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Compulsive Sexual Behavior in Humans and Preclinical Models

  • Lindsey B. Kuiper
  • Lique M. Coolen
Preclinical and Psychophysiology (F Guarraci and L Marson, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Preclinical and Psychophysiology

Abstract

Purpose of Review

Compulsive sexual behavior (CSB) is widely regarded as a “behavioral addiction,” and is a major threat to quality of life and both physical and mental health. However, CSB has been slow to be recognized clinically as a diagnosable disorder. CSB is co-morbid with affective disorders as well as substance use disorders, and recent neuroimaging studies have demonstrated shared or overlapping neural pathologies disorders, especially in brain regions controlling motivational salience and inhibitory control.

Recent Findings

Clinical neuroimaging studies are reviewed that have identified structural and/or function changes in prefrontal cortex, amygdala, striatum, and thalamus in individuals suffering from CSB. A preclinical model to study the neural underpinnings of CSB in male rats is discussed consisting of a conditioned aversion procedure to examine seeking of sexual behavior despite known negative consequences. Using this preclinical model, a role of the medial prefrontal cortex was identified, including neural plasticity during comorbidity of CSB and psychostimulant abuse.

Summary

This review summarizes recent human behavioral and neuroimaging studies, in addition to preclinical models that can be used to study the underlying neurobiology of CSB.

Keywords

Compulsive sexual behavior Hypersexuality Addiction Prefrontal cortex Limbic system Sexual behavior 

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major Importance

  1. 1.
    Derbyshire KL, Grant JE. Compulsive sexual behavior: a review of the literature. J Behav Addict. 2015;4:37–43.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Werner M, Stulhofer A, Waldorp L, Jurin T. A network approach to Hypersexuality: insights and clinical implications. J Sex Med. 2018;15:373–86.CrossRefPubMedGoogle Scholar
  3. 3.
    Kingston DA. Moving forward on Hypersexuality. Arch Sex Behav. 2017;46:2257–9.CrossRefPubMedGoogle Scholar
  4. 4.
    Walton MT, Cantor JM, Bhullar N, Lykins AD. Hypersexuality: a critical review and introduction to the "Sexhavior cycle". Arch Sex Behav. 2017;46:2231–51.CrossRefPubMedGoogle Scholar
  5. 5.
    Kuhn S, Gallinat J. Neurobiological basis of Hypersexuality. Int Rev Neurobiol. 2016;129:67–83.CrossRefPubMedGoogle Scholar
  6. 6.
    Kraus SW, Voon V, Potenza MN. Neurobiology of compulsive sexual behavior: emerging science. Neuropsychopharmacology. 2016;41:385–6.CrossRefPubMedGoogle Scholar
  7. 7.
    Blais-Lecours S, Vaillancourt-Morel MP, Sabourin S, Godbout N. Cyberpornography: time use, perceived addiction, sexual functioning, and sexual satisfaction. Cyberpsychol Behav Soc Netw. 2016;19:649–55.CrossRefPubMedGoogle Scholar
  8. 8.
    Lee K, Hutton HE, Lesko CR, Monroe AK, Alvanzo A, McCaul ME, et al. Associations of drug use, violence, and depressive symptoms with sexual risk behaviors among women with alcohol misuse. Womens Health Issues. 2018;Google Scholar
  9. 9.
    Reid RC, Dhuffar MK, Parhami I, Fong TW. Exploring facets of personality in a patient sample of hypersexual women compared with hypersexual men. J Psychiatr Pract. 2012;18:262–8.CrossRefPubMedGoogle Scholar
  10. 10.
    Dhuffar MK, Griffiths MD. Understanding the role of shame and its consequences in female hypersexual behaviours: a pilot study. J Behav Addict. 2014;3:231–7.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    K. Romer Thomsen et al. Impulsivity traits and addiction-related behaviors in youth. J Behav Addict. 2018;1–14.Google Scholar
  12. 12.
    Reid RC, Kafka MP. Controversies about hypersexual disorder and the DSM-5. Curr Sex Health Rep. 2014;6:259–64.CrossRefGoogle Scholar
  13. 13.
    A. P. Association. Diagnostic and statistical manual of mental disorders. 5th ed. Arlington, VA: American Psychiatric Publishing; 2013.CrossRefGoogle Scholar
  14. 14.
    •• Krueger RB. Diagnosis of hypersexual or compulsive sexual behavior can be made using ICD-10 and DSM-5 despite rejection of this diagnosis by the American Psychiatric Association. Addiction. 2016;111:2110–1. This commentary supports the clinical diagnosis of compulsive sexual behavior based on the ICD-10 and ICD-11, if not based on DSM-V. CrossRefPubMedGoogle Scholar
  15. 15.
    Emond FC, Nolet K, Cyr G, Rouleau J-L, Gagnon J. Sexual impulsivity and problematic sexual behaviors in adults: towards innovative domain-specific behavioral measures. J Sexol. 2015;25:184–90.CrossRefGoogle Scholar
  16. 16.
    Walton MT, Bhullar N. Compulsive sexual behavior as an impulse control disorder: awaiting field studies data. Arch Sex Behav. 2018;47:1327–31.CrossRefPubMedGoogle Scholar
  17. 17.
    • Gola M, Potenza MN. The proof of the pudding is in the tasting: data are needed to test models and hypotheses related to compulsive sexual behaviors. Arch Sex Behav. 2018). This letter highlights the importance of empirically-defined definitions of compulsive sexual behavior, and calls for more neuroscientific studies of the disorder.;47:1323–5.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Hook JN, Hook JP, Davis DE, Worthington EL Jr, Penberthy JK. Measuring sexual addiction and compulsivity: a critical review of instruments. J Sex Marital Ther. 2010;36:227–60.CrossRefPubMedGoogle Scholar
  19. 19.
    Tull MT, Gratz KL. Major depression and risky sexual behavior among substance dependent patients: the moderating roles of distress tolerance and gender. Cognit Ther Res. 2013;37:483–97.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Weiss NH, Tull MT, Sullivan TP, Dixon-Gordon KL, Gratz KL. Posttraumatic stress disorder symptoms and risky behaviors among trauma-exposed inpatients with substance dependence: the influence of negative and positive urgency. Drug Alcohol Depend. 2015;155:147–53.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Weiss NH, Tull MT, Dixon-Gordon K, Gratz KL. Assessing the negative and positive emotion-dependent nature of risky behaviors among substance dependent patients. Assessment. 2016:107319111666590.Google Scholar
  22. 22.
    Tull MT, Gratz KL, Weiss NH. Exploring associations between borderline personality disorder, crack/cocaine dependence, gender, and risky sexual behavior among substance-dependent inpatients. Personal Disord. 2011;2:209–19.CrossRefPubMedGoogle Scholar
  23. 23.
    Torrisi M, Cacciola A, Marra A, de Luca R, Bramanti P, Calabrò RS. Inappropriate behaviors and hypersexuality in individuals with dementia: an overview of a neglected issue. Geriatr Gerontol Int. 2017;17:865–74.CrossRefPubMedGoogle Scholar
  24. 24.
    Bronner G, Aharon-Peretz J, Hassin-Baer S. Sexuality in patients with Parkinson's disease, Alzheimer's disease, and other dementias. Handb Clin Neurol. 2015;130:297–323.CrossRefPubMedGoogle Scholar
  25. 25.
    Schenck CH, Arnulf I, Mahowald MW. Sleep and sex: what can go wrong? A review of the literature on sleep related disorders and abnormal sexual behaviors and experiences. Sleep. 2007;30:683–702.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Reid RC, Harper JM, Anderson EH. Coping strategies used by hypersexual patients to defend against the painful effects of shame. Clin Psychol Psychother. 2009;16:125–38.CrossRefPubMedGoogle Scholar
  27. 27.
    Weiss NH, Tull MT, Viana AG, Anestis MD, Gratz KL. Impulsive behaviors as an emotion regulation strategy: examining associations between PTSD, emotion dysregulation, and impulsive behaviors among substance dependent inpatients. J Anxiety Disord. 2012;26:453–8.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Watter DN. Existential issues in sexual medicine: the relation between death anxiety and Hypersexuality. Sex Med Rev. 2018;6:3–10.CrossRefPubMedGoogle Scholar
  29. 29.
    Chatzittofis A, Arver S, Öberg K, Hallberg J, Nordström P, Jokinen J. HPA axis dysregulation in men with hypersexual disorder. Psychoneuroendocrinology. 2016;63:247–53.CrossRefPubMedGoogle Scholar
  30. 30.
    Jokinen J, Boström AE, Chatzittofis A, Ciuculete DM, Öberg KG, Flanagan JN, et al. Methylation of HPA axis related genes in men with hypersexual disorder. Psychoneuroendocrinology. 2017;80:67–73.CrossRefPubMedGoogle Scholar
  31. 31.
    Walton MT, Lykins AD, Bhullar N. Sexual arousal and sexual activity frequency: implications for understanding Hypersexuality. Arch Sex Behav. 2016;45:777–82.CrossRefPubMedGoogle Scholar
  32. 32.
    Kingston DA, Graham FJ, Knight RA. Relations between self-reported adverse events in childhood and Hypersexuality in adult male sexual offenders. Arch Sex Behav. 2017;46:707–20.CrossRefPubMedGoogle Scholar
  33. 33.
    Liljegren M, Naasan G, Temlett J, Perry DC, Rankin KP, Merrilees J, et al. Criminal behavior in frontotemporal dementia and Alzheimer disease. JAMA Neurol. 2015;72:295–300.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Mendez MF, Shapira JS. Hypersexual behavior in frontotemporal dementia: a comparison with early-onset Alzheimer's disease. Arch Sex Behav. 2013;42:501–9.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    M. R. Lo Monaco et al., Prevalence of impulsive-compulsive symptoms in elderly Parkinson's disease patients: a case-control study. J Clin Psychiatry. 2018;79.Google Scholar
  36. 36.
    De Sousa SM, Chapman IM, Falhammar H, Torpy DJ. Dopa-testotoxicosis: disruptive hypersexuality in hypogonadal men with prolactinomas treated with dopamine agonists. Endocrine. 2017;55:618–24.CrossRefPubMedGoogle Scholar
  37. 37.
    Frohmader KS, Pitchers KK, Balfour ME, Coolen LM. Mixing pleasures: review of the effects of drugs on sex behavior in humans and animal models. Horm Behav. 2010;58:149–62.CrossRefPubMedGoogle Scholar
  38. 38.
    Volkow ND, et al. Stimulant-induced enhanced sexual desire as a potential contributing factor in HIV transmission. Am J Psychiatry. 2007;164:157–60.CrossRefPubMedGoogle Scholar
  39. 39.
    Ahmadi K, Javadinia SA, Saadat SH, Ramezani MA, Sedghijalal H. Triangular relationship among risky sexual behavior, addiction, and aggression: a systematic review. Electron Physician. 2017;9:5129–37.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Johnson MW, Bruner NR. The sexual discounting task: HIV risk behavior and the discounting of delayed sexual rewards in cocaine dependence. Drug Alcohol Depend. 2012;123:15–21.CrossRefPubMedGoogle Scholar
  41. 41.
    •• M. S. Berry, M. W. Johnson, Does being drunk or high cause HIV sexual risk behavior? A systematic review of drug administration studies. Pharmacol Biochem Behav 164, 125–138 (2018). This systematic review summarizes the recent links within the published literature, in both men and women, between substance use and compulsive sexual behavior. Google Scholar
  42. 42.
    Rawson RA, Washton A, Domier CP, Reiber C. Drugs and sexual effects: role of drug type and gender. J Subst Abus Treat. 2002;22:103–8.CrossRefGoogle Scholar
  43. 43.
    Semple SJ, Grant I, Patterson TL. Female methamphetamine users: social characteristics and sexual risk behavior. Women Health. 2004;40:35–50.CrossRefPubMedGoogle Scholar
  44. 44.
    Semple SJ, Patterson TL, Grant I. A comparison of injection and non-injection methamphetamine-using HIV positive men who have sex with men. Drug Alcohol Depend. 2004;76:203–12.CrossRefPubMedGoogle Scholar
  45. 45.
    Zapata LB, Hillis SD, Marchbanks PA, Curtis KM, Lowry R. Methamphetamine use is independently associated with recent risky sexual behaviors and adolescent pregnancy. J Sch Health. 2008;78:641–8.CrossRefPubMedGoogle Scholar
  46. 46.
    Cartier JJ, Greenwell L, Prendergast ML. The persistence of HIV risk behaviors among methamphetamine-using offenders. J Psychoactive Drugs. 2008;40:437–46.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Mausbach BT, Semple SJ, Strathdee SA, Patterson TL. Predictors of safer sex intentions and protected sex among heterosexual HIV-negative methamphetamine users: an expanded model of the theory of planned behavior. AIDS Care. 2009;21:17–24.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Saw YM, Saw TN, Chan N, Cho SM, Jimba M. Gender-specific differences in high-risk sexual behaviors among methamphetamine users in Myanmar-China border city, muse, Myanmar: who is at risk? BMC Public Health. 2018;18(209):209.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Mitchell SG, Kelly SM, Brown BS, O'Grady KE, Schwartz RP. HIV sex-risk behaviors among in- versus out-of-treatment heroin-addicted adults. Am J Drug Alcohol Abuse. 2012;38:328–33.CrossRefPubMedGoogle Scholar
  50. 50.
    Hartzler B, Beadnell B, Calsyn DA. Use of sexual risk assessment and feedback at intake to promote counselor awareness of subsequent client risk behavior during early treatment. Subst Use Misuse. 2014;49:1270–7.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Mastroleo NR, Operario D, Barnett NP, Colby SM, Kahler CW, Monti PM. Prevalence of heavy drinking and risky sexual behaviors in adult emergency department patients. Alcohol Clin Exp Res. 2015;39:1997–2002.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Wray TB, Celio MA, Kahler CW, Barnett NP, Mastroleo NR, Operario D, et al. Daily co-occurrence of alcohol use and high-risk sexual behavior among heterosexual, heavy drinking emergency department patients. Drug Alcohol Depend. 2015;152:109–15.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    MacKillop J, Celio MA, Mastroleo NR, Kahler CW, Operario D, Colby SM, et al. Behavioral economic decision making and alcohol-related sexual risk behavior. AIDS Behav. 2015;19:450–8.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    • M. W. Johnson, P. S. Johnson, E. S. Herrmann, M. M. Sweeney, Delay and probability discounting of sexual and monetary outcomes in individuals with cocaine use disorders and matched controls. PLoS One 10, e0128641 (2015). This study demonstrates that individuals with cocaine use disorders make impulsive choices for less-favorable outcomes, such as risky sexual behavior without a condom, in both sexual and monetary hypothetical delay discounting tasks. Google Scholar
  55. 55.
    Semple SJ, Strathdee SA, Zians J, Patterson TL. Life events and sexual risk among HIV-negative, heterosexual, methamphetamine users. J Sex Res. 2010;47:355–63.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Green AI, Halkitis PN. Crystal methamphetamine and sexual sociality in an urban gay subculture: an elective affinity. Culture, Health & Sexuality. 2006;8:317–33.CrossRefGoogle Scholar
  57. 57.
    Halkitis PN, Parsons JT, Stirratt MJ. A double epidemic: crystal methamphetamine drug use in relation to HIV transmission among gay men. J Homosex. 2001;41:17–35.CrossRefPubMedGoogle Scholar
  58. 58.
    Mckirnan DJ, Vanable PA, Ostrow DG, Hope B. Expectancies of sexual "escape" and sexual risk among drug and alcohol-involved gay and bisexual men. J Subst Abus. 2001;13:137–54.CrossRefGoogle Scholar
  59. 59.
    Peugh J, Belenko S. Alcohol, drugs and sexual function: a review. J Psychoactive Drugs. 2001;33:223–32.CrossRefPubMedGoogle Scholar
  60. 60.
    Fisher DG, Reynolds GL, Napper LE. Use of crystal methamphetamine, Viagra, and sexual behavior. Curr Opin Infect Dis. 2010;23:53–6.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Somlai AM, Kelly JA, McAuliffe TL, Ksobiech K, Hackl KL. Predictors of HIV sexual risk behaviors in a community sample of injection drug-using men and women. AIDS Behav. 2003;7:383–93.CrossRefPubMedGoogle Scholar
  62. 62.
    Frosch D, Shoptaw S, Huber A, Rawson RA, Ling W. Sexual HIV risk among gay and bisexual male methamphetamine abusers. J Subst Abus Treat. 1996;13:483–6.CrossRefGoogle Scholar
  63. 63.
    Zenilman JM. Behavioral interventions--rationale, measurement, and effectiveness. Infect Dis Clin N Am. 2005;19:541–62.CrossRefGoogle Scholar
  64. 64.
    Semple SJ, Patterson TL, Grant I. The context of sexual risk behavior among heterosexual methamphetamine users. Addict Behav. 2004;29:807–10.CrossRefPubMedGoogle Scholar
  65. 65.
    Springer AE, Peters RJ, Shegog R, White DL, Kelder SH. Methamphetamine use and sexual risk behaviors in U.S. high school students: findings from a national risk behavior survey. Prevention science : the official journal of the Society for Prevention Research. 2007;8:103–13.CrossRefGoogle Scholar
  66. 66.
    Semple SJ, Patterson TL, Grant I. Motivations associated with methamphetamine use among HIV men who have sex with men. J Subst Abus Treat. 2002;22:149–56.CrossRefGoogle Scholar
  67. 67.
    Schilder AJ, Lampinen TM, Miller ML, Hogg RS. Crystal methamphetamine and ecstasy differ in relation to unsafe sex among young gay men. Canadian journal of public health. 2005;96:340–3.PubMedGoogle Scholar
  68. 68.
    Lyons T, Chandra G, Goldstein J, Ostrow DG. Breaking the bond between stimulant use and risky sex: a qualitative study. Subst Abus. 2010;31:224–30.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Sánchez J, Comerford M, Chitwood DD, Fernandez MI, McCoy CB. High risk sexual behaviours among heroin sniffers who have no history of injection drug use: implications for HIV risk reduction. AIDS Care: Psychological and Socio-medical Aspects of AIDS/HIV. 2002;14:391–8.CrossRefGoogle Scholar
  70. 70.
    Fisher DG, Reynolds GL, Ware MR, Napper LE. Methamphetamine and Viagra use: relationship to sexual risk behaviors. Arch Sex Behav. 2009;Google Scholar
  71. 71.
    Raj A, Saitz R, Cheng DM, Winter M, Samet JH. Associations between alcohol, heroin, and cocaine use and high risk sexual behaviors among detoxification patients. The American Journal of Drug and Alcohol Abuse. 2007;33:169–78.CrossRefPubMedGoogle Scholar
  72. 72.
    Crowe LC, George WH. Alcohol and human sexuality: review and integration. Psychol Bull. 1989;105:374–86.CrossRefPubMedGoogle Scholar
  73. 73.
    Herrmann ES, Hand DJ, Johnson MW, Badger GJ, Heil SH. Examining delay discounting of condom-protected sex among opioid-dependent women and non-drug-using control women. Drug Alcohol Depend. 2014;144:53–60.CrossRefPubMedGoogle Scholar
  74. 74.
    •• Johnson MW, Herrmann ES, Sweeney MM, LeComte RS, Johnson PS. Cocaine administration dose-dependently increases sexual desire and decreases condom use likelihood: the role of delay and probability discounting in connecting cocaine with HIV. Psychopharmacology. 2017;234:599–612. This study demonstrates that accute cocaine intoxication directly increases sexual desire and impulsive choice (delay discounting) in hypothetical behavioral economics tasks. CrossRefPubMedGoogle Scholar
  75. 75.
    Johnson MW. An efficient operant choice procedure for assessing delay discounting in humans: initial validation in cocaine-dependent and control individuals. Exp Clin Psychopharmacol. 2012;20:191–204.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Johnson MW, Bruner NR. Test-retest reliability and gender differences in the sexual discounting task among cocaine-dependent individuals. Exp Clin Psychopharmacol. 2013;21:277–86.CrossRefPubMedGoogle Scholar
  77. 77.
    •• Koffarnus MN, Johnson MW, Thompson-Lake DGY, Wesley MJ, Lohrenz T, Montague PR, et al. Cocaine-dependent adults and recreational cocaine users are more likely than controls to choose immediate unsafe sex over delayed safer sex. Exp Clin Psychopharmacol. 2016;24:297–304. This study confirms that in addition to individuals with cocaine use disorders (see Johnson et al. 2015 PLoS One ), recreational cocaine users also demonstrate impulsive, risky sexual decision making compared to controls in a hypothetical delay-discounting task. CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Monga TN, Monga M, Raina MS, Hardjasudarma M. Hypersexuality in stroke. Arch Phys Med Rehabil. 1986;67:415–7.PubMedGoogle Scholar
  79. 79.
    De Giorgi R, Series H. Treatment of inappropriate sexual behavior in dementia. Curr Treat Options Neurol. 2016;18(41):41.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Eghwrudjakpor P, Essien A. Hypersexual behavior following craniocerebral trauma an experience with five cases. Libyan J Med. 2008;3:192–4.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Miller BL, Cummings JL, McIntyre H, Ebers G, Grode M. Hypersexuality or altered sexual preference following brain injury. J Neurol Neurosurg Psychiatry. 1986;49:867–73.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Kile SJ, Ellis WG, Olichney JM, Farias S, DeCarli C. Alzheimer abnormalities of the amygdala with Kluver-Bucy syndrome symptoms: an amygdaloid variant of Alzheimer disease. Arch Neurol. 2009;66:125–9.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Strahler J, Kruse O, Wehrum-Osinsky S, Klucken T, Stark R. Neural correlates of gender differences in distractibility by sexual stimuli. Neuroimage. 2018;176:499–509.CrossRefPubMedGoogle Scholar
  84. 84.
    •• J. W. Seok, J. H. Sohn, Neural Substrates of Sexual Desire in Individuals with Problematic Hypersexual Behavior. Front Behav Neurosci 9, 321 (2015). This study measures fMRI activity correlating with viewing sexual stimuli, and observed greater activation in the caudate nucleus, inferior parietal lobe, dorsal anterior cingulate gyrus, thalamus, and dorsolateral prefrontal cortex, i.e. areas that are also activated in drug-users when exposed to drug cues. Google Scholar
  85. 85.
    Voon V, Mole TB, Banca P, Porter L, Morris L, Mitchell S, et al. Neural correlates of sexual cue reactivity in individuals with and without compulsive sexual behaviours. PLoS One. 2014;9:e102419.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    •• Schmidt C, Morris LS, Kvamme TL, Hall P, Birchard T, Voon V. Compulsive sexual behavior: prefrontal and limbic volume and interactions. Hum Brain Mapp. 2017;38:1182–90. This study is a first step in identifying functional brain connectivity in compulsive sexual behavior subjects at resting state, and demonstrates a decrease in resting state functional connectivity between prefrontal cortex and amygdala which correlated with greater left amygdala gray matter volume. CrossRefPubMedGoogle Scholar
  87. 87.
    Kuhn S, Gallinat J. Common biology of craving across legal and illegal drugs - a quantitative meta-analysis of cue-reactivity brain response. Eur J Neurosci. 2011;33:1318–26.CrossRefPubMedGoogle Scholar
  88. 88.
    Chang L, Alicata D, Ernst T, Volkow N. Structural and metabolic brain changes in the striatum associated with methamphetamine abuse. Addiction. 2007;102(Suppl 1):16–32.CrossRefPubMedGoogle Scholar
  89. 89.
    Goldstein RZ, Volkow ND. Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci. 2011;12:652–69.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Childress AR, Ehrman RN, Wang Z, Li Y, Sciortino N, Hakun J, et al. Prelude to passion: limbic activation by "unseen" drug and sexual cues. PLoS One. 2008;3:e1506.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Moeller SJ, Zilverstand A, Konova AB, Kundu P, Parvaz MA, Preston-Campbell R, et al. Neural correlates of drug-biased choice in currently using and abstinent individuals with cocaine use disorder. Biol Psychiatry Cogn Neurosci Neuroimaging. 2018;3:485–94.CrossRefPubMedGoogle Scholar
  92. 92.
    Kuhn S, Gallinat J. A quantitative meta-analysis on cue-induced male sexual arousal. J Sex Med. 2011;8:2269–75.CrossRefPubMedGoogle Scholar
  93. 93.
    Stoleru S, Fonteille V, Cornelis C, Joyal C, Moulier V. Functional neuroimaging studies of sexual arousal and orgasm in healthy men and women: a review and meta-analysis. Neurosci Biobehav Rev. 2012;36:1481–509.CrossRefPubMedGoogle Scholar
  94. 94.
    Clark VP, Beatty GK, Anderson RE, Kodituwakku P, Phillips JP, Lane TDR, et al. Reduced fMRI activity predicts relapse in patients recovering from stimulant dependence. Hum Brain Mapp. 2014;35:414–28.CrossRefPubMedGoogle Scholar
  95. 95.
    Paulus MP, Tapert SF, Schuckit MA. Neural activation patterns of methamphetamine-dependent subjects during decision making predict relapse. Arch Gen Psychiatry. 2005;62:761–8.CrossRefPubMedGoogle Scholar
  96. 96.
    Chu XA. A., Sociosexual interactions in rats: are they relevant for understanding human sexual behavior? International Journal of Psychological Research. 2016;9:76–95.CrossRefGoogle Scholar
  97. 97.
    Le Moene O, Agmo A. The neuroendocrinology of sexual attraction. Front Neuroendocrinol. 2017;Google Scholar
  98. 98.
    Veening JG, Coolen LM, Gerrits PO. Neural mechanisms of female sexual behavior in the rat; comparison with male ejaculatory control. Pharmacol Biochem Behav. 2014;121:16–30.CrossRefPubMedGoogle Scholar
  99. 99.
    Veening JG, Coolen LM. Neural mechanisms of sexual behavior in the male rat: emphasis on ejaculation-related circuits. Pharmacol Biochem Behav. 2014;121:170–83.CrossRefPubMedGoogle Scholar
  100. 100.
    Persinger MA. Maintained hypersexuality between male rats following chronically induced limbic seizures: implications for bisexuality in complex partial epileptic seizures. Psychol Rep. 1994;74:647–52.CrossRefPubMedGoogle Scholar
  101. 101.
    •• Davis JF, Loos M, di Sebastiano AR, Brown JL, Lehman MN, Coolen LM. Lesions of the medial prefrontal cortex cause maladaptive sexual behavior in male rats. Biol Psychiatry. 2010;67:1199–204. This study is the first description of conditioned sex aversion as a model for compulsive sexual behavior, in male rats, and demonstrates a critical role of the medial prefrontal cortex. CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Peters RH. Learned aversions to copulatory behaviors in male rats. Behav Neurosci. 1983;97:140–5.CrossRefPubMedGoogle Scholar
  103. 103.
    Agmo A. Copulation-contingent aversive conditioning and sexual incentive motivation in male rats: evidence for a two-stage process of sexual behavior. Physiol Behav. 2002;77:425–35.CrossRefPubMedGoogle Scholar
  104. 104.
    Kwok DWS, Boakes RA. Situational relevance: context as a factor in serial overshadowing of taste aversion learning. Q J Exp Psychol (Hove). 2017:1–35.Google Scholar
  105. 105.
    Barker JM, Zhang H, Villafane JJ, Wang TL, Torregrossa MM, Taylor JR. Epigenetic and pharmacological regulation of 5HT3 receptors controls compulsive ethanol seeking in mice. Eur J Neurosci. 2014;39:999–1008.CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Frohmader KS, Bateman KL, Lehman MN, Coolen LM. Effects of methamphetamine on sexual performance and compulsive sex behavior in male rats. Psychopharmacology. 2010;212:93–104.CrossRefPubMedGoogle Scholar
  107. 107.
    •• Frohmader KS, Lehman MN, Laviolette SR, Coolen LM. Concurrent exposure to methamphetamine and sexual behavior enhances subsequent drug reward and causes compulsive sexual behavior in male rats. J Neurosci. 2011;31:16473–82. This study demonstrates the experience with methamphetamine concurrently with sexual behavior results in compulsive sexual behavior in male rats. CrossRefPubMedGoogle Scholar
  108. 108.
    •• Kuiper LB, Frohmader KS, Coolen LM. Maladaptive sexual behavior following concurrent methamphetamine and sexual experience in male rats is associated with altered neural activity in frontal cortex. Neuropsychopharmacology. 2017). This study is a first preclinical study showing the neural correlates of conditioned sex aversion, and compulsive sexual behavior, in male rats.;42:2011–20.CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Neurobiology and Anatomical SciencesThe University of Mississippi Medical CenterJacksonUSA
  2. 2.Department of Physiology and BiophysicsThe University of Mississippi Medical CenterJacksonUSA

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