Chemical Senses Vol. 29 No. 9 © Oxford
University Press 2004; all rights reserved
Positive Emotional Priming of Facial Affect Perception in Females is Diminished by Chemosensory Anxiety Signals
Institute of Psychology, Christian-Albrechts-University, Kiel, Germany
Correspondence to be sent to: Bettina M. Pause, Institute of Psychology, Christian-Albrechts-University, Olshausenstr. 62, 24098 Kiel, Germany. e-mail: bmpause{at}psychologie.uni-kiel.de
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Abstract |
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Chemosensory communication of anxiety is a common phenomenon in vertebrates and improves perceptual and responsive behaviour in the perceiver in order to optimize ontogenetic survival. A few rating studies reported a similar phenomenon in humans. Here, we investigated whether subliminal face perception changes in the context of chemosensory anxiety signals. Axillary sweat samples were taken from 12 males while they were waiting for an academic examination and while exercising ergometric training some days later. 16 subjects (eight females) participated in an emotional priming study, using happy, fearful and sad facial expressions as primes (11.7 ms) and neutral faces as targets (47 ms). The pooled chemosensory samples were presented before and during picture presentation (920 ms). In the context of chemosensory stimuli derived from sweat samples taken during the sport condition, subjects judged the targets significantly more positive when they were primed by a happy face than when they were primed by the negative facial expressions (P = 0.02). In the context of the chemosensory anxiety signals, the priming effect of the happy faces was diminished in females (P = 0.02), but not in males. It is discussed whether, in socially relevant ambiguous perceptual conditions, chemosensory signals have a processing advantage and dominate visual signals or whether fear signals in general have a stronger behavioural impact than positive signals.
Key words: anxiety, chemosensory communication, emotional priming, facial expression
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Introduction |
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Socially relevant emotions like aggression (Rich and Hurst, 1998
), anxiety and stress
(von Frisch, 1941), or the
reproductive state (Penn,
2002) are chemosensorily communicated in many vertebrates (see
Wyatt, 2003). These
signals evoke physiological and behavioural adaptations in the perceiver,
fostering ontogenetic and probably phylogenetic survival also (see
Hildebrand, 1995;
Schaal et al.,
2003; for a critical review on pheromones in mammals, see
Doty, 2003).
In mammals, transmission of chemosensory fear signals was first
described by
Valenta and Rigby
(1968) using a rat model. Following studies with mice indicated
that the perception of these pheromonal signals is transmitted via the
olfactory system (Rottman and Snowdon,
1972). Rodents generally respond to chemosensory signals of anxious
conspecifics with withdrawal behaviour (Carr et al., 1970;
Mackay-Sim and Laing,
1981;
Zalaquett and Thiessen,
1991): they avoid the odour source and show increased motor
activity (defensive action). However, if the odour donors are strongly
stressed, the signal receivers respond with freezing-like behaviour (defensive
immobility;
Mackay-Sim and Laing,
1981). Additionally, it has been shown that the avoidance of
chemosensory anxiety signals is reduced in those mice which were socially
isolated after weaning (Rottman and
Snowdon, 1972). The withdrawal behaviour is associated with
vegetative alterations, such as hyperthermia (Kikusui et al., 2001) and changes within
the neuropeptide and immune system (Fanselow, 1985;
Cocke et al.,
1993;
Moynihan et al.,
2000). These vegetative changes are considered to reflect the
classical stress-induced physiological adaptations (Fanselow, 1985;
Moynihan et al.,
2000;
Kikusui et al.,
2001).
So far, in humans, only a few studies examined whether emotional
states can be communicated via chemosensory signals. Performing a subjective
rating study,
Owen (1981)
investigated body odours from anxious, sexually aroused and relaxed subjects
and concluded that anxiety might contribute most to the production of
emotion-specific chemosignals.
Chen and Haviland-Jones
(2000) exposed male and female odour donors to funny and
frightening movies, collected their axillary sweat and asked male and female
participants to identify the emotions of the donors by smelling the sweat
samples. The results indicate that fear odour could be better identified than
the odour of happy people; however, this effect could only be observed when the
body odour samples were taken from males and not from females. Moreover,
females were found to show higher identification rates than males. In a third
study, only females were recruited as odour donors and as perceivers
(Ackerl et al.,
2002). Underarm sweat was sampled from women watching either a
neutral or a horror film. The odour samples taken in the anxiety condition were
judged to be more intense, less pleasant and more aggressive-like than the
samples taken in the control condition. However, they were not described as
fear-like.
The aim of the present study was to investigate whether chemical
substances, taken from subjects during the experience of high state anxiety,
modulate implicit social perception. In contrast to the aforementioned studies,
we changed two main conditions. First, we did not induce anxiety by frightening
movies. Instead, sweat samples were taken while students were waiting for their
academic examination, in order to realize an ecologically valid emotional
situation. Thereby, we expected the sweat donors to experience a high and not
only a moderate (see
Chen and Haviland-Jones,
2000;
Ackerl et al.,
2002) degree of anxiety. Similarly, we expected anxiety,
experienced during a meaningful und relevant situation, to be accompanied by
arousal (see
Bradley and Lang,
1994). An experience of arousal may be necessary in order to
initiate some behavioural effects of stress hormones (e.g. adrenocorticotropin
or cortisol;
McGaugh, 2000;
Buchanan and Lovallo,
2001). These stress hormones, in turn, are also considered to
mediate the production of alarm chemosignals in rats (Abel, 1994).
Secondly, we expected the chemosensory effects to be processed
implicitly rather than explicitly. The phenomenon that undetectable
chemosensory stimuli have significant effects on the behaviour and physiology
in humans has often been described (overview in
Köster, 2002;
Jellinek, 2003).
Highly time-sensitive measures of brain activity, such as EEG methods, could
reveal that brain activity changes during the presentation of undetectable
odours (Lorig, 1989, 2000)
and that body odours can be differentiated on a pre-attentive level (Pause et al., 1999a,b).
Additionally, undetectable putative pheromones activate specific brain regions
in humans (Sobel et al.,
1999). Finally, strong evidence for pheromonal effects in humans
has been provided by investigating nonodourous substances from the human axilla
(Stern and McClintock,
1998).
Here, we have chosen a priming task based on the perception of facial
expressions. It has been reliably documented that affective judgements can be
changed by subliminal exposure to visual primes (Kunst-Wilson and Zajonc, 1980). Consecutive
studies demonstrated that subliminally presented facial expressions
successfully serve as biologically relevant primes (Murphy and Zajonc, 1993; overview in
Öhman, 2004).
For the present study, we adopted the priming design of
Höschel and Irle
(2001).
The subjects had to judge a neutral facial expression which was preceded by subliminal presentations of emotional facial expressions. The chemosensory stimuli were presented at the threshold level and implemented as context cues for the picture presentation. As the subjects were not aware of the primed nature of their judgements, an effect of the chemosensory stimuli on these judgements would demonstrate that chemosensory anxiety signals are implicitly processed as important biological signals.
We hypothesized that such signals should affect subliminal face perception, either by strengthening the perception of fearful faces or, more generally, of negative facial expressions, or by weakening the perception of happy faces. Thus, in either case, the percentage of negative judgements should be increased in the context of chemosensory anxiety signals. The unidirectional nature of our hypotheses is based on the fact, that all studies on the effects of chemical communication of anxiety in mammals indicate that the signal receivers show a stress-typical physiology and withdrawal behaviour.
Considering the results of the study from
Chen and Haviland-Jones
(2000), we collected the sweat samples only from male students and
investigated the responses of male and female subjects separately. In order to
avoid a confound of trait and state anxiety, we excluded sweat donors who were
generally anxious. Similarly, we only investigated subjects who scored low on
social anxiety (see
Rottman and Snowdon,
1972).
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Materials and methods |
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Participants
Twenty subjects reporting no history of chronic medication, of
neurological, psychiatric, endocrine or immunological diseases, or of diseases
related to the upper respiratory tract participated voluntarily in the
experiment (due to these criteria, six subjects had to be excluded prior to the
experiment). All participating subjects had to fill in a German questionnaire
on social uncertainty (U-Fragebogen;
Ullrich and Ullrich,
1977); two females who scored 1.5 standard deviations above the
standardized mean for social anxiety (factor II) were excluded. As two further
male subjects had to be excluded (one subject could identify the control face
during the priming procedure, another subject was omitted due to technical
problems during the picture presentation), 16 subjects (eight females) remained
in the final sample and could be analysed. They had a mean age of 22.6 years
(SD = 3.0; range = 19–29 years) and four of them described
themselves as smokers. Seven females used oral contraceptives and the eighth
stated that she had a regular menstrual cycle. All participants gave written,
informed consent and were paid for participation. The study was conducted in
accordance with the declaration of Helsinki.
Sweat donors and presentation of chemosensory stimuli
Fourteen male university students agreed to donate axillary sweat
(collected on cotton pads). However, one donor was excluded because he did not
fix the pads properly and another, because he scored too high in trait-anxiety
[according to the State-Trait-Anxiety Inventory, STAI,
Laux et al.
(1981), his degree of trait anxiety was in the upper 2% of
the standard sample]. The remaining 12 donors indicated that they did not
suffer from any medical disease, especially not from a metabolic disease, nor
did they chronically use medication. They were on average 25.4 years old (SD
= 4.7, range = 20–38 years); two described themselves as
smokers. As all donors participated in the anxiety as well as in the sport
condition (see below); a possible effect of smoking on body odour was balanced
between the conditions.
The donors had to collect their sweat from both axillae for a duration of 1.5 h in two conditions (steroid stress hormones are secreted with a relatively long latency of 20–30 min; accordingly, we collected the sweat for a relatively long period). The first situation (anxiety condition) took place at the university and was an oral examination to obtain an academic degree (eight bachelor, four master examinations in psychology, medicine or pharmacology). The cotton pad was fixed while the students were waiting for their examination and removed immediately before the examination started. During the second, control condition, the donors were asked to exercise on a bicycle ergometer (three times for 10 min with a constant heart rate of 110, separated by 10 min breaks). The pads were fixed 30 min before the sport session started and removed after the 1 h long session. The control condition was carried out on average 8.5 days (SD = 6.3) after the anxiety condition; the time of day of both situations was held constant within subjects (range 0.5 h). The donors were asked to refrain from using deodorants and to wash their armpits exclusively with water 1 day before the sweat was collected. Furthermore, they were requested to refrain from eating onions, garlic or asparagus. All donors participated voluntarily and gave written, informed consent. They were paid for both donations at the end of the sport condition.
Immediately before their academic examination and during the first
break in the control condition, the subjects had to describe their emotions on
two questionnaires. First, they rated the intensity of six basic emotions (each
on a nine-point-scale, ranging from 0 to 8). Figure
1 demonstrates
that the students experienced significantly more anxiety [t(11)
= 11.1, P < 0.001] and less pleasure
[t(11) = 5.6, P < 0.001] during the first
condition than during the second one. These mean differences reflect the
observation that all subjects, without exception, experienced more anxiety and
less pleasantness in the anxiety condition. Feelings of anger, disgust, sadness
and surprise were not significantly different between both situations.
Secondly, they described their emotions on the three dimensions of valence
(happiness versus sadness), arousal (aroused versus calm) and dominance
(dominant versus submissive) on language-free, graphic nine-point scales
(Self-Assessment-Manikin, SAM;
Bradley and Lang,
1994). When waiting for their examination, they felt less happy
[t(11) = 3.6, P < 0.01], more aroused
[t(11) = 7.0, P < 0.001] and less
dominant [t(11) = 3.7, P < 0.01] than
during the ergometer exercise.
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The cotton pads were stored at –20°C. After all samples had been collected, they were homogenized and pooled according to the emotional condition. For the priming session, the pooled samples were placed into glass chambers (mean = 1.07 g cotton pad in each chamber, SD = 8 mg) of a constant flow (2*3 channel-) olfactometer (Burghart Co., Wedel, Germany; see Kobal, 2003
).
Chemosensory stimuli were presented birhinally by independent airstreams
(100 ml/s) for 920 ms each with an interstimulus interval of 13 s. The
temperature of the air flow at the exit of the olfactometer was 37°C and
the humidity >80%. White noise of 
75 dB (A) was presented
binaurally in order to prevent the participants from hearing the switching
valves. A visual sign (white cross) was presented 1.26 s before activation of
the odorous airflow and informed the subjects to start to inhale. The breathing
procedure was practised before the test commenced and was easily learnt by all
subjects. Emotional priming
Pictures of faces (24.5 x 27.0 cm) were presented on a
computer screen (19 in.) at eye level at a distance of 0.95 m. All images
are part of the Karolinska Directed Emotional Faces System (KDEF;
Lundqvist et al.,
1998) and represent standardized facial expressions of emotions,
presented by amateur actors.
The procedure was designed according to
Höschel and Irle
(2001): Task items consisted of the presentation of the prime (11.7
ms) followed by the presentation of a patterned mask (11.7 ms) and a target
(47.0 ms). The prime–mask–target sequence was presented four times,
with a free interval of 50 ms (Figure
2). Thereafter,
subjects were instructed to press either the left button of a computer mouse if
they believed they had seen a pleasant facial expression or the right button if
they believed they had seen an unpleasant facial expression. The choice had to
be made within 2 s and was accompanied by a visual presentation of a plus (to
the left) and a minus (to the right) sign on the screen. After this, the
subject’s decision was displayed on the monitor (duration = 1 s).
A break of 8.6 s (black screen) was included and 1.7 s before the next sequence
started a white cross was presented in order to indicate the next picture
presentation and to initiate inhaling. The odour was presented 1.26 s after the
appearance of the cross and 0.44 s before the image sequence started and lasted
until the sequence ended. The subjects were instructed to ignore the odours and
to attend to the valence of the facial expressions.
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Whereas the patterned mask and the target were always the same in each item, the primes varied between conditions. Images of a light-brown short-haired man served as primes and as target (Figure 2; according to a pre-test in our laboratory with 23 subjects, these images revealed best priming results.). A male face was chosen in order to be compatible to the male sweat signals. The target presented a neutral facial expression (KDEF No. AM17NES) and the primes presented a happy (KDEF No. AM17HAS), a sad (KDEF No. BM17SAS), or a fearful face (KDEF No. AM17AFS). Perceptional control items were interspersed among task items in order to control for a possible conscious perception of the primes. These control items consisted of images of a person who was clearly different from the light-brown haired male (dark- and long-haired; KDEF Nos AM01HAS, AM01SAS, AM01AFS). At the end of the experiment the subjects were asked whether they had seen a light-brown haired man only, or a light-brown haired man and additional persons, or different persons but no light-brown haired man. All but one subject stated that they had seen the light-brown haired man only, one male claimed to have also seen other people and was excluded from all further analyses (see Participants section).
Design and procedure
At the beginning of the session, normal visual acuity was assessed using a standard line test (Oculus Co., Germany). Visus was a least 83% in all subjects. Thereafter, the subjects’ ability to olfactorily detect the chemosensory samples was measured using a brief screening procedure. The participants had to discriminate the body odour from room air (three alternative task; test and control air were presented for 1 s each by the olfactometer, the presentation conditions were the same as in the priming experiment). Two trials were carried out for each chemosensory condition. Participants who failed to detect one of the body odours once were defined as non-detectors.
Afterwards, the participants were asked to subjectively judge the intensity, pleasantness, unpleasantness and familiarity of the chemosensory stimuli. Furthermore, they had to indicate whether the stimuli changed their emotional state. The quality and intensity of the participants’ emotions were assessed with the same inventories used for the odour donors (SAM scale, basic emotions questionnaire).
The priming procedure started with a practise session, introducing the picture sequences and odour administration. This practise session comprised six trials. By this protocol, it was assured that the subjects understood the task correctly and adjusted their inhaling phases as instructed.
For the main priming session, 30 trials were undertaken (see Table
1). Each prime
(facial expression of anxiety, sadness, happiness) was associated with each
chemosensory condition (anxiety or sport) four times. During six trials the
perceptional control primes were presented (each of the three facial
expressions twice in conjunction with each odour condition). The whole priming
procedure lasted 7 min. At the end of the session the subjects rated the
degree of their social anxiety on a questionnaire (U-Fragebogen;
Ullrich and Ullrich,
1977).
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Statistical analyses
It was hypothesized that the chemosensory stimuli derived from sweat samples from the sport (control) condition do not alter the general priming effect of the facial expressions. Therefore, a one-way analysis of variance (ANOVA) was performed between the three priming conditions, and within the sports condition only. This test should reveal that positive primes (facial expression of happiness) evoke more positive judgements than negative primes (facial expressions of fear or sadness).
The main hypotheses focused on the effect of the chemosensory
stimuli released by the sweat samples of the anxiety condition. However, so far
it had not been possible to predict which priming condition will be affected by
the anxiety-related samples. For example, it could be possible, that facial
expressions of fear become more distinct in the context of the chemosensory
anxiety signals or that, generally, facial expressions of negative affect
become more distinct or that facial expressions of happiness become less
distinct. Moreover, as the only study on sex-specific effects of chemosensory
anxiety communication in humans, revealed gender differences, we had to carry
out six independent tests, separated according to each sex and each priming
condition. One-tailed t-tests (see Introduction) were carried out
across the difference-values of positive judgements (%) between the
sport and the anxiety condition (As no trials were missing in either subject or
condition, the transformation from the original data to percentage data was a
simple linear transformation.) Due to the directed nature of our hypotheses, an
overall analysis (e.g. by ANOVA) was not appropriate and the a priori
t-tests were chosen (kurtosis and skewness analyses revealed that the
difference-values of the positive judgements were normally distributed in each
test). Additional analyses across the three priming conditions and within one
odour condition only were avoided, because the effectiveness of putative
chemosensory anxiety signals can only be interpreted with regard to the control
condition. A Bonferoni correction of the 
-error was calculated to
prevent coincidental significance of the six parallel tests.
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Results |
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Odour detection
Nine subjects (56.3%) could discriminate the sport odour from room air and 10 subjects (62.5%) the anxiety odour. Both detection rates did not differ significantly (McNemar test, P > 0.20). Six subjects (37.5%) were able to detect both odours. Due to this small number of subjects who had an olfactory impression of both chemosensory samples, it was abandoned to carry out statistical analyses of the body odour ratings.
Priming of facial affect perception in the context of chemosensory sweat signals
In the context of chemosensory signals of samples taken during
exercise (control condition) the target faces were judged to be more positive
when they were primed by the presentation of a happy face, than in the negative
priming conditions with sad and fearful faces [F(1,30) =
4.22, P = 0.02, power (related to an -error of
5%) = 0.70; see Figure
3]. Single
comparisons revealed that the degree of different responses between the
positive and the sad priming condition [t(15) = 2.88,
P = 0.01] was similar to the degree of different responses
between the positive and the fear priming condition [t(15)
= 2.54, P = 0.02]. Targets primed with sad or
fearful faces were judged to be equally negative [t(15) =
0.43, P > 0.20].
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In the context of chemosensory signals of samples taken during a state of high anxiety, females judged targets primed with happy faces significantly less positive than in the control (sport) condition [t(7) = 3.74, P (
, corr.) = 0.02,
power (related to an -error of 5%) = 0.95; see Table
2]. However,
the chemosensory stimuli from the anxiety sweat did not change the negative
judgements of targets primed with sad or fearful faces. Face perception in
males did not change with the condition of sweat collection.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
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The present study could demonstrate that in females, positive priming of face perception is diminished in the context of chemosignals derived from sweat samples taken during a high state of anxiety. Basically, one could interpret the effect in the opposite direction and argue that the happy prime generally only works in the context of chemical signals of sweat sampled during a sport condition, whereas the chemosensory anxiety signals might have no effect. However, this argument is highly unlikely for two reasons: First, the visual priming paradigm has been established in a number of laboratories and yields robust priming effects of facial expressions (Murphy and Zajonc, 1993
;
Höschel and Irle,
2001;
Öhman, 2004).
Moreover, we used pictures from a standardized system (Lundqvist et al., 1998) and our
pre-tests confirmed the effectiveness of the primes. Second, to our knowledge
there are neither animal data nor theoretical assumptions on the communicative
function of chemicals derived from exercise sweat. On the other hand, the
communication of anxiety (stress) has been well documented in many vertebrate
species (see
Wyatt, 2003).
Summarizing, all empirical and theoretical evidence we are aware of, supports
the conclusion, that the reported effect is due to the effectiveness of
chemosensory anxiety signals. Chemosensory anxiety signals do not change the perception of negative facial expressions (sadness, fear). Thus, if negative emotional information is transmitted simultaneously via chemosensory and visual cues, chemosensory signals of anxiety do not seem to deliver additional salient information. It seems most probable that the percentage of negative responses reached a ceiling-level, which could not be changed in the context of additional negative social chemosignals.
However, if the two sensory channels deliver incompatible information
(happiness and anxiety) the anxiety-related information seems to dominate
stimulus processing. In general, it could be possible that either chemosensory
signals are behaviourally more relevant in perceptual conditions delivering
contrary multimodal social information, or that information related to a threat
has a processing advantage compared to neutral or positive information.
Chemosensory olfactory information is transmitted via the olfactory bulb
directly to the medial and cortical amygdala (see
Carmichael et al.,
1994;
Otto et al.,
2000). Brain imaging studies revealed that the human amygdala is
activated during odour perception (Savic et al., 2000;
Poellinger et al.,
2001), especially if the odours have a negative emotional valence
(Zald and Pardo, 1997), or
if they are emotionally salient and intense (Anderson et al., 2003). Studies
investigating the role of the amygdala in behavioural control showed that it is
responsible for implicit immediate behavioural adaptations in emotionally
meaningful situations (LeDoux,
2002). Therefore, the intrinsic connection between the olfactory
bulb and the amygdala could explain the processing advantage of chemosensory
olfactory information in brain structures responsible for the automatic
initiation of behavioural responses (see
Pause et al.,
2003). However, there is evidence that the human amygdala also
processes auditory and visual social fear signals (Adolphs et al., 1994;
Morris et al.,
1996;
Scott et al.,
1997). Even subliminal presentations of facial expressions of fear
result in amygdala activations (Whalen
et al., 1998). Thus, fear signals of either modality could
have an processing advantage, because they may initiate reflexive motor and
physiological responses via the amygdala, independent of neocortical control
(Armony and LeDoux,
2000).
The effectiveness of chemosensory anxiety signals reversing the
priming effect of happy faces could be demonstrated exclusively in females.
This result is in accordance with the study from
Chen and Haviland-Jones
(2000), who concluded that females can identify the emotional state
of body odour donors better than males (however, in contrast to Chen and
Haviland-Jones, we presented chemosensory substances from male donors only and
can not rule out the possibility that males respond to emotional chemosignals
collected from females). In line with the results of the present study, some
studies indicate that odour perception in females is better than male odour
perception (e.g.
Yousem et al.,
1999). Moreover, it has recently been reported that the processing
of visual emotional information activates different brain areas in males and
females and that these differences are most prominent for negatively valenced
stimuli (Lee et al.,
2002;
Wrase et al.,
2003). As females responded with stronger brain activations to sad
faces and emotionally negative pictures,
Wrase et al.
(2003) concluded that females may be more sensitive to aversive
material in general. Thus, the observation that chemosensory anxiety signals
affected females, but not males, could be due to a higher olfactory sensitivity
or to a higher sensitivity to negative emotional situations in females.
The sweat donors participating in the present study described
themselves as highly anxious, while waiting for their examination (anxiety
condition). This contrasts with the medium level of anxiety of the subjects
viewing anxiety-evoking movies (Chen
and Haviland-Jones, 2000;
Ackerl et al.,
2002). Moreover, the self-ratings suggest that all other basic
feelings (pleasure, anger, sadness, disgust, surprise) were experienced at a
very low level. Such an emotion-specific state during sweat sampling was not
assessed by
Chen and Haviland-Jones
(2000) or by
Ackerl et al.
(2002). However, the donors also described themselves as being less
dominant, and more aroused in the anxiety condition. Low dominance and high
arousal might be intrinsically connected to ecologically valid anxiety
conditions. An effect of arousal on the intensity of the sweat odours is
unlikely because the olfactory detection rate for the pooled sweat samples was
similar for both conditions. Moreover, the presentation of the chemosensory
anxiety signals did not generally change the response behaviour to the primed
facial expressions, but the effect was specific for the reversal of positive
priming. This emotion-specific result strongly supports the conclusion that the
chemosensory signals delivered anxiety related rather than arousal related
information. However, in further studies, the arousal of the odour donors
between different emotional conditions should be comparable. In our study, the
lower arousal in the sport condition could be due to the fact that the ratings
were taken during the first break (after 10 min of exercising) and not at the
end of the sport condition (after 30 min of exercising).
So far, the mechanisms responsible for the production of emotional
chemosignals remain speculative. Whereas traditionally it has been considered
that emotional sweat is produced by apocrine glands (Boucsein, 1992), recent studies indicate that
apoeccrine glands also contribute to the hedonic profile of body odour
(Heckmann et al.,
2003). The production of emotional sweat in humans seems to be
controlled by limbic brain areas, especially the amygdala (Asahina et al., 2003).
Furthermore, studies in rodents suggest that the release of chemosensory
anxiety signals is related to the activity of the
hypothalamus–pituitary–adrenal system (Mackay-Sim and Laing, 1981;
Abel, 1994).
Even though the mediating systems in the production and perception of
emotional chemosignals are not yet fully understood, we conclude that the
results reported here strongly indicate that anxiety in humans can be
chemosensorily communicated. Like in many other taxa of social animals, the
release of alarm pheromones seems to be evolutionarily advantageous. The
induction of a fright response (alertness associated with defensive action) in
vertebrates (von Frisch,
1941) and mammals (Carr
et al., 1970;
Mackay-Sim and Laing,
1981;
Zalaquett and Thiessen,
1991) is obviously beneficial for the receiver as well as for the
species, in socially living animals. As the benefit for the signaller is less
obvious, the evolution of the specific response might be secondary to
substances which are general products of fighting of injured animals
(Wyatt, 2003).
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Acknowledgements |
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The authors greatly acknowledge the technical assistance of Dipl.-Phys. Bernfried Sojka during data acquisition. The study was supported by a grant from the German Research Foundation (DFG) to B.M.P. and R.F. (PA 937 1-1).
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Accepted September 22, 2004
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