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J Neurosci Psychol Econ. Author manuscript; available in PMC 2017 June 01. Published in final edited form as: J Neurosci Psychol Econ. 2016 June ; 9(2): 88–99. doi:10.1037/npe0000055.

The Putative Chemosignal Androstadienone Makes Women More Generous Valentina Perrotta, Department of Knowledge, Autonomous Province of Trento, via Gilli, 3, I-38122 Trento TN, Italy

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Michele Graffeo, Department of Economics and Management, University of Trento, Via Inama 5, I-38122 Trento, Italy Nicolao Bonini, and Department of Economics and Management, University of Trento, Via Inama 5, I-38122 Trento, Italy Jay A. Gottfried Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA Valentina Perrotta: [email protected]; Michele Graffeo: [email protected]; Nicolao Bonini: [email protected]; Jay A. Gottfried: [email protected]

Abstract Author Manuscript Author Manuscript

Putative human chemosignals have been shown to influence mood states and emotional processing, but the connection between these effects and higher-order cognitive processing is not well established. This study utilized an economic game (Dictator Game) to test whether androstadienone (AND), an odorous compound derived from testosterone, impacts on altruistic behavior. We predicted that the female participants would act more generously in the AND condition, exhibiting a significant interaction effect between gender and AND on Dictator Game contributions. We also expected that the presence of AND should increase the positive mood of the female participants, compared to a control odor condition and also compared to the mood of the male participants. The results confirm our hypotheses: for women the subliminal perception of AND led to larger monetary donations, compared to a control odor, and also increased positive mood. These effects were absent or significantly weaker in men. Our findings highlight the capacity of human putative chemosignals to influence emotions and higher cognitive processes – in particular the processes used in the context of economic decisions – in a gender-specific way.

Keywords androstadienone; olfaction; mood; generosity; Dictator Game

Corresponding author: Michele Graffeo, Department of Economics and Management, University of Trento, Via Inama 5, I-38122 Trento, Italy. phone: (+) 39 0461-282100, fax: (+) 39 0461-282241, [email protected].

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INTRODUCTION “Odors have a power of persuasion stronger than that of words, appearances, emotions, or will. The persuasive power of an odor cannot be fended off, it enters into us like breath into our lungs, it fills us up, imbues us totally. There is no remedy for it.” (Süskind, 1985/2001, p.82).

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The assumption that human beings act in their own self interest has been a dominant model of studies on economic decision-making. However, altruistic behavior is a central element of modern societies that challenges this assumption (see Oppenheimer and Olivola, 2010, for a recent review on experimental studies on charity). Indeed, generosity is part of human nature, and in this study we show that it can be enhanced by chemical signals. As Süskind implies, odors may have a stronger influence than other incidental information (i.e., not related to the problem at hand) in guiding our everyday behavior, perhaps reflecting the intimate anatomical overlap between the olfactory system and limbic brain networks regulating emotionally based responses (Gottfried, 2010). For example, in the context of pro-social decisions, Liljenquist, Zhong, and Galinsky (2010) showed that a “clean” odor increases the propensity to donate money for charities. The effect of odors becomes stronger if the ambient scent is semantically congruent with the evaluated object, for example a public good (e.g., lemon odor increases donations for lemon gardens; Bonini, Graffeo, Hadjichristidis & Perrotta, 2015). Interestingly, not only detectable and pleasant odors – but also putative olfactory chemosignals – are capable of eliciting behavioral changes. For example, the presence of a putative chemosignal (4,16-androstadien-3-one; AND, a testosterone-derived molecule) was shown to increase women’s attraction to men in a speed dating context (Saxton, Lyndon, Little, & Roberts, 2008). AND has been identified in human sweat, semen, and plasma (Kwan, Trafford, Makin, Mallet, & Gower, 1992; Labows, 1988; Nixon, Mallet, & Gower, 1988; Rennie, Holland, Mallet, Watkins, & Gower, 1990), ovaries and adrenal glands (McClintock, 2000; Smals & Weusten, 1991), and on the skin and axillary hair (Preti & Wysocki, 1999). Several studies indicate that AND improves positive mood (Bensafi, Tsutsui, Khan, Levenson, & Sobel, 2004b; Jacob & McClintock, 2000) and activates brain areas associated with attention, emotional processes, and sexual behavior (Gulyas, Keri, O’Sullivan, Decety, & Roland, 2004; Jacob, Kinnunen, Metz, Cooper, & McClintock, 2001; Savic, Berglund, Gulyas, & Roland, 2001). Taken together these data suggest that AND might possess chemosignaling properties that modulate emotional states and behaviors.

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Congruent with the concept of a sex chemosignal, many of the effects of AND seem to be gender-specific, such that this compound has a particular effect on emotional states (e.g., mood and attractiveness ratings) in females. The current investigation shifts the behavioral focus of AND from its well-known influence on attention and emotional states to the psychological processes involved in economic decisions such as choices in a task known as the Dictator Game (DG; Kahneman, Knetsch, & Thaler, 1986). This is an economic game typically used to measure altruism in a social context. In the DG, the first player, “the dictator”, determines an allocation (split) of a monetary endowment. The second player, “the receiver”, must accept the proposal. This game was first used to test the Homo Economicus J Neurosci Psychol Econ. Author manuscript; available in PMC 2017 June 01.

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model of individual behavior (Fehr & Gachter, 2000; Rodriguez-Sickert, 2009), namely, a model in which individuals are only concerned with their own economic well-being. If this is the case, then the dictators would always allocate the entire sum to themselves. However, experimental results indicate that individuals are often generous: they allocate some money to the receivers, by reducing the amount of money they keep for themselves. Prior work on the DG has not reported systematic evidence for gender differences in the amount of donations (Camerer, 2003; Croson & Buchan, 1999).

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The connection between generosity and androstadienone has been shown in male participants (Huoviala & Rantala, 2013), though this study did not compare the differential effect of AND between men and women, nor did it take into account that AND can modify the emotional states of the participants. Here we hypothesized that AND unconsciously modulates altruistic behavior in this decision-making task, increasing the propensity to donate, over and above the effects of AND on mood per se. Congruent with the notion of a putative sex chemosignal, we also predicted that the effects would be stronger for female participants. Our findings support the idea that AND affects higher cognitive processes used in the context of economic decisions, increasing generosity in contrast with the predictions of the Homo Economicus model.

METHODS Participants

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Thirty-seven university students (19 women), with a mean age of 24 years (range 18–40 years), took part in this experiment. All of the participants were naïve to the purpose of the study and they all completed an informational questionnaire in order to verify that they had a normal sense of smell, no history of olfactory dysfunction, and no drug use including contraceptives. In addition, because cyclic variations in hormone levels can influence how olfactory information is processed (Pause, Sojka, Krauel, Fehm-Wolfsdorf, & Ferstl, 1996), all female participants were asked about the current phase of their menstrual cycle, in order to limit their participation to the ovulatory period (12th–18th day post-menstruation).

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Before the beginning of the game the participants read the instructions and were given the opportunity to ask questions. They were also informed that they would be paid according to their decisions. This incentive scheme would encourage participants to make a careful decision (payment range: from 8 to 24 euro). Specifically, they received the amount of money that they kept (as dictators) in two trials selected at random (one from the experimental condition and one from the control condition), plus €8 as show-up fee. The Northwestern University Institutional Review Board approved the present experiment and the associated informed consent form. All the participants provided a written informed consent and the experiment was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. Compounds AND was obtained from Steraloids Inc. (Newport, RI, USA). For the experimental condition we dissolved 5mg of AND into 3ml of limonene (R(+); 97% purity; Sigma-Aldrich, USA);

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the AND concentration was 650μM. We used this concentration because this dosage has an enhancing effect on positive mood mainly in females (Bensafi et al., 2004b). Limonene is a terpene with a light lemon-citrus odor and flavor commonly used in alimentary and cosmetic products. This odorant served as both carrier and mask (containing AND) and as a control odor (presented without AND). AND was undetectable in this solution (see next section below). We used limonene as the carrier because clove oil, a commonly used carrier in studies on chemosignals (Havlicek, Murray, Saxton, & Roberts, 2010), was too persistent and pungent for subjects in pilot testing.

PROCEDURE Discrimination screening

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To ensure that the AND was not detectable within the limonene carrier solution, we tested the participants’ ability to discriminate these stimuli using a three-way forced-choice (“triangle”) test (Amoore, 1979). We presented three opaque jars: one with the AND/ limonene solution and two with limonene alone, and the task was to find which one of three bottles had a different odor. Six screening trials were performed in order to exclude participants who could detect AND, and to be sure that the two liquids were perceived as the same odor. On each trial participants sniffed from each bottle seven times, ensuring that they had sufficient opportunity to try and detect the AND-containing stimulus. We discarded all the participants with a good performance in this task (5 or 6 correct identifications out of six trials). By this criterion we ended up excluding 1 female participant. Participants with a lower performance were recruited for the main study that was run a few days after this screening.

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Experimental design

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We used a within-subjects experimental design (Figure 1) with AND stimulation (AND in limonene vs. limonene only) as the independent variable and the amount of money donated in the DG as the dependent variable. In order to minimize any possible carryover effect due to the presentation of the odors, the two odor conditions (control vs. experimental) were run on different days (usually within 48 hours and always during the fertile menstrual phase), counterbalancing their order. Exclusion criteria (e.g., nasal congestion, menstrual phase) were double-checked before the second session started. The testing room was approximately 23.4 cubic meters in volume and was well-ventilated, ensuring that any residual odor did not linger in the room. As described in detail below, upon entering the testing room, subjects first completed an informed consent, a baseline mood assessment, an odor evaluation (the odorant, limonene, or AND in limonene, was first introduced only at this point in time), an informational questionnaire, and a “first mood” assessment, prior to beginning the Dictator Game. The DG task ended 20 minutes after the odor exposure, i.e., before the effects of AND on physiology and behavior began to diminish (Grosser, Monti-Bloch, JenningsWhite, & Berliner, 2000; Saxton et al., 2008). Tasks and Phases 1. Informed Consent—First, participants read and signed the informed consent form which outlined the experimental procedure. J Neurosci Psychol Econ. Author manuscript; available in PMC 2017 June 01.

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2. Baseline mood assessment—Participants then filled out a paper-and-pencil questionnaire adapted from Ekman, Freisen, & Ancoli, (1980) to rate their current mood (“baseline mood”) in a non-scented room. They reported how strongly they were experiencing each of 16 different affective states (afraid, amused, angry, annoyed, anxious, bored, calm, confident, content, contemptuous, disgusted, embarrassed, happy, interested, sad, and stressed) on a 9-point scale. The scale ranges from 1 = “not at all” to 9 = “very strongly”. In addition, we added the item “sexual arousal” to the original version (again on a 9-point scale).

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3. Odor exposure—In this task the participants were exposed to the odorants, i.e., the mask odor (limonene) or the mask odor plus chemosignal (AND in limonene). We decided to present the compounds in a jar (rather than via an olfactometer or epidermal application), and we asked the participants to sniff the content of the jar and then make a rating. The task was set up in this way in order to preserve the ecological validity of this study and to minimize the chance that participants might have become aware of the experimental aims and hypotheses of our study. The participants used the Labeled Magnitude Scale (Green, Dalton, Cowart, Shaffer, Rankin, & Higgins, 1996) to assess odor intensity, as well as pleasantness, familiarity, unpleasantness, and sensuality of the content of the jar. Participants sniffed the bottle 7 times for each descriptor and reported their evaluations on a paper-andpencil questionnaire. This task lasted up to 5 minutes. 4. Informational Questionnaire—The participants completed an informational questionnaire, reporting information about their health and drug usage and, if female, about their menstrual cycle.

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5. First mood assessment—In the following steps of the experiment we used E-Prime 1.0 software (Psychology Software Tools, Inc; Schneider, Eschman, & Zuccolotto, 2002a,b). Participants again rated their mood (“first mood”) after the initial evaluation of the odors, using the same scale utilized for the baseline mood assessment. 6. Dictator Game—The participants played 24 trials of the Dictator Game, in each of them the participants divided €8 with a person (the receiver) presented on a computer screen. We used E-Prime 1.0 to show the pictures, which were taken from the NimStim set of facial expressions (Caucasian and Hispanic adult faces with neutral expressions were chosen; equal numbers of male and female faces; Tottenham et al., 2009). The pictures were delivered in randomized order and they remained on the screen till the participants decided the allocation (no time limit for the decision).

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7. Second mood assessment—Finally, the last mood rating (“second mood”) was presented, using the same method as above. Mood rating analysis Because participants were asked to provide ratings of 16 different affective states, analysis of different mood ratings was streamlined, by collapsing the rating scales (Ekman et al.,

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1980) into three clusters, “positive mood”, “high arousal negative mood”, and “low arousal negative mood”, following prior work (Bensafi et al., 2004b). Statistical analyses method

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For the statistical analyses of the donation amounts (see the paragraph “Androstadienone and Dictator donations”, below) we ran a mixed regression model. We chose this model in order to include two factors (the individual differences that characterize each participant; and the different pictures of the Receivers) that can be treated as “random factors”, i.e., variables whose levels are drawn “from a large (potentially very large) population in which the individuals differ in many ways, but we do not know exactly how or why they differ” (Crawley, 2007; p. 628). The mixed regression model (unlike ANOVA and simple linear regression) provides a way to take into account the added variation caused by differences between the levels of the random factors (Baayen, Davidson, & Bates, 2008; Fugard, Pfeifer, Mayerhofer, & Kleiter, 2011). After the mixed regression model, and following Baayen et al. (2008), we ran a Markov chain Monte Carlo (MCMC) simulation based on 50,000 samples, in order to assess statistical significance. This approach involves calculating the Highest Posterior Density (HPD) 95% interval, which indicates the extremes of the shortest possible interval that includes the parameters of the model with a 95% probability, and from which the corresponding p-values for the actual data can be derived.

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In addition, the standard error of the mean (s.e.m.) of the within-subject analyses reported below are calculated with a method that removes the across-subject variability. Specifically, we corrected the participant means (i.e., the average score of a single participant across all the within conditions) so that they are all equal to the grand mean, as suggested by Cousineau (2005). This method provides variability estimates consistent with the error terms used in the critical within-subject comparisons (see, for an example, Antony, Gobel, O’Hare, Reber, & Paller, 2012).

RESULTS Androstadienone and Dictator donations

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We first examined the effect of AND on donations. The analysis on the amount of the donation (the dependent continuous variable) is based on a mixed regression model with the following factors: AND stimulation (a categorical, within-subjects variable with two levels), gender (a categorical, between-subject variable), mood variation (three continuous covariates: Δpositive mood, Δhigh-arousal negative mood, and Δlow-arousal negative mood). The three mood variation factors were calculated by subtracting baseline mood values from first mood values, so these factors indexes the mood change generated by the odor stimulation. We also considered the following interactions: AND stimulation by participants’ gender, and all interactions between the three Δmood clusters, AND stimulation, and the participants’ gender. The model indicated that the interaction of AND stimulation by participants’ gender was statistically significant (Coefficient Estimate: 0.46, SD: 0.18, t-value: 2.575, HPD95lower: 0.12, HPD95upper: 0.83, p-value: 0.01). Notably, there was a differential effect of AND on female and male participants: AND increased the

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donation of female participants more than AND increased male participants’ donations (see Figure 2). The remaining factors and interactions were not significant. Androstadienone and Mood Given prior reports of AND on mood (Bensafi et al., 2004b), we next examined whether presentation of AND had a significant influence on the positive, high arousal negative, and low arousal negative mood states, as well as on the “sexual arousal” scale. A repeatedmeasures 3×2×2 ANOVA on positive mood (dependent variable) was carried out with 3 independent variables: time (3 levels within-subject: baseline, first, and second mood assessments), odor (2 levels within-subject: AND with limonene, and limonene alone), and the participants’ gender (2 levels, between-subject). This analysis identified a significant effect of time (F (2, 34) = 10.65; p < .001) and a significant three-way odor-by-gender-bytime interaction (F (2, 34) = 4.25; p = .022) on positive mood.

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In order to characterize the comparative effect of AND on males and females more explicitly, we calculated the mood variation between baseline mood (before odorant exposure) and first mood (after odorant exposure), then ran a repeated-measures 2×2 ANOVA (factors: odor and gender). The analysis revealed a significant odor-by-gender interaction effect (F (1, 35) = 5.1; p = .03), showing a larger mood increase for female (vs. male) participants in the AND (vs. limonene) condition (see Figure 3).

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We also repeated the 3×2×2 ANOVA (time, gender, and odor) for the other mood clusters. There was no evidence for a significant three-way interaction showing an influence of AND on these other mood ratings in the female participants. However, several other effects were observed: (1) both high- and low-arousal negative moods decreased over time (high arousal: F(2, 34) = 8.7; p = .001; low arousal: F (2, 34) = 4.25; p = .023); (2) low-arousal negative mood decreased more in the AND condition (time-by-odor interaction, F (2, 34) = 4.27; p = .022), but this effect was not gender-specific; and (3) high-arousal negative mood decreased more for female participants, compared to males (time-by-gender interaction, F (2, 34) = 5.44; p = .009). No significant effects were seen regarding ratings of “sexual arousal”.

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Given that AND appeared to have independent effects on DG donations as well as positive mood, we tested whether there was a systematic relationship between these two variables. To this end, we computed the correlations between the amount of donation and the three mood variations, separately for gender and experimental conditions. We found a strong and significant correlation between donation amount and positive mood change for the female participants (r(19)= 0.58, p= .010), Notably, this effect was present only in the AND condition (see Figure 4a), whereas the same female participants did not show this effect in the control (limonene only) condition (r(19) = −0.04, p = .86; see Figure 4b). Interestingly, in the presence of limonene, the baseline positive mood in men was somewhat higher than in women, and theoretically could have obscured any effect of AND on mood ratings in men. To address this issue, we also computed scatterplots of the correlations between mood changes and donations for the male participants. As shown in Figures 4c and 4d, none of these correlations was significant (limonene: r(18) = −.26, p = .302; AND: r(18)

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= −.08, p = .747). The analyses on the two negative mood variations show no significant correlation between negative moods and the donation amounts. In conclusion, these data provide further support that AND had a specific effect on women, and moreover suggest that any baseline differences in mood did not interfere with this effect.

DISCUSSION

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The goal of the experiment was to investigate if putative human chemosignals can affect higher-order cognitive processes, in addition to mood states. We focused on a specific higher-order cognitive factor – generosity – which has been extensively studied in the economic domain through the Dictator Game, which uses a familiar and easy to interpret scale of values (money). Previous research on chemosignals showed their ability to increase the perceived attractiveness of newly met people (Saxton et al., 2008). Hence, our expectation in the context of the Dictator Game is that people exposed to AND should be more generous. In fact, our new findings show that androstadienone increases the propensity to behave pro-socially by inducing a person to be a more generous dictator. More generous behaviors do not have only economic consequences; they can have an effect also in terms of social cohesion, strengthening interpersonal bonds among people.

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The fact that AND is known to exert a direct influence at the physiological level could provide a unifying explanation for the effect on altruistic behavior, irrespective of mood changes per se. It is well established that the presence of AND modifies endocrine state (Wyart et al., 2007) and modulates autonomic responses (Bensafi, Brown, Khan, Levenson, & Sobel, 2004a; Grosser et al., 2000; Jacob, Hayreh, & McClintock, 2001; Monti-Bloch and Grosser, 1991). It is also known that some of these modifications are specific to woman (Bensafi et al., 2004b; Boulkroune et al., 2007; Chopra et al., 2008; Jacob and McClintock, 2000) and this is well mirrored by our findings, which indicate that the modulatory effects of AND on altruistic behavior are more likely to occur for females (Figure 2). This interaction nicely dovetails with the differential impact of androstadienone on self-assessed current mood: females reported a stronger improvement of their mood, compared to males (Figure 3) (as in Bensafi et al., 2004b). Linking these independent findings together, a very strong correlation between donation amount and positive mood change was identified only in women, and only when they were exposed to AND (Figure 4). This element suggests that – in addition to the direct effect of AND – the positive mood change might have an additive influence on the increased generosity of the female participants.

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One potential concern is that in the absence of olfactory threshold testing, the women in this study might have had better odor sensitivity than the men, and this might have introduced perceptual biases between genders. However, as per published procedures (Amoore, 1979), we asked all participants to complete a three-way alternative forced-choice “triangle” test, as a screening procedure to verify whether any of the participants was able to detect the presence of AND in the limonene solution. Only one person was able to detect AND, and she was excluded from the experiment. Therefore, based on this screening, we are fairly confident that all of the individuals who took part in the study (both women and men) had similar inability to detect AND. Whether the female participants might have had heightened

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sensitivity to limonene, or to other odors, cannot be ruled out, but we feel that the central effects of AND on donation amounts was not driven by gender-specific sensitivity differences to the putative chemosignal.

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One other possible limitation of the present study concerns the method used to ascertain the menstrual cycle phase at which participants took part in the experiment. The use of selfreport evaluations of the ovulatory period, as was done here, is unable to reliably establish the cycle phase, unlike the use of serum hormone measurements. That said, we surmise that even if some of the participants had actually been in the luteal phase (characterized by a completely different hormone profile that could affect processing of sex chemosignals), then this would have only reduced the size of our observed effects on donation amounts. It is also worth noting that while our data are most consistent with AND having a direct effect on altruistic behavior in the female participants, prior work has shown that AND increases the perceived attractiveness of people who were recently met for the first time (Saxton et al., 2008). As such, it is conceivable that the participants donated more money under AND because they perceived the pictures in the Dictator game to be more attractive. Our findings are in broad agreement with the previous literature indicating an effect of AND on mood ratings in a gender-specific way. However, the results presented here mark a novel extension of these findings by highlighting a specific and independent effect of AND on prosocial behavior. From a neurobiological perspective the fact that AND had partially separable influences on positive mood and on donations suggests that AND mediates its effects on altruistic behavior through dual and dissociable neural pathways. Future work that combines these paradigms with functional neuroimaging techniques will be important to test these predictions.

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In conclusion, this study opens up a new multidisciplinary approach that combines putative olfactory chemosignals with economic models of decision-making to address questions about implicit olfactory control of higher-order cognitive operations. Our work also has potential implications for development of new studies aiming to induce mood states in the absence of overt awareness. Based on the findings presented here, it seems likely that not only smiles and gifts (Isen, 2008; Mellers, Haselhuhn, Tetlock, Silva, & Isen, 2010), but also odorous signals, can induce changes in affective states that interact with our choice “to be, or not to be” a generous person.

Acknowledgments Author Manuscript

Valentina Perrotta gratefully acknowledges the financial support of the Autonomous Province of Trento, Italy. Michele Graffeo gratefully acknowledges the financial support of the European Union and of the Autonomous Province of Trento, Italy (7th Framework Program “People”, Marie Curie Action – COFUND, project PEOCC). This work was also supported by an NIH grant to J.A.G. from the National Institute on Deafness and Other Communication Disorders (#R01 DC010014).

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Figure 1. Schematic depicting experimental paradigm (upper panel) and typical trial sequence during the Dictator Game (lower panel)

Each participant was tested with both odors (androstadienone in limonene, limonene alone). Key: IC, informed consent; LMS, Labeled Magnitude Scale; IQ, informational questionnaires; DG, Dictator Game. The pictures presented in the figure are part of the NimStim set (Tottenham et al., 2009).

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Figure 2. Donation amounts for male and female participants, in the control (limonene) and in the putative chemosignal (AND in limonene) condition

The error bars represent the standard error of the mean (s.e.m.) for each condition. The asterisk and the horizontal line indicate an odor-by-gender interaction significant at the 0.05 level.

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Author Manuscript Author Manuscript Figure 3. Variation of the positive mood level from the baseline mood rating to the first mood rating, differentiated by odor stimulus type and gender

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The error bars represent the standard error of the mean (s.e.m.) for each condition. The asterisk and the horizontal line indicate an odor-by-gender interaction significant at the 0.05 level.

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Figure 4.

Scatterplots describing the correlation between donation amounts and positive

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The Putative Chemosignal Androstadienone Makes Women More Generous.

Putative human chemosignals have been shown to influence mood states and emotional processing, but the connection between these effects and higher-ord...
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