Who, What, Where, When (and Maybe Even Why)? How the Experience of Sexual Reward Connects Sexual Desire, Preference, and Performance

Abstract

Although sexual behavior is controlled by hormonal and neurochemical actions in the brain, sexual experience induces a degree of plasticity that allows animals to form instrumental and Pavlovian associations that predict sexual outcomes, thereby directing the strength of sexual responding. This review describes how experience with sexual reward strengthens the development of sexual behavior and induces sexually-conditioned place and partner preferences in rats. In both male and female rats, early sexual experience with partners scented with a neutral or even noxious odor induces a preference for scented partners in subsequent choice tests. Those preferences can also be induced by injections of morphine or oxytocin paired with a male rat’s first exposure to scented females, indicating that pharmacological activation of opioid or oxytocin receptors can “stand in” for the sexual reward-related neurochemical processes normally activated by sexual stimulation. Conversely, conditioned place or partner preferences can be blocked by the opioid receptor antagonist naloxone. A somatosensory cue (a rodent jacket) paired with sexual reward comes to elicit sexual arousal in male rats, such that paired rats with the jacket off show dramatic copulatory deficits. We propose that endogenous opioid activation forms the basis of sexual reward, which also sensitizes hypothalamic and mesolimbic dopamine systems in the presence of cues that predict sexual reward. Those systems act to focus attention on, and activate goal-directed behavior toward, reward-related stimuli. Thus, a critical period exists during an individual’s early sexual experience that creates a “love map” or Gestalt of features, movements, feelings, and interpersonal interactions associated with sexual reward.

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Acknowledgments

The research reported from our laboratory was funded by grants from the Canadian Institutes for Health Research (MOP-74563, MOP-111254), Natural Sciences and Engineering Research Council of Canada (OGP-138878), and by Fonds de recherche du Québec-Santé (FRQS Groupe de recherche) to the Center for Studies in Behavioral Neurobiology at Concordia University. All animal procedures conformed to the guidelines of the Canadian Council on Animal Care and were approved by the Concordia University Animal Research Ethics Committee. We would like to thank Drs. Anders Ågmo, J. Michael Bailey, Greg Ball, Jacques Balthazart, John Bancroft, Jill Becker, Ray Blanchard, Lori Brotto, James Cantor, Meredith Chivers, Lique Coolen, Michael Domjan, Mary Erskine, Barry Everitt, Helen Fisher, Janniko Georgiadis, Annamaria Geraldi, Irwin Goldstein, Fay Guarraci, Julia Heiman, Heather Hoffmann, Elaine Hull, Barry Komisaruk, Ellen Laan, Jorge Manzo, Peg McCarthy, Martha McClintock, John Money, Stephanie Ortigue, Raúl Parades, Michael Perelman, Don Pfaff, Alessandra Rellini, Gabriela Rodríguez-Manzo, Michael Sand, Michael Seto, Jane Stewart, Fred Toates, Paul Vasey, Larry Young, Kim Wallen, Roy Wise, Naomi Wolf, Barbara Woodside, and Ken Zucker for many useful discussions that have helped put our findings into perspective. The first author is indebted to Dr. W. Jake Jacobs for helping him translate a fuzzy idea of “post-orgasmic learning” into a set of testable hypotheses that eventually led to a major research thrust on learning and sexual reward funded by the Canadian Institutes for Health Research. A version of this article was presented at the University of Lethbridge Workshop, The Puzzle of Sexual Orientation: What Is It and How Does It Work?, Lethbridge, AB, Canada, June 2010.

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Pfaus, J.G., Kippin, T.E., Coria-Avila, G.A. et al. Who, What, Where, When (and Maybe Even Why)? How the Experience of Sexual Reward Connects Sexual Desire, Preference, and Performance. Arch Sex Behav 41, 31–62 (2012). https://doi.org/10.1007/s10508-012-9935-5

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Keywords

  • Sexual reward
  • Sexual preference
  • Conditioning
  • Critical periods
  • Opioids
  • Dopamine