2013

NPC Natural Product Communications Vol. 8

No. 11
Human Body Scents: Do they Influence our Behavior? 1651 - 1662
Sophie Mildner and Gerhard Buchbauer*

Department of Clinical Pharmacy and Diagnostics, University of Vienna, A-1090 Vienna, Austria

gerhard.buchbauer@univie.ac.at

Received: June 6th, 2013; Accepted: August 19th, 2013

Pheromonal communication in the animal world has been of great research interest for a long time. While extraordinary discoveries in this field have been
made, the importance of the human sense of smell was of far lower interest. Humans are seen as poor smellers and therefore research about human olfaction
remains quite sparse compared with other animals. Nevertheless amazing achievements have been made during the past 15 years. This is a collection of
available data on this topic and a controversial discussion on the role of putative human pheromones in our modern way of living. While the focus was
definitely put on behavioral changes evoked by putative human pheromones this article also includes other important aspects such as the possible existence of a
human vomeronasal organ. If pheromones do have an influence on human behavior there has to be a receptor organ. How are human body scents secreted and
turned into odorous substances? And how can con-specifics detect those very odors and transmit them to the brain? Apart from that the most likely candidates
for human pheromones are taken on account and their impact on human behavior is shown in various detail.

Keywords: Human pheromones, Sex, Behavior, Chemosignals, MHC, HLA, Mate choice, Mood, Body scents.

Social signals spread with the individual’s body odor, so called
pheromones, transmit a wide range of information. While
chemosensory-based communication is commonly known as a vital
signaling tool in many species, the importance of the human sense
of smell has by far been underestimated.
The term “pheromone” derives from the Greek words “pherein” and
“horman” – to transfer and to excite. Karlson and Luscher first
introduced pheromones as hormone like substances that are yet very
different: They are being secreted outside the body in order to serve
communication between conspecifics rather than being secreted into
the blood for humoral correlation [1].
Wilson et al. [2] defined the existence of two pheromone classes.
“Signal or releaser pheromones” have short term effects on
behavior and function as attractants and repellents while “primer
pheromones” produce a more enduring impact on the receiver’s
physiology via the hypothalamic-pituitary-adrenal activation.
Signal, releaser and primer pheromones might be the only main
mammalian pheromones, whereas the others are often restricted to
invertebrates. These can be categorized in “aggregation
pheromones, alarm pheromones, epideictic pheromones, territorial
pheromones, trail pheromones, information pheromones and mating
pheromones” [3-9].
The increasing knowledge about pheromones in many different
species has led researchers to question the human world of odors.
Unfolding the hidden mysteries of smells and the way they are
transmitted as well as perceived in humans means to face some
critical questions. Humans do not fall instinctively into behaviors in
response to an odor, and their sexual activity is not limited to the
moment of ovulation as it is in most other animals. This brings up
the necessity to differentiate learned associative responses from
instinctive responses to putative pheromones. To work out a
separating line between these two in experimentally controlled
studies seems to be nearly impossible as humans are thinking
individuals with the power of judgment and self-assessment.
Moreover, studies in a laboratory environment might not truthfully
reflect what is happening in real life as most of human behavior
seems to be highly context specific.
Human olfaction was long underestimated as humans are believed
to be microsmatic (poor smellers), while featuring highly developed
powers of vision [10]. Certainly visual and verbal cues are of utter
importance in human communication, especially at a distance.
However, between closely connected individuals, smells also play
an important role, for example between mothers and infants and for
a variety of sociosexual behaviors.
The human’s main odor-producing organ is the skin with its
apocrine glands. These are located all over the body surface, but
have a far higher concentration in some areas: the axillae, the
nipples, the pubic, circumoral, genital and circumanal regions, as
well as eyelids and outer ear. The intensive hair growth in the
axillae and the genital regions enables the odor to be spread by
evaporation over a large surface. The axillae are also well situated
in order to bring the individuals body odor as close as possible to
the nose of other conspecifics. The warmth of those body parts also
helps the circulation of odors and produces a perfect climate for
bacterial activity: Coryneform bacteria transform the odorless
androstadienol and androstadienone into the odorous 5α-
androstenone [11-13].
Tirindelli et al. [14] summarized the fact that most mammals have a
main olfactory system as well as an accessory olfactory system, the
vomeronasal organ (VNO). In contrast to earlier interpretations,
both are actively involved in pheromonal communication.
Therefore, a functional VNO is of utmost importance for
communication purposes of many animals and insects.
According to this knowledge the question derives how putative
pheromones are processed in humans. In humans, an anatomically
similar structure to the VNO is situated in the anterior third of the
nasal septum, approximately 1 cm dorsal to the columella and 1 mm
above the floor of the nose [15]. The size of these pits ranges from
~1mm to ~2.5 mm [16] and shows up as a duct-like invagination of
the epithelium. It is surrounded by numerous exocrine glands with
short ducts. The fine structure of these glands suggests a serous
secretion. In the depth of the invagination, pseudostratified
columnar epithelial cells are seen that have plump processes,
kinocilia and microvilli at the apical cell membrane [17].
1652 Natural Product Communications Vol. 8 (11) 2013
This structure is unique in its morphology and definitely different
from the VNO found in other species. Various researchers tried to
estimate the percentage of humans expressing VN pits at all. The
overall results showed a huge variety depending on the method used
to detect the VNO. Bhatnagar et al. [18] proved that serial histology
is the only proper way to identify the VNO. Some false results may
be explained as well through misidentification of the nasopalatine
duct [19] or fossa [18] for the VN pit.
Probably the most representative study in this context was
conducted by Trotier et al. [16]. They aimed to obtain a good
estimation of the percentage of human VNO by using a really large
population. Based on a very carefully conducted study setting,
13.2% of the examined individuals showed a pit on each side of the
septum, 13.4% had a pit only on the left and 12.4% of the subjects
had a pit only on the right side. In summary, 39% of the human
population has at least one well-defined vomeronasal pit [16].
Knecht et al. [20] found similar evidence and also showed that
expression of a VNO is not age or gender dependent.
However, although the vomeronasal organ is found, it is still not
sure whether or not the VNO has a function in humans. Foltan and
Sedy [21], for example, are one of the very few research groups that
postulate a functional VNO in humans. They provided no data to
support their hypothesis and wrongly cited articles. They present
rodent data when speaking about the human VNO and do not
mention research articles that suggest that the adult human VNO is
non-functional.
Monti-Bloch et al. and Monti-Bloch and Grosser [22,23] showed
that stimulation of the VNO with the putative human pheromone
androstadienone evoked a voltage change in terms of negative
potentials. This finding led the researchers to the conclusion that the
VNO is functional in adults. However, in this case, vomeronasal
receptor neurons and nerve bundles as a neuronal connection with
the brain should be detectable.
Olfactory marker protein (OMP) is a reliable detector for
functioning olfactory neurons as it can be found in mature neurons
of the olfactory epithelium [24,25] and in the functional
vomeronasal organ of other species [26,27]. Takami et al. [28] were
unable to find OMP in the human VNO. Trotier et al. [16] used
anti-OMP in order to detect OMP. This antibody against the
olfactory marker protein failed to stain any VNO cells of humans,
suggesting that chemosensory vomeronasal neurons are not present.
Instead, most vomeronasal epithelium cells express keratin proteins,
a marker of epithelial cells that is not expressed by olfactory
neurons. [16]
Vomeronasal nerve bundles do not seem to exist either, as protein
S-100 (expressed in Schwann cells) could not be detected by the use
of antibodies [15,29]. Recently, important compounds for VNO
sensory transduction, such as the V1R, V2R and V3R receptors
[30,31], and the ion channel TRPC2 have been identified [32-34].
The presence of TRPC2 channels is shown to be essential for a
functioning VNO [35,36]. Similarly, mice that are deficient in
expressing V1R genes develop serious behavior problems due to the
loss of VNO function [37]. They fail to defend themselves and their
offspring against intruder males and TRPC2 mutant males
vigorously accost other mice, disregarding their gender.
Interestingly, the TRPC2 gene and the vast majority of V1R, V2R,
and V3R genes are pseudogenized in humans [35,38-41]. In order
for messages to be sent from the vomeronasal receptor cells to the
brain, neurons would need to build a connection to an accessory
olfactory bulb. However, such a bulb is absent in humans [29,42].
This loss of VNO signaling components leads to the belief that the
Mildner & Buchbauer
VNO is vestigial. Nevertheless, the notion of a non- functional
VNO does not explicitly exclude that humans communicate through
pheromones. It might only be evidence that humans are using a
different olfactory structure than other animals. Even though the
accessory olfactory bulb is not present in adult humans it can be
found in fetuses of different gestation stages (8, 18 and 26 weeks)
[42-44]. Afterwards, however, the bulb regresses leaving a vestige
behind [42].
The VNO does not seem to have a function in later life, but it surely
plays an important role for the migration of GnRH-secreting cells
towards the hypothalamus. Just like in other mammals, nerve fibers
emerge embryonically from the developing organ to the brain [45]
as specific cells can be detected in the bilateral vomeronasal organs
of 8-12 weeks old fetuses [46]. This is an essential step for gonad
function after puberty which totally depends on hormonal secretion.
In people with Kallmann's syndrome (a genetic endocrine disorder)
for example the migration does not take place, which leads to no
secretion of hypothalamic GnRH [47] and, therefore, to
hypogonadism. People with Kallmann's syndrome might not even
respond to putative human pheromones at all [10] and are most
often anosmic.
However, after the initial step of GnRH-secreting cell migration, the
neuronal connections disappear and the organ regresses: No
neuronal connections are found between the VNO and the brain
after week 32 in gestation [16,29,42], whereas between weeks 8 and
14.5 the VNO appeared to increase in complexity [48]. According
to all the evidence listed earlier it would be quite surprising if the
VNO could be stimulated by putative human pheromones such as
estratetraenol, androstadienone and androstenone.
In the past couple of years several meaningful studies were
conducted. The idea behind them seems to be logical: If the VNO is
a functional organ, the perception of putative human pheromones
should be altered when the VNO is manipulated. Knecht et al. [49],
for example, measured sensitivity towards androstenone and tried to
figure out whether there was a difference in olfactory function when
the VNO was occluded or not. Interestingly, subjects with occluded
VNO showed no difference when stimulated with androstenone. In
the same study setting, Knecht et al. found that subjects without
detectable VNO did not show different olfactory sensitivity towards
androstenone compared with their counterparts with a VNO.
However, androstenone is not generally accepted to be a human
pheromone, whereas androstadienone (AND) is supposed to be the
most likely candidate for such a chemosignal [50]. Frasnelli et al.
[51] therefore stimulated different subjects with androstadienone
and discovered that functional occlusion of the VNO neither altered
the perception of AND nor changed the patterns of brain activation .
Another approach was to test patients that suffered from severe
nasal polyposis. As odors can no longer reach the olfactory cleft,
those people are anosmic. However, this should not affect the
function of the more distally located VNO as long as the VNO is
considered as functional. When Savic et al. [52] confronted healthy
subjects with estreatetraenol (EST), it typically activated the
hypothalamus. Such an effect could not be observed in the patient
group. All this different evidence strongly indicates that the VNO is
not a functional organ in humans but only vestigial. This knowledge
does not conflict with the idea that pheromones do indeed play a
role in human life, but it leaves the question of which sense organ is
actually capable of transmitting the olfactory information to the
brain. Just like the VNO, the Grüneberg ganglion has been detected
only in fetuses and regresses during gestation [53]. Therefore, the
only sensory channel that would possibly allow pheromone
Human Body Scents
detection seems to be the main olfactory system itself [51,52]. The
finding of the V1RL1 vomeronasal receptor in human olfactory
mucosa may support this hypothesis [54] as it shows that the
humans accessory olfactory system has most likely been integrated
into the main olfactory system [54].
Nevertheless, common odors are processed differently from
putative pheromones. Common odors “engage only the olfactory
brain (amygdala, orbitofrontal and insular cortex)” [55], while
pheromones activate the anterior hypothalamus. Yet the reception
mechanism of putative pheromones and their detailed transmission
to the central nervous system remain unclear. Therefore, more
studies are needed to shed light on the role of the main olfactory
system in human pheromone sensation.
Pheromones are known to specify the species and sex of a being,
but the body scent also marks an individual member of a species
with a unique coding [56]. From where does this individual body
scent derive? The major histocompatibility complex (MHC) seems
to be genuinely involved. The MHC is a very diverse cluster of
genes (see also [57]) that occurs on the cell surface. Its main task is
the coding for proteins and, to a lesser extent, the processing and
presentation of antigens. The increased genetic diversity is
associated with a better immune system and, consequently,
enhances the offspring’s health and fitness advantages. Therefore,
the MHC is well known for immune recognition of “self” and “non-
self” and is also linked to transplantation rejection [58,59].
Conflicting results have been reported as to whether humans are
actively trying to avoid homogeneity in MHC or not. They find
individuals attractive or unattractive in ways that are somewhat
correlated with underlying differences or similarity in MHC
genotype, and this might lead unconsciously to mating that
produces heterogeneous offspring. Thus, it only seems as if MHC
related mate choice does indeed influence some human populations
but not all of them. In a study that involved 200 couples from South
Amerindian tribes no evidence for avoidance of MCH similarity
was found [60]. The results were comparable with those of random
mating. However, Ober et al. [61] took a look at Hutterites, a small
genetically isolated religious sect nowadays located in North
America. They scanned 411 couples for HLA types and found
remarkably fewer HLA matches among partners than would be
expected by chance alone. European American couples also showed
more MHC-dissimilarity than random spouses [62]. Such
congruence cannot be explained by demographic processes, but
leads to the hypothesis of disassortive mating.
But how is it possible that humans unconsciously mate with MHC
dissimilar partners? This brings us back to the initially proposed
main function of the MHC: The immune system and, as an
incidental byproduct, also the body scent. Some studies lead to the
belief that MHC-based olfactory signaling does take place [63] and
it is assumed that during cellular turnover MHC gene fragments are
being excreted, together with body fluids [54]. This process
obviously maintains the unique individual body odor.
Several different study settings were conducted between 1980 and
2009 [for example, 64-67], with rather interesting discoveries about
human olfaction and MHC involvement. Though Schleidt and
Schleidt et al. [68,69] did not study directly MHC, they found that
individuals were able to identify their own odor as well as the ones
of their closest relatives by smelling axillary odor. They could even
distinguish between the two sexes. Other experimenters showed that
parents could differ between the different odors of their own
children, which shows that body scents allow authentic kin
recognition, even among humans [70].
Natural Product Communications Vol. 8 (11) 2013 1653
Later, Wedekind et al. [71] focused his interest on putative MHC-
dependent mate preferences in humans. Several male students were
asked to wear the same T-shirt for a couple of nights without using
any additional odorants like soap or deodorant. Afterwards a group
of female students rated the odors of these T-Shirts for pleasantness.
They scored the T-shirts of men with fewer MHC genes in common
as more pleasant than the ones that were more MHC similar. This
effect did not occur once the women took the contraceptive pill. In
another study setting, Wedekind and Furi [72] made men and
women score the pleasantness of T-shirt odors and came to the
same conclusion. The unpleasantness was linked to the degree of
MHC similarity between smeller and wearer as long as the women
did not use oral contraceptives. The subjects also were reminded of
their own partner’s odor when smelling a dissimilar MHC-type,
which leads to the suggestion that also in real life they
unconsciously go for disassortive mating.
In another sweaty T-shirt experiment, however, males and females
were chosen from different ethnicities. Here, females preferred
paternally matching HLA-associated odors to those that showed
fewer matches to their own [58]. The lack of congruence in the
research results shows that MHC-dependent mate choice in humans
still needs deeper consideration. Yet there is one aspect that
scientists agree about: Women are better in naming ability rather
than olfactory acuity than men [73-75]. However, such detection
abilities are rather non sex-dependent and this does not mean that
men do not have a good sense of smell. One interesting aspect is
that men are more attracted to the smell of female bodies during
certain times of a woman’s menstrual cycle.
For sexual reproduction and fertilization purposes the women’s
body goes through periodical and physiological changes. Led by the
endocrine systems, three different phases occur: the follicular phase,
the ovulation and the luteal phase. There are many interesting facts
showing that the female menstrual cycle is closely linked to human
body scents. For example, the timing, as well as the length, can be
modulated only by perceiving the right odors. Already in 1971
McClintock [76] showed that the menstrual cycles of young women
living together tend to synchronize. Over the years different studies
have proven this finding, as well as in close friends and/or room-
mates [77-79], co-workers [80,81] and female members of Bedouin
families [82].
Consequently women who spend a lot of time together are shown to
experience menstrual synchrony. However, it does not explain
whether this effect is due to similar environmental stimuli or if it
really derives from a pheromonal influence. Therefore, some studies
were conducted without social contact of the subjects. Only female
axillary extracts were applied to the nose of other women for a
certain period. The recipients experienced a time shift of their
menstrual onset according to the donor’s one. [83,84] These
underarm compounds either delay or accelerate the luteinizing-
hormone surge of the recipient women [85] and are also able to
speed up the pulsatile frequency of luteinizing hormone. [86]
However, this is not the only pheromonal influence on the
menstrual cycle. Beside the synchronization, Jacob et al. [87] were
able to observe the exact counter effect. They collected the body
odor of breastfeeding women by making them wear a pad between
underarm and breast. These breastfeeding compounds then
disrupted the cyclicity of nulliparous women and increased the
variability of ovarian cycles. In addition to that finding, sexual
motivation (desire and fantasies) of non-lactating women were
increased by the body odor of breastfeeding women [88].
Those were only effects of female body scents, but also men’s
pheromones lead to alteration of the ovarian cycle. Cutler et al. [89]
1654 Natural Product Communications Vol. 8 (11) 2013
chose women with unusual cycle length and were able to show that
their cycles became more regular when they were exposed to male
underarm compounds over a certain period. Just like female axillary
odor, men’s underarm compounds also affected the pulsing of
luteinizing hormone [90]. Another effect of men’s hormones on
female bodies might be that girls who grow up in single-mother
homes experience later puberty than the ones that grow up with a
stepfather [91]. The women’s menstrual cycle in relation to human
pheromones plays a major role on women. Not only the timing of
the menstrual cycle is being addressed by body scents, but also the
female ability to smell, their mood, and the perception of men’s
attractiveness are dependent on the different phases of the menstrual
cycle.
Morofushi et al. [79] found that the synchronization of women’s
ovarian cycle is linked to the ability to smell androstenol. Women
who have a higher detection threshold for androstenol are most
likely not synchronizing their menstrual cycle with other female
subjects, while synchronized women can detect androstenol also in
rather low quantities. In the context of smell sensitivity, another
finding is highly interesting: Women’s smell sensitivity towards the
male pheromone androstenone varies throughout the different
menstrual cycle phases. It reaches its highest peak at the moment of
ovulation as long as no contraceptive pill is being used [92]. When
conception is most likely, women’s emotional perception of
androstenone is triggered in order for it to appear more pleasant
[93,94]. More recently, Watanabe et al. [95] wanted to verify the
previous findings. As a marker, they used the “olfactory contrast”,
which is defined “as a slope of the dose-response relation and,
therefore, provides recognition ability for the changed intensity of
odorant”. According to Watanabe et al. [95], the olfactory contrast
was significantly increased during ovulation.
It is well known that attractiveness and facial symmetry are
important criteria for human mate choice. Men with more
symmetrical faces are supposed to be physically fitter and show
fewer signs of depression and anxiety [96,97]. They also have more
sexual partners than their asymmetrical counterparts [98]. Several
researchers dared to ask whether human body odor might be linked
to mate quality in any way. Rikowski and Grammer [99] measured
the facial symmetry of 16 male and 19 female subjects. The women
did not use oral contraceptives and were all in different phases of
their menstrual cycle. The subjects were requested to wear the same
T-shirts for two nights in a row and afterwards rate photographs of
the opposite sex and their corresponding T-shirts for attractiveness
and pleasantness. One positive correlation was found: Women who
were in the most fertile phase of their menstrual cycle judged the
odor of symmetrical men as more pleasant than that of the
asymmetrical ones.
Gangestad and Thornhill [100] conducted a similar study. Fifty-two
women rated the odor of 41 men’s T-shirts. Women at a low fertile
moment within their menstrual cycle, as well as contraceptive pill
users, showed no preference for any of the men’s odors. However,
high fertility women once more rated “symmetrical-face-odor” as
more pleasant. One year later, Thornhill and Gangestad [101]
conducted another study even more carefully. They took a larger
sample (80 men and 82 women) and made sure they controlled
various factors that were not taken into account in the previous
study. Again they came to the same results, therefore suggesting
that “the scent of symmetry” may be an additional index for male
mate quality. Non-verbal behavior traits might also belong to such
indices. Most recently Roberts et al. [102] revealed that “the
attractiveness of male non-verbal behavior is predicted by perceived
quality of their body odor”.
Mildner & Buchbauer
The odor of dominant men is also preferred by non-single women
during ovulation. Havlicek et al. [103] asked 48 male students to fill
in a questionnaire on dominance and collected axillary odor
samples from them. Afterwards they questioned women for their
odor preferences and tried to find correlations between odor
pleasantness and male dominance. Such correlation was found for
non-single women during their fertile phase, but not for non-
ovulatory or single women. Even if men do not experience a
rhythmic change in their hormonal status like women, they are still
being affected by human body scents. Berliner et al. [104] found
out that putative pheromones change the pulsatile frequency of
luteinizing hormone in men too. Even the so called copulins of the
female vagina were shown to have an impact on men [10]: The fatty
acids stimulate male androgen secretion and have a positive impact
on men’s rating of female photographs.
The above mentioned phenomenon of women preferring men’s odor
at the time of ovulation is closely linked to the fact that men also
find the scent of an ovulatory women more pleasant than during
other phases of the menstrual cycle [105,106]. Even though the
moment of ovulation is not perceived consciously by humans [10]
this shows clearly that olfaction plays an unconscious role in
properly timed reproduction. Chemosignals are able to trigger
men’s and women’s need for sexual intercourse in a way that
remained unnoticed for a long time. Nevertheless, human’s sexual
activity is more complex and not only limited to the moment of
ovulation. Therefore, it is sure that many different aspects play
together in this issue.
When Martha McClintock [76] in the 1970s started her research
about the influence of body scents on the female menstrual cycle it
was not certain whether human pheromones exist or not. The more
recent papers cited above show clearly that such chemosignals do
indeed play a role in human’s life. However, what are the
substances that can be seen as pheromones? It is likely that
pheromones have evolved from hormones [107]. Hormones are
biochemical messengers that are being produced by special donor
cells and transported via the bloodstream towards their receiver
cells in order to create a highly specific effect. One particular
hormone family is the sex hormones, chemically seen as sex
steroids. Several derivatives of these sex steroids are the most likely
candidates for human pheromones and, therefore, it is necessary to
take a closer look, especially at androstadienone, androstenone,
estratetraenol and androstenol.
Androstadienone (4,16-androstadien-3-one) is an androstene found
mainly in men’s axillary secretion. The concentration in female
axillae is 20 times lower than in those of men. Androstadienone
detection was shown to be experience dependent [108]. When
subjects are repetitively exposed to the odor of androstadienone
they show an increase in sensitivity [109], with a decreasing
threshold, as well as changes in the way they perceive the odor
[110,111]. While the threshold is still low, the smell is pleasantly
described as floral, minty and fruity [107], but, with rising
sensitivity, it changes to urine, musky and unpleasant [112,113].
Such an increase in odor sensitivity is very exceptional as usually
habituation or generalization would take place.
Jacob et al. [108] have tried to explain this phenomenon through the
existence of two different odor channels. One pleasant channel with
low-affinity receptors and one unpleasant channel represented by
high-affinity receptors. With increasing sensitivity the high-affinity
channel is activated at thresholds far below the ones necessary for
the channel with pleasant odor-qualities. That would explain why
the odor quality becomes putrid. Savic et al. [55] came up with an
even broader hypothesis: They suggest the existence of a separate
Human Body Scents
neuronal olfactory pathway. Also Lundström et al. [50] believed
this was the only possible explanation to the fact that
androstadienone elicits between 13% and 20% faster than
chemically similar control odorants. This finding cannot merely be
explained by learned responses or by different odor perception.
Schild and Restrepo [114] showed that the mucus transfer of
chemically different odor types can lead to variable processing
times. However, Lundström et al. choose chemically very similar
odors. The hypothesis that less pleasant chemosignals are processed
faster [115] cannot shed light on this question either as
androstadienone should then elicit slower than its control substances
and not faster. Therefore, Lundström et al. claim the existence of a
neuronal subsystem for androstadienone, as was found in Old-
World monkeys [116].
Another plausible explanation not mentioned by Lundström et al.
might be adaptation towards environmental stimuli [117]. The odor
of androstadienone might be of such high relevance for humans that
it is processed faster than stimuli of less importance. Gottfried [118]
emphasizes the importance of learning and experience in human
olfactory perception. Olfactory-learning has a modulatory effect on
our odor perception, even though it is surely different from learning
in other contexts. Very recent research validated this suggestion.
Women who already had sexual experience with one or more
partners rated the smell of androstenone as more pleasant than
women who had had no sexual contact [110].
Androstenone (5α-androst-16-en-3-one) can also be found in
humans. It is a known pheromone in boars which leads females to
acceptance behavior towards males and is supposed to have
important effects on human behavior too [119]. Just as people can
increase their sensitivity towards androstadienone, the same effect
was proved for androstenone [120].
Estratetraenol (1,3,5(10),16-estratetraen-3-ol) is another possible
candidate for human pheromones and shows a similar structure to
estrogens. It can be found in female urine. Jacob et al. [121]
conducted a double-blind, repeated-measures experiment and found
that estratetraenol has an influence on men: It raises skin
temperature and increases skin conductance.
Another steroid, androstenol (5α-16-androsten-3α-ol), is also
regularly mentioned in the discussions about human pheromones.
Ebster and Kirk-Smith [122], for example, showed that men’s
product choice can be manipulated by androstenol. They rated male
magazines as better and more masculine when exposed to the
putative pheromone.
This little excursus of the sex steroids of the human body shows
clearly that those compounds are unlike the vast majority of odors
and smells. However, what makes them become so different?
Future studies should try to address this very issue more deeply.
Several studies have looked not at behavioral effects but at
physiological changes of human pheromones and have come to
remarkable results. Very recently, Marazziti et al. [123] suggested
that “the application of male axillary extracts to women may modify
the affinity of their platelet 5-HT transporter”. Van Toller [124]
reported an increase of skin conductance when subjects were
exposed to androstenone. Androstadienone and estratetraenol also
increase skin conductance and they both raise skin temperature in
men while lowering it in women [121]. Wyart et al. [125] showed
that androstadienone influences the endocrine state of women as it
leads to an increase in cortisol levels, while Berliner et al. [104]
observed changes in respiratory rate and cardiac frequency.
Natural Product Communications Vol. 8 (11) 2013 1655
As mentioned before, pheromones and common odors activate
different regions of the brain. Human pheromones activate the
hypothalamus in both men and women, but there are slight
differences: The center of activation in females is the preoptic and
ventromedial hypothalamus while men’s activation focuses on the
paraventricular and dorsomedial part [126]. Those are areas that are
associated with olfaction as well as with sexual behavior, emotions,
social skills and the ability of being focused [127,128].
In contrast to the described effect, more recent studies came to a
different interpretation. The hypothalamic activation does not only
depend on gender, but mainly on the subject’s sexual orientation
[129]. The sexual identity and orientation of a person is an
individual pattern dependant on the attraction to the opposite
gender, the same gender or both sexes referred to as heterosexuality,
homosexuality or bisexuality. But how does sexual orientation
manifest itself in an individual? Some experiments in context with
human pheromones are able to answer some striking questions.
When stimulated with androstadienone, homosexual men showed
the same brain activation as heterosexual women rather than
heterosexual men [55], even though they used the same processing
as heterosexual men when exposed to common odors. As described
above, heterosexual women process androstadienone via the
anterior hypothalamus. Lesbian women, however, do not share this
profile, but use the main olfactory system instead [130].
Furthermore, homosexual women are processing estratetraenol just
like heterosexual men.
Savic et al. [131] managed to prove later on that these findings
cannot be explained by learned responses but by neurobiological
discoveries. They used positron emission tomography and magnetic
resonance imaging in order to show “sex-atypical cerebral
asymmetry and functional connections in homosexual subjects”
[132]. In summary, homosexual men share similar brain activity
with heterosexual women and homosexual women have more in
common with heterosexual men. Homosexual men and heterosexual
women do not only have the same hypothalamus activity when
stimulated with human pheromones. They also have a high affinity
for the odor of androstenone. Pause [107] sprayed seats with
androstenone and showed that heterosexual men tried to avoid those
impregnated chairs, while heterosexual women and homosexual
men were actively looking for them.
Most recently Lübke et al. [130] once again put their focus on
olfaction related brain processing and found that body scents also
carry information about a person being a potential partner.
Homosexual and heterosexual subjects consistently showed shorter
P2 (a component of brain evoked response potential) latencies when
smelling the odors of their sexually preferred gender, while they
showed longer P3 amplitudes for undesirable partners. Sergeant et
al. [133] made another interesting discovery. Sexual orientation
does not only seem to influence olfactory perception but also human
odor production. Women rated homosexual men differently from
heterosexual men. They preferred the smell of homosexuals, but did
not rate them any different than unused T-Shirts.
Emotions and moods are great markers for a person’s mind set. In
general, moods are described through positive or negative scales
simplified by speaking of being in a bad or a good mood. Our
emotions are triggered by different stimuli or events and also
depend on a person’s temperament or personality. Those triggers
can be of very different nature and recent research shows that
olfaction and emotion synergize with one another on the social
level. Jacob and McClintock [134] postulated that androstadienone
and estratetraenol modulate people’s mood state. Both steroids had
positive mood effects in women while they decreased positive
1656 Natural Product Communications Vol. 8 (11) 2013
mood in men. Bensafi et al. [135] also tested the effect of
androstadienone and estratetraenol. The subjects were put into
different situational contexts that were either neutral, happy, sad or
sexually arousing. Only during the sad situations did
androstadienone manage to keep female subjects in a positive state
of mind, while it developed negative feelings in men. Women also
tend to be more sympathetic under the influence of androstadienone
[136]. In general, this steroid is able to reduce stress and other
negative feelings in female subjects [137]. Above all it leads to
more relaxed feelings [90] and has a positive influence on women’s
ability to be focused [138]. All these effects do not change
according to the menstrual cycle phase but are independent of it.
Villemure and Bushnell [139] made another interesting discovery:
Androstadienone seems to have an effect on pain perception. The
researchers exposed subjects to androstadienone while inducing
pain. Compared with unscented air, androstadienone improved
mood in women, as mentioned above. This effect only occurred
when pain was still absent. As soon as women received painful
stimulation the perception of it was increased in combination with
the smell of androstadienone. Chen and Haviland-Jones [140] went
one step further: They hypothesized that human odors in general
lessen other humans’ depressive mood. This effect is not supposed
to depend on either the amount or pleasantness of the perceived
odor, but on age and gender. According to them, women have a
greater positive mood effect than men, and the same goes for older
people compared with younger people. Therefore, older women’s
odor best reduces the negative mood.
It is questionable whether this finding is a real breakthrough in the
scientific world. After careful examination of the data given one can
understand that there is no report of increased positive mood at all,
but only a decreased negative mood [141]. Furthermore, as a tool
for mood ratings they used the DES (Differential emotional scale),
which is meant to find out how often subjects go through mood
changes rather than commenting on their actual mood state.
Participants were asked to rate their mood only two minutes after
the perceived odor, which does not make much sense according to
the nature of the DES. Above all, Chen and Haviland-Jones failed
to compare their results with a valid placebo effect [140].
The same two researchers also found that humans can detect other
people’s emotions only by smelling their body scents [142]. Odor
samples of fearful people activated areas in the brain that are in
charge of processing anxiety signals. However, once again, a
broader study setting would have been useful in order to verify the
truthfulness of this finding. The researchers investigated only
anxiety signals, leaving a placebo control and all the other social
emotions totally behind.
On the other hand, Ackerl et al. [143] suggest that women have
indeed the ability to receive the “scent of fear”. Women’s axillary
odor was taken while watching either a frightening or a neutral film.
Before and after this presentation the researchers took saliva
cortisol samples in order to measure the hormonal reaction towards
the fear. When those odors were presented to other female subjects
they were able to differentiate between the frightened and non-
frightened odor. Prehn et al. [144] discovered that chemosensory
anxiety signals have an increasing effect on the startle reflex,
suggesting that it is part of our unconscious defensive behavior.
Also Pause et al. [145] studied this issue. They collected sweat pads
from students either waiting for an oral exam or doing sports
exercise. The subjects perceiving the anxiety odor showed an
augmenting startle reflex compared with the control odor.
Mildner & Buchbauer
Two works used neuroimaging in order to examine neural
perception of human chemosensory alarm signals. Mujica-Parodi et
al. [146] took sweat samples of people during their first time
tandem skydive. Recipients of this anxious sweat showed a specific
amygdala activation compared with non-stressed odor. The fMRI
results of Prehn-Kristensen et al. [147] verify that: “chemosensory
signals of anxiety activate brain areas involved in the processing of
social anxiety signals (fusiform gyrus), and structures which
mediate the internal representation of the emotional state of others
(insula, precuneus, cingulate cortex). In addition, the physiological
adjustments to chemosensory anxiety signals include attentional
control systems (dorsomedial prefrontal cortex, thalamus) and a
supramodal unit, timing the different emotional processing systems
(vermis, cerebellum).”
Another study investigated the effect of stress odors on neural
activity. Rubin et al. [148] collected sweat samples of subjects
during a stress condition (first time skydive) and a control situation
(exercise) and made them watch pictures of neutral, ambiguous or
angry faces. As expected, the late positive potential (a brain
potential that is important for recognition memory) during the
control condition was larger for threatening than for neutral or
ambiguous faces. However, in the stress condition, the late positive
potential was increased for all face expressions. In general, it is
interesting that “the processing of almost odorless chemosensory
anxiety signals requires enhanced neuronal energy” measured as an
increased P3 amplitude [149].
However, chemosensory anxiety and stress cues do not only
influence humans’ brain activity but also their behavior. Zhou and
Chen [150] found that fearful odor changes the affective perception
of women: They rated ambiguous faces as more fearful when
smelling anxiety sweat samples. When the facial expressions were
clearer, this effect did not occur. Therefore the researchers postulate
that olfaction can sharpen visual emotional perception. A similar
effect was observed for men. They rated ambiguously happy faces
as less happy while smelling anxiety cues compared with the
control condition [151].
Also Pause et al. [152] took anxiety and control sweat samples.
They primed subjects with sad, happy or fearful faces and made
them rate neutral facial expressions afterwards. Women primed by
happy faces rated neutral faces as more positive when smelling
control odor, but when smelling chemosensory anxiety signals the
priming effect of happy faces was clearly reduced. It was also
shown that the odor of men who are in an anxious state of mind is
able to escalate fear in women recipients [153]. Chen, Katdare and
Lucas [154] explored human cognitive performance in relation to
fearful odors. Subjects who went through a word-association task
while smelling anxiety body scents were more accurate and still not
slower than those who found themselves in a neutral condition.
It is also known that people with a high personal fear show a higher
risk taking behavior when it comes to decision-making. Also, as
fearful chemosignals and the process of decision-making show very
similar brain activation patterns, Haegler et al. [155] decided to
search for similar effects on risk taking behavior between fearful
odor and high trait anxiety. Male donors collected their sweat either
during a high rope course (anxiety sweat) or an exercise condition
(control odor). Female recipients were asked to play a computerized
risk game during odor exposure. The women showed a seriously
higher venturous behavior towards the most risky choices when
smelling fearful odor. Overall it seems as if people with high social
anxiety vary in their way to process fearful odors [156]. Their
neural processing of social fear signals is slower than that of non-
socially anxious individuals [148].
Human Body Scents
However, olfactory communication of emotions is not only
restricted to stress and fear but also includes other feelings.
Emotional tears and sadness are another field of recent research.
Emotional crying is a behavior that was found uniquely in humans.
Gelstein et al. [157] exposed men to women’s tears of sadness
collected on pads. An obvious reduction of “self-rated sexual
arousal, physiological measures of arousal, levels of testosterone”
and hypothalamus activity was observed. Consequently, weeping
reduces women’s attractiveness through the eyes of a man [158],
but might also lower men’s violence due to lower testosterone
levels. Additionally Oh et al. [159] wanted to find whether there is a
correlation between smelling sad tears and human appetite. The
researchers could find no change in food intake through tears odor,
but verified the reduction in testosterone levels.
In other animals, chemosignals of competition are very often used
to help those species adapt their behavior according to the actual
situation. Those signals seem to be also communicated between
humans. A badminton match served as the research condition for
collecting competition sweat samples. The testosterone levels of
those donors were higher than the ones of the control subjects
during exercise. When odor recipients were exposed to either
competition chemosensory signals or control odors they showed a
larger skin conductance response during the competition condition
[160]. Reproduction of animals is another behavior that is influenced
by pheromones. A large number of studies managed to confirm
pheromonal effects on animals’ socio-sexual behavior and mate
choice. But even though most of the recent scientists are optimistic
that pheromones do exist in humans, it remains questionable
whether they also influence human sexual reproductive behavior.
Several studies have investigated this topic and yet the outcome is
disputably discussed. The different methodologies in laboratory
settings make comparisons difficult and carefully conducted
double-blind, placebo-controlled, crossover studies are sparse.
One of those very few studies was carried out by Thorne et al. [161]
who asked women to rate male vignette characters and faces for
attractiveness. Women under the influence of male axillary
pheromones rated men as significantly more attractive than the
control subjects. Also Cutler and Genovese [162] showed that
topical application of a synthesized pheromone raises sexual
attractiveness in female subjects. Even the earlier mentioned “scent
of fear” seems to have an impact on female attractiveness ratings.
Male sweat samples collected during a theoretical exam were rated
as less pleasant than odors of sweat donors with low cortisol levels
[163].
Several other studies investigated not only ratings of attractiveness
but actual changes in social interactions evoked by pheromone
exposure. They all have examined whether sexual intercourses of
subjects would increase under the influence of human pheromones.
Cowley and Brooksbank [164] asked 38 men and women to wear a
necklace for one night which was either prepared with odor of the
opposite sex or a control odor. The following morning the subjects
made statements about their sexual behaviors. Women who were
exposed to androstenol reported far more interactions with men then
the other groups. Also McCoy and Pitino [165] were setting their
focus on socio-sexual behaviors in women. After a baseline period
of 2 weeks the women’s preferred perfume was infused with either
a synthetic female pheromone or a control liquid. While all subjects
showed no obvious difference during baseline period, the
pheromone group significantly increased its sexual intercourses,
sleeping next to a partner and formal dates afterwards.
Nevertheless, the frequency of masturbation did not differ in any
kind of way.
Natural Product Communications Vol. 8 (11) 2013 1657
Cutler et al. [166] asked men to make records on 6 different socio
sexual behaviors after adding up either placebo or a male
pheromone to their aftershave. Once again the pheromone group
showed a higher number of sexual intercourses and nights spent
beside a female partner, but no difference in masturbation. All three
studies show that the reported changes involve an individual of the
other sex, while masturbation does not vary. Therefore, human
pheromones are acting as sex attractants rather than increasing
sexual motivation. More recently, Friebely and Rako [167]
confirmed the earlier findings once again. Their subjects
(postmenopausal women) increased the amount of kissing, petting
and romantic exchanges when exposed to human pheromones.
However, there is still need for more representative studies in this
field as the methodology of all those researchers could have been
far better. For example, no assessment of the actual subjects’
attractiveness was used. If the individuals in the pheromone group
were more attractive than in the placebo group, it was probably
easier for them to increase their sexual intercourse. Also the
important personal status within the groups was not taken on
account. Some subjects were singles, others in relationships or even
married, which makes comparisons rather difficult. Above that, the
different studies made no record of other factors that might cause
behavioral changes. Also a romantic weekend trip or a birthday
party could have been a plausible reason, besides the suggested
pheromones. Therefore a clear analysis is difficult and maybe false
interpretations have been made.
As described before, putative human pheromones very often elicit
mood effects in humans. Nevertheless it has also been shown that
these mood changes only appear under certain conditions. The
positive mood shift in women presented by Jacob et al. [121], for
example, occurred only when a male tester was present. Lundström
and Olsson [168] verified this finding in a double-blind, within-
group study. When women were tested by another woman, no mood
shifts were detectable. This result shows that pheromones need a
sufficient context to follow their intention.
Lundström and Olsson [168] seem to adduce further evidence for
this suggestion: They were not able to confirm women’s increased
attractiveness ratings when exposed to androstadienone. For their
experiment, Lundström and Olsson used pictures (only neck and
face) of men shown to women on a computer. It might be possible
that this situation was not ecologically valid enough in order to
evoke a pheromonal response in female subjects. In general, it is
disputable whether a laboratory environment provides a sufficient
context for investigating behavioral effects of putative human
pheromones.
According to these thoughts, Saxton et al. [169,170] tried to work
out a study setting that would respect the normal social
circumstances as much as possible in a scientific experiment. They
decided that a speed dating environment would probably meet these
requirements best. Speed dating is a form to introduce socially
singles to one another. Each participant meets each person from the
opposite-sex for a certain amount of time and if two individuals
agree to like each other they exchange contact details. The goal is to
estimate in a short amount of time whether the counterpart could be
a potential partner or not. Therefore, speed dating is seen as an
adequate surrounding for investigating the influence of human
pheromones on mate choice.
In a first study Saxton et al. [169] selected 22 males and 25 females
and topically applied either androstadienone masked with clove oil,
clove oil alone or water above the women’s upper lip. While
participating to the speed dating, women were asked to evaluate
1658 Natural Product Communications Vol. 8 (11) 2013 Mildner & Buchbauer

men’s attractiveness. Subjects who were infused with
androstadienone rated men as significantly more attractive than the
two control groups. Also the second experiment of Saxton et al.
[170] used a speed-dating context for their research. In three
different cycles women under the influence of either
androstadienone or control substances rated men’s attractiveness
and once again judgments of the pheromone group were more
positive. This finding provides strong evidence that men’s
chemosignals are able to modulate women’s judgments. On the
other hand, one cannot rule out the possibility that men behaved
differently too. They may have also perceived the odor, even if they
were further from the odor source.
Most interestingly, men’s odor does not only influence female
behavior towards the opposite sex, but also intrasexual competitive
behavior [171]. Women during different phases of their menstrual
cycle were asked to have a look at different male and female faces.
While the researchers recorded the women’s eye-movements,
participants were also exposed to either androstadienone odor or a
control substance. Those subjects who were close to the moment of
possible conception were looking much oftener at female faces than
at men’s ones. No differences between odor or control group were
found. On the other hand, low fertile women exposed to
androstadienone increased their competitive behavior towards
women through looking at female faces far more often. Thus the
authors suggest that certain pheromones can lead to competition
among humans of the same sex.
mediated is mainly unknown and further investigation is needed in
order to identify related pathways, including receptors and ligands.
Another important aspect is that common odors and pheromones are
processed differently and also activate different brain areas.
Pheromones are supposed to trigger social responses and the fact
that hypothalamic activation depends on sexual orientation very
well meets this criterion. Even though several studies have
demonstrated strong evidence for androstadienone and
estratetraenol to be pheromonal substances, no compound has been
undisputedly accepted so far.
Many different behavioral responses have been detected by now.
Among the first reports was the synchronization of the menstrual
cycle in women that live together. Also humans’ ability to
recognize sexual orientation, gender and kin was a big discovery
and finally detection of genetic MHC-differences only via
chemosignals seems to be proof enough. While pheromones have
been shown to evoke mood shifts, recent research efforts were put
into the effects of chemosensory anxiety and sadness signals.
It is highly visible that many intersexual behavioral effects only
exist due to pheromonal communication. Most of it seems to come
down to sociosexual and mating behavior. All these present data
demonstrate that human pheromones do indeed exist. Nevertheless,
it remains unclear to which extent pheromones impact our course of
action as human behavior is very complex and led by many
different cues.

All this evidence shows that chemosensory signals transmitted by
olfactory receptors well influence human sexual behavior and,
therefore, help to choose the right partner.
Obviously gametes also experience a little guided help towards
fertilization. Just as rat sperm is known to express olfactory
receptors [172], it was possible to show that human sperm
chemotaxis also exists [173]. Human sperm responds immediately
to a chemoattractant [174].
Olfaction is one of our five basic senses providing the ability to
immerse into a unique world of sensations. This review aimed to
figure out whether pheromones play a role in human
communication or not. It was shown that humans do indeed spread
body odors, mainly via the skin and some researchers suggest they
function as chemosignals rather than pheromones. Looking at the
human vomeronasal organ makes us believe that this opinion might
be right: Although the presence of a VNO is generally accepted in
the early life of a fetus, it degenerates during gestation, leaving
many neurochemical and neuroanatomical evidence for a non-
functioning vomeronasal organ behind. Yet the notion of a vestigial
VNO is no proof for the absence of pheromones in human life. It is
most likely that pheromones can be transmitted via the main
olfactory system. However, the way human pheromones are
The knowledge of human chemosensory communication raises
further questions. How does our modern striving for inodorousness
and cleanliness cope with the outcomes of all these cited studies?
Are we not depriving ourselves from a natural way to communicate
by trying to erase those traces of communication from our bodies?
Also, how do industrial perfumes interfere with these elemental
behavioral cues? So far nobody can explicitly answer those
questions. However, interestingly it could be shown that the
artificial fragrances do still have positive effects. Capparuccini et al.
[175] figured that the use of perfumes is “potentially involved in
mate choice and may elicit strong hedonic responses that can
dominate visual signs, with a cross-modal interaction”. Those
fragrances do not only mask our body odor, but are instinctively
chosen by the individual to interact well with the personal odor. The
mix of a subject’s body scent with the preferred perfume is rated as
more pleasant than the mix of this body odor with a randomly
chosen fragrance [176]. Additionally, the self-confidence and self-
perceived attractiveness of men are enhanced by the use of
fragrances with antimicrobial agents that make them appear more
attractive to women [177]. This interference between personal body
pheromones and industrial perfumes is another possible field for
further examination on human pheromones.

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