Arch Sex Behav (2012) 41:1403–1408 DOI 10.1007/s10508-011-9804-7
ORIGINAL PAPER
Pleasantness of the Odor of Androstenone as a Function of Sexual Intercourse Experience in Women and Men Antti Knaapila • Hely Tuorila • Eero Vuoksimaa Kaisu Keskitalo-Vuokko • Richard J. Rose • Jaakko Kaprio • Karri Silventoinen
•
Received: 3 March 2011 / Revised: 2 June 2011 / Accepted: 11 June 2011 / Published online: 2 July 2011 Springer Science+Business Media, LLC 2011
Abstract Androstenone (5a-androst-16-en-3-one) and other androstenes, body odor components occurring in apocrine secretions, may play a role in human chemosignaling. We hypothesized that the odor of androstenone may gain hedonic value from sexual intercourse experiences via associative learning. Young adults (N = 397, 61.5% women, age 21–24 years, randomly sampled regarding sexual experience) rated the intensity and pleasantness of the odors of androstenone, cinnamon, chocolate, isovaleric acid, lemon, and turpentine. Among women who were able to perceive androstenone, the odor was rated as more pleasant (less unpleasant) by those who had had
experienced sexual intercourse with at least one partner (n = 175) than by those who reported never having experienced intercourse (n = 12, p = .006). The difference was specific to women. The results suggest that, among women, sexual experience may modify the pleasantness of the odor of androstenone. Keywords AndrostenesAssociativelearningBodyodor Evaluative conditioning Olfaction Smell
Introduction A. Knaapila (&) Monell Chemical Senses Center, 3500 Market St., Philadelphia, PA 19104, USA e-mail:
[email protected] H. Tuorila Department of Food and Environmental Sciences, University of Helsinki, Helsinki, Finland E. Vuoksimaa K. Keskitalo-Vuokko J. Kaprio Department of Public Health, University of Helsinki, Helsinki, Finland R. J. Rose DepartmentofPsychological&BrainSciences,IndianaUniversity, Bloomington, IN, USA J. Kaprio Department of Mental Health and Alcohol Abuse Services, National Institute for Health and Welfare, Helsinki, Finland J. Kaprio Institute for Molecular Medicine, University of Helsinki, Helsinki, Finland K. Silventoinen Population Research Unit, Department of Social Research, University of Helsinki, Helsinki, Finland
Pleasantness of an odor is attributed mainly to associative learning: The odor acquires the hedonic value of the (emotional) context in which the odor is first experienced (Herz, 2001, 2005; Herz, Beland, & Hellerstein, 2004). Associative learning demonstrably modifies the pleasantness of odors, particularly odors related to foods (Yeomans, 2006, 2010). Experimentally, classical conditioning paradigms (Pavlovian conditioning) have been shown to modify the responses to odors, not only in animals but also in humans (olfactory conditioning) (Chu, 2008). In olfactory conditioning an olfactory stimulus is the conditioned stimulus that has been paired with an unconditioned stimulus (e.g., taste). For instance, the pleasantness of odors with originally neutral hedonic value was improved after the odors were paired as few as three times with the pleasant unconditioned stimulus, sweet taste (Barkat, Poncelet, Landis, Rouby, & Bensafi, 2008).This type of conditioning, where liking of a stimulus changes because the stimulus has been paired with another, positive or negative, stimulus is called evaluative conditioning (De Houwer, Thomas, & Bayens, 2001). Naturally occurring evaluative conditioning may be important also in modifying the pleasantness of a partner’s body odors (condi-
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tioned stimulus) that are encountered initially during affection and sexual intercourse (unconditioned stimulus), because the sexual experiences presumably provide strong, positive, emotional context. Searches for human pheromones have focused on androstenes (Pause, 2004), androgen steroids occurring in apocrine secretions, for example, axillary (underarm) sweat (Gower, Holland, Mallet, Rennie, & Watkins, 1994), motivated by the fact that one of them, androstenone (5a-androst-16-en-3-one), functions as a sex pheromone in pigs. However, some 20–40% of adult humans, depending on age and sex, cannot smell androstenone, although their sense of smell is otherwise intact (Wysocki & Gilbert, 1989). To date, no convincing evidence exists to demonstrate, that any single compound is able to functionasasexualattractantinhumans,althoughseveralothertypes of pheromonal effects (e.g., kin recognition) have been observed (Wysocki & Preti, 2009). While many studies have explored potential physiological and behavioral effects of the odors of androstenes (for a review, see Havlicek, Murray, Saxton, & Roberts, 2010), we asked a different question: Could an odor (conditioned stimulus) that is perceived during sexual intercourse gain hedonic value from the intercourse experience (presumably a pleasant unconditioned stimulus) through associative learning? While experimental challenges limit human studies of this kind, we approached the question by asking young adults, randomly sampled regarding the level of sexual experience and olfactory function, to rate the pleasantness of body-related (androstenone and isovaleric acid) and control odorants (chocolate, cinnamon, lemon, and turpentine). We compared the responses of participants with and without experience in sexual intercourse and hypothesized that those with intercourse experience would rate the pleasantness of the odor of androstenone higher than would those without such experience. Our hypothesis rests on the assumption that androstenone, but not the other studied odorants, would be more likely encountered during close intimate sexual contacts than in other life situations, and that the sexual experiences would act as a positive unconditioned stimulus thereby increasing the pleasantness of the odor of androstenone (conditioned stimulus) through naturally occurring evaluative conditioning.
Method Participants Data from 397 individuals, between the ages of 21 and 24 years (M = 22.7 years, SD = 0.5), including 244 women and 153 men, were available for our present analyses. The participants were Finnish twins: 83 monozygotic and 97 dizygotic complete twin pairs, and 37 individuals (17 women and 20 men) without data from their co-twin. The monozygotic pairs included 59 sister–
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sister and 24 brother–brother pairs. The dizygotic pairs included 58 same-sex pairs (35 sister–sister and 23 brother–brother pairs) and 39 opposite-sex (sister-brother) pairs. Procedure The olfactory data were collected from the twins during a laboratoryprotocoloftheFinnTwin12study(Kaprio,Pulkkinen,& Rose, 2002). In advance of the laboratory study, participants completed extensive postal questionnaires on a wide range of medical, psychological, and social factors, including a question about sexual intercourse experience. The participants rated olfactory stimuli during their visit to the twin research unit, where they also provided other data not reported here. The participants arrived at the unit in the morning after 12 h overnight fast, and a trained test administrator collected the olfactory data from a group of one to six individuals per day before the group was served breakfast. Each participant provided informed consent before inclusion in the study and was paid a modest honorarium, as permitted by Finnish law, to compensate the time and effort they donated. The study protocols were approved by the Institutional Review Board of Indiana University (Bloomington, IN) and the Ethics Committee of the Hospital District of Helsinki and Uusimaa (Helsinki, Finland). Measures The method for collecting the olfactory data was previously reported in detail (Knaapila et al., 2008). Briefly, the participants reported the perceived intensity, pleasantness, and identity of a set of six scratch-and-sniff odor stimuli (androstenone, chocolate, cinnamon, lemon, isovaleric acid, and turpentine). Perceived intensity was rated using a 9-point scale having endpoints labeled with‘‘No odor’’(1) and‘‘Extremely strong odor’’(9). Pleasantness wasratedusinga9-pointscalewhichwaslabeledwith‘‘Extremely unpleasant’’(1),‘‘Neither pleasant nor unpleasant’’(5), and ‘‘Extremelypleasant’’(9).Twotofiveindividualsdidnotprovidea valid response to a specific stimulus. Self-reportsofsexualintercourseexperiencewereobtainedin response to the question:‘‘Withhow many partners have you had sexual intercourse’’?, The response alternatives were:‘‘I havenot had [intercourse],’’‘‘one,’’‘‘two,’’‘‘three or four,’’ and ‘‘five or more.’’ Information about intercourse experience was missing from one woman and three men. No information on whether intercourse had been heterosexual or homosexual was requested (for details on the questionnaire item, see Mustanski, Viken, Kaprio, Winter, & Rose, 2007). Statistical Analysis Iftheintensityofanodorwasratedas‘‘noodor,’’neitherresponse to the pleasantness nor intensity for this odor was included in further analyses. In the present analyses, the participants
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Women who had had at least one sexual intercourse partner (n = 175, including 50 twin pairs and 75 individuals without their co-twin in this group; age M = 22.6 years; 71.4% lived in a relationship at time of data collection) rated the odor of androstenone as more pleasant than women who had not experienced sexual intercourse (n = 12, including two twin pairs and eight individuals without their co-twin in this group; age M = 22.7 years; none lived in a relationship at time of data collection), Wald test F(1, 132) = 7.89, p = .006, d = 0.83 (Table 1). Pleasantness ratings by both groups were below the neutral point of the scale (5); hence, more specifically, women who had experienced sexual intercourse with at least one partner rated the odor of androstenone as less unpleasant than did women without this experience. We confirmed the significance of the difference between the groups by calculation of an empirical p value: We randomly sampled 12 individuals from among the 187 women 1000 times and compared the means of the ratings of the pleasantness of androstenonebetweenthegroupsof12and175individuals.Ten out of the 1000 random samplings yielded an effect size (d) that was higher than that of the observed data (0.83), resulting in an empirical p value of 0.01. In addition, among the women, we observed a small but significant correlation between the pleasantness of androstenone and the number of sexual partners (n = 187, Spearman’s q = .17, p = .02). In men, the ratings of androstenone were not associated with sexual intercourse experience. Instead, men who had had at least one sexual partner (n = 127) rated the pleasantness of turpentine as more pleasant than did the men who had not experienced intercourse (n = 22), F(1, 104) = 4.75, p = .03,
who reported having nointercourse experience were compared to those who provided any other response, using a two-sided Wald test corrected for the paired structure of the data (clusteringintwinpairs)implementedinthestatisticalpackageStata 11.0(StataCorpLP,CollegeStation,TX,USA).Thecorrection takes into account the effect of within pair correlation between co-twins on the standard error, i.e., the fact that because of this correlation the co-twin produces less information than if unrelatedindividualswouldhavebeensampled.TheWaldtestis equivalent to a standard chi-square test for independence, and in it the Pearson chi-square statistic is corrected for the survey design with the second-order correction of Rao and Scott (1984) and is converted into an F statistic, with appropriate degrees of freedom. In addition, an empirical p value was calculated to explore significance of a difference between two groups when size of one group was small and very different from that of the other group.
Results The odor of androstenone was not detected (defined as rating 1, ‘‘Noodor’’)by55(23%)womenand36(24%)men(twowomen and one man did not provide a response). Among the 303 individuals who were able to detect the odor of androstenone, women (n = 187, M = 4.2, SD = 1.9) rated the odor as more intense than did men (n = 116, M = 3.5, SD = 1.5), Wald test F(1, 216) = 7.54, p = .007, d = 0.40, but the ratings of the pleasantness did not differ significantly between women (M = 4.4, SD = 1.7) and men (M = 4.6, SD = 1.4).
Table 1 Women’s ratings of the odor stimuli by sexual intercourse experience Rating
No partners
One or more partners
Comparison of the groups
n
M
(SD)
n
M
(SD)
d
F(1, dferr)
dferr
p
Androstenone
12
5.2
(1.9)
175
4.1
(1.9)
0.55
2.60
132
ns
Cinnamon
15
5.1
(1.8)
207
4.8
(1.8)
0.16
0.41
142
ns
Chocolate
17
4.9
(1.9)
222
5.4
(1.6)
0.35
1.47
149
ns
Intensity
Isovaleric acid
17
6.1
(1.8)
221
5.8
(1.7)
0.16
0.39
149
ns
Lemon
17
7.1
(1.9)
224
6.7
(1.4)
0.27
0.60
148
ns
Turpentine
17
5.9
(1.7)
222
6.4
(1.6)
0.30
1.13
149
ns
Androstenone
12
3.1
(1.5)
175
4.5
(1.7)
0.83
7.89
132
.006
Cinnamon Chocolate
15 17
6.3 5.1
(1.4) (1.7)
207 222
6.0 4.9
(1.7) (1.8)
0.22 0.14
0.69 0.45
147 149
ns ns
Pleasantness
Isovaleric acid
17
3.4
(2.3)
221
2.9
(1.8)
0.30
0.86
149
ns
Lemon
17
5.2
(2.2)
224
4.9
(1.8)
0.18
0.38
149
ns
Turpentine
17
5.2
(1.7)
221
4.9
(1.9)
0.16
0.90
149
ns
Note: The variation in sample size is due to the variation in the number of women who rated the intensity of an odor stimulus as‘‘no odor’’as they were excluded from further analyses of the respective odor, and due to the variation in the number of missing responses. d = Cohen’s d (effect size); F(1, dferr) = F value from the Wald test comparing the groups; dferr = error df from the Wald test after correcting the data for clustering in twin pairs. Potential range for the ratings was 1–9
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Depue,1987), personality dimensions (NEO-FFI; Costa & McCrae, 1992), use of hormonal contraceptives, or the age of initiation of sexual intercourses (data not shown).
d = 0.42 (Table 2). However, this association was not confirmed by the empirical p value of .06, calculated in an analogous way as above for the pleasantness of androstenone in women. No other associations were observed between sexual intercourse experience and ratings of the odors in either sex (Tables 1, 2). We found no association between sexual intercourse experience and detection of the odor of androstenone in either sex (Table 3). Among twin sister pairs who were concordant for being able to detect androstenone (n = 54 pairs), only two pairs were discordant for having had sexual partners (none/one or more), permitting no useful within-pair comparisons. Our supplementary analyses found no association between the pleasantness of androstenone and depression (GBI;
Discussion Among young adults who were able to detect the odor of androstenone, women who had had at least one sexual intercourse partner rated the odor as more pleasant (less unpleasant) than did women who had had no sexual partners. The women with intercourse experience may have encountered the odor of androstenone during sexual contacts in a romantic relationship and paired the presumably positive hedonic value of the sexual
Table 2 Men’s ratings of the odor stimuli by sexual intercourse experience Rating
No partners
One or more partners n
M
Comparison of the groups (SD)
d
F(1, dferr)
dferr
p
n
M
(SD)
Androstenone
16
4.0
(1.7)
97
3.4
(1.5)
0.39
1.44
89
ns
Cinnamon Chocolate
18 21
4.9 5.8
(1.8) (1.5)
118 127
4.8 5.7
(1.8) (1.6)
0.06 0.07
0.06 0.13
103 103
ns ns
Intensity
Isovaleric acid
22
5.6
(1.8)
128
5.7
(1.8)
0.05
0.04
104
ns
Lemon
22
6.2
(1.8)
127
6.4
(1.5)
0.13
0.28
104
ns
Turpentine
22
5.9
(1.6)
127
6.1
(1.7)
0.12
0.28
104
ns
Androstenone
16
4.4
(1.5)
97
4.7
(1.4)
0.22
0.64
89
ns
Cinnamon
18
5.8
(1.6)
118
5.9
(1.7)
0.10
0.81
102
ns
Chocolate
21
4.5
(1.6)
127
4.8
(1.8)
0.14
0.87
104
ns
Isovaleric acid
22
2.9
(1.1)
128
2.7
(1.3)
0.17
0.66
104
ns
Lemon
22
5.2
(2.2)
126
5.3
(1.7)
0.09
0.14
103
ns
Turpentine
22
4.8
(1.3)
127
5.5
(1.7)
0.42
4.75
104
.03
Pleasantness
Note: The variation in sample size is due to the variation in the number of men who rated the intensity of an odor stimulus as‘‘no odor’’as they were excluded from further analyses of the respective odor, and due to the variation in the number of missing responses. d = Cohen’s d (effect size); F(1, dferr) = F value from the Wald test comparing the groups; dferr = error df from the Wald test after correcting the data for clustering in twin pairs. Potential range for the ratings was 1–9
Table 3 Detection of the odor of androstenone in women and men by sexual intercourse experience Detection of androstenonea
Womenb
Menc
No partners
One or more partners
No partners
12 (70.6%)
175 (78.1%)
16 (72.7%)
97 (76.4%)
5 (29.4%)
49 (21.9%)
6 (27.3%)
30 (23.6%)
Total
17 (100.0%)
224 (100.0%)
22 (100.0%)
127 (100.0%)
Fisher’s exact test (2-sided)
p = .55
Yes (perceived) No (not perceived)
a
One or more partners
p = .79
Participants were classified according to the intensity ratings for the androstenone stimulus: Individuals who rated the intensity as 1 (‘‘no odor’’) were regarded as not having perceived the odor and the others (rating 2–9) were regarded as having perceived the odor
b
Three women out of 244 had no information about partners or the intensity rating
c
Four men out of 153 had no information about partners or the intensity rating
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experience with the odor. Thus, associative learning may underlie the relationship between sexual intercourse experience and the pleasantness of the odor of androstenone. In mice, male sexual pheromones having critical non-volatile components detected by the vomeronasal organ (VNO) are innately attractive to female mice, whereas volatile malederived olfactory stimuli are not. However, it has been shown that after repeated exposure of female mice to male-soiled bedding, the female mice developed an acquired preference for male odors, presumably due to pairing with the intrinsically attractive pheromones (Martinez-Garcia et al., 2009). In the absence of a functional VNO in humans, we speculate that women may substitute actual mating experience for VNOdetection of non-volatile chemosignals to increase the positive valence of the volatile steroid, androstenone. Novelty of a stimulus is central for associative learning to occur, which may explain why the association was specific to women. Androstenone is found in higher concentrations in apocrine secretions of men than those of women (Gower et al., 1994). Yet, androstenone was not found among volatile organic compounds from nonaxillary skin (upper back and forearm), which harbored isovaleric acid (Gallagher et al., 2008). This suggests that exposure to androstenone (but not isovaleric acid) maybespecifictoaclosecontactwithaman.Thus,men(regardless of sexual experience) may be more familiar with the odor of androstenone than are women without sexual experience. Furthermore, the perception of androstenone is sexually bimodal in humans: Women, in general, perceive the odor as stronger than do men (Wysocki & Gilbert, 1989), as also observed in the present study. Our supplementary analyses did not reveal additional factors being associated with the pleasantness of androstenone. Although an inverse association between the pleasantness of partner odor (natural mixture of odorants) and depression and anxiety was recently reported (204 men and 452 women, age M = 41.9 years,SD = 0.7;Sookoian,Burgueno,Gianotti,Marillet, & Pirola, 2010), we did not find a correlation between the score of depression symptoms and the pleasantness of androstenone, a single body odor component. Limitations of our study include its cross-sectional design, which leaves causality of the association between sexual experience and the pleasantness of the odor of androstenone uncertain. Further, among women who were able to detect the odor of androstenone, only 12 had not had sexual intercourse. However, the association between intercourse experience and thepleasantnessofandrostenonewasstatisticallysignificantby both a two-sided Wald test and an empirically calculated p value; thus, the sample size was sufficient to show the association.Yet,wedonotknowwhetherthewomenperceivedtheodor of androstenone during sexual intercourse. However, we analyzed data only from participants who perceived an odor from androstenone and, even if the concentration of this lab stimulus was higher than androstenone perceived in natural contexts, the
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natural concentration may be sufficient to serveas a conditioned stimulus, because even weak, unnoticed olfactory stimuli can induce conditioned hedonic responses in humans (Kirk-Smith, VanToller,&Dodd,1983;Zucco,Paolini,&Schaal,2009).Nor did we ask if a participant’s sexual experience was with a samesex partner, even though sexual orientation influences preference for human body odors (Martins et al., 2005). The sexual orientation of men has been reported to be associated with sensitivitytoandrostenone,yetitwasnotrelatedtotheirhedonic or emotional responses to the odor (Lu¨bke, Schablitzky, & Pause, 2009). Finally, we cannot be certain whether the intercourseexperienceoftheparticipantswaspleasant,asweassumed. Since we could not show that the conditioning actually took place, an alternative interpretation of our results, without associative learning, can be proposed. Perceived intensity and pleasantnessoftheodorofandrostenoneismodifiedbyvariants of the olfactory receptor gene OR7D4 (Keller, Zhuang, Chi, Vosshall, & Matsunami, 2007). Women who are genetically primed to perceive the odor of androstenone as highly intense and unpleasant may also find male odor aversive and thus, be lesslikelytohavesexualintercoursewithamanthanarewomen whocannotsmellandrostenoneorwhoperceiveitasaneutralor pleasant odor. In conclusion, the present results suggest that sexual experience may increase the hedonic value of the odor of androstenone through associative learning in women. Thus, the possibility of naturally occurring evaluative conditioning should be taken into account when exploring chemosignals emanating from the human body. Acknowledgments This study was supported by Kone Foundation (K.S. & A.K.) and Monell Chemical Senses Center (A.K.). Data collection from twins was supported by National Institutes of Health grant AA-12502 (R.J.R.), Academy of Finland grants 100499 & 205585 (J.K.) and 206327 (H.T.), the Academy of Finland Centre of Excellence in Complex Disease Genetics (J.K.), and the DIOGENES, project supported by the European Union (Contract no. FP6-513946). A.K. thanks Dr. Charles Wysocki for helpful discussions and constructive comments onthemanuscript andLiang-Dar(Daniel) Hwang, MSc.,forassistancein calculation of the empirical p values.
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