–6
–4
–2
0
2
4
0–510
5 0 –5 10
0 0.005
X= –24, Y= 24, Z=50
0.010
0 0.005
X= 53, Y= –60, Z=22
0.010
5 0 –5 10 5 0 –5
5 0 –5 10 5 0 –5
0 mV m–2
Figure 3. CSD difference maps (two-dimensional smoothing for a view across all electrodes) of differential CSERPs of male participants in response to female
aggression minus female control sweat (left, top), and female participants in response to male aggression minus male control sweat (left, bottom) at the
time of the total mean P3-1 peak latency (810 ms). Red colours represent cortical activation (neuronal sources) and blue colours represent cortical deactivation
(neuronal sinks). LORETA maps depicting the location of the maximum current density (in µA mm
2
) at the time of the total mean P3-1 peak latency
(810 ms) of men responding to female aggression sweat (in contrast with female control sweat, right, top), and women responding to male aggression
sweat (in contrast with male control sweat, right, bottom).
royalsocietypublishing.org/journal/rstb Phil. Trans. R. Soc. B 375: 20190270
7
and neuronal inhibition within fronto-lateral regions (CSD
maps). However, similar but weaker activations appear in
women in response to all sweat samples. It is suggested that
these findings reflect the activation of the mirror neuron
system, indicative of contagious effects of social emotions
[41], and the inhibition of brain structures related to higher-
order reasoning, such as executive functions (dorsolateral pre-
frontal cortex, [42]). Brain activity specifically related to male
aggression signals in women is supposedly located in the
dorsomedial prefrontal cortex (DMPFC, BA 8, LORETA differ-
ence maps). Activation of the DMPFC seems to be intimately
connected to social cognition and is considered to be involved
in a self-referential evaluation of others [43], and in the
translation of negative social experiences into threat-related
physiological responding [44]. Thus, as indicated by the
prolonged P3 latencies and the LORETA analyses, male aggres-
sion sweat warrants not only a fine-tuned sensory analysis, but
in addition an immediate response selection. This is especially
important for women, as globally, about one-third of ever-
partnered women have experienced physical and/or sexual
intimate partner violence [45].
Men, however, respond to a lesser extent to all sweat
samples, but still do show a differential brain response to
aggression as contrasted to control sweat. This response
occurs at a relatively late processing stage (P3-2) and is more
prominent in response to female sweat. However, as male par-
ticipants show almost no response to female control sweat, the
significant difference is due to the fact that they still show a
slight response to female aggression signals. A heightened sen-
sitivity to same-sex aggression in males, as proposed by some
authors [22], could not be statistically confirmed by the present
data. However, a weak differentiation of male aggression
signals from male control signals in male participants is
suggested by visual inspection of the grand averages (figure 1)
and direct effect testing (P3-2 amplitude: EMO within male
sweat within men F
1,46
= 4.14, p= 0.048). Whereas brain
responses to male aggression sweat in females could be partly
due to the fact that male aggression sweat was slightly odorous
but male control sweat was not, the brain responses to female
aggression sweat in male participants cannot be explained by
any odour-related effects.
In conclusion, chemosensory aggression signals, derived
from highly angry and aggressively behaving sweat donors,
were obtained from and presented to both genders. The
sweat samples were only weakly odorous, they failed to
convey a distinct odour quality profile, and intensity ratings
were not associated with the emotional state of the odour
donors. The human brain strongly responds to male aggression
signals, and, especially in women, a pattern of distinct acti-
vated and deactivated neuronal assemblies can be observed.
Thus, in contrast to chemosensory anxiety signals, the meaning
of chemosensory aggression signals varies with the gender
of signal sender and perceiver. It is hypothesized that aggres-
sion signals not only need to be processed preferentially, but
also prompt immediate response selection strategies, in order
for the perceiver to be able to cope with the potential threat.
As chemosensory communication in humans is far less prone
to the effects of learning and culture than any other kind of
communication, it is further suggested that the investigation
of human chemosensory communication offers a unique but
easy way to understand social behaviour in biologically rel-
evant settings.
Data accessibility. All original data reported in the study can be accessed
via the electronic supplementary material.
Authorscontributions. B.M.P. conceived the study idea and design,
supervised the performing of the experiments and the statistical ana-
lyses, and wrote the manuscript. D.S. performed the experiments,
carried out the statistical analyses under the supervision of K.T.L.
and B.M.P., and participated in drafting the manuscript. K.T.L. con-
ceived the study design, supervised the computational analyses,
and participated in performing the experiments as well in manuscript
drafting and editing. All authors read and approved the manuscript.
Competing interests. We declare we have no competing interests.
Funding. We received no funding for this study.
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... As receivers take on the fearful facial expression mimicking the state of the sender, the chemical communication of fear (as an unconditioned response to threat) or anxiety (as a conditioned response to threat-related internal and external stimuli; LeDoux & Pine, 2016) resembles a physiologically ancient form of empathy that results in the contagion of emotions (de Groot et al., 2012;Prehn-Kristensen et al., 2009; for emotional-contagion theory, see Hatfield et al., 1993). In addition, human aggression-related body odorants (sampled from sweat donors in response either to competitive sport contests or to frustration) can provide cues to social status and dominance, as shown by their effects on physiological, behavioral, and neural responses in receivers (Mutic et al., 2017;Pause et al., 2020). ...
... The perception of, and responsiveness to, semiochemicals can vary greatly between individuals. Differential effects occur in men and women (de Groot et al., 2014a;Pause et al., 2010Pause et al., , 2020, with women usually outperforming men in processing fear-and anxiety-related volatiles and in responsiveness to them. This may reflect an adaptive sex difference, and such differences can also manifest in other intriguing ways. ...
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... Another study investigated brain responses to aggression-related sweat by means of chemosensory event-related potentials (CSERPs, Pause et al., 2020). Here, sweat was obtained from male and female donors being exposed to the Point Subtraction Aggression Paradigm (PSAP). ...
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Humans have highly developed social and olfactory competencies. It is the aim of this review to summarize the empirical evidence and theoretical considerations, indicating that both of these performances are intimately linked and possibly coevolved during mammalian evolution. In detail, the necessity of fine-tuned social stimulus processing and flexible social behavior for humans’ self-definition, well-being, health, and survival rate is described. Further, the highly developed chemosensory competencies in humans are summarized. Specifically, I will focus on the feasibility of harm avoidance through chemosensory communication of stress, fear, anxiety, and aggression. In addition, possible specific peripheral and central processing systems are discussed, and the findings of specific emotional stimulus responses summarized. Further, individual differences in the perception of and response to social chemosensory signals are introduced. Regarding psychological disorders, recent studies point to important clinical implications due to deviant chemical communication. Finally, I outline that olfactory performances are linked to social network size and social skills. I conclude that the individual adjustment to social volatiles is a core feature of social intelligence.
... Following Kamiloğlu and colleagues (2018), all the participants were heterosexual, Caucasian, right-handed, non-smoking women with no reported neurological or psychiatric disorders, chronic respiratory diseases, and no allergic reactions, illnesses, or colds at the moment of the data collection. Only females were recruited due to their higher sensitivity toward emotional signals (Pause et al. 2020) and their superior sense of smell (relative to men; e.g. Brand and Millot 2001). Notably, only heterosexual participants were included because research shows that women perceive male sweat differently as a function of the donors' and their sexual orientation (e.g. ...
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... Following Kamiloğlu and colleagues (2018), all the participants were heterosexual, Caucasian, right-handed, non-smoking women with no reported neurological or psychiatric disorders, chronic respiratory diseases, and no allergic reactions, illnesses, or colds at the moment of the data collection. Only females were recruited due to their higher sensitivity toward emotional signals (Pause et al. 2020) and their superior sense of smell (relative to men; e.g. Brand and Millot 2001). Notably, only heterosexual participants were included because research shows that women perceive male sweat differently as a function of the donors' and their sexual orientation (e.g. ...
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Social communication refers to a basic human need, and findings accumulate that show humans communicate numerous kinds of social information via chemosignals. Briefly, it will be introduced which chemicals are conveyed through body fluids and which sensory systems are considered to process social chemosignals. Then, it will be shown that pheromones in humans have not yet been discovered. Studies on putative pheromones in humans often are performed disregarding the biological underpinnings of chemical communication and seem randomly to investigate volatile substances without any theoretical background. However, evidence will be provided that human chemosensory communication has been well demonstrated, using natural body fluids (e. g., sweat) as the source of chemosignals. Humans can decode information about the immunogenetic profile and the level of sexual hormones from volatiles released from the sweat of other individuals. These chemical signals are considered to affect mate choice. However, the signal extraction also depends on the sexual orientation of the perceiver. Furthermore, the recognition of kin and mother-infant communication comprise the release and decoding of chemosignals. Both phenomena are important prerequisites for the formation of social bonding and harm protection. Finally, the communication of stress and anxiety in humans will be presented as an example of a chemical transmission of emotional states. At the end of the chapter it will be questioned whether chemosensory communication is a skill, protective for certain mental disorders.
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Although the sense of smell is involved in numerous survival functions, the processing of body odor emitted by dangerous individuals is far from understood. The aim of the study was to explore how human fight chemosignals communicating aggression can alter brain activation related to an attentional bias and danger detection. While the anterior cingulate cortex (ACC) was seen involved in processing threat-related emotional information, danger detection and error evaluation, it still remains unknown whether human chemosignals communicating aggression can potentially modulate this activation. In the fMRI experiment, healthy male and female normosmic odor recipients (n = 18) completed a higher-order processing task (emotional Stroop task with the word categories anger, anxiety, happiness and neutral) while exposed to aggression and exercise chemosignals (collected from a different group of healthy male donors; n = 16). Our results provide first evidence that aggression chemosignals induce a time-sensitive attentional bias in chemosensory danger detection and modulate limbic system activation. During exposure to aggression chemosignals compared to exercise chemosignals, functional imaging data indicates an enhancement of thalamus, hypothalamus and insula activation (p < 0.05, FWE-corrected). Together with the thalamus, the ACC was seen activated in response to threat-related words (p < 0.001). Chemosensory priming and habituation to body odor signals is discussed.
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This article is part of a Special Issue "Chemosignals and Reproduction" Across phyla, chemosensory communication is crucial for mediating a variety of social behaviors, which form the basis for ontogenetic and phylogenetic survival. In the present paper, evidence on chemosensory communication in humans, with special reference to reproduction and survival, will be presented. First, the impact of chemosignals on human reproduction will be reviewed. Work will be presented, showing how chemosensory signals are involved in mate choice and partnership formation by communicating attractiveness and facilitating a partner selection, which is of evolutionary advantage, and furthermore providing information about the level of sexual hormones. In addition to direct effects on phylogenetic survival, chemosignals indirectly aid reproductive success by fostering harm protection. Results will be presented, showing that chemosensory communication aids the emotional bond between mother and child, which in turn motivates parental caretaking and protection, leading to infant survival. Moreover, the likelihood of group survival can be increased through the use of stress-related chemosignals. Stress-related chemosignals induce a stress-related physiology in the perceiver, thereby priming a fight-flight-response, which is necessary for an optimum adaption to environmental harm. Finally, effects of sexual orientation on chemosensory communication will be discussed in terms of their putative role in stabilizing social groups, which might indirectly provide harm protection and foster survival. An integrative model of the presented data will be introduced. In conclusion, an outlook, focusing on the involvement of chemosensory communication in human social behavior and illustrating a novel approach to the significance of chemosensory signals in human survival, will be given. Copyright © 2014 Elsevier Inc. All rights reserved.