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A Meta-Analysis of Menstrual Cycle Variation in Olfactory Sensitivity

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A Meta-Analysis of Menstrual Cycle Variation in Olfactory Sensitivity Lenka Martinec Nováková, Jan Havlíček, S. Craig Roberts Olfactory processing and odor specificity ANTHROPOLOGICAL REVIEW • Vol. 77 (3), 331–345 (2014) ANTHROPOLOGICAL REVIEW Available online at: www.degruyter.com Journal homepage: www.ptantropologiczne.pl Olfactory processing and odor specificity: a meta-analysis of menstrual cycle variation in olfactory sensitivity Lenka Martinec Nováková1, 2, Jan Havlíček2, S. Craig Roberts3 1Department of Anthropology, Faculty of Humanities, Charles University, Prague, Czech Republic 2Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic 3School of Natural Sciences, University of Stirling, Stirling, UK ABSTRACT: Cycle-correlated variation in olfactory threshold, with women becoming more sensitive to odors mid-cycle, is somewhat supported by the literature but the evidence is not entirely consistent, with several studies finding no, or mixed, effects. It has been argued that cyclic shifts in olfactory threshold might be limited to odors relevant to the mating context. We aimed to test whether the evidence currently available points in the direction of odor-specific or, rather, general changes in olfactory sensitivity and, if the former is the case, to what group of odorants in particular. We carried out a meta-analysis of relevant studies which together used a variety of different odorants, including some found in food, body odor, and some that occur in neither of these. First we tested whether there appears to be an overall effect when all studies are included. Next, we hypothesised that if cyclic changes in olfactory processing are odor-specific and tuned to biologically relevant odors, we should find changes in detection thresholds only for odorants found in body odor, or for those that are perceptually similar to it. In contrast, if threshold patterns are linked to more general fluctuations in odor processing across the cycle, we would not expect changes in relation to any particular odorant group. The results support the view that there is significant cycle-correlated variation. Thresholds were in general significantly lower in the fertile than the non-fertile phases, with effect sizes consistently in this direction. This same conclusion applied to both ‘food’ and ‘musky’ odorants, despite their different evolutionary significance, and to the androgen steroids (androstadienone, androstenone, and androsterone), but could not be applied to phenyl-ethyl alcohol. The results indicate that olfactory sensitivity may be a non-adaptive by-product of the general physiological fluctuations or differences in neural processing experienced across the cycle to a broad spectrum of odor- ants, rather than being specifically selected for mate choice-related odors. KEY WORDS: menstrual cycle, mate choice, odor threshold, human oestrus, olfaction Original Article: Received: 16 October 2014; Accepted for publication: 5 November 2014 DOI: 10.2478/anre-2014-0024 © 2014 Polish Anthropological Society 332 Lenka Martinec Nováková, Jan Havlíček, S. Craig Roberts Introduction – to three – day intervals. In general, he found an increase in sensitivity (decrease In recent years, researchers interested in in odor threshold) in all cycles follow- the evolutionary underpinnings of hu- ing menstruation but, at the same time, man behaviour have recorded in women the individual cycles varied considerably a variety of behavioural and perceptual in the timing and magnitude of this in- changes associated with menstrual cycle crease. For instance, while in some cases phase (review in Gangestad and Thorn- sensitivity peaked shortly after menstru- hill 2008). The cyclic shifts in sensory ation, in others it took longer. Moreover, perception seem to cut across sensory he also noted a second peak in sensitivity modalities (Doty et al. 1982; Dye 1992; during the late luteal phase in three cas- Kuga et al. 1999) and may be linked to es. However, no such changes in sensitiv- general physiological fluctuations or ity to safrole, guaiacol, amyl salicylate, or differences in neural processing experi- pyridine were noted in a smaller number enced across the menstrual cycle. Doty of tested women, except for a mixture of and Cameron (2009) reviewed the ways cholesterol and testosterone. Hence, it through which such a general effect would seem that menstrual cycle-relat- would be possible. They put forward ed changes in olfactory sensitivity would the idea that cyclic changes may reflect pertain exclusively to musky-smelling fluctuations in hormones other than the odorants, suggesting that they might be primary ovarian steroids, suggesting the of special ecological significance to hu- potential involvement of the corticotrop- mans. ic releasing hormone (CRH) – adren- In contrast to the findings ofLe Magnen ocorticotropic hormone (ACTH) – ad- (1952), Mair et al. (1978), who employed renal axis. Alternatively, they propose a signal detection paradigm, reported that these shifts may be controlled by women’s better performance during ovu- central nervous system centres or net- lation compared to menstruation for pen- works such as those that control various tadecalactone (Exaltolide) as well as for other rhythms (e.g. Rusak and Zucker coumarin and cinnamyl butyrate (but not 1979), for instance specific or non-spe- amyl acetate). Other researchers have also cific effects of neurotransmitters or other noted significant cyclic variation in sensi- neuroactive substances that fluctuate on tivity not only to pentadecalactone (Good a monthly basis. et al. 1976; Vierling and Rock 1967), but Of the various sensory modalities, also to other musk-smelling odorants, among the most hotly debated is cyclic such as 5α-androst-16-en-3-one (andros- variation in olfactory thresholds for both tenone; e.g. Renfro and Hoffmann 2013; social (i.e. human body odor-related) Sueda et al. 2003) or musk-ketone (Caru- and non-social odors (review in Doty and so et al. 2001), as well as those that are Cameron 2009). The suggestion that ol- not considered to be of biological rele- factory detection thresholds vary across vance to humans, such as ammonia, anise the menstrual cycle was first reported essence, citral, eugenol (clove odor), fur- over 50 years ago (Le Magnen 1952). In fural, or pyridine (e.g. Caruso et al. 2001; one study, he measured thresholds for Doty et al. 1981). Navarrete-Palacios et al. pentadecalactone (Exaltolide) across ten (2003) also reported menstrual cycle-re- menstrual cycles of five women with two lated fluctuations in amyl acetate thresh- Olfactory processing and odor specificity 333 olds, contrary to the findings of Mair et the present topic, measures of odor de- al. (1978). On the other hand, some re- tection performance, body temperature, searchers have not found any significant heart rate, plasma FSH, LH, progester- changes in sensitivity to androstenone, one, and total estrogens were taken twice citral, pure lemon extract, n-butanol, ni- a day. Most notably, they observed a pos- cotine, pure peppermint extract, pheny- itive correlation between body tempera- lethyl alcohol, or rose water (Hummel et ture and olfactory sensitivity. al. 1991; McNeil et al. 2013; Pause et al. Thus, cycle-correlated variation in 1996; Renfro and Hoffmann 2013). olfactory threshold, with women becom- A major contribution to the debate ing more sensitive to odors mid-cycle, is comes from Doty et al. (1981), who, somewhat supported by the literature but employing a signal detection paradigm, the evidence is not entirely consistent, tested odor detection performance for with several studies finding no, or mixed, furfural every other day across 2 con- effects. A major question that arises is secutive menstrual cycles of both oral whether the evidence currently available contraceptive non-users and users. Fur- points in the direction of odor-specific thermore, concomitant measures of body or, rather, general changes in olfactory temperature, blood pressure, heart rate, sensitivity. Furthermore, if the former nasal airflow, and respiration rate were is the case, what group(s) of odorants also taken as well as levels of estradiol, in particular are affected? For example, estrone, follicle stimulating hormone might increased mid-cycle sensitivity be (FSH), luteinizing hormone (LH), pro- specific to musky-smelling odorants and gesterone, and testosterone. To handle the androstenes, which may possess bi- problems related to averaging data across ological relevance through an influence menstrual cycles of different lengths, the on mate choice? Consistent with this authors used a procedure devised by Doty idea, Lundström et al. (2005) found that (1979). They found three peaks in aver- menstrual cycle stage influenced sensi- age olfactory sensitivity: in the middle of tivity to a biologically-relevant odorant the cycle (around ovulation), in the mid- androsta-4,16,-dien-3-one (androstadi- dle of the luteal phase, and in the second enone), but not to phenylethyl alcohol half of the menstrual phase. Remarkably, (PEA, rose odor). Similarly, Renfro and these fluctuations were observed in both Hoffmann (2013) reported cyclic varia- oral contraceptive non-users and users, tion in sensitivity to androstenone and suggesting that there may not be a caus- 3α-hydroxy-5α-andro stan-17-one (an- al relationship between levels of gonadal drosterone), but not to pure lemon or hormones and hypophyseal gonadotro- peppermint extract, or rose water. pins and olfactory thresholds but, rather, Here we aimed to further test whe- a correlation. ther the menstrual
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