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Behavioral, Neural, and Molecular Mechanisms of Conditioned Mate Preference: The Role of Opioids and First Experiences of Sexual Reward

. 2022 Aug 10 ; 23 (16) : . [epub] 20220810

Language English Country Switzerland Media electronic

Document type Journal Article, Review

Grant support
MOP-74563 CIHR - Canada
MOP-111254 CIHR - Canada
OGP-138878 Natural Sciences and Engineering Research Council
2007-2008 Fonds de recherche du Québec-Santé

Although mechanisms of mate preference are thought to be relatively hard-wired, experience with appetitive and consummatory sexual reward has been shown to condition preferences for partner related cues and even objects that predict sexual reward. Here, we reviewed evidence from laboratory species and humans on sexually conditioned place, partner, and ejaculatory preferences in males and females, as well as the neurochemical, molecular, and epigenetic mechanisms putatively responsible. From a comprehensive review of the available data, we concluded that opioid transmission at μ opioid receptors forms the basis of sexual pleasure and reward, which then sensitizes dopamine, oxytocin, and vasopressin systems responsible for attention, arousal, and bonding, leading to cortical activation that creates awareness of attraction and desire. First experiences with sexual reward states follow a pattern of sexual imprinting, during which partner- and/or object-related cues become crystallized by conditioning into idiosyncratic "types" that are found sexually attractive and arousing. These mechanisms tie reward and reproduction together, blending proximate and ultimate causality in the maintenance of variability within a species.

See more in PubMed

Perelman M.A. A New Combination Treatment for Premature Ejaculation: A Sex Therapist’s Perspective. J. Sex. Med. 2006;3:1004–1012. doi: 10.1111/j.1743-6109.2006.00238.x. PubMed DOI

Pfaus J.G. Neurobiology of Sexual Behavior. Curr. Opin. Neurobiol. 1999;9:751–758. doi: 10.1016/S0959-4388(99)00034-3. PubMed DOI

Pfaus J.G. REVIEWS: Pathways of Sexual Desire. J. Sex. Med. 2009;6:1506–1533. doi: 10.1111/j.1743-6109.2009.01309.x. PubMed DOI

Bancroft J., Janssen E. The Dual Control Model of Male Sexual Response: A Theoretical Approach to Centrally Mediated Erectile Dysfunction. Neurosci. Biobehav. Rev. 2000;24:571–579. doi: 10.1016/S0149-7634(00)00024-5. PubMed DOI

Moll A. Das Sexualleben Des Kindes. Vogel; Eindhoven, The Netherlands: 1908.

Masters W.H., Johnson V.E. Human Sexual Response. Bantam Books; New York, NY, USA: 1966.

Whalen R.E. Sexual Motivation. Psychol. Rev. 1966;73:151. doi: 10.1037/h0023026. PubMed DOI

Salu Y. The Roots of Sexual Arousal and Sexual Orientation. Med. Hypotheses. 2011;76:384–387. doi: 10.1016/j.mehy.2010.10.048. PubMed DOI

Bindra D. Neuropsychological Interpretation of the Effects of Drive and Incentive-Motivation on General Activity and Instrumental Behavior. Psychol. Rev. 1968;75:1–22. doi: 10.1037/h0025306. DOI

Bindra D. A Motivational View of Learning, Performance, and Behavior Modification. Psychol. Rev. 1974;81:199. doi: 10.1037/h0036330. PubMed DOI

Bolles R.C. Reinforcement, Expectancy, and Learning. Psychol. Rev. 1972;79:394. doi: 10.1037/h0033120. DOI

Toates F.M. Motivational Systems. Cambridge University Press; Cambridge, UK: 1986.

Pfaus J.G., Kippin T.E., Coria-Avila G. What Can Animal Models Tell Us about Human Sexual Response? Annu. Rev. Sex Res. 2003;14:1–63. PubMed

Georgiadis J.R., Kringelbach M.L., Pfaus J.G. Sex for Fun: A Synthesis of Human and Animal Neurobiology. Nat. Rev. Urol. 2012;9:486–498. doi: 10.1038/nrurol.2012.151. PubMed DOI

Stendhal H.B. De l’amour. Le Devian; Paris, France: 1822.

Von Krafft-Ebing R.F. Psychopathia Sexualis: Eine Klinisch-Forensische Studie. Adamant Media Corporation; Chestnut Hill, MA, USA: 1886.

Money J. Lovemaps: Clinical Concepts of Sexual/Erotic Health and Pathology, Paraphilia, and Gender Transposition in Childhood, Adolescence, and Maturity. Prometheus Books; Buffalo, NY, USA: 1986.

Díaz-Estrada V.X., Barradas-Moctezuma M., Herrera-Covarrubias D., Manzo J., Coria-Avila G.A. Nature and Nurture of Sexual Partner Preference: Teachings from Prenatal Administration of Acetaminophen in Male Rats. Horm. Behav. 2020;124:104775. doi: 10.1016/j.yhbeh.2020.104775. PubMed DOI

Pfaus J.G., Kippin T.E., Coria-Avila G.A., Gelez H., Afonso V.M., Ismail N., Parada M. Who, What, Where, When (and Maybe Even Why)? How the Experience of Sexual Reward Connects Sexual Desire, Preference, and Performance. Arch. Sex. Behav. 2012;41:31–62. doi: 10.1007/s10508-012-9935-5. PubMed DOI

Pfaff D.W. Drive: Neurobiological and Molecular Mechanisms of Sexual Motivation. The MIT Press; Cambridge, MA, USA: 1999.

Toates F. How Sexual Desire Works. Cambridge University Press; Cambridge, UK: 2014.

Pfaus J.G., Gorzalka B.B. Opioids and Sexual Behavior. Neurosci. Biobehav. Rev. 1987;11:1–34. doi: 10.1016/S0149-7634(87)80002-7. PubMed DOI

Pfaus J.G., Quintana G.R., Mac Cionnaith C.E., Gerson C.A., Dubé S., Coria-Avila G.A. Conditioning of Sexual Interests and Paraphilias in Humans Is Difficult to See, Virtually Impossible to Test, and Probably Exactly How It Happens: A Comment on Hsu and Bailey (2020) Arch. Sex. Behav. 2020;49:1403–1407. doi: 10.1007/s10508-020-01739-2. PubMed DOI

Gray J.A., Hinde R. The Psychology of Fear and Stress. Volume 5. CUP Archive; Cambridge, UK: 1987.

Pavlov I. Conditioned Reflexes; An Investigation of the Physiological Activity of the Cerebral Cortex. Oxford University Press; London, UK: 1927. PubMed PMC

Dominguez J.M., Hull E.M. Dopamine, the Medial Preoptic Area, and Male Sexual Behavior. Physiol. Behav. 2005;86:356–368. doi: 10.1016/j.physbeh.2005.08.006. PubMed DOI

Melis M.R., Argiolas A. Dopamine and Sexual Behavior. Neurosci. Biobehav. Rev. 1995;19:19–38. doi: 10.1016/0149-7634(94)00020-2. PubMed DOI

Tagliamonte A., Fratta W., Del Fiacco M., Gessa G.L. Possible Stimulatory Role of Brain Dopamine in the Copulatory Behavior of Male Rats. Pharmacol. Biochem. Behav. 1974;2:257–260. doi: 10.1016/0091-3057(74)90061-6. PubMed DOI

Rodríguez-Manzo G. Yohimbine Interacts with the Dopaminergic System to Reverse Sexual Satiation: Further Evidence for a Role of Sexual Motivation in Sexual Exhaustion. Eur. J. Pharmacol. 1999;372:1–8. doi: 10.1016/S0014-2999(99)00140-5. PubMed DOI

Pfaus J.G., Phillips A.G. Role of Dopamine in Anticipatory and Consummatory Aspects of Sexual Behavior in the Male Rat. Behav. Neurosci. 1991;105:727–743. doi: 10.1037/0735-7044.105.5.727. PubMed DOI

Ismail N., Laroche C., Girard-Bériault F., Ménard S., Greggain-Mohr J.A., Pfaus J.G. Conditioned Ejaculatory Preference in Male Rats Paired with Haloperidol-Treated Females. Physiol. Behav. 2010;100:116–121. doi: 10.1016/j.physbeh.2010.02.007. PubMed DOI

Hull E.M., Rodríguez-Manzo G. Male Sexual Behavior. Elsevier; Amsterdam, The Netherlands: 2010.

Clark J.T. The Pharmacology of Sexual Function and Dysfunction. Volume 1995. Elsevier; Amsterdam, The Netherlands: 1995. Sexual Arousal and Performance Are Modulated by Adrenergic-Neuropeptide-Steroid Interactions; pp. 55–68.

McIntosh T.K., Barfield R.J. Brain Monoaminergic Control of Male Reproductive Behavior. III. Norepinephrine and the Post-Ejaculatory Refractory Period. Behav. Brain Res. 1984;12:275–281. doi: 10.1016/0166-4328(84)90153-0. PubMed DOI

Carter C.S. Oxytocin and Sexual Behavior. Neurosci. Biobehav. Rev. 1992;16:131–144. doi: 10.1016/S0149-7634(05)80176-9. PubMed DOI

Cantor J.M., Binik Y.M., Pfaus J.G. Chronic Fluoxetine Inhibits Sexual Behavior in the Male Rat: Reversal with Oxytocin. Psychopharmacology. 1999;144:355–362. doi: 10.1007/s002130051018. PubMed DOI

Kita I., Yoshida Y., Nishino S. An Activation of Parvocellular Oxytocinergic Neurons in the Paraventricular Nucleus in Oxytocin-Induced Yawning and Penile Erection. Neurosci. Res. 2006;54:269–275. doi: 10.1016/j.neures.2005.12.005. PubMed DOI

Meyerson B.J. The effect of neuropharmacological agents on hormone-activated estrus behaviour in ovariectomised rats. Arch. Int. Pharmacodyn. Ther. 1964;150:4–33. PubMed

Dalló J. Effect of Two Brain Serotonin Depletors on the Sexual Behavior of Male Rats. Pol. J. Pharmacol. Pharm. 1977;29:247–251. PubMed

Paredes R.G. Opioids and Sexual Reward. Pharmacol. Biochem. Behav. 2014;121:124–131. doi: 10.1016/j.pbb.2013.11.004. PubMed DOI

Garduño-Gutiérrez R., León-Olea M., Rodríguez-Manzo G. Different Amounts of Ejaculatory Activity, a Natural Rewarding Behavior, Induce Differential Mu and Delta Opioid Receptor Internalization in the Rat’s Ventral Tegmental Area. Brain Res. 2013;1541:22–32. doi: 10.1016/j.brainres.2013.10.015. PubMed DOI

Szechtman H., Hershkowitz M., Simantov R. Sexual Behavior Decreases Pain Sensitivity and Stimulated Endogenous Opioids in Male Rats. Eur. J. Pharmacol. 1981;70:279–285. doi: 10.1016/0014-2999(81)90161-8. PubMed DOI

Coolen L.M., Fitzgerald M.E., Yu L., Lehman M. Activation of μ Opioid Receptors in the Medial Preoptic Area Following Copulation in Male Rats. Neuroscience. 2004;124:11–21. doi: 10.1016/j.neuroscience.2003.10.045. PubMed DOI

Balfour M.E., Yu L., Coolen L.M. Sexual Behavior and Sex-Associated Environmental Cues Activate the Mesolimbic System in Male Rats. Neuropsychopharmacology. 2004;29:718–730. doi: 10.1038/sj.npp.1300350. PubMed DOI

Van Ree J.M., Gerrits M.A.F.M., Vanderschuren L.J.M.J. Opioids, Reward and Addiction: An Encounter of Biology, Psychology, and Medicine. Pharmacol. Rev. 1999;51:341–396. PubMed

Hughes A.M., Everitt B.J., Herbert J. Selective Effects of β-Endorphin Infused into the Hypothalamus, Preoptic Area and Bed Nucleus of the Stria Terminalis on the Sexual and Ingestive Behaviour of Male Rats. Neuroscience. 1987;23:1063–1073. doi: 10.1016/0306-4522(87)90181-3. PubMed DOI

Chessick R.D. The “Pharmacogenic Orgasm” in the Drug Addict. Arch. Gen. Psychiatry. 1960;3:545–556. doi: 10.1001/archpsyc.1960.01710050095010. PubMed DOI

Yamazaki K., Boyse E.A., Miké V., Thaler H.T., Mathieson B.J., Abbott J., Boyse J., Zayas Z.A., Thomas L. Control of Mating Preferences in Mice by Genes in the Major Histocompatibility Complex. J. Exp. Med. 1976;144:1324–1335. doi: 10.1084/jem.144.5.1324. PubMed DOI PMC

Kendrick K.M., Hinton M.R., Atkins K., Haupt M.A., Skinner J.D. Mothers Determine Sexual Preferences. Nature. 1998;395:229–230. doi: 10.1038/26129. PubMed DOI

Rescorla R., Wagner A. A Theory of Pavlovian Conditioning: Variations in the Effectiveness of Reinforcement and Nonreinforcement. Appleton-Century; New York, NY, USA: 1972.

Domjan M., Hall S. Determinants of Social Proximity in Japanese Quail (Coturnix Coturnix Japonica): Male Behavior. J. Comp. Psychol. 1986;100:59–67. doi: 10.1037/0735-7036.100.1.59. PubMed DOI

Agmo A., Berenfeld R. Reinforcing Properties of Ejaculation in the Male Rat: Role of Opioids and Dopamine. Behav. Neurosci. 1990;104:177–182. doi: 10.1037/0735-7044.104.1.177. PubMed DOI

Pfaus J.G., Jones S.L., Flanagan-Cato L.M., Blaustein J.D. Female Sexual Behavior. Knobil Neills Physiol. Reprod. 2015;2:2287–2370.

Paredes R.G., Vazquez B. What Do Female Rats like about Sex? Paced Mating. Behav. Brain Res. 1999;105:117–127. doi: 10.1016/S0166-4328(99)00087-X. PubMed DOI

Kippin T., Talianakis S., Schattmann L., Bartholomew S., Pfaus J. Olfactory Conditioning of Sexual Behavior in the Male Rat (Rattus Norvegicus) J. Comp. Psychol. 1998;112:389–399. doi: 10.1037/0735-7036.112.4.389. DOI

Graham J.M., Desjardins C. Classical Conditioning: Induction of Luteinizing Hormone and Testosterone Secretion in Anticipation of Sexual Activity. Science. 1980;210:1039–1041. doi: 10.1126/science.7434016. PubMed DOI

Kippin T., Pfaus J. The Development of Olfactory Conditioned Ejaculatory Preferences in the Male Rat: I. Nature of the Unconditioned Stimulus. Physiol. Behav. 2001;73:457–469. doi: 10.1016/S0031-9384(01)00484-X. PubMed DOI

Ménard S., Gelez H., Jacubovitch M., Coria-Avila G.A., Pfaus J.G. Appetitive Olfactory Conditioning in the Neonatal Male Rat Facilitates Subsequent Sexual Partner Preference. Psychoneuroendocrinology. 2020;121:104858. doi: 10.1016/j.psyneuen.2020.104858. PubMed DOI

Domjan M., Huber-McDonald M., Holloway K.S. Conditioning Copulatory Behavior to an Artificial Object: Efficacy of Stimulus Fading. Anim. Learn. Behav. 1992;20:350–362. doi: 10.3758/BF03197958. DOI

Köksal F., Domjan M., Kurt A., Sertel O., Orüng S., Bowers R., Kumru G. An Animal Model of Fetishism. Behav. Res. Ther. 2005;42:1421–1434. doi: 10.1016/j.brat.2003.10.001. PubMed DOI

Ismail N., Jones S.L., Graham M.D., Sylvester S., Pfaus J.G. Partner Preference for Strain of Female in Long–Evans Male Rats. Physiol. Behav. 2011;102:285–290. doi: 10.1016/j.physbeh.2010.09.005. PubMed DOI

Quintana G.R., Desbiens S., Marceau S., Kalantari N., Bowden J., Pfaus J.G. Conditioned Partner Preference in Male and Female Rats for a Somatosensory Cue. Behav. Neurosci. 2019;133:188–197. doi: 10.1037/bne0000300. PubMed DOI

Quintana G.R., González B., Borduas E., Lemay V., Yarur F., Pfaus J.G. Naloxone Disrupts the Development of a Conditioned Ejaculatory Preference Based on a Somatosensory Cue in Male Rats. Behav Neurosci. 2019;133:198–202. doi: 10.1037/bne0000302. PubMed DOI

Pfaus J.G., Erickson K.A., Talianakis S. Somatosensory Conditioning of Sexual Arousal and Copulatory Behavior in the Male Rat: A Model of Fetish Development. Physiol. Behav. 2013;122:1–7. doi: 10.1016/j.physbeh.2013.08.005. PubMed DOI

Paredes R.G., Alonso A. Sexual Behavior Regulated (Paced) by the Female Induces Conditioned Place Preference. Behav. Neurosci. 1997;111:123–128. doi: 10.1037/0735-7044.111.1.123. PubMed DOI

Pfaus J.G., Smith W.J., Coopersmith C.B. Appetitive and Consummatory Sexual Behaviors of Female Rats in Bilevel Chambers. I. A Correlational and Factor Analysis and the Effects of Ovarian Hormones. Horm. Behav. 1999;35:224–240. doi: 10.1006/hbeh.1999.1516. PubMed DOI

Erskine M.S. Effects of Paced Coital Stimulation on Estrus Duration in Intact Cycling Rats and Ovariectomized and Ovariectomized-Adrenalectomized Hormone-Primed Rats. Behav. Neurosci. 1985;99:151. doi: 10.1037/0735-7044.99.1.151. PubMed DOI

Coria-Avila G.A., Ouimet A.J., Pacheco P., Manzo J., Pfaus J.G. Olfactory Conditioned Partner Preference in the Female Rat. Behav. Neurosci. 2005;119:716–725. doi: 10.1037/0735-7044.119.3.716. PubMed DOI

Coria-Avila G.A., Solomon C.E., Vargas E.B., Lemme I., Ryan R., Ménard S., Gavrila A.M., Pfaus J.G. Neurochemical Basis of Conditioned Partner Preference in the Female Rat: I. Disruption by Naloxone. Behav. Neurosci. 2008;122:385–395. doi: 10.1037/0735-7044.122.2.385. PubMed DOI

Coria-Avila G.A., Jones S.L., Solomon C.E., Gavrila A.M., Jordan G.J., Pfaus J.G. Conditioned Partner Preference in Female Rats for Strain of Male. Physiol. Behav. 2006;88:529–537. doi: 10.1016/j.physbeh.2006.05.001. PubMed DOI

Meerts S.H., Clark A.S. Artificial Vaginocervical Stimulation Induces a Conditioned Place Preference in Female Rats. Horm. Behav. 2009;55:128–132. doi: 10.1016/j.yhbeh.2008.09.003. PubMed DOI PMC

Parada M., Chamas L., Censi S., Coria-Avila G., Pfaus J.G. Clitoral Stimulation Induces Conditioned Place Preference and Fos Activation in the Rat. Horm. Behav. 2010;57:112–118. doi: 10.1016/j.yhbeh.2009.05.008. PubMed DOI

Parada M., Abdul-Ahad F., Censi S., Sparks L., Pfaus J.G. Context Alters the Ability of Clitoral Stimulation to Induce a Sexually-Conditioned Partner Preference in the Rat. Horm. Behav. 2011;59:520–527. doi: 10.1016/j.yhbeh.2011.02.001. PubMed DOI

Ismail N., Gelez H., Lachapelle I., Pfaus J.G. Pacing Conditions Contribute to the Conditioned Ejaculatory Preference for a Familiar Female in the Male Rat. Physiol. Behav. 2009;96:201–208. doi: 10.1016/j.physbeh.2008.09.013. PubMed DOI

Mac Cionnaith C.E., Lemay A., Gomez-Perales E.L., Robert G., Cernik R., Brake W.G., Pfaus J.G. Fos Expression Is Increased in Oxytocin Neurons of Female Rats with a Sexually Conditioned Mate Preference for an Individual Male Rat. Horm. Behav. 2020;117:104612. doi: 10.1016/j.yhbeh.2019.104612. PubMed DOI

Thorndike E.L. Animal Intelligence: Experimental Studies. Macmillan Press; New York, NY, USA: 1911.

Skinner B.F. The Behavior of Organisms: An Experimental Analysis. Appleton-Century; Oxford, UK: 1938.

Ferster C.B., Skinner B.F. Schedules of Reinforcement. Appleton-Century; New York, NY, USA: 1957.

Beck J. Instrumental Conditioned Reflexes with Sexual Reinforcement in Rats. Acta Neurobiol. Exp. 1971;313:251–252. PubMed

Jowaisas D., Taylor J., Dewsbury D.A., Malagodi E.F. Copulatory Behavior of Male Rats under an Imposed Operant Requirement. Psychon. Sci. 1971;25:287–290. doi: 10.3758/BF03335879. DOI

Sheffield F.D., Wulff J.J., Backer R. Reward Value of Copulation without Sex Drive Reduction. J. Comp. Physiol. Psychol. 1951;44:3–8. doi: 10.1037/h0060074. PubMed DOI

Anderson E.E. Interrelationship of Drives in the Male Albino Rat. I. Intercorrelations of Measures of Drives. J. Comp. Psychol. 1937;24:73–118. doi: 10.1037/h0062846. DOI

Jiang S., Zhang Y., Zheng X., Luo H., Liu Z., Bai Y. A Conflict Model of Reward-Seeking Behavior in Male Rats. JoVE. 2019;144:e59141. doi: 10.3791/59141. PubMed DOI

Warner L.H. A Study of Sex Behavior in the White Rat by Means of the Obstruction Method. Comp. Psychol. Monogr. 1927;4:58.

Everitt B.J., Cador M., Robbins T.W. Interactions between the Amygdala and Ventral Striatum in Stimulus-Reward Associations: Studies Using a Second-Order Schedule of Sexual Reinforcement. Neuroscience. 1989;30:63–75. doi: 10.1016/0306-4522(89)90353-9. PubMed DOI

Everitt B.J., Stacey P. Studies of Instrumental Behavior with Sexual Reinforcement in Male Rats (Rattus Norvegicus): II. Effects of Preoptic Area Lesions, Castration, and Testosterone. J. Comp. Psychol. 1987;101:407–419. doi: 10.1037/0735-7036.101.4.407. PubMed DOI

Randich A., LoLordo V.M. Associative and Nonassociative Theories of the UCS Preexposure Phenomenon: Implications for Pavlovian Conditioning. Psychol. Bull. 1979;86:523–548. doi: 10.1037/0033-2909.86.3.523. PubMed DOI

Taylor J.A. Level of Conditioning and Intensity of the Adaptation Stimulus. J. Exp. Psychol. 1956;51:127–130. doi: 10.1037/h0042941. PubMed DOI

Rankin C.H., Abrams T., Barry R.J., Bhatnagar S., Clayton D.F., Colombo J., Coppola G., Geyer M.A., Glanzman D.L., Marsland S. Habituation Revisited: An Updated and Revised Description of the Behavioral Characteristics of Habituation. Neurobiol. Learn. Mem. 2009;92:135–138. doi: 10.1016/j.nlm.2008.09.012. PubMed DOI PMC

Quintana G.R., Guizar A., Rassi S., Pfaus J.G. First Sexual Experiences Determine the Development of Conditioned Ejaculatory Preference in Male Rats. Learn. Mem. 2018;25:522–532. doi: 10.1101/lm.048090.118. PubMed DOI PMC

Parada M., Jafari N., Pfaus J.G. Sexual Experience Blocks the Ability of Clitoral Stimulation to Induce a Conditioned Place Preference in the Rat. Physiol. Behav. 2013;119:97–102. doi: 10.1016/j.physbeh.2013.06.005. PubMed DOI

Lubow R.E., Moore A.U. Latent Inhibition: The Effect of Nonreinforced Pre-Exposure to the Conditional Stimulus. J. Comp. Physiol. Psychol. 1959;52:415–419. doi: 10.1037/h0046700. PubMed DOI

Rodríguez G., Alonso G. Latent Inhibition as a Function of CS Intensity in Taste Aversion Learning. Behav. Processes. 2002;60:61–67. doi: 10.1016/S0376-6357(02)00119-5. PubMed DOI

Schmajuk N.A. Latent Inhibition and Its Neural Substrates. Kluwer Academic Publishers; Dordrecht, The Netherlands: 2002.

Zamble E., Mitchell J.B., Findlay H. Pavlovian Conditioning of Sexual Arousal: Parametric and Background Manipulations. J. Exp. Psychol. Anim. Behav. Processes. 1986;12:403–411. doi: 10.1037/0097-7403.12.4.403. PubMed DOI

Quintana G.R., Jackson M., Nasr M., Pfaus J.G. Effect of CS Preexposure on the Conditioned Ejaculatory Preference of the Male Rat: Behavioral Analyses and Neural Correlates. Learn. Mem. 2018;25:513–521. doi: 10.1101/lm.048108.118. PubMed DOI PMC

Ménard S., Gelez H., Girard-Bériault F., Coria-Avila G., Pfaus J.G. Differential Role of Oxytocin and Vasopressin in the Conditioned Ejaculatory Preference of the Male Rat. Physiol. Behav. 2019;208:112577. doi: 10.1016/j.physbeh.2019.112577. PubMed DOI

Holley A., Shalev S., Bellevue S., Pfaus J.G. Conditioned Mate-Guarding Behavior in the Female Rat. Physiol. Behav. 2014;131:136–141. doi: 10.1016/j.physbeh.2014.04.034. PubMed DOI

McClintock M.K. Advances in the Study of Behavior. Volume 14. Elsevier; Amsterdam, The Netherlands: 1984. Group Mating in the Domestic Rat as a Context for Sexual Selection: Consequences for the Analysis of Sexual Behavior and Neuroendocrine Responses; pp. 1–50.

Holley A., Bellevue S., Vosberg D., Wenzel K., Roorda S., Pfaus J.G. The Role of Oxytocin and Vasopressin in Conditioned Mate Guarding Behavior in the Female Rat. Physiol. Behav. 2015;144:7–14. doi: 10.1016/j.physbeh.2015.02.039. PubMed DOI

Holley A., Joulakian L., Wenzel K., Roorda S., Jr., Gonzalez B., Sparks L., Pfaus J.G. Inhibition of Lysine-Specific Demethylase Enzyme Disrupts Sexually Conditioned Mate Guarding in the Female Rat. Physiol. Behav. 2018;196:78–83. doi: 10.1016/j.physbeh.2018.08.005. PubMed DOI

Herrera-Morales W.V., Herrera-Solís A., Núñez-Jaramillo L. Sexual Behavior and Synaptic Plasticity. Arch. Sex. Behav. 2019;48:2617–2631. doi: 10.1007/s10508-019-01483-2. PubMed DOI

Piergies A.M.H., Hicks M.E., Jr., Schwartz J.P., Meerts S.H. Sexually Experienced, but Not Naïve, Female Rats Show a Conditioned Object Preference (COP) for Mating after a Single Training Trial. Physiol. Behav. 2019;198:42–47. doi: 10.1016/j.physbeh.2018.09.017. PubMed DOI

Sanna F., Poddighe L., Serra M.P., Boi M., Bratzu J., Sanna F., Corda M.G., Giorgi O., Melis M.R., Argiolas A. C-Fos, ΔFosB, BDNF, TrkB and Arc Expression in the Limbic System of Male Roman High-and Low-Avoidance Rats That Show Differences in Sexual Behavior: Effect of Sexual Activity. Neuroscience. 2019;396:1–23. doi: 10.1016/j.neuroscience.2018.11.002. PubMed DOI

Sigl-Glöckner J., Maier E., Takahashi N., Sachdev R., Larkum M., Brecht M. Effects of Sexual Experience and Puberty on Mouse Genital Cortex Revealed by Chronic Imaging. Curr. Biol. 2019;29:3588–3599. doi: 10.1016/j.cub.2019.08.062. PubMed DOI

Meerts S.H., Park J.H., Sekhawat R. Sexual Experience Modulates Partner Preference and MPOA Nitric Oxide Synthase in Female Rats. Behav. Neurosci. 2016;130:490. doi: 10.1037/bne0000163. PubMed DOI

Nutsch V.L., Will R.G., Hattori T., Tobiansky D.J., Dominguez J.M. Sexual Experience Influences Mating-Induced Activity in Nitric Oxide Synthase-Containing Neurons in the Medial Preoptic Area. Neurosci. Lett. 2014;579:92–96. doi: 10.1016/j.neulet.2014.07.021. PubMed DOI

Ménard S., Gelez H., Coria-Avila G., Pfaus J.G. Sexual Experience Increases Oxytocin, but Not Vasopressin, Receptor Densities in the Ventromedial Hypothalamus and Central Amygdala of Male Rats. 2022. Submitted . PubMed

Pfaus J.G., Damsma G., Nomikos G.G., Wenkstern D.G., Blaha C.D., Phillips A.G., Fibiger H.C. Sexual Behavior Enhances Central Dopamine Transmission in the Male Rat. Brain Res. 1990;530:345–348. doi: 10.1016/0006-8993(90)91309-5. PubMed DOI

Pfaus J.G., Damsma G., Wenkstern D., Fibiger H.C. Sexual Activity Increases Dopamine Transmission in the Nucleus Accumbens and Striatum of Female Rats. Brain Res. 1995;693:21–30. doi: 10.1016/0006-8993(95)00679-K. PubMed DOI

Sanna F., Bratzu J., Piludu M.A., Corda M.G., Melis M.R., Giorgi O., Argiolas A. Dopamine, Noradrenaline and Differences in Sexual Behavior between Roman High and Low Avoidance Male Rats: A Microdialysis Study in the Medial Prefrontal Cortex. Front. Behav. Neurosci. 2017;11:108. doi: 10.3389/fnbeh.2017.00108. PubMed DOI PMC

Wenkstern D., Pfaus J.G., Fibiger H.C. Dopamine Transmission Increases in the Nucleus Accumbens of Male Rats during Their First Exposure to Sexually Receptive Female Rats. Brain Res. 1993;618:41–46. doi: 10.1016/0006-8993(93)90426-N. PubMed DOI

Pitchers K., Di Sebastiano A., Coolen L. MGluR5 Activation in the Nucleus Accumbens Is Not Essential for Sexual Behavior or Cross-Sensitization of Amphetamine Responses by Sexual Experience. Neuropharmacology. 2016;107:122–130. doi: 10.1016/j.neuropharm.2016.03.002. PubMed DOI

Coria-Avila G.A., Pfaus J.G. Neuronal Activation by Stimuli That Predict Sexual Reward in Female Rats. Neuroscience. 2007;148:623–632. doi: 10.1016/j.neuroscience.2007.05.052. PubMed DOI

Kippin T.E., Cain S.W., Pfaus J.G. Estrous Odors and Sexually Conditioned Neutral Odors Activate Separate Neural Pathways in the Male Rat. Neuroscience. 2003;117:971–979. doi: 10.1016/S0306-4522(02)00972-7. PubMed DOI

Pfaus J.G., Heeb M.M. Implications of Immediate-Early Gene Induction in the Brain Following Sexual Stimulation of Female and Male Rodents. Brain Res. Bull. 1997;44:397–407. doi: 10.1016/S0361-9230(97)00219-0. PubMed DOI

Goldstein A., Tachibana S., Lowney L.I., Hunkapiller M., Hood L. Dynorphin-(1-13), an Extraordinarily Potent Opioid Peptide. Proc. Natl. Acad. Sci. USA. 1979;76:6666–6670. doi: 10.1073/pnas.76.12.6666. PubMed DOI PMC

Lewis R.V., Stern A.S., Kimura S., Rossier J., Stein S., Udenfriend S. An about 50,000-Dalton Protein in Adrenal Medulla: A Common Precursor of [Met]- and [Leu]Enkephalin. Science. 1980;208:1459–1461. doi: 10.1126/science.7384787. PubMed DOI

Nakanishi S., Inoue A., Kita T., Numa S., Chang A.C., Cohen S.N., Nunberg J., Schimke R.T. Construction of Bacterial Plasmids That Contain the Nucleotide Sequence for Bovine Corticotropin-Beta-Lipotropin Precursor. Proc. Natl. Acad. Sci. USA. 1978;75:6021–6025. doi: 10.1073/pnas.75.12.6021. PubMed DOI PMC

Desjardins G.C., Brawer J.R., Beaudet A. Distribution of Mu, Delta, and Kappa Opioid Receptors in the Hypothalamus of the Rat. Brain Res. 1990;536:114–123. doi: 10.1016/0006-8993(90)90015-4. PubMed DOI

Mansour A., Fox C.A., Burke S., Meng F., Thompson R.C., Akil H., Watson S.J. Mu, Delta, and Kappa Opioid Receptor MRNA Expression in the Rat CNS: An in Situ Hybridization Study. J. Comp. Neurol. 1994;350:412–438. doi: 10.1002/cne.903500307. PubMed DOI

Gaudriault G., Nouel D., Dal Farra C., Beaudet A., Vincent J.-P. Receptor-Induced Internalization of Selective Peptidic μ and δ Opioid Ligands. J. Biol. Chem. 1997;272:2880–2888. doi: 10.1074/jbc.272.5.2880. PubMed DOI

Pfaus J.G., Smith W.J., Byrne N., Stephens G. Appetitive and Consummatory Sexual Behaviors of Female Rats in Bilevel Chambers. Horm. Behav. 2000;37:96–107. doi: 10.1006/hbeh.1999.1562. PubMed DOI

Van Furth W.R., van Emst M.G., van Ree J.M. Opioids and Sexual Behavior of Male Rats: Involvement of the Medial Preoptic Area. Behav. Neurosci. 1995;109:123–134. doi: 10.1037/0735-7044.109.1.123. PubMed DOI

Rodrıguez-Manzo G., Asai M., Fernández-Guasti A. Evidence for Changes in Brain Enkephalin Contents Associated to Male Rat Sexual Activity. Behav. Brain Res. 2002;131:47–55. doi: 10.1016/S0166-4328(01)00371-0. PubMed DOI

Arletti R., Calza L., Giardino L., Benelli A., Cavazzuti E., Bertolini A. Sexual Impotence Is Associated with a Reduced Production of Oxytocin and with an Increased Production of Opioid Peptides in the Paraventricular Nucleus of Male Rats. Neurosci. Lett. 1997;233:65–68. doi: 10.1016/S0304-3940(97)00478-3. PubMed DOI

Matuszewich L., Dornan W.A. Bilateral Injections of a Selectiveμ-Receptor Agonist (Morphiceptin) into the Medial Preoptic Nucleus Produces a Marked Delay in the Initiation of Sexual Behavior in the Male Rat. Psychopharmacology. 1992;106:391–396. doi: 10.1007/BF02245424. PubMed DOI

Leyton M., Stewart J. The Stimulation of Central κ Opioid Receptors Decreases Male Sexual Behavior and Locomotor Activity. Brain Res. 1992;594:56–74. doi: 10.1016/0006-8993(92)91029-E. PubMed DOI

Gessa G., Paglietti E., Quarantotti B.P. Induction of Copulatory Behavior in Sexually Inactive Rats by Naloxone. Science. 1979;204:203–205. doi: 10.1126/science.432642. PubMed DOI

Pfaus J.G., Wilkins M.F. A Novel Environment Disrupts Copulation in Sexually Naive but Not Experienced Male Rats: Reversal with Naloxone. Physiol. Behav. 1995;57:1045–1049. doi: 10.1016/0031-9384(94)00394-K. PubMed DOI

Rodriguez-Manzo G., Fernández-Guasti A. Opioid Antagonists and the Sexual Satiation Phenomenon. Psychopharmacology. 1995;122:131–136. doi: 10.1007/BF02246087. PubMed DOI

Myers B.M., Baum M.J. Facilitation by Opiate Antagonists of Sexual Performance in the Male Rat. Pharmacol. Biochem. Behav. 1979;10:615–618. doi: 10.1016/0091-3057(79)90242-9. PubMed DOI

Pfaus J.G., Pfaff D.W. Mu-, Delta-, and Kappa-Opioid Receptor Agonists Selectively Modulate Sexual Behaviors in the Female Rat: Differential Dependence on Progesterone. Horm. Behav. 1992;26:457–473. doi: 10.1016/0018-506X(92)90014-M. PubMed DOI

Acosta-Martinez M., Etgen A.M. Activation of μ-Opioid Receptors Inhibits Lordosis Behavior in Estrogen and Progesterone-Primed Female Rats. Horm. Behav. 2002;41:88–100. doi: 10.1006/hbeh.2001.1741. PubMed DOI

Johnson C., Hong W., Micevych P. Optogenetic Activation of β-Endorphin Terminals in the Medial Preoptic Nucleus Regulates Female Sexual Receptivity. Eneuro. 2020;7:ENEURO.0315-19.2019. doi: 10.1523/ENEURO.0315-19.2019. PubMed DOI PMC

Bozarth M.A., Wise R.A. Intracranial Self-Administration of Morphine into the Ventral Tegmental Area in Rats. Life Sci. 1981;28:551–555. doi: 10.1016/0024-3205(81)90148-X. PubMed DOI

Shippenberg T.S., Elmer G.I. The Neurobiology of Opiate Reinforcement. Crit. Rev. Neurobiol. 1998;12:267–303. doi: 10.1615/CritRevNeurobiol.v12.i4.10. PubMed DOI

Stolerman I. Motivational Effects of Opioids: Evidence on the Role of Endorphins in Mediating Reward or Aversion. Pharmacol. Biochem. Behav. 1985;23:877–881. doi: 10.1016/0091-3057(85)90086-3. PubMed DOI

Van Ree J.M., Niesink R.J., Van Wolfswinkel L., Ramsey N.F., Van Furth W.R., Vanderschuren L.J., Gerrits M.A., Van den Berg C.L. Endogenous Opioids and Reward. Eur. J. Pharmacol. 2000;405:89–101. doi: 10.1016/S0014-2999(00)00544-6. PubMed DOI

Wise R.A. The Brain and Reward. Oxford University Press; New York, NY, USA: 1989.

Ågmo A., Gómez M. Conditioned Place Preference Produced by Infusion of Met-Enkephalin into the Medial Preoptic Area. Brain Res. 1991;550:343–346. doi: 10.1016/0006-8993(91)91339-3. PubMed DOI

Garduño-Gutiérrez R., León-Olea M., Rodríguez-Manzo G. Opioid Receptor and β-Arrestin2 Densities and Distribution Change after Sexual Experience in the Ventral Tegmental Area of Male Rats. Physiol. Behav. 2018;189:107–115. doi: 10.1016/j.physbeh.2018.03.019. PubMed DOI

Herz A. Opioid Reward Mechanisms: A Key Role in Drug Abuse? Can. J. Physiol. Pharmacol. 1998;76:252–258. doi: 10.1139/y98-017. PubMed DOI

Laurent V., Morse A.K., Balleine B.W. The Role of Opioid Processes in Reward and Decision-making. Br. J. Pharmacol. 2015;172:449–459. doi: 10.1111/bph.12818. PubMed DOI PMC

Raehal K.M., Schmid C.L., Groer C.E., Bohn L.M. Functional Selectivity at the μ-Opioid Receptor: Implications for Understanding Opioid Analgesia and Tolerance. Pharm. Rev. 2011;63:1001–1019. doi: 10.1124/pr.111.004598. PubMed DOI PMC

Pfaus J.G., Mendelson S.D., Phillips A.G. A Correlational and Factor Analysis of Anticipatory and Consummatory Measures of Sexual Behavior in the Male Rat. Psychoneuroendocrinology. 1990;15:329–340. doi: 10.1016/0306-4530(90)90058-H. PubMed DOI

Van Furth W.R., Wolterink-Donselaar I.G., van Ree J.M. Endogenous Opioids Are Differentially Involved in Appetitive and Consummatory Aspects of Sexual Behavior of Male Rats. Am. J. Physiol. 1994;266:R606–R613. doi: 10.1152/ajpregu.1994.266.2.R606. PubMed DOI

Burkett J.P., Spiegel L.L., Inoue K., Murphy A.Z., Young L.J. Activation of μ-Opioid Receptors in the Dorsal Striatum Is Necessary for Adult Social Attachment in Monogamous Prairie Voles. Neuropsychopharmacol. 2011;36:2200–2210. doi: 10.1038/npp.2011.117. PubMed DOI PMC

Quintana G.R., Birrel M., Marceau S., Kalantari N., Bowden J., Bachoura Y., Borduas E., Lemay V., Payne J.W., Cionnaith C.M., et al. Differential Disruption of Conditioned Ejaculatory Preference in the Male Rat Based on Different Sensory Modalities by Micro-Infusions of Naloxone to the Medial Preoptic Area or Ventral Tegmental Area. Psychopharmacology. 2019;236:3613–3623. doi: 10.1007/s00213-019-05334-9. PubMed DOI

Kalivas P.W., Duffy P. Effects of Daily Cocaine and Morphine Treatment on Somatodendritic and Terminal Field Dopamine Release. J. Neurochem. 1988;50:1498–1504. doi: 10.1111/j.1471-4159.1988.tb03036.x. PubMed DOI

Kalivas P.W., Stewart J. Dopamine Transmission in the Initiation and Expression of Drug-and Stress-Induced Sensitization of Motor Activity. Brain Res. Rev. 1991;16:223–244. doi: 10.1016/0165-0173(91)90007-U. PubMed DOI

Kalivas P.W., Weber B. Amphetamine Injection into the Ventral Mesencephalon Sensitizes Rats to Peripheral Amphetamine and Cocaine. J. Pharmacol. Exp. Ther. 1988;245:1095–1102. PubMed

Robinson T.E., Berridge K.C. The Neural Basis of Drug Craving: An Incentive-Sensitization Theory of Addiction. Brain Res. Rev. 1993;18:247–291. doi: 10.1016/0165-0173(93)90013-P. PubMed DOI

Pert A., Post R., Weiss S.R. Conditioning as a Critical Determinant of Sensitization Induced by Psychomotor Stimulants. NIDA Res. Monogr. 1990;97:208–241. PubMed

Deniau J., Thierry A., Feger J. Electrophysiological Identification of Mesencephalic Ventromedial Tegmental (VMT) Neurons Projecting to the Frontal Cortex, Septum and Nucleus Accumbens. Brain Res. 1980;189:315–326. doi: 10.1016/0006-8993(80)90093-1. PubMed DOI

Oades R.D., Halliday G.M. Ventral Tegmental (A10) System: Neurobiology. 1. Anatomy and Connectivity. Brain Res. Rev. 1987;12:117–165. doi: 10.1016/0165-0173(87)90011-7. PubMed DOI

Swanson L.W. nd The Projections of the Ventral Tegmental Area and Adjacent Regions: A Combined Fluorescent Retrograde Tracer and Immunofluorescence Study in the Rat. Brain Res. Bull. 1982;9:321–353. doi: 10.1016/0361-9230(82)90145-9. PubMed DOI

Aragona B.J., Liu Y., Curtis J.T., Stephan F.K., Wang Z. A Critical Role for Nucleus Accumbens Dopamine in Partner-Preference Formation in Male Prairie Voles. J. Neurosci. 2003;23:3483–3490. doi: 10.1523/JNEUROSCI.23-08-03483.2003. PubMed DOI PMC

Curtis J.T., Wang Z. Ventral Tegmental Area Involvement in Pair Bonding in Male Prairie Voles. Physiol. Behav. 2005;86:338–346. doi: 10.1016/j.physbeh.2005.08.022. PubMed DOI

Di Chiara G. Nucleus Accumbens Shell and Core Dopamine: Differential Role in Behavior and Addiction. Behav. Brain Res. 2002;137:75–114. doi: 10.1016/S0166-4328(02)00286-3. PubMed DOI

Li Y.-L., Wei S., Liu Q., Gong Q., Zhang Q.-J., Zheng T.-G., Yong Z., Chen F., Lawrence A.J., Liang J.-H. Mu-Opioid Receptors in Septum Mediate the Development of Behavioural Sensitization to a Single Morphine Exposure in Male Rats. Addict. Biol. 2022;27:e13066. doi: 10.1111/adb.13066. PubMed DOI

Stewart J. Conditioned and Unconditioned Drug Effects in Relapse to Opiate and Stimulant Drug Self-Adminstration. Prog. Neuro-Psychopharmacol. Biol. Psychiatry. 1983;7:591–597. doi: 10.1016/0278-5846(83)90030-1. PubMed DOI

Graham M.D., Gardner Gregory J., Hussain D., Brake W.G., Pfaus J.G. Ovarian Steroids Alter Dopamine Receptor Populations in the Medial Preoptic Area of Female Rats: Implications for Sexual Motivation, Desire, and Behaviour. Eur. J. Neurosci. 2015;42:3138–3148. doi: 10.1111/ejn.13121. PubMed DOI

Tobiansky D.J., Will R.G., Lominac K.D., Turner J.M., Hattori T., Krishnan K., Martz J.R., Nutsch V.L., Dominguez J.M. Estradiol in the Preoptic Area Regulates the Dopaminergic Response to Cocaine in the Nucleus Accumbens. Neuropsychopharmacology. 2016;41:1897–1906. doi: 10.1038/npp.2015.360. PubMed DOI PMC

Barrot M., Sesack S.R., Georges F., Pistis M., Hong S., Jhou T.C. Braking Dopamine Systems: A New GABA Master Structure for Mesolimbic and Nigrostriatal Functions. J. Neurosci. 2012;32:14094–14101. doi: 10.1523/JNEUROSCI.3370-12.2012. PubMed DOI PMC

Fields H.L., Margolis E.B. Understanding Opioid Reward. Trends Neurosci. 2015;38:217–225. doi: 10.1016/j.tins.2015.01.002. PubMed DOI PMC

Grace A.A. Phasic versus Tonic Dopamine Release and the Modulation of Dopamine System Responsivity: A Hypothesis for the Etiology of Schizophrenia. Neuroscience. 1991;41:1–24. doi: 10.1016/0306-4522(91)90196-U. PubMed DOI

Blackburn J.R., Pfaus J.G., Phillips A.G. Dopamine Functions in Appetitive and Defensive Behaviours. Prog. Neurobiol. 1992;39:247–279. doi: 10.1016/0301-0082(92)90018-A. PubMed DOI

Mitchell J.B., Stewart J. Facilitation of Sexual Behaviors in the Male Rat Associated with Intra-VTA Injections of Opiates. Pharmacol. Biochem. Behav. 1990;35:643–650. doi: 10.1016/0091-3057(90)90302-X. PubMed DOI

McConnell S.K., Baum M.J., Badger T.M. Lack of Correlation between Naloxone-Induced Changes in Sexual Behavior and Serum LH in Male Rats. Horm. Behav. 1981;15:16–35. doi: 10.1016/0018-506X(81)90032-5. PubMed DOI

Childers S.R. Opioid Receptor-Coupled Second Messenger Systems. Life Sci. 1991;48:1991–2003. doi: 10.1016/0024-3205(91)90154-4. PubMed DOI

Kramer H.K., Simon E.J. μ and δ-Opioid Receptor Agonists Induce Mitogen-Activated Protein Kinase (MAPK) Activation in the Absence of Receptor Internalization. Neuropharmacology. 2000;39:1707–1719. doi: 10.1016/S0028-3908(99)00243-9. PubMed DOI

Samways D.S., Henderson G. Opioid Elevation of Intracellular Free Calcium: Possible Mechanisms and Physiological Relevance. Cell. Signal. 2006;18:151–161. doi: 10.1016/j.cellsig.2005.08.005. PubMed DOI

Ammon-Treiber S., Höllt V. Morphine-induced Changes of Gene Expression in the Brain. Addict. Biol. 2005;10:81–89. doi: 10.1080/13556210412331308994. PubMed DOI

Björk K., Tronci V., Thorsell A., Tanda G., Hirth N., Heilig M., Hansson A.C., Sommer W.H. β-Arrestin 2 Knockout Mice Exhibit Sensitized Dopamine Release and Increased Reward in Response to a Low Dose of Alcohol. Psychopharmacology. 2013;230:439–449. doi: 10.1007/s00213-013-3166-x. PubMed DOI PMC

Argiolas A., Melis M.R. Neuropeptides and Central Control of Sexual Behaviour from the Past to the Present: A Review. Prog. Neurobiol. 2013;108:80–107. doi: 10.1016/j.pneurobio.2013.06.006. PubMed DOI

Bratzu J., Bharatiya R., Manca E., Cocco C., Argiolas A., Melis M.R., Sanna F. Oxytocin Induces Penile Erection and Yawning When Injected into the Bed Nucleus of the Stria Terminalis: A Microdialysis and Immunohistochemical Study. Behav. Brain Res. 2019;375:112147. doi: 10.1016/j.bbr.2019.112147. PubMed DOI

Corona G., Isidori A.M., Aversa A., Burnett A.L., Maggi M. Endocrinologic Control of Men’s Sexual Desire and Arousal/Erection. J. Sex. Med. 2016;13:317–337. doi: 10.1016/j.jsxm.2016.01.007. PubMed DOI

Gelez H., Poirier S., Facchinetti P., Allers K.A., Wayman C., Alexandre L., Giuliano F. Neuroanatomical Evidence for a Role of Central Melanocortin-4 Receptors and Oxytocin in the Efferent Control of the Rodent Clitoris and Vagina. J. Sex. Med. 2010;7:2056–2067. doi: 10.1111/j.1743-6109.2010.01760.x. PubMed DOI

Carter C.S., Williams J.R., Witt D.M., Insel T.R. Oxytocin and Social Bonding. Ann. N. Y. Acad. Sci. 1992;652:204–211. doi: 10.1111/j.1749-6632.1992.tb34356.x. PubMed DOI

Insel T.R., Young L., Wang Z. Central Oxytocin and Reproductive Behaviours. Rev. Reprod. 1997;2:28–37. doi: 10.1530/ror.0.0020028. PubMed DOI

Insel T.R., Winslow J.T., Wang Z., Young L.J. Oxytocin, Vasopressin, and the Neuroendocrine Basis of Pair Bond Formation. Vasopressin Oxytocin. 1998;449:215–224. PubMed

Johnson Z.V., Young L.J. Oxytocin and Vasopressin Neural Networks: Implications for Social Behavioral Diversity and Translational Neuroscience. Neurosci. Biobehav. Rev. 2017;76:87–98. doi: 10.1016/j.neubiorev.2017.01.034. PubMed DOI PMC

Winslow J.T., Hastings N., Carter C.S., Harbaugh C.R., Insel T.R. A Role for Central Vasopressin in Pair Bonding in Monogamous Prairie Voles. Nature. 1993;365:545–548. doi: 10.1038/365545a0. PubMed DOI

Young L.J., Lim M.M., Gingrich B., Insel T.R. Cellular Mechanisms of Social Attachment. Horm. Behav. 2001;40:133–138. doi: 10.1006/hbeh.2001.1691. PubMed DOI

Young L.J., Wang Z. The Neurobiology of Pair Bonding. Nat. Neurosci. 2004;7:1048–1054. doi: 10.1038/nn1327. PubMed DOI

Panaro M.A., Benameur T., Porro C. Hypothalamic Neuropeptide Brain Protection: Focus on Oxytocin. J. Clin. Med. 2020;9:1534. doi: 10.3390/jcm9051534. PubMed DOI PMC

Althammer F., Grinevich V. Diversity of Oxytocin Neurones: Beyond Magno- and Parvocellular Cell Types? J. Neuroendocrinol. 2018;30:e12549. doi: 10.1111/jne.12549. PubMed DOI

Knobloch H.S., Charlet A., Hoffmann L.C., Eliava M., Khrulev S., Cetin A.H., Osten P., Schwarz M.K., Seeburg P.H., Stoop R., et al. Evoked Axonal Oxytocin Release in the Central Amygdala Attenuates Fear Response. Neuron. 2012;73:553–566. doi: 10.1016/j.neuron.2011.11.030. PubMed DOI

Landgraf R., Neumann I.D. Vasopressin and Oxytocin Release within the Brain: A Dynamic Concept of Multiple and Variable Modes of Neuropeptide Communication. Front. Neuroendocr. 2004;25:150–176. doi: 10.1016/j.yfrne.2004.05.001. PubMed DOI

Eliava M., Melchior M., Knobloch-Bollmann H.S., Wahis J., da Silva Gouveia M., Tang Y., Ciobanu A.C., Triana del Rio R., Roth L.C., Althammer F., et al. A New Population of Parvocellular Oxytocin Neurons Controlling Magnocellular Neuron Activity and Inflammatory Pain Processing. Neuron. 2016;89:1291–1304. doi: 10.1016/j.neuron.2016.01.041. PubMed DOI PMC

Lim M.M., Murphy A.Z., Young L.J. Ventral Striatopallidal Oxytocin and Vasopressin V1a Receptors in the Monogamous Prairie Vole (Microtus Ochrogaster) J. Comp. Neurol. 2004;468:555–570. doi: 10.1002/cne.10973. PubMed DOI

Zhang X., Filippi S., Vignozzi L., Morelli A., Mancina R., Luconi M., Donati S., Marini M., Vannelli G., Forti G. Identification, Localization and Functional in Vitro and in Vivo Activity of Oxytocin Receptor in the Rat Penis. J. Endocrinol. 2005;184:567–576. doi: 10.1677/joe.1.05885. PubMed DOI

Mac Cionnaith C.E., Gomez-Perales E.L., Ismail H., Lacasse J., Pfaus J.G., Brake W.G. Peripheral Oxytocin Signalling Promotes Estrous Termination and Conditioned Mate Preferences in Long-Evans Female Rats. 2022. Submitted .

Coria-Avila G.A., Pfaus J.G., Hernandez M.E., Manzo J., Pacheco P. Timing between Ejaculations Changes Paternity Success. Physiol. Behav. 2004;80:733–737. doi: 10.1016/j.physbeh.2003.12.008. PubMed DOI

Melis M.R., Argiolas A. Central Control of Penile Erection: A Re-Visitation of the Role of Oxytocin and Its Interaction with Dopamine and Glutamic Acid in Male Rats. Neurosci. Biobehav. Rev. 2011;35:939–955. doi: 10.1016/j.neubiorev.2010.10.014. PubMed DOI

Crews D. Epigenetics and Its Implications for Behavioral Neuroendocrinology. Front. Neuroendocrinol. 2008;29:344–357. doi: 10.1016/j.yfrne.2008.01.003. PubMed DOI PMC

Elvir L., Duclot F., Wang Z., Kabbaj M. Epigenetic Regulation of Motivated Behaviors by Histone Deacetylase Inhibitors. Neurosci. Biobehav. Rev. 2019;105:305–317. doi: 10.1016/j.neubiorev.2017.09.030. PubMed DOI PMC

Roth T.L. Epigenetic Mechanisms in the Development of Behavior: Advances, Challenges, and Future Promises of a New Field. Dev. Psychopathol. 2013;25:1279–1291. doi: 10.1017/S0954579413000618. PubMed DOI PMC

Wang H., Duclot F., Liu Y., Wang Z., Kabbaj M. Histone Deacetylase Inhibitors Facilitate Partner Preference Formation in Female Prairie Voles. Nat. Neurosci. 2013;16:919–924. doi: 10.1038/nn.3420. PubMed DOI PMC

Metzger E., Wissmann M., Yin N., Müller J.M., Schneider R., Peters A.H., Günther T., Buettner R., Schüle R. LSD1 Demethylates Repressive Histone Marks to Promote Androgen-Receptor-Dependent Transcription. Nature. 2005;437:436–439. doi: 10.1038/nature04020. PubMed DOI

Ran X., Yang Y., Meng Y., Li Y., Zhou L., Wang Z., Zhu J. Distribution of D1 and D2 Receptor-Immunoreactive Neurons in the Paraventricular Nucleus of the Hypothalamus in the Rat. J. Chem. Neuroanat. 2019;98:97–103. doi: 10.1016/j.jchemneu.2019.04.002. PubMed DOI

Zhou L., Zhang Y., Lian H., Li Y., Wang Z. Colocalization of Dopamine Receptors in BDNF-Expressing Peptidergic Neurons in the Paraventricular Nucleus of Rats. J. Chem. Neuroanat. 2020;106:101794. doi: 10.1016/j.jchemneu.2020.101794. PubMed DOI

Hess M.E., Hess S., Meyer K.D., Verhagen L.A., Koch L., Brönneke H.S., Dietrich M.O., Jordan S.D., Saletore Y., Elemento O. The Fat Mass and Obesity Associated Gene (Fto) Regulates Activity of the Dopaminergic Midbrain Circuitry. Nat. Neurosci. 2013;16:1042–1048. doi: 10.1038/nn.3449. PubMed DOI

Lee H.C., Deng Q.W., Zhao Y.J. The Calcium Signaling Enzyme CD38—A Paradigm for Membrane Topology Defining Distinct Protein Functions. Cell Calcium. 2022;101:102514. doi: 10.1016/j.ceca.2021.102514. PubMed DOI

Chong A., Tolomeo S., Xiong Y., Angeles D., Cheung M., Becker B., Lai P.S., Lei Z., Malavasi F., Tang Q. Blending Oxytocin and Dopamine with Everyday Creativity. Sci. Rep. 2021;11:16185. doi: 10.1038/s41598-021-95724-x. PubMed DOI PMC

Higashida H. Somato-Axodendritic Release of Oxytocin into the Brain Due to Calcium Amplification Is Essential for Social Memory. J. Physiol. Sci. 2016;66:275–282. doi: 10.1007/s12576-015-0425-0. PubMed DOI PMC

Kim S., Kim T., Lee H.-R., Jang E.-H., Ryu H.-H., Kang M., Rah S.-Y., Yoo J., Lee B., Kim J.-I. Impaired Learning and Memory in CD38 Null Mutant Mice. Mol. Brain. 2016;9:16. doi: 10.1186/s13041-016-0195-5. PubMed DOI PMC

Quintana D.S., Rokicki J., van der Meer D., Alnæs D., Kaufmann T., Córdova-Palomera A., Dieset I., Andreassen O.A., Westlye L.T. Oxytocin Pathway Gene Networks in the Human Brain. Nat. Commun. 2019;10:668. doi: 10.1038/s41467-019-08503-8. PubMed DOI PMC

Sadikaj G., Moskowitz D., Zuroff D.C., Bartz J.A. CD38 Is Associated with Communal Behavior, Partner Perceptions, Affect and Relationship Adjustment in Romantic Relationships. Sci. Rep. 2020;10:12926. doi: 10.1038/s41598-020-69520-y. PubMed DOI PMC

Zhong J., Amina S., Liang M., Akther S., Yuhi T., Nishimura T., Tsuji C., Tsuji T., Liu H.-X., Hashii M. Cyclic ADP-Ribose and Heat Regulate Oxytocin Release via CD38 and TRPM2 in the Hypothalamus during Social or Psychological Stress in Mice. Front. Neurosci. 2016;10:304. doi: 10.3389/fnins.2016.00304. PubMed DOI PMC

Peñagarikano O. Oxytocin in Animal Models of Autism Spectrum Disorder. Dev. Neurobiol. 2017;77:202–213. doi: 10.1002/dneu.22449. PubMed DOI

Zhang R., Zhang H.-F., Han J.-S., Han S.-P. Genes Related to Oxytocin and Arginine-Vasopressin Pathways: Associations with Autism Spectrum Disorders. Neurosci. Bull. 2017;33:238–246. doi: 10.1007/s12264-017-0120-7. PubMed DOI PMC

Flood M. Exposure to Pornography Among Youth in Australia. J. Sociol. 2007;43:45–60. doi: 10.1177/1440783307073934. DOI

Wright P.J. U.S. Males and Pornography, 1973–2010: Consumption, Predictors, Correlates. J. Sex Res. 2013;50:60–71. doi: 10.1080/00224499.2011.628132. PubMed DOI

Bonierbale-branchereau M., Hontanx J., Boubli L. The Sexual Behavior of Young French People. Contracept. Fertil. Sex. 1987;15:61–67. PubMed

Darling C.A., Davidson J.K. Coitally Active University Students: Sexual Behaviors, Concerns, and Challenges. Adolescence. 1986;21:403. PubMed

Meston C.M., Levin R.J., Sipski M.L., Hull E.M., Heiman J.R. Women’s Orgasm. Annu. Rev. Sex Res. 2004;15:173–257. PubMed

Opperman E., Braun V., Clarke V., Rogers C. “It Feels so Good It Almost Hurts”: Young Adults’ Experiences of Orgasm and Sexual Pleasure. J. Sex Res. 2014;51:503–515. doi: 10.1080/00224499.2012.753982. PubMed DOI

Pfaus J.G., Scardochio T., Parada M., Gerson C., Quintana G.R., Coria-Avila G.A. Do Rats Have Orgasms? Socioaffect. Neurosci. Psychol. 2016;6:31883. doi: 10.3402/snp.v6.31883. PubMed DOI PMC

Chadwick S.B., Francisco M., van Anders S.M. When Orgasms Do Not Equal Pleasure: Accounts of “Bad” Orgasm Experiences during Consensual Sexual Encounters. Arch. Sex. Behav. 2019;48:2435–2459. doi: 10.1007/s10508-019-01527-7. PubMed DOI

Kingsberg S.A., Wysocki S., Magnus L., Krychman M.L. Vulvar and Vaginal Atrophy in Postmenopausal Women: Findings from the REVIVE (REal Women’s VIews of Treatment Options for Menopausal Vaginal ChangEs) Survey. J. Sex. Med. 2013;10:1790–1799. doi: 10.1111/jsm.12190. PubMed DOI

Rowland D., Donarski A., Graves V., Caldwell C., Hevesi B., Hevesi K. The Experience of Orgasmic Pleasure during Partnered and Masturbatory Sex in Women with and without Orgasmic Difficulty. J. Sex Marital Ther. 2019;45:550–561. doi: 10.1080/0092623X.2019.1586021. PubMed DOI

Rowland D.L., Kolba T.N. Relationship of Specific Sexual Activities to Orgasmic Latency, Pleasure, and Difficulty during Partnered Sex. J. Sex. Med. 2019;16:559–568. doi: 10.1016/j.jsxm.2019.02.002. PubMed DOI

Sanders S.A., Graham C.A., Milhausen R.R. Predicting Sexual Problems in Women: The Relevance of Sexual Excitation and Sexual Inhibition. Arch. Sex. Behav. 2008;37:241–251. doi: 10.1007/s10508-007-9235-7. PubMed DOI

Vandereycken W. On Desire, Excitement, and Impotence in Modern Sex Therapy. Psychother. Psychosom. 1987;47:175–180. doi: 10.1159/000288015. PubMed DOI

Pfaus J.G., Quintana G.R., Mac Cionnaith C., Parada M. The Whole versus the Sum of Some of the Parts: Toward Resolving the Apparent Controversy of Clitoral versus Vaginal Orgasms. Socioaffect. Neurosci. Psychol. 2016;6:32578. doi: 10.3402/snp.v6.32578. PubMed DOI PMC

Van Anders S.M., Herbenick D., Brotto L.A., Harris E.A., Chadwick S.B. The Heteronormativity Theory of Low Sexual Desire in Women Partnered with Men. Arch. Sex. Behav. 2022;51:391–415. doi: 10.1007/s10508-021-02100-x. PubMed DOI PMC

Costa R.M., Brody S. Women’s Relationship Quality Is Associated with Specifically Penile-Vaginal Intercourse Orgasm and Frequency. J. Sex Marital Ther. 2007;33:319–327. doi: 10.1080/00926230701385548. PubMed DOI

Van Roijen J.H., Slob A.K., Gianotten W.L., Dohle G.R., van der Zon A.T., Vreeburg J.T., Weber R.F. Sexual Arousal and the Quality of Semen Produced by Masturbation. Hum. Reprod. 1996;11:147–151. doi: 10.1093/oxfordjournals.humrep.a019008. PubMed DOI

El Amiri S., Brassard A., Rosen N.O., Rossi M.A., Beaulieu N., Bergeron S., Péloquin K. Sexual Function and Satisfaction in Couples with Infertility: A Closer Look at the Role of Personal and Relational Characteristics. J. Sex. Med. 2021;18:1984–1997. doi: 10.1016/j.jsxm.2021.09.009. PubMed DOI

Gonçalves W.S., Gherman B.R., Abdo C.H.N., Coutinho E.S.F., Nardi A.E., Appolinario J.C. Prevalence of Sexual Dysfunction in Depressive and Persistent Depressive Disorders: A Systematic Review and Meta-Analysis. Int. J. Impot. Res. 2022:1–10. doi: 10.1038/s41443-022-00539-7. PubMed DOI

Kalmbach D.A., Ciesla J.A., Janata J.W., Kingsberg S.A. Specificity of Anhedonic Depression and Anxious Arousal with Sexual Problems among Sexually Healthy Young Adults. J. Sex. Med. 2012;9:505–513. doi: 10.1111/j.1743-6109.2011.02533.x. PubMed DOI

Trovao J.N., Serefoglu E.C. Neurobiology of Male Sexual Dysfunctions in Psychiatric Disorders: The Cases of Depression, Anxiety, Mania and Schizophrenia. Int. J. Impot. Res. 2018;30:279–286. doi: 10.1038/s41443-018-0077-8. PubMed DOI

Baldwin D.S., Manson C., Nowak M. Impact of Antidepressant Drugs on Sexual Function and Satisfaction. CNS Drugs. 2015;29:905–913. doi: 10.1007/s40263-015-0294-3. PubMed DOI

Clayton A.H., Croft H.A., Handiwala L. Antidepressants and Sexual Dysfunction: Mechanisms and Clinical Implications. Postgrad. Med. 2014;126:91–99. doi: 10.3810/pgm.2014.03.2744. PubMed DOI

Grimsley S., Jann M.W. Paroxetine, Sertraline, and Fluvoxamine: New Selective Serotonin Reuptake Inhibitors. Clin. Pharm. 1992;11:930–957. PubMed

Hirschfeld R.M. Efficacy of SSRIs and Newer Antidepressants in Severe Depression: Comparison with TCAs. J. Clin. Psychiatry. 1999;60:6242. doi: 10.4088/JCP.v60n0511. PubMed DOI

Lorenz T., Rullo J., Faubion S. Antidepressant-Induced Female Sexual Dysfunction. Volume 91. Elsevier; Amsterdam, The Netherlands: 2016. pp. 1280–1286. PubMed PMC

Rothmore J. Antidepressant-induced Sexual Dysfunction. Med. J. Aust. 2020;212:329–334. doi: 10.5694/mja2.50522. PubMed DOI

Zajecka J., Fawcett J., Schaff M., Jeffriess H., Guy C. The Role of Serotonin in Sexual Dysfunction: Fluoxetine-Associated Orgasm Dysfunction. J. Clin. Psychiatry. 1991;52:66–68. PubMed

Segraves R.T. Antidepressant-Induced Orgasm Disorder. J. Sex Marital Ther. 1995;21:192–201. doi: 10.1080/00926239508404398. PubMed DOI

Kinsey A.C., Pomeroy W.B., Martin C.E. Sexual Behavior in the Human Male. Saunders; Oxford, UK: 1948. PubMed PMC

Kinsey A.C., Pomeroy W.B., Martin C.E., Gebhard P.H. Sexual Behavior in the Human Female. Saunders; Oxford, UK: 1953.

Faulkenberry J.R., Vincent M., James A., Johnson W. Coital Behaviors, Attitudes, and Knowledge of Students Who Experience Early Coitus. Adolescence. 1987;22:321. PubMed

Meston C.M., Hamilton L.D., Harte C.B. Sexual Motivation in Women as a Function of Age. J. Sex. Med. 2009;6:3305–3319. doi: 10.1111/j.1743-6109.2009.01489.x. PubMed DOI PMC

Kleinplatz P.J., Ménard A.D., Paquet M.-P., Paradis N., Campbell M., Zuccarino D., Mehak L. The Components of Optimal Sexuality: A Portrait of “Great Sex”. Can. J. Hum. Sex. 2009;18:1–13.

Boul L., Hallam-Jones R., Wylie K.R. Sexual Pleasure and Motivation. J. Sex Marital Ther. 2008;35:25–39. doi: 10.1080/00926230802525620. PubMed DOI

Bischof-Campbell A., Hilpert P., Burri A., Bischof K. Body Movement Is Associated with Orgasm during Vaginal Intercourse in Women. J. Sex Res. 2019;56:356–366. doi: 10.1080/00224499.2018.1531367. PubMed DOI

Buss D.M. Sociobiology and Psychology: Ideas, Issues, and Applications. Lawrence Erlbaum; Mahwah, NJ, USA: 1987. Sex Differences in Human Mate Selection Criteria: An Evolutionary Perspective; pp. 335–352.

Meston C.M., Buss D.M. Why Humans Have Sex. Arch. Sex. Behav. 2007;36:477–507. doi: 10.1007/s10508-007-9175-2. PubMed DOI

Bateson P. Sexual Imprinting and Optimal Outbreeding. Nature. 1978;273:659–660. doi: 10.1038/273659a0. PubMed DOI

Bateson P. Mate Choice. Cambridge University Press; Cambridge, UK: 1983.

Lorenz K. Der Kumpan in Der Umwelt Des Vogels. J. Ornithol. 1935;83:137–213. doi: 10.1007/BF01905355. DOI

Fillion T.J., Blass E.M. Infantile Experience with Suckling Odors Determines Adult Sexual Behavior in Male Rats. Science. 1986;231:729–731. doi: 10.1126/science.3945807. PubMed DOI

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Do Sex and Gender Have Separate Identities?

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