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The Neurochemistry of Sexual Desire and Sexual Pleasure

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The Neurochemistry of Sexual Desire and Sexual Pleasure 10/9/2018 The neurochemistry of sexual desire and sexual pleasure James G. Pfaus, PhD, IF Center for Studies in Behavioral Neurobiology Department of Psychology, Concordia University Montréal, QC, Canada 2018 Meeting of the North American Menopause Society Presidential symposium “Sexual desire: Wired for wild” 3 October 2018 Acknowledgements –Jim Pfaus Grants: Canadian Institutes for Health Research (CIHR), Fonds de la recherche en santé du Québec (FRSQ), and the Natural Sciences and Engineering Research Council (NSERC). Contracts/Ad Boards/Honoraria: Acadia Pharmaceuticals, Emotional Brain LLC; Palatin Technologies/AMAG Pharmaceuticals. 1 10/9/2018 Masters and Johnson’s (1966) EPOR Model, after Moll (1908) Male Female Voluptuous acme Equable voluptuous sensations Albert Moll (1862‐1939) The Onset Tumescence drive Detumescence drive and as modified by Kaplan (1974) and Georgiadis et al. (2012) William Masters and Virginia E. Johnson (1915‐2001) (1925‐2013) Helen Singer Kaplan (1929‐1995) Janniko Georgiadis (1973‐ ) Female Sexual Response Cycle Phases RESTING EXCITEMENT ORGASMIC PLATEAU Salonia A, Giraldi A, Chivers ML, Georgiadis JR, Levin R, Maravilla KR, McCarthy MM.: Physiology of women's sexual function: basic knowledge and new findings. J Sex Med. 2010;7:2637‐60. 2 10/9/2018 Female Sexual Response Cycle Faces RESTING EXCITEMENT ORGASMIC PLATEAU Salonia A, Giraldi A, Chivers ML, Georgiadis JR, Levin R, Maravilla KR, McCarthy MM.: Physiology of women's sexual function: basic knowledge and new findings. J Sex Med. 2010;7:2637‐60. Definitions • Sexual Arousal Increased genital blood flow; heart rate; sweating, pupil dilation • Sexual Desire/Interest Wanting or craving sexual activity; behaviors aimed at acquiring sex partners or sexual reward • Sexual Reward Pleasure; orgasm; intimacy; bonding; control; other rewards • Sexual Inhibition Satiety; primary aversion; secondary avoidance 3 10/9/2018 (At least) two types of sexual systems 1.Reflexive (autonomic activation; genital reflexes and sensations, innate copulatory behaviors); involves hypothalamus, brainstem, spinal cord. 2. Incentive (Pavlovian associations between sexual stimuli and reward or punishment, and operant associations between behavior and reward or punishment); involves limbic and cortical structures that interact with certain hypothalamic nuclei. Georgiadis, Kringelbach, Pfaus (2012) Nature Rev Urol, 9, 486‐498 4 10/9/2018 Basson’s Model of Desire Numerous Sexual Incentives for Receptiveness Sex Rewards: Innate Sexual Sexual and Desire Sexual Stimuli Non-Sexual (hormonally driven) Sexual Responsive Arousal Desire (experientially driven) Basson (2002) J Sex Mar Ther 28, 1‐10. after Perelman (2006) J Sex Med, 3, 1004-1012 5 10/9/2018 INHIBITION (Reward/Satiety, Stress, or Aversion) Opioids- 5-HT- CBs- NE/OT+ X NE/OT+ DA/MCs+ DA/MCs+ X X Pfaus, Scepkowski, 2005, Curr Sex Health Rep, 2, 95‐100 Female sexual desire Precopulatory sexual solicitations in female rats and macaques are predictive of sexual interest and desire in women, and are driven by similar hormonal and neurochemical mechanisms • Facilitative effects of estradiol and androgens •Dopamine and melanocortin activation of solicitations and desire • Inhibition of 5‐HT2A receptors activates solicitations and desire over time. • Combination of testosterone and PDE‐5Is increase solicitations and responsive desire in both rats and women. Gelez H et al., JSM,2013:10:1231‐1239 Pfaus JG, Guiliano F., Gelez, H. JSM, 2007;4 (suppl. 4) 269‐279 Pfaus JG, Jones SL, Flanagan‐Cato LM, Blaustein, JD. Chapter 50, Physiology of Reproduction, 2015 New York:Elsevier Snoeren EMS et al., JSM 2011,8:989‐1001 6 10/9/2018 Excitatory Systems of the Brain + + Dopamine (DA) Noradrenaline (NA) ENDOCRINE, AUTONOMIC Cell bodies in locus coeruleus REGULATION, Projections to hypothalamic, limbic, and cortical regions; descending projections to MOTIVATION, ATTENTION, cerebellum and spinal cord. DESIRE, REWARD MOVEMENT AROUSAL Pfaus (2009) J Sex Med, 6, 1506‐1533. Neural excitatory systems Zona incerta 7 10/9/2018 Dopamine release in the mPOA is a general neural switch that controls sympathetic and parasympathetic blood flow in the presence of sexual cues. Pfaus (2009). J Sex Med, 6, 1506‐1533. Response to visual erotica (non‐clinical samples) mPOA mPOA Arnow et al. (2009) Neuroscience, 158, 484‐502; Arnow et al. (2002), Brain, 125, 1014‐1023 8 10/9/2018 mPOA D1 activation is critical for sexual desire and modulating sympathetic outflow SEXUAL SENSORY STIMULI Cortial and limbic systems mPOA CLITORIS OR PENILE CORPUS GENITALS OR PENIS Flaccid Erect Round ligament Suspensory of the uterus ligament Bladder Bladder Pubic bone Erect shaft Blood-filled Suspensory Hood ligament Closed valve Vagina cavern Empty cavern inside artery Pudendal vein Leg Pudendal vein Pudendal artery Pudendal artery Leg Glans Shaft Hood Glans Paraurethral Paraurethral duct duct Inner lip Perineal Perineal sponge Outer lip Inner lip sponge Outer lip Urethral Clitoral opening Urethral Closed valve opening Urethral to the vagina opening inside vein sponge Bulb Vulvovaginal Urethral Clitoral opening Vulvovaginal Bulb gland sponge to the vagina gland Sympathetic activation causes blood to accumulate in the spongiosum of the clitoris and labia, increasing the diameter of the glans clitoris, and exposing more tactile sensory nerve endings in both clitoris and labia. 9 10/9/2018 Sensory Input mPOA Mesolimbic Nigrostriatal Genital Appetitive Somatomotor Responses Behaviors Patterns Hull, Lorrain, Du, Matuszewich, Lumley, Putnam, Moses (1999) Behav Brain Res, 105, 105‐116 Excitatory Systems of the Brain ++ Melanocortins Oxytocin DESIRE, AROUSAL AROUSAL, BONDING 10 10/9/2018 Melanocortins and Sex • POMC peptides, including ACTH, and α‐MSH, have pronounced effects on the sexual behavior of female and male rats • α‐MSH facilitates lordosis in estrogen‐primed females and erection in gonadally‐intact males • α‐MSH levels in anterior hypothalamus increased by estrogen, suggesting that it may be one of several intermediaries of estrogen action Melanocortins in the brain • Cells originate in the arcuate nucleus of the hypothalamus and nucleus of the solitary tract. • Axons innervate other hypothalamic regions, limbic regions midbrain, brainstem, and spinal cord. • Melanocortin receptors exist in these regions, along with organs in the periphery. Arcuate nucleus POMC neurons POMC projections Melanocortin receptors 11 10/9/2018 Bremelanotide: (formerly PT-141) Ac-Nle-Asp-His-DPhe-Arg-Trp-Lys-OH α-MSH: Ser-Tyr-Ser-Met-Glu-His-Phe-Arg-Trp-Gly-Lys-Pro-Val . Binds to MC3R and MC4R in brain . Induces erections in healthy men . Induces erections in healthy rats . Induces erections in men with mild-to-moderate erectile dysfunction and in men who do not respond well to PDE-5 inhibitors . Rapid effect in rats (within 5 to 20 min) . Facilitates solicitations selectively in female rats Effects of bremelanotide in female rats Dose of BMT (μg/kg) mPOA DA release after BMT D1 D2 12 10/9/2018 Effects of bremelanotide in female rats Conditioning Odor Final Test Conditioned Partner Preference test Females received 5 trials each with scented males in a paced condition (partition), and unscented males in a nonpaced condition Unscented Scented male male (no partition). (Scented) (Unscented) (nonpreferred) (preferred) On the final test, females were Injected with BMT (200 μg/kg, sc) or SAL and given a choice No evidence that BMT disrupted conditioned of two males, one scented (preferred) and one unscented (nonpreferred) in an open field. partner preference. It increased solicitations only for the preferred partner. mPOA saline bremelanotide (100 µg/kg) bremelanotide (200 µg/kg) Pfaus, Giuliano, Gelez, 2007, J Sex Med, 4 (suppl 4), 269-279 13 10/9/2018 Neuronal activation induced by bremelanotide Brain Region Activity Significance mPOA +++ Solicitation (Proceptivity) VTA +++ Incentive Salience Attention NAc +++/++ Incentive Salience shell/core Attention PIR +++ Conditioned Arousal BLA +++ Reward-Related Learning VMH - Lordosis Pfaus, Giuliano, Gelez (2007). J Sex Med, 4 (suppl 4), 269-279 Action of melanocortins in the mPOA Resting (unstimulated) DA release Stimulated DA release MC4R MC4R MC4R MC4R α‐MSH/BMT D1 dopamine D1 dopamine receptor receptor Decreased release Increased release of dopamine of dopamine Graham et al. (2015). Eur J Neurosci, 42, 3138‐3148 14 10/9/2018 GABA projections from the mPOA to the VTA activate mesolimbic dopamine through disinhibition. mPFC GLU Serotonin mPOA Cannabinoids NAc Mesolimbic activation of appetitive responses Opioids/Opiates Graham et al. (2015). Eur J Neurosci, 42, 3138‐3148 Inhibitory Systems of the Brain -- Opioids Serotonin (5-HT) Nucleus Paragigantocellularis Proopiomelanocortin (POMC) systems: (nPGi) Cell bodies found in periarcuate regions Cell bodies in Raphe nuclei of hypothalamus and brainstem. Ascending projections to hypothalamic, limbic, and cortical regions; Diffuse projections to hypothalamic, Descending projections to spinal cord limbic, cortical, midbrain, and brainstem regions. SATIETY REWARD/PLEASURE 15 10/9/2018 GLU+ Mu opioid receptors (MORs) exist in all regions of the sexual reward/bonding circuit. β‐END+ Opioids sensitize β‐END‐ DA release; naloxone inhibits conditioned Opioids inhibit appetitive responses copulation; naloxone facilitates Van Furth, Van Ree, (1995) copulation under stress; Pitchers et al. (2014) MORs internalize after multiple ejaculations. Hughes, Everitt, Herbert (1990) Coolen et al. (2007) Opioids sensitize mesolimbic
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