Abstract
Patterns of genital arousal in response to gendered sexual stimuli (i.e., sexual stimuli presenting members of only one sex at a time) are more predictive of men’s than of women’s sexual orientations. Additional lines of evidence may shed light on the nature of these differences. We measured neural activation in homosexual and heterosexual men and women using fMRI while they viewed three kinds of gendered sexual stimuli: pictures of nude individuals, pictures of same-sex couples interacting, and videos of individuals self-stimulating. The primary neural region of interest was the ventral striatum (VS), an area of central importance for reward processing. For all three kinds of stimuli and for both VS activation and self-report, men’s responses were more closely related to their sexual orientations compared with women’s. Furthermore, men showed a much greater tendency to respond more positively to stimuli featuring one sex than to stimuli featuring the other sex, leading to higher correlations among men’s responses as well as higher correlations between men’s responses and their sexual orientations. Whole-brain analyses identified several other regions showing a similar pattern to the VS, and none showed an opposite pattern. Because fMRI is measured identically in men and women, our results provide the most direct evidence to date that men’s sexual arousal patterns are more gender specific than women’s.
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Notes
It is important to stipulate that even the best objective measure of male sexual arousal, genital assessment, has measurement error (sometimes substantial error, especially when response is low). Thus, it is a man’s score on the latent variable “sexual arousal pattern” and not that on any one assessment that defines his sexual orientation.
References
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Press.
Arnow, B. A., Millheiser, L., Garrett, A., Lake Polan, M., Glover, G. H., Hill, K. R., … Desmond, J. E. (2009). Women with hypoactive sexual desire disorder compared to normal females: a functional magnetic resonance imaging study. Neuroscience,158(2), 484–502. https://doi.org/10.1016/j.neuroscience.2008.09.044.
Bailey, J. M. (2009). What is sexual orientation and do women have one? Nebraska Symposium on Motivation,54, 43–63.
Bailey, J. M. (2014). The evolution of male sexual orientation. Paper presented at the meeting of the American Association for the Advancement of Science, Chicago, IL.
Bailey, J. M., Vasey, P. L., Diamond, L. M., Breedlove, S. M., Vilain, E., & Epprecht, M. (2016). Sexual orientation, controversy, and science. Psychological Science in the Public Interest,17(2), 45–101. https://doi.org/10.1177/1529100616637616.
Baumeister, R. F. (2000). Gender differences in erotic plasticity: The female sex drive as socially flexible and responsive. Psychological Bulletin,126(3), 347–374.
Brett, M., Anton, J.-L., Valabregue, R., & Poline, J.-B. (2002). Region of interest analysis using an SPM toolbox. Paper presented at the International Conference on Functional Mapping of the Human Brain, Sendai, Japan.
Carmichael, C. Y., & Wainford, R. D. (2015). Hypothalamic signaling mechanisms in hypertension. Current Hypertension Reports. https://doi.org/10.1007/s11906-015-0550-4.
Chivers, M. L. (2017). The specificity of women’s sexual response and its relationship with sexual orientations: A review and ten hypotheses. Archives of Sexual Behavior,46(5), 1161–1179. https://doi.org/10.1007/s10508-016-0897-x.
Chivers, M. L., Rieger, G., Latty, E., & Bailey, J. M. (2004). A sex difference in the specificity of sexual arousal. Psychological Science,15(11), 736–744. https://doi.org/10.1111/j.0956-7976.2004.00750.x.
Chivers, M. L., Seto, M. C., & Blanchard, R. (2007). Gender and sexual orientation differences in sexual response to sexual activities versus gender of actors in sexual films. Journal of Personality and Social Psychology,93(6), 1108–1121. https://doi.org/10.1037/0022-3514.93.6.1108.
Chivers, M. L., Seto, M. C., Lalumière, M. L., Laan, E., & Grimbos, T. (2010). Agreement of self-reported and genital measures of sexual arousal in men and women: A meta-analysis. Archives of Sexual Behavior,39(1), 5–56. https://doi.org/10.1007/s10508-009-9556-9.
de Araujo, I. E. T., Kringelbach, M. L., Rolls, E. T., & McGlone, F. (2003). Human cortical responses to water in the mouth, and the effects of thirst. Journal of Neurophysiology,90(3), 1865–1876. https://doi.org/10.1152/jn.00297.2003.
Diamond, L. M. (2016). Sexual fluidity in male and females. Current Sexual Health Reports,8(4), 249–256. https://doi.org/10.1007/s11930-016-0092-z.
Diekhof, E. K., Kaps, L., Falkai, P., & Gruber, O. (2012). The role of the human ventral striatum and the medial orbitofrontal cortex in the representation of reward magnitude: An activation likelihood estimation meta-analysis of neuroimaging studies of passive reward expectancy and outcome processing. Neuropsychologia,50(7), 1252–1266. https://doi.org/10.1016/j.neuropsychologia.2012.02.007.
Evans, K. C., Banzett, R. B., Adams, L., McKay, L., Frackowiak, R. S. J., & Corfield, D. R. (2002). BOLD fMRI identifies limbic, paralimbic, and cerebellar activation during air hunger. Journal of Neurophysiology,88(3), 1500–1511.
Ferris, C. F., Melloni, R. H., Jr., Koppel, G., Perry, K. W., Fuller, R. W., & Delville, Y. (1997). Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in golden hamsters. Journal of Neuroscience,17(11), 4331–4340.
Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J.-P., Frith, C. D., & Frackowiak, R. S. J. (1994). Statistical parametric maps in functional imaging: A general linear approach. Human Brain Mapping,2(4), 189–210. https://doi.org/10.1002/hbm.460020402.
Gallese, V., Keysers, C., & Rizzolatti, G. (2004). A unifying view of the basis of social cognition. Trends in Cognitive Sciences,8(9), 396–403. https://doi.org/10.1016/j.tics.2004.07.002.
Georgiadis, J., & Kringelbach, M. L. (2012). The human sexual response cycle: Brain imaging evidence linking sex to other pleasures. Progress in Neurobiology,98(1), 49–81. https://doi.org/10.1016/j.pneurobio.2012.05.004.
Georgiadis, J., Kringelbach, M. L., & Pfaus, J. G. (2012). Sex for fun: A synthesis of human and animal neurobiology. Nature Reviews Urology,9(9), 486–498. https://doi.org/10.1038/nrurol.2012.151.
Greene, A. J., Gross, W. L., Elsinger, C. L., & Rao, S. M. (2006). An FMRI analysis of the human hippocampus: Inference, context, and task awareness. Journal of Cognitive Neuroscience,18(7), 1156–1173. https://doi.org/10.1162/jocn.2006.18.7.1156.
Haber, S. N., & Knutson, B. (2010). The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology,35(1), 4–26. https://doi.org/10.1038/npp.2009.129.
Hamann, S., Herman, R. A., Nolan, C. L., & Wallen, K. (2004). Men and women differ in amygdala response to visual sexual stimuli. Nature Neuroscience,7(4), 411–416. https://doi.org/10.1038/nn1208.
Hu, S.-H., Wei, N., Wang, Q.-D., Yan, L.-Q., Wei, E.-Q., Zhang, M.-M., … Xu, Y. (2008). Patterns of brain activation during visually evoked sexual arousal differ between homosexual and heterosexual men. American Journal of Neuroradiology,29(10), 1890–1896. https://doi.org/10.3174/ajnr.A1260.
Huberman, J. S., Maracle, A. C., & Chivers, M. L. (2014). Gender-specificity of women’s and men’s self-reported attention to sexual stimuli. Journal of Sex Research,52(9), 983–995. https://doi.org/10.1080/00224499.2014.951424.
Kagerer, S., Klucken, T., Wehrum, S., Zimmermann, M., Schienle, A., Walter, B., … Stark, R. (2011). Neural activation toward erotic stimuli in homosexual and heterosexual males. Journal of Sexual Medicine,8(11), 3132–3143. https://doi.org/10.1111/j.1743-6109.2011.02449.x.
Karama, S., Lecours, A. R., Leroux, J.-M., Bourgouin, P., Beaudoin, G., Joubert, S., & Beauregard, M. (2002). Areas of brain activation in males and females during viewing of erotic film excerpts. Human Brain Mapping,16(1), 1–13.
Kinsey, A. C., Pomeroy, W. R., & Martin, C. E. (1948). Sexual behavior in the human male. Philadelphia: W. B. Saunders.
Knutson, B., Wimmer, G. E., Kuhnen, C. M., & Winkielman, P. (2008). Nucleus accumbens activation mediates the influence of reward cues on financial risk taking. NeuroReport,19(5), 509–513. https://doi.org/10.1097/WNR.0b013e3282f85c01.
Ko, C.-H., Liu, G.-C., Hsiao, S., Yen, J.-Y., Yang, M.-J., Lin, W.-C., … Chen, C.-S. (2009). Brain activities associated with gaming urge of online gaming addiction. Journal of Psychiatric Research,43(7), 739–747. https://doi.org/10.1016/j.jpsychires.2008.09.012.
Kranz, F., & Ishai, A. (2006). Face perception is modulated by sexual preference. Current Biology,16(1), 63–68. https://doi.org/10.1016/j.cub.2005.10.070.
Kringelbach, M. L. (2005). The human orbitofrontal cortex: Linking reward to hedonic experience. Nature Reviews Neuroscience,6(9), 691–702. https://doi.org/10.1038/nrn1747.
Kühn, S., & Gallinat, J. (2011). Common biology of craving across legal and illegal drugs—A quantitative meta-analysis of cue-reactivity brain response. European Journal of Neuroscience, 33, 1318–1326. https://doi.org/10.1111/j.1460-9568.2010.07590.x.
Kühn, S., & Gallinat, J. (2012). The neural correlates of subjective pleasantness. NeuroImage,61(1), 289–294. https://doi.org/10.1016/j.neuroimage.2012.02.065.
Lee, S. W., Jeong, B. S., Choi, J., & Kim, J.-W. (2015). Sex differences in interactions between nucleus accumbens and visual cortex by explicit visual erotic stimuli: An fMRI study. International Journal of Impotence Research,27(5), 161. https://doi.org/10.1038/ijir.2015.8.
LeVay, S. (1991). A difference in hypothalamic structure between heterosexual and homosexual men. Science,253(5023), 1034–1037.
Levy, D. J., & Glimcher, P. W. (2012). The root of all value: A neural common currency for choice. Current Opinion in Neurobiology,22(6), 1027–1038. https://doi.org/10.1016/j.conb.2012.06.001.
Lykins, A. D., Meana, M., & Strauss, G. P. (2008). Sex differences in visual attention to erotic and non-erotic stimuli. Archives of Sexual Behavior,37(2), 219–228. https://doi.org/10.1007/s10508-007-9208-x.
Maldjian, J. A., Laurienti, P. J., Kraft, R. A., & Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage,19(3), 1233–1239.
Mannella, F., Gurney, K., & Baldassarre, G. (2013). The nucleus accumbens as a nexus between values and goals in goal-directed behavior: A review and a new hypothesis. Frontiers in Behavioral Neuroscience,7, 135. https://doi.org/10.3389/fnbeh.2013.00135.
Metzger, C. D., Eckert, U., Steiner, J., Sartorius, A., Buchmann, J. E., Stadler, J., … Walter, M. (2010). High field FMRI reveals thalamocortical integration of segregated cognitive and emotional processing in mediodorsal and intralaminar thalamic nuclei. Frontiers in Neuroanatomy,4, 138. https://doi.org/10.3389/fnana.2010.00138.
Oei, N. Y. L., Both, S., van Heemst, D., & van der Grond, J. (2014). Acute stress-induced cortisol elevations mediate reward system activity during subconscious processing of sexual stimuli. Psychoneuroendocrinology,39, 111–120. https://doi.org/10.1016/j.psyneuen.2013.10.005.
Parrish, T. B., Gitelman, D. R., LaBar, K. S., & Mesulam, M. M. (2000). Impact of signal-to-noise on functional MRI. Magnetic Resonance in Medicine,44(6), 925–932.
Paul, T., Schiffer, B., Zwarg, T., Krüger, T. H. C., Karama, S., Schedlowski, M., … Gizewski, E. R. (2008). Brain response to visual sexual stimuli in heterosexual and homosexual males. Human Brain Mapping,29(6), 726–735. https://doi.org/10.1002/hbm.20435.
Ponseti, J., Bosinski, H. A., Wolff, S., Peller, M., Jansen, O., Mehdorn, H. M., … Siebner, H. R. (2006). A functional endophenotype for sexual orientation in humans. NeuroImage,33(3), 825–833. https://doi.org/10.1016/j.neuroimage.2006.08.002.
Rieger, G., & Savin-Williams, R. C. (2012). The eyes have it: Sex and sexual orientation differences in pupil dilation patterns. PLoS One,7(8), e40256. https://doi.org/10.1371/journal.pone.0040256.
Rieger, G., Savin-Williams, R. C., Chivers, M. L., & Bailey, J. M. (2016). Sexual arousal and masculinity-femininity of women. Journal of Personality and Social Psychology,111(2), 265–283. https://doi.org/10.1037/pspp0000077.
Roselli, C. E., & Stormshak, F. (2010). The ovine sexually dimorphic nucleus, aromatase, and sexual partner preferences in sheep. Journal of Steroid Biochemistry and Molecular Biology,118(4–5), 252–256. https://doi.org/10.1016/j.jsbmb.2009.10.009.
Rosenthal, A. M., Sylva, D., Safron, A., & Bailey, J. M. (2012). The male bisexuality debate revisited: Some bisexual men have bisexual arousal patterns. Archives of Sexual Behavior,41(1), 135–147.
Rupp, H. A., & Wallen, K. (2009). Sex-specific content preferences for visual sexual stimuli. Archives of Sexual Behavior,38(3), 417–426. https://doi.org/10.1007/s10508-008-9402-5.
Sabatinelli, D., Flaisch, T., Bradley, M. M., Fitzsimmons, J. R., & Lang, P. J. (2004). Affective picture perception: Gender differences in visual cortex? NeuroReport,15(7), 1109–1112.
Safron, A., Barch, B., Bailey, J. M., Gitelman, D. R., Parrish, T. B., & Reber, P. J. (2007). Neural correlates of sexual arousal in homosexual and heterosexual men. Behavioral Neuroscience,121(2), 237–248. https://doi.org/10.1037/0735-7044.121.2.237.
Safron, A., Klimaj, V., Sylva, D., Rosenthal, A. M., Li, M., Walter, M., & Bailey, J. M. (2018). Neural correlates of sexual orientation in heterosexual, bisexual, and homosexual women. Scientific Reports,8(1), 673. https://doi.org/10.1038/s41598-017-18372-0.
Safron, A., Sylva, D., Klimaj, V., Rosenthal, A. M., Li, M., Walter, M., & Bailey, J. M. (2017). Neural correlates of sexual orientation in heterosexual, bisexual, and homosexual men. Scientific Reports,7, 41314. https://doi.org/10.1038/srep41314.
Sewards, T. V., & Sewards, M. A. (2003). Representations of motivational drives in mesial cortex, medial thalamus, hypothalamus and midbrain. Brain Research Bulletin,61(1), 25–49.
Spreckelmeyer, K. N., Krach, S., Kohls, G., Rademacher, L., Irmak, A., Konrad, K., … Gründer, G. (2009). Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women. Social Cognitive and Affective Neuroscience,4(2), 158–165. https://doi.org/10.1093/scan/nsn051.
Stark, R., Schienle, A., Girod, C., Walter, B., Kirsch, P., Blecker, C., … Vaitl, D. (2005). Erotic and disgust-inducing pictures–differences in the hemodynamic responses of the brain. Biological Psychology,70(1), 19–29. https://doi.org/10.1016/j.biopsycho.2004.11.014.
Succu, S., Sanna, F., Melis, T., Boi, A., Argiolas, A., & Melis, M. R. (2007). Stimulation of dopamine receptors in the paraventricular nucleus of the hypothalamus of male rats induces penile erection and increases extra-cellular dopamine in the nucleus accumbens: Involvement of central oxytocin. Neuropharmacology,52(3), 1034–1043. https://doi.org/10.1016/j.neuropharm.2006.10.019.
Suschinsky, K. D., & Lalumière, M. L. (2010). Prepared for anything? An investigation of female genital arousal in response to rape cues. Psychological Science,22(2), 159–165. https://doi.org/10.1177/0956797610394660.
Suschinsky, K. D., Lalumière, M. L., & Chivers, M. L. (2009). Sex differences in patterns of genital sexual arousal: Measurement artifacts or true phenomena? Archives of Sexual Behavior,38(4), 559–573. https://doi.org/10.1007/s10508-008-9339-8.
Sylva, D., Safron, A., Rosenthal, A. M., Reber, P. J., Parrish, T. B., & Bailey, J. M. (2013). Neural correlates of sexual arousal in heterosexual and homosexual women and men. Hormones and Behavior, 64, 673–684. https://doi.org/10.1016/j.yhbeh.2013.08.003.
Tang, D. W., Fellows, L. K., Small, D. M., & Dagher, A. (2012). Food and drug cues activate similar brain regions: A meta-analysis of functional MRI studies. Physiology and Behavior,106(3), 317–324. https://doi.org/10.1016/j.physbeh.2012.03.009.
Tye, K. M., & Deisseroth, K. (2012). Optogenetic investigation of neural circuits underlying brain disease in animal models. Nature Reviews Neuroscience,13(4), 251–266. https://doi.org/10.1038/nrn3171.
van der Laan, L. N., de Ridder, D. T. D., Viergever, M. A., & Smeets, P. A. M. (2011). The first taste is always with the eyes: A meta-analysis on the neural correlates of processing visual food cues. NeuroImage,55(1), 296–303. https://doi.org/10.1016/j.neuroimage.2010.11.055.
Van Dijk, K. R. A., Sabuncu, M. R., & Buckner, R. L. (2012). The influence of head motion on intrinsic functional connectivity MRI. NeuroImage,59(1), 431–438. https://doi.org/10.1016/j.neuroimage.2011.07.044.
Walter, M., Bermpohl, F., Mouras, H., Schiltz, K., Tempelmann, C., Rotte, M., … Northoff, G. (2008). Distinguishing specific sexual and general emotional effects in fMRI-subcortical and cortical arousal during erotic picture viewing. NeuroImage,40(4), 1482–1494. https://doi.org/10.1016/j.neuroimage.2008.01.040.
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The authors would like to thank the American Institute of Bisexuality for its support in funding this research.
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Safron, A., Sylva, D., Klimaj, V. et al. Neural Responses to Sexual Stimuli in Heterosexual and Homosexual Men and Women: Men’s Responses Are More Specific. Arch Sex Behav 49, 433–445 (2020). https://doi.org/10.1007/s10508-019-01521-z
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DOI: https://doi.org/10.1007/s10508-019-01521-z