The Quarterly Journal of Experimental Psychology
Section B
ISSN: 0272-4995 (Print) 1464-1321 (Online) Journal homepage: http://www.tandfonline.com/loi/pqjb20
Sex differences in human olfaction: Between
evidence and enigma
Gérard Brand & Jean-Louis Millot
To cite this article: Gérard Brand & Jean-Louis Millot (2001) Sex differences in human olfaction:
Between evidence and enigma, The Quarterly Journal of Experimental Psychology Section B,
54:3, 259-270
To link to this article: http://dx.doi.org/10.1080/713932757
Published online: 22 Oct 2010.
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THE QUARTERLY JOURNAL OF EXPERIMENTAL PSYCHOLOGY, 2001, 54B (3), 259–270
Sex differences in human olfaction: Between
evidence and enigma
Gérard Brand and Jean-Louis Millot
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Faculté des Sciences et Techniques, Besançon, France
The sex of individuals plays an important part in determining their olfactory abilities, with
females generally being superior to males. The present review examines the way in which sex differences influence sensitivity, identification, familiarity, and recognition of odours. It also examines whether sex differences are more pronounced with some odours than others, and how sex
differences are affected by the manner of testing. Two different explanations for the superiority of
females over males in olfaction are evaluated.
In the field of human perception, the chemical senses (taste and smell) have received little
attention from research compared with auditory, visual, and even tactile senses. In the case of
olfaction, it would appear from publications over the last few years that there is a move to overcome this lack of research (see Doty, 1997; Herz & Engen, 1996; Larsson, 1997; Schaal, 1996,
for more recent reviews). Interpersonal variations in responding to odorants is a hallmark of
olfactory perception. Many factors, such as genetic factors and life-long experiences, contribute to this variation, but age and sex also appear to be important. Major alterations in olfactory
processing are now well documented in advanced age (Doty, 1991a, 1997; Lehrner, Glück, &
Laska, 1999). The concept of sex differences in relation to olfactory abilities is also of interest
to differential psychology and biological disciplines and dates back a long time. A century ago,
Toulouse and Vaschide (1899a, b) claimed that the sensitivity, perception, and discrimination
abilities of women were superior to those of men. Based on the study of 237 subjects of both
sexes and all ages (the odorants were camphor water and floral odours) these authors also
found that females developed their abilities earlier than males. This female superiority in
olfactory perception also appears to be a common and universal belief. In an ambitious “Smell
Survey” involving 1.5 million people in collaboration with the National Geographic Society,
Wysocki and Gilbert (1989) noted that women had a higher opinion (the survey included a
self-rating scale) of their olfactory capabilities than men whatever their age, from 10 to 90 years
of age. Nevertheless, a number of questions relating to sex differences in olfactory perception
remain unresolved. Numerous studies have been concerned with sex differences in various
aspects of olfactory perception and their conclusions can be contradictory and confusing.
Requests for reprints should be sent to Gérard Brand, Laboratoire de Neurosciences, Faculté des Sciences et
Techniques, 1 Place Leclerc, 2500 Besançon, France. Email: [email protected]
Ó 2001 The Experimental Psychology Society
http://www.tandf.co.uk/journals/pp/02724995.html
DOI:10.1080/02724990143000045
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In order to resolve differences among research findings, it is necessary to carefully examine
(1) the different aspects of olfaction that have been tested (sensitivity, familiarity, identification, etc.); (2) the types of odours that are used for testing (artificial and human odours may
have different ecological meanings or properties), (3) the subjects, methods, and contexts of
the studies, and the relationships between the results obtained in the different methods
(psychophysical, electrophysiological, cerebral imagery, etc.). Finally, a review could provide
elements to assess the origins and functions of sex differences in olfaction.
Perception of odours without social significance
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Detection and sensitivity
These are the first steps in the olfactory processes, and they have been documented by different studies. Some studies failed to find any significant differences between males and
females in sensitivity thresholds for many odors: n-butanol (Koelega, 1970); safrol (Koelega &
Köster, 1974); pyridine (spoiled-milk odour; Dorries, Schmidt, Beauchamp, & Wysocki,
1989); phenyl ethyl alcohol (rose like; Segal, Topolski, Wilson, Brown, & Araki, 1995; Stevens
& O’Connell, 1991; Zatorre & Jones-Gotman, 1990). Although it is difficult to draw conclusions from non-significant results, it must be noted that the superiority of women is statistically established by other studies. The National Geographic Smell Survey (NGSS) dealt with
detection ability (only one concentration of microencapsulated odorants was presented in a
“scratch and sniff test”. There were obvious differences between males and females (Wysocki
& Gilbert, 1989). The odours tested were isoamylacetate (banana like), eugenol (cloves), mercaptans (sulfur compounds added to natural gas), and rose. The perceived intensity of these
odorants was rated higher by females than by males, when there was a difference between 10 to
60 years of age. The sex difference appeared greater for the oldest subjects.
Koelega (1970, 1994) and Koelega and Köster (1974) tried to solve this question of sex differences with some detailed investigations. Their results showed lower thresholds in women
than in men for pyridine and m-xylene (benzene odour) from 20 years of age. There was a difference for amyl acetate as early as the prepubertal period (9–10 years of age). Olfactory acuity
is also affected by some pathologies, according to sex. The performance of olfactory acuity was
significantly lower in male schizophrenic patients than in female schizophrenic patients
(Kopala & Clark, 1990; Kopala, Clark, & Hurwitz, 1989). It is also know that a defective
olfaction coexists with sexual immaturity in men affected by the X-chromosome-linked
Kallman syndrome (Bouloux, Munroe, Kirk, & Besser, 1991).
Hedonicity
The hedonic valency (pleasant/unpleasant character of an odour) is a major characteristic
of olfactory perception, but it has rarely been the subject of comparative analysis between the
sexes. In the NGSS (Wysocki & Gilbert, 1989) the participants were asked to rate the quality
of the odorants. The results showed that the pleasantness rating depended on the type of
odour: for example, higher for amyl acetate and mercaptan in men, higher for eugenol and rose
in women.
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Discrimination, recognition, and identification
The ability of human beings to recognize an individual odorant is very limited, and the difficulty of identifying with the correct name a particular odour is a major characteristic of
olfaction compared to the other sensory systems. Early differences have been described: identification scores (five odorants were tested: baby powder, bubble gum, candy cane, fish,
orange) tended to be better for girls than for boys throughout childhood, from 3.5 to 13 years
of age (Richman, Post, Sheehe, & Wright, 1992). Adult abilities in identification have also
been investigated by the NGSS (Wysocki & Gilbert, 1989). When there was a sex difference, it
was always in favour of the females. Engen (1987) found similar results. The difference was
also greater for the older subjects (80–90 years of age). Other studies involving a large population (nearly 4000 people) have been carried out using the University of Pennsylvania Smell
Identification test (UPSIT). This “scratch and sniff” test is standardized, has high reliability,
and includes 40 microencapsulated odorants. Differences are obvious for the youngest and the
oldest people: 5 to 9 years of age and over 60 years (Doty, 1997). The decrease in the olfactory
ability with age is in part attributed to structural modifications in the olfactory system
(Meisami, Mikhail, Baim, & Bhatnagar, 1998). In the first published longitudinal study
assessing olfaction in adulthood, Ship, Pearson, Cruise, Brant, and Metter (1996) replicated
and extended earlier cross-sectional results (Ship & Weiffenbach, 1993) by showing that the
pattern of deterioration in odour identification with age was similar in males and females, but
delayed by approximately 20 years in women: Males experienced a more precipitous and earlier decline, by the age of 55 years, in smell identification than did women, by the age of 75
years. Recent works suggest that healthy women up to 80 years of age show only slight changes
in sensory functioning in relation to younger females (Larsson & Bäckman, 1993, 1997). The
superiority of women has been confirmed whatever the ethnic or cultural background: white,
black, Korean Americans, and native Japanese (Doty, 1997; Doty, Applebaum, Zusho, &
Settle, 1985; Doty, et al., 1984). This difference was also confirmed not only in forced-choice
tests, as was the case of UPSIT, but also in free recall tests (Cain, 1982). These identification
abilities could have a stronger genetic basis in men than in women as was suggested by Segal et
al. (1995). They found a reduced resemblance between the UPSIT scores of monozygotic
female twins compared to that of monozygotic male twins. These results are also interpreted
by these authors as an increased sensitivity of the female identification ability to environmental and endocrinological influences.
Many studies investigated the processes of odour memory (see Annett, 1996; Herz &
Engen, 1996; Schab & Crowder, 1995). Some of them found that short-term memory and
long-term recognition was not affected by the sex of the subjects (Richardson & Zucco, 1989).
However, Klukty (1990) found a significant advantage in olfaction memory tasks for women,
compared to auditory or visual memory scores, which showed no such differences. Bromley
and Doty (1995) observed that in an odour recognition short-term memory test (nine items
selected from the UPSIT), women, and not men, improved their odour memory performance
from a first to a second test session. Lehrner (1993) tested odour recognition memory with a
two-alternative forced-choice test for retention intervals up to 21 days: Women performed
better than men for all retention intervals. This author attributed the superiority of women to
sensory rather than cognitive factors.
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Perception of odours with potential social significance
According to Doty (1991b), there could be sex differences for olfactory abilities as early as the
first few days after birth. Female newborns (13 to 17 days of age) preferentially turned their
head towards a gauze pad impregnated with the breast odour of a feeding mother compared to
a control gauze pad, but there was no significant difference for male newborns (Makin & Porter, 1989). Similar results have been described by Balogh and Porter (1986). However, further
studies are needed to determine if this preferential orientation of females and not males is actually determined by sex differences in olfaction or is only the result of premature motor asymmetry (Marlier, Schaal, & Soussignan, 1998). Sex differences also exist in older children
(Verron & Gaultier, 1976): They found that 4–5-year old children could identify correctly
their playmates from their body odour, and the performance of girls was superior to that of
boys (69% vs. 33% of correct identifications). Furthermore, the familiarity (in terms of frequency of proximal contacts in the playground) between the discriminator and the donor of
odours influenced the female’s performance more than that of the males (Marlier & Schaal,
1989). Girls also outperformed boys in their capabilities to identify the odour of a brother or a
sister (Porter & Moore, 1981).
In adults, most research has been concerned with androstenone (variable quality: sweaty,
musky, urine like, or no odour) and related odorants. Androstenone was first isolated in the
saliva of the boar and identified as a chemical signal in the sexual behaviour of this species. It
has also been isolated in human axillary secretions and urine. Consequently, sex differences in
either the sensitivity or the behavioural effects of this compound have been extensively investigated over the past decades in order to study a putative sex pheromone in humans. There was
a considerable proportion of normal adults who were unable to detect this substance as well as
a strong sex difference: According to the studies, 26.8% to 44.3% of the male population and
7.6% to 25% of the female population are unable to detect androstenone (Baydar, Petrzilka, &
Schott, 1993; Dorries et al., 1989; Griffiths & Patterson, 1970). However, a large proportion of
subjects classified as anosmic to androstenone can detect it after repeated exposure to it
(Wysocki, Dorries, & Beauchamp, 1989). As well, subjects characterized by this specific
anosmia have revealed psychophysiological reactions such as an electrodermal response to this
odorant. Van Toller, Kirk-Smith, Wood, Lombard, and Dodd (1983) showed differences
linked to sex in relation to both time latency and duration or amplitude of the electrodermal
response.
Sex differences concerning androstenone sensitivity appear at an early age (Dorries et al.,
1989) and the superiority of females in the detection of this odorant was found at all ages, with
an increase in the difference with age (Wysocki & Gilbert, 1989), and in different populations—American or African (Barber, 1997; Wysocki & Beauchamp, 1991). The NGSS also
indicated a constant increasing difference in the intensity rating of odours between men and
women from 20 to 80 years of age. The pleasantness ratings for androstenone were also marked
by sex differences. Men found this odour more pleasant than women did (Griffiths &
Patterson, 1970; Koelega, 1980; Wysocki & Gilbert, 1989). However, the hedonic ratings by
female subjects changed significantly during their menstrual cycle, at least when they did not
take oral contraceptives (Grammer, 1993). In the study of Filsinger, Braun, Monte, and
Linder (1984) there was a significant interaction of sex and the rating of a target male’s passivity, with men rating him as more passive than women, who rated themselves as less sexy in the
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presence of alpha-androstenone than they did in pleasant (methyl anthranilate: floral odour),
unpleasant (skatole: faecal odour), or no-odour control conditions. Filsinger, Braun, and
Monte (1990) also showed sex differences in response to alpha-androstenone; when men
found this odour pleasant they tended to rate the target male positively.
Androstenone influences the preference, according to sex, for objects or places. KirkSmith and Booth (1980) recorded the frequency of use of seats impregnated or not with
androstenone in a doctor’s waiting room and found that women were attracted by the seats
impregnated with this odorant and that men avoided it.
Androstenol, which is characterized by a musk odour, is also a compound present in
axillary sweat. As early as 1961, Kloek reported (Kloek, 1961) that specific anosmias in relation
to this molecule were more frequent in males (38%) than in females (22%). Koelega and
Koster (1974) reported a greater sensitivity of women with two different forms of androstenol.
Gustavson, Dawson, and Bonett (1987) investigated the effect of the odour of androstenol on
restroom-stall choices compared with a control odour. Men avoided the stalls treated with
androstenol, but neither odour affected female stall selection. In a recent study, Jacob and
MacClintock (2000) showed that steroidal chemosignals can modify mood. The two tested
steroids increased positive mood state in women, but decreased it in men.
Some studies have been concerned with other musk-like compounds that might have similar effects to those of body secretions such as androstenol. A pioneer was Le Magnen who
tested Exaltolide (pentedecanolide). He found that the sensitivity in adults was much higher in
women than in men (about half of them were anosmic to Exaltolide) and also that oestrogens
increased sensitivity, whereas androgens had the opposite effect (Le Magnen, 1952). Koelega
and Koster (1974) and Koelega (1994) found a sex difference in sensitivity to the odour of
musk R-1 (oxohexadecanolide) in favour of the females. A synthetic musky compound
(galaxolide) was tested in the NGSS. Women exceeded men in both their detection and identification abilities. Women rated the perceived intensity and the pleasantness of this compound
higher than did men (Wysocki & Gilbert, 1989). More recently, Baydar et al. (1993) showed
that more women than men had simultaneous anosmia to galaxolide and androstenone and
deduced that there was a sex-modulated linkage between the characteristics of androstenone
smelling and galaxolide smelling.
Better female scores in identification tasks (i.e., to identify the gender of the donor) or body
odours have been confirmed by studies of odours from various body areas: axillary (Doty,
1977; Schleidt, Hold, & Attili, 1981), hand (Wallace, 1977), or breath (Doty, Green, Ram, &
Yankell, 1982). Body odour probably plays a role in interindividual attractiveness as suggested
by Rikowski and Grammar (1999), who found positive relationships between body odour and
attractiveness for female subjects. This phenomenon could be due to a genetic influence
(Wedekine & Füri, 1997).
Discussion
Some conclusions can be drawn from the data cited earlier. When a difference between sexes is
demonstrated, concerning either the sensitivity or the ability to discriminate or categorize, it is
always in favour of women. This effect has been found with other modalities such as hearing,
taste, and skin sensitivity (Velle, 1992). It could be argued that men and women simply differ
in their motivation to concentrate and perform well in particular test settings. Psychophysical
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studies are based on responses that are, in most cases, subjective reports of the sensations experienced. This argument is made less plausible by the results from studies that show a superiority in men for other sensory abilities (e.g., visual acuity, visual-spatial ability). Furthermore
gender differences also appear in studies of large populations (as was the case for the NGSS
and the UPSIT) and can hardly be refuted as unfounded.
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Interpretation of sex differences in olfaction
First, it is possible that sex differences are due to anatomical and/or physiological differences directly implicated in the processing of olfactory information. Anatomical differentiation in the structure of the nasal airways between males and females could be involved. Few
studies have specifically dealt with this issue and several aspects such as respiratory tract, surface of the olfactory epithelium, and its vascularization have never been the subject of comparative analyses. Leopold (1988) showed that the differences above the middle turbinate were
the most important. Hornung, Donald, and Leopold (1999) found that the size of compartments of the nasal cavity around the olfactory cleft was generally positively correlated with
olfactory abilities and suggested that the anatomical differences in nasal structures between
men and women could contribute to their different olfactory abilities. At this peripheral level,
differences in oral practice hygiene could also be involved (Griep et al., 1996).
Differences between males and females in brain structure used for the processing of olfactory perception should also be considered. In humans, there are sexual dimorphisms of the
cerebral hemispheres (Conklin & Polemics, 1997) and a cerebral asymmetry, which could conceivably affect olfactory processing and which is more marked in men than in women (Brand,
1999; Doty, Bromley, Moberg, & Hummell, 1997). Although this difference in anatomical
asymmetry is correlated with behavioural asymmetry during smelling tasks (Millot & Brand,
2000), the correspondence with precise functional aspects has not been well identified. New
cerebral imagery techniques could be used to investigate this issue further. In previous studies
based on electroencephalography (EEG), women showed larger EEG amplitude and larger
evoked responses amplitude than men (Gale, Brown, Osborne, & Smallbone, 1978; Cohn,
Kircher, Emmerson, & Dustman, 1985; Evans, Cui, & Starr, 1995). Unfortunately, the samples observed in studies using cerebral imagery are usually too small to permit a comparative
analysis. In the study of Levy et al. (1997) there was a lower brain activation in women than in
men to all the olfactory stimuli (pyridine, menthone, amyl acetate; no special olfactory tasks
were required). In this study, measurement techniques did not yield detailed anatomical areas
of localization. On the contrary, and more recently, Yousem et al. (1999), using relatively
selective odorants for olfactory (and not trigeminal) nerve stimulation (a phenyl ethyl alcohol)
observed a statistically significant increase in right and left inferior frontal lobe activation in
women, which could be the correlate of the differences observed in psychophysical studies.
Nevertheless, and despite current interest in these techniques, there is not sufficient information to give a clear indication of functional gender differences in olfaction. Differences in hormonal status between men and women have also been used to account for differences in
olfaction (Doty, 1986; Le Magnen, 1982). Well-known examples are the variations in the sensitivity of women during their menstrual cycle. Olfactory performance reaches a peak during
ovulation and then decreases during menstruation (Doty, Snyder, Huggins, & Lowry, 1981;
Koelega & Köster, 1974; Velle, 1987). However, these variations were also found in women
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SEX DIFFERENCES IN HUMAN OLFACTION
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who were taking a contraceptive pill (Doty, 1987; Doty, Hall, Flickinger, & Sondheimer,
1982), which suggests that the variations in sensitivity were determined by an infradian
rhythm activated by the central nervous system and were not hormone dependent. Two artificial odorants were tested in this study (furfural, which smells like bitter almonds, and phenyl
ethyl alcohol), and it would be of interest to have more data concerning odours with potential
social significant for which the sensitivity or the hedonic ratings by women can change during
their menstrual cycle (negative to neutral for androstenone in Grammer’s study, 1993). The
mechanisms underlying the correlations between odour perception and hormonal status still
have to be clarified. To support this proposal, the study of Laska, Koch, Heid, and Hudson
(1996) can be cited. These authors evaluated various aspects of olfaction (sensitivity, discrimination, pleasantness) of 12 odours by pregnant women and by a control group. They concluded that there were no consistent differences in olfactory sensitivity or odour evaluation
between the two groups. Only galaxolide and androstenone were tested as odours of social significance in this study, and they were the only ones to be rated as significantly more intense
during pregnancy.
Second, it can be suggested that gender differences observed in olfaction are just a marginal
expression of complex differences in higher levels of brain organization and function. This
may particularly be true in the case of tasks such as identification or recognition. The belief
that sex differences in specific cognitive abilities exist was quite common even before they
were systematically documented (Ellis, 1928). It is known that women perform better than
men in verbal tasks and that there are sex differences in the functional organization of the brain
for language (Shaywitz et al., 1995). Thus, the superiority of women in olfaction could reflect a
type of cognitive advantage that is also found in the other senses or situations. A strong similarity between odour and language perception has been advanced by Lorig (1999). For this
author, odour information processing shares some of the cortical resources used in processing
language. In this way it would not be surprising if an advantage in verbal tasks is correlated
with an advantage in olfactory perception.
Another aspect that has received too little attention concerns the way in which odour suggestion or imagination produces a significant sex-related interaction (Gilbert, Knasko, &
Sabini, 1997). The studies of Levy et al. (1999) have opened the way to valuable investigations.
Using fMRI to measure the response to imagined odours (banana and peppermint), they
showed that brain activation was significantly greater in men than in women, as was previously
reported for the actual smell of the odour of amyl acetate (Levy et al., 1997). However, the relative ratios of these responses were quite different: The ratio of brain activation by imagining
banana odour to activation by actual amyl acetate odour (N.B., amyl acetate odour is banana
like) was about twice as high in women as in men. This would suggest that some olfactory stimuli might have greater meaning, and consequently greater effect, for women than men. These
results are consistent with the hypothesis of Henkins (1997) that women may respond more
efficiently to some olfactory stimuli than men and that this is related in part to sex differences
in cognitive style.
Two explanations for sex differences in olfaction
1. From an ontogenetic point of view, it is possible that men and women differ in the
degree to which they have experienced or learned various odour stimuli. This hypothesis
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suggests that women in general encounter olfactory cues more often than do men so that they
might simply have more experience with more odorants. It is well documented that familiarization with an odour results in long-term storing of memory traces of this odour (Jehl, Royet,
& Holley, 1995; see also Hudson, 1999). The ability to perceive an odour can also be induced in
anosmic subjects by repetitive exposure (Wysocki et al., 1989). From these studies it might be
thought that women will be superior to men in identifying the “stereotypically female” odours
(i.e., present in their daily environment) and inferior to men in identifying “stereotypically
male” odours. Unfortunately, it has been shown that the superiority of women is extended to
“male” odours (Cain, 1982). It must also be noted that differences are shown at a very early
age. Thus, the cause of the superiority of females could not be restricted to differences in experiences with odours. Differences in smoking habits have also been suspected, but when this
factor is taken into account it appears of minor importance (Koelega, 1994).
2. From an evolutionary point of view, sex differences have been selected to improve the
probability of survival of the individuals and their offspring, and it is possible to explain the
superiority of females to males in olfaction from this perspective.
Women are characterized by a physical strength that is weaker than that of men. More
developed sensitivity, discrimination, and recognition abilities could compensate for weaker
defensive aptitudes by greater capacities in the analysis of the environment and of its perils.
If the assumption of an early division of labour is accepted, it implies a main involvement of
women in gathering food supply essentially of plant origin. Thus, a superiority of the chemical
senses (taste and olfaction) would be present for women in order to distinguish between the
very large diversity of odours and tastes characterizing the different toxic and non-toxic plants
and their nutritional values (Velle, 1992).
Sex differences concerned by human biological odours are of a particular interest in this
framework. It is clear that human odours play a role in social communication (Hold &
Schleidt, 1977), particularly in parent–child interactions (Schaal, 1988). In adults the effect of
axillary odours on menstrual cycle between women, suspected by MacClintock (1971), and
recently been confirmed by Stern and MacClintock (1998), demonstrates specifically female
olfactory abilities. The greater sensitivity of women than men in detecting androstenone (produced in far greater quantities in males than females) or related compounds suggests that these
odours could play a role in sexual attractiveness. However, the results of the hedonic valency
of this odour have been contradictory. It is possible that laboratory experimental studies are
not really appropriate for discovering the complex intimacy of the role of odours in sexual
behaviour. The odour of a sexual partner can be found pleasant in close relations, but judged
unpleasant in public, “academic” situations. This issue needs to be addressed in a variety of
ecological situations. Studies cited earlier (Gustavson et al., 1987; Kirk-Smith & Booth, 1980)
have been criticized for the validity of some aspects of their methodological procedures, but
they open the way to this type of valuable approach.
Conclusions
To summarize, sex differences have been shown in sensitivity-detection and recognitionidentification tasks, and the superiority of women is more evident in these instances when the
odours are related to a human origin. These greater abilities may be attributed to both proximal and ultimate causes and either as direct or indirect consequences. Several issues remain to
SEX DIFFERENCES IN HUMAN OLFACTION
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be addressed. There is a need to determine if observed sex differences are exclusively limited
to olfaction, or of they also occur in other systems of chemical perception such as the
trigeminal sensitivity or the vomero-nasal organ. This has not been established for most of the
compounds used in the previously quoted experiments. Additionally, recent progress in cerebral imagery could contribute to a better understanding of the processes linked to gender differences with protocols adapted to accurately analyse aspects of olfaction. Finally, the real
impact of these gender differences should be assessed from different naturalistic, behavioural
approaches to take into account their validity, importance, and function in the daily environment of men and women.
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Manuscript received 20 July 2000
Accepted revision received 17 January 2001