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Doi:10.1016/j.biopsycho.2005.07.00

Biological Psychology xxx (2005) xxx–xxx Effects of reproductive state on olfactory sensitivity Johan N. Lundstro¨m ,Martha K. McClintock , Mats J. Olsson a Department of Psychology, Uppsala University, Box 1225, SE-75142 Uppsala, Sweden b Institute for Mind and Biology, University of Chicago, Chicago, 940 57th Street, 60637, IL, USA Received 6 December 2004; accepted 1 July 2005 Previous studies of reproductive state and olfactory sensitivity in women have not directly compared thresholds for social and environmental odors. Here, we used successive dilutions presented in a staircase protocol to determine olfactory thresholds for andros-tadienone, a social odor produced by men, and rose, an environmental odor signaling a source of micronutrients essential for successfulimplantation, prenatal development and maternal health. Fertile women were more sensitive to the social than the environmental odor, whilewomen using oral contraceptives, a non-fertile hormonal state similar to early pregnancy, were more sensitive to the environmental odor. Thispreliminary study sets the stage for further work on the interaction between hormonal states and sensitivity to specific odors with reproductivesignificance.
# 2005 Elsevier B.V. All rights reserved.
Keywords: Odor; Oral contraceptives; Reproduction; Social odor; Individual sensitivity In this initial study, we choose rose (phenyl–ethyl alcohol, PEA) a well-characterized environmental odorant.
Previous studies investigating the effects of different Rose petals, leaves, roots, and hips are used in salads, reproductive states on women’s olfactory sensitivity have conserves and medicines and they contain high concentra- not distinguished between their effects on social and tions of micronutrients essential for implantation, embryo- environmental odors. We hypothesized that spontaneously nic development and maternal health (e.g., Vitamins A and C ovulating women would be more sensitive to social than environmental odors, particularly in the fertile or estrogen ). Androstadienone was chosen as the social odorant, as dominant phase of the menstrual cycle, while women in this steroid is present in the sweat, urine and semen of men progesterone dominant states would be more sensitive to environmental odors. Our hypothesis derives from the animal literature demonstrating that social cues enhance ). Even in very high concentrations neither andros- whereas environmental odors, particularly those asso- activates the trigeminal system, which ensured that only ciated with nutrition, signal foods that reduce risk of olfactory sensitivity was assessed by the method used here.
perimplantation loss, prenatal malformations and malnu- We compared women who were ovulating spontaneously to non-ovulating women using oral contraceptives. These contraceptives create a hormonal profile with equally highlevels of estrogens and progestins, more similar to the lutealphase and early pregnancy than to the estrogen dominant * Corresponding author. Tel.: +46 18 471 6221; fax: +46 18 471 2123.
E-mail address: johan.lundstrom@psyk.uu.se (J.N. Lundstro¨m).
0301-0511/$ – see front matter # 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.biopsycho.2005.07.001 J.N. Lundstro¨m et al. / Biological Psychology xxx (2005) xxx–xxx Threshold tests were of an ascending staircase, three- alternative, no feedback, forced-choice design. Each trial Fifty-two women (23 Æ 3.4 years) with self-reported included one target (a container with the odorant in absence of nasal congestion, infection, and olfactory propylene glycol) and two control stimuli (containers with dysfunctions participated in the study. All reported stable only propylene glycol). Odorants were presented in menstrual cycles (29 Æ 3 days; range 26–33 days). Oral ascending concentrations until the participant correctly contraceptive users (n = 30) had been doing so for longer discerned the odorant in two successive trials, which than six months prior to testing. Of the spontaneously ovulating women, 11 were deemed to be in the fertile ended after seven reversals of the staircase. The mean of the phase (Days 7–15 post menses onset by self report). This concentration at the last four reversal points was calculated time span incorporates the follicular and periovulatory to estimate the olfactory threshold. The position of the target phases, and was designated the fertile phase when container was randomized with each trial as was the order of conception is possible (sperm live 3–5 days in the determining PEA and androstadienone thresholds.
fallopian tubes). An equal number of women (N = 11)were in the non-fertile phase: menses Days 1–6 or 15–33post menses onset.
Although defining menstrual cycle phase relative to self-reported menses onset is standard clinical practice, wefully recognize that this referrant alone is not as precise as As hypothesized, greater sensitivity for social or also measuring the preovulatory LH surge and thereby environmental odors was the opposite in non-fertile and fertile women [see ; interaction, F(1, 50) = 8.63, this study’s criteria for the fertile phase with our P < .01, no main effect of odorant, F(1, 50) = .90, P ns, no laboratory’s large sample of menstrual cycles (N = 300) main effect of oral contraceptive use, F(1, 50) = .21, P ns].
with both self-reported menses onset and the day of the Women taking contraceptive pills had a higher sensitivity for preovulatory LH surge documented by hormone assay.
PEA than androstadienone [10.01 Æ .64 versus 7.73 Æ .61 Given that all women in this study had menstrual cycles dilution steps; t(50) = 2.20, P < .05]. Conversely, sponta- between 26 and 33 days long, the previously collected data neously ovulating women tended to have a higher sensitivity indicate that the criteria used in this study had a high for androstadienone than PEA [9.09 Æ .65 versus 7.93 Æ .67 probability of accurately assigning 98.6% of women to the dilution steps; t(50) = 1.50, P < .10]. This apparently fertile phase, with only 0.04% misclassified as non-fertile.
weaker difference in spontaneously ovulating women was This slight misclassification serves as a conservative an artifact of combining data from women who were in the constraint since it reduces the probability of detecting a fertile and non-fertile phases of spontaneous menstrual difference between the fertile phase and the rest of the cycles. Women in the fertile phase were more sensitive to the social odorant androstadienone than were women in the non-fertile phase, t(20) = 2.35, P < .05, who in turn were indistinguishable from women using oral contraceptives[see ; fertile period = 10.48 Æ .55 dilution steps, non- Detection thresholds for PEA were assessed using the fertile period = 7.71 Æ 1.0 dilution steps, and oral contra- well-validated ‘‘Sniffin Sticks’’ set (); ceptive users = 7.73 Æ .61 dilution steps]. There was no felt-tip pens filled with PEA in different concentrations.
difference in sensitivity to PEA between spontaneously Detection threshold for androstadienone was assessed with250 ml polypropylene squeeze bottles, with pop-up spouts,containing 15 ml solution. Plastic squeeze bottles wereused to present androstadienone, a heavy molecule thatmight be retained in the felt-tip of the pen. Differences inthresholds using these two types of presentation containershave been shown to be insignificant (Both compounds were diluted in pure propylene glycol,PEA ranged from 16.3 mM (dilution 16) to 0.54 M(dilution 1) in a geometric series consisting of 16 stepswith dilution ratio of 1:2. Androstadienone ranged from0.091 mM (dilution 16) to 3000 mM (dilution 1) in a Fig. 1. Effect of usage of contraceptive pills on olfactory sensitivity to geometric series consisting of 16 steps with a dilution ratio phenyl–ethyl alcohol (an environmental odor) and androstadienone (a social odor). Error bars in graph denote S.E.M.
J.N. Lundstro¨m et al. / Biological Psychology xxx (2005) xxx–xxx hormonal states and sensitivity to specific odors withreproductive significance.
Supported by the Swedish Council for Research in Social Science and Humanities (HSFR:F0868), the Bank ofSweden Tercentenary Foundation (J2004-0828) to MJO,the Thord Gray Memorial Fund, American Scandinavian Fig. 2. Androstadienone thresholds for women during their fertile period (FP), non-fertile period (NFP) and oral contraceptive users (OC). Error barsin graph denote S.E.M.
ovulating women in the fertile phase and non-fertile phases, Archunan, G., Dominic, C.J., 1989. Nutritional stress-induced implantation failure in newly inseminated mice: effect of the presence of stud males.
Thus, the effect of a women’s reproductive state on her Experimental and Clinical Endocrinology 94 (3), 233–238.
Broman, D.A., Olofsson, J.K., Murphy, C., Nordin, S., 2003. Changes in olfactory sensitivity depends on the identity of the odorant, olfactory sensitivity and perception in pregnancy. In: Paper Presented at corroborating earlier studies of non-biological odorants the Society for Neuroscience, New Orleans, LA.
Bullivant, S.B., Sellergren, S.A., Stern, K., Spencer, N.A., Jacob, S., women’s sensitivity to androstadienone, a male social odor, Mennella, J.A., et al., 2004. Women’s sexual experience during the is highest in the fertile phase, when estrogen is predominant, menstrual cycle: identification of the sexual phase by noninvasivemeasurement of luteinizing hormone. Journal of Sex Research 41 consistent with its potential function as a human social Doty, R.L., 2003. Handbook of Olfaction and Gustation, vol. 57, second ed.
Conversely, sensitivity to an environmental odor was Doty, R.L., Snyder, P.J., Huggins, G.R., Lowry, L.D., 1981. Endocrine, highest in contraceptive pill users, whose profile is more cardiovascular, and psychological correlates of olfactory sensitivitychanges during the human menstrual cycle. Journal of Comparative like that of women in early stages of pregnancy. Indeed, Physiology and Psychology 95 (1), 45–60.
pregnant women seem to have an altered olfactory Gower, D.B., Ruparelia, B.A., 1993. Olfaction in humans with special reference to odorous 16-androstenes: their occurrence, perception and a sensitivity that others have suggested act as a sentinel for possible social, psychological and sexual impact. Journal of Endocri- Grases, F., Masarova, L., Costa-Bauza, A., March, J.G., Prieto, R., Tur, J.A., our data suggests that the olfactory system of pregnant 1992. Effect of ‘‘Rosa Canina’’ infusion and magnesium on the urinary women is primed to detect sources of nutrition or teratogenic risk factors of calcium oxalate urolithiasis. Planta Medica 58 (6), 509– threats. Future work is needed to determine if our findings hold for other odorants relevant to maternal and fetal health, Gu, G., Varoqueaux, F., Simerly, R.B., 1999. Hormonal regulation of as well as for other types of environmental odors.
glutamate receptor gene expression in the anteroventral periventricularnucleus of the hypothalamus. Journal of Neuroscience 19 (8), 3213– In addition, women’s reproductive state could have differentially affected sensitivity to these particular odorants Hummel, T., Sekinger, B., Wolf, S.R., Pauli, E., Kobal, G., 1997. ‘Sniffin’ because they also represent a contrast in masculine/feminine sticks’: olfactory performance assessed by the combined testing of odor odors, as well as odors with negative/positive emotional identification, odor discrimination and olfactory threshold. Chemical valence. Future work, employing direct measures of Jacob, S., McClintock, M.K., 2000. Psychological state and mood effects of hormonal state, will be needed to distinguish among these steroidal chemosignals in women and men. Hormones and Behavior 37 alternative hypotheses. Doing so will also elucidate whether these state-dependent effects on olfactory thresholds are Kay, L.M., Laurent, G., 1999. Odor- and context-dependent modulation of driven by central changes in motivational state and meaning mitral cell activity in behaving rats. Nature Neuroscience 2 (11), 1003– systems that regulate the peripheral mechanisms of the Kolble, N., Hummel, T., von Mering, R., Huch, A., Huch, R., 2001.
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Lundstrom, J.N., Goncalves, M., Esteves, F., Olsson, M.J., 2003a. Psycho- demonstration of an odorant-dependent variation in olfac- logical effects of subthreshold exposure to the putative human pher- tory sensitivity during the human menstrual cycle and sets omone 4,16-androstadien-3-one. Hormones and Behavior 44 (5), 395– the stage for further work on the interaction between J.N. Lundstro¨m et al. / Biological Psychology xxx (2005) xxx–xxx Lundstrom, J.N., Hummel, T., Olsson, M.J., 2003b. Individual differences in Navarro Becerra, N., Grigorjev, C., Munaro, N., 1996. Glutamic sensitivity to the odor of 4,16-androstadien-3-one. Chemical Senses 28 acid decarboxylase in rat olfactory bulb: effect of ovarian steroids or male pheromones. European Journal of Pharmacology 312 (1), McClintock, M.K., 2003. Pheromones, odors, and vasanas: the neuroendo- crinology of social chemosignals in humans and animals. In: Pfaff, D.W.
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