1 Women’s Neural Activation in Response to Potential Sexual Partners Changes Across the Menstrual Cycle Heather Rupp Julia Heiman Thomas James Ellen Ketterson Dale Sengelaub Erick Janssen

2 Sex is risky…. And rewarding

3 Risk Reward Hormones

4 Women’s Sexual Interest Changes Across the Cycle Increased sexual desire, masturbation, and sexual initiation closer to ovulation (eg. Bullivant et al., 2004; Harvey 1987; Tarin & Gomez- Piquer, 2002; Wallen, 1990). Women are also more likely to engage in extra-pair copulation and have sexual fantasies about men other than their primary partners at this time (Bellis & Baker, 1990; Gangestad et al., 2002). But how are hormones influencing sexual interest and behavior?

5 Women’s Neural Activation Changes Across the Cycle in Response to Rewards Increased activation to monetary reward in the limbic system in women tested closer to ovulation (Dreher et al., 2007) Increased activation in response to erotic videos in the limbic system in women tested closer to ovulation (Gizewski et al., 2006) The administration of exogenous hormones to postmenopausal women increased limbic neural activation in response to erotic videos (Archer et al., 2006). But what about the real world? How do women get to be involved in a sexual encounter?

6 Sexual Behavior Potential Sexual Encounter Does neural activation change across the menstrual cycle during the evaluation of male faces as potential sexual partners? Hormones

7 fMRI

8 Methods 12 normal cycling females aged Screened for inclusion of women with heterosexual preference, and not currently in a relationship. Tested at two phases of the menstrual cycle (follicular, days ; luteal, days 19-23) in a counterbalanced order. Before each test session blood samples collected for assay of testosterone, estrogen, and progesterone.

9 Methods Stimuli Pictures of male faces accompanied by description of previous # sexual partners (LOW, 2-5; HIGH, 10-13) and condom use (usually, rarely) to vary risk of potential partner. Pictures of houses accompanied by description of rental cost (LOW, $200-$500; HIGH, $ ) and landlord maintenance (usually, rarely) to vary risk of rental.

10 Rarely 10

11 Rarely 1

12 4 secs 2, 4, 6 secs Pictures presented across 8 runs in an event related design.

13 Methods Stimuli All subjects presented same scenarios in which to judge… “How likely would you be to have sex with this person” 1=very unlikely, 2=unlikely, 3=likely, 4=very likely “How likely would you be to rent this house?” 1=very unlikely, 2=unlikely, 3=likely, 4=very likely

No overall difference in subjective ratings across the cycle for faces or houses (mean Faces= 1.90, Houses= 2.39). Total Testosterone was related to women’s ratings. 14 Subjective Ratings

15 Increased Activation During the Follicular Phase in Visual and Reward Processing Areas, and Decreased Activation in Frontal and Parietal Cortices. Faces Follicular – Faces Luteal p<.001 FDR corrected

16 Subjective ratings were positively correlated with activation in sensory processing regions, including the lateral occipital cortex (R(24)=.34, p=.05; Pearson Bivariate one-tailed). Activation in the lateral occipital cortex was positively correlated with total testosterone (BA19, R(24)=.45, p=.02; BA37, R(24)=.34, p=.05). Activation in the left ventral middle frontal cortex was positively correlated with free testosterone (R(24)=.37, p=.04). Activation in the angular gyrus was negatively associated with women’s Estradiol/Progesterone ratio (R(24)=-.38, p=.03). Neural Activation in Sensory and Reward Processing Areas Associated with Hormones

17 Increased Activation During the Follicular Phase in Visual Processing Areas, and Decreased Activation in Frontal Cortex Houses Follicular – Houses Luteal

18 Women’s patterns of neural activation in response to male faces and houses were phase dependent. When tested during the follicular phase, women exhibited more neural activation in areas related to reward and face processing, specifically the ventral middle frontal cortex, fusiform gyrus, and lateral occipital cortex during the evaluation of male faces. Activation in visual areas predicted women’s subjective evaluations. During the luteal phase, women showed more activation in regions related to higher order cognitive function and control, specifically in frontal and parietal cortical regions. When tested during the follicular phase, during the evaluation of houses, women exhibited more neural activation in areas related to visual processing. Therefore, cyclic differences may not be stimulus specific. SUMMARY of fMRI Results

19 Rarely 10 Are differences in neural activation in brain regions associated with differences in attention?

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21 Methods 12 (5 tested) normal cycling females aged Screened for inclusion of women with heterosexual preference, and not currently in a relationship. Tested at two phases of the menstrual cycle (follicular, days ; luteal, days 19-23) in a counterbalanced order. Before each test session saliva samples collected for assay of testosterone, estrogen, and progesterone. Saw the same stimuli across 8 blocks while a SMI desktop mounted eye tracker measured eye movements.

22 S11 S09 Follicular Luteal

23 Rarely 10

24 Rar ely 10 Follicular Luteal Percent Looking 77.0% 73.5% Follicular Luteal Percent Looking 14.8% 13.9%

25 Follicular Luteal Percent Looking 70.9% Follicular Luteal Percent Looking 19.4% 18.7%

26 CONCLUSIONS Previously observed fluctuations in sexual interest and behavior across the cycle may be due to hormone influences in the brain in regions related to reward and sensory processing. Bias may be towards reward seeking around ovulation while later in the cycle the bias may be towards risk aversion and behavioral inhibition. These differences may be due to changes in hormonally mediated attention to cues of reward and risk.

27 Acknowledgements Indiana University Imaging Research Facility Common Themes in Reproductive Diversity

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