Sex for fun: A synthesis of human and animal neurobiology

Nature Reviews Urology

Volumn 9, Issue 9, 2012, Pages 486-498

  Georgiadis, Janniko R ^a   Kringelbach, Morten L ^b   Pfaus, James G ^c  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c Concordia University ^*  (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE;

BRAIN FUNCTION; CLITORIS; EJACULATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INHIBITION KINETICS; LIBIDO; NEUROBIOLOGY; NEUROIMAGING; NONHUMAN; ORGASM; PENIS; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RECREATION; REVIEW; REWARD; SENSORY STIMULATION; SEXUAL AROUSAL; SEXUAL BEHAVIOR; SEXUAL FUNCTION; VAGINA;

HUMANS; MALE; NERVOUS SYSTEM PHYSIOLOGICAL PHENOMENA; PLEASURE; SEXUALITY;

EID: 84865961891     PISSN: 17594812     EISSN: 17594820     Source Type: Journal    
DOI: 10.1038/nrurol.2012.151     Document Type: Review

References (131)

1. Bancroft, J., Loftus, J. & Long, J.S. Distress about sex: a national survey of women in heterosexual relationships. Arch. Sex. Behav. 32, 193-208 (2003). (Pubitemid 38090835)
2. Waldinger, M.D. & Schweitzer, D.H. Changing paradigms from a historical DSM-III and DSM-IV view toward an evidence-based definition of premature ejaculation. Part II-proposals for DSM-V and ICD-11. J. Sex. Med. 3, 693-705 (2006).
3. Mark, K.P. & Murray, S.H. Gender differences in desire discrepancy as a predictor of sexual and relationship satisfaction in a college sample of heterosexual romantic relationships. J. Sex. Marital Ther. 38, 198-215 (2012).
4. Mark, K.P., Janssen, E. & Milhausen, R.R. Infidelity in heterosexual couples: demographic, interpersonal, and personality-related predictors of extradyadic sex. Arch. Sex. Behav. 40, 971-982 (2011).
5. Montesi, J.L. et al. On the relationship among social anxiety, intimacy, sexual communication, and sexual satisfaction in young couples. Arch. Sex. Behav. doi:10.1007/s10508-012-9929-3.
6. Georgiadis, J.R. & Kringelbach, M.L. The human sexual response cycle: neuroimaging evidence linking sex to other pleasures. Prog. Neurobiol. 98, 49-81 (2012).
7. Pfaus, J.G. et al. Who, what, where, when (and maybe even why)? How the experience of sexual reward connects sexual desire, preference, and performance. Arch. Sex. Behav. 41, 31-62 (2012).
8. Pfaus, J.G. Pathways of sexual desire. J. Sex. Med. 6, 1506-1533 (2009).
9. 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. 57, 112-118 (2010).
10. Masters, W.H. & Johnson, V.E. Human Sexual Response (Little, Brown and Company, Boston, 1966).
11. Kringelbach, M.L. & Berridge, K.C. Towards a functional neuroanatomy of pleasure and happiness. Trends Cogn. Sci. 13, 479-487 (2009).
12. Kringelbach, M.L. The human orbitofrontal cortex: linking reward to hedonic experience. Nat. Rev. Neurosci. 6, 691-702 (2005). (Pubitemid 43160318)
13. Giuliano, F. & Rampin, O. Central neural regulation of penile erection. Neurosci. Biobehav. Rev. 24, 517-533 (2000). (Pubitemid 30398513)
14. Truitt, W.A. & Coolen, L.M. Identification of a potential ejaculation generator in the spinal cord. Science 297, 1566-1569 (2002). (Pubitemid 34971006)
15. Everaert, K. et al. Neuroanatomy and neurophysiology related to sexual dysfunction in male neurogenic patients with lesions to the spinal cord or peripheral nerves. Spinal Cord 48, 182-191 (2010).
16. Agmo, A. Functional and Dysfunctional Sexual Behaviour: a Synthesis of Neuroscience and Comparative Psychology (Academic Press, London, 2007).
17. von Krafft-Ebing, R. Psychopathia Sexualis (Physicians and Surgeons Book Co., New York, 1929).
18. Pfaff, D.W. Drive: Neurobiological and molecular mechanisms of sexual motivation (MIT Press, Cambridge, 1999).
19. Georgescu, M., Sabongui, C., Del Corpo, A., Marsan, L. & Pfaus, J.G. Vaginocervical stimulation induces Fos in glutamate neurons in the ventromedial hypothalamus: attenuation by estrogen and progesterone. Horm. Behav. 56, 450-456 (2009).
20. Whalen, R.E. Sexual motivation. Psychol. Rev. 73, 151-163 (1966).
21. Wallen, K. in Sexual nature sexual culture (eds Abramson, P.R. & Pinkerton, S.D.) 57-79 (University of Chicago Press, Chicago, 1995).
22. Jiang, Y., Costello, P., Fang, F., Huang, M. & He, S. A gender- and sexual orientation-dependent spatial attentional effect of invisible images. Proc. Natl Acad. Sci. USA 103, 17048-17052 (2006). (Pubitemid 44737375)
23. Childress, A.R. et al. Prelude to passion: limbic activation by "unseen" drug and sexual cues. PLoS ONE 3, e1506 (2008).
24. Oei, N.Y., Rombouts, S.A., Soeter, R.P., van Gerven, J.M. & Both, S. Dopamine modulates reward system activity during subconscious processing of sexual stimuli. Neuropsychopharmacology 37, 1729-1737 (2012).
25. Yacubian, J. et al. Gene-gene interaction associated with neural reward sensitivity. Proc. Natl Acad. Sci. USA 104, 8125-8130 (2007). (Pubitemid 47185886)
26. Guo, G., Tong, Y., Xie, C.W. & Lange, L.A. Dopamine transporter, gender, and number of sexual partners among young adults. Eur. J. Hum. Genet. 15, 279-287 (2007).
27. Guo, G. & Tong, Y.Y. Age at first sexual intercourse, genes, and social context: evidence from twins and the dopamine D4 receptor gene. Demography 43, 747-769 (2006). (Pubitemid 44914502)
28. Hagemann, J.H. et al. Effects of visual sexual stimuli and apomorphine SL on cerebral activity in men with erectile dysfunction. Eur. Urol. 43, 412-420 (2003). (Pubitemid 36427461)
29. Montorsi, F. et al. Apomorphine-induced brain modulation during sexual stimulation: a new look at central phenomena related to erectile dysfunction. Int. J. Impot. Res. 15, 203-209 (2003). (Pubitemid 36928913)
30. Archer, J.S., Love-Geffen, T.E., Herbst-Damm, K.L., Swinney, D.A. & Chang, J.R. Effect of estradiol versus estradiol and testosterone on brain-activation patterns in postmenopausal women. Menopause 13, 528-537 (2006).
31. Gizewski, E.R. et al. There are differences in cerebral activation between females in distinct menstrual phases during viewing of erotic stimuli: a fMRI study. Exp. Brain Res. 174, 101-108 (2006). (Pubitemid 44337551)
32. Redouté, J. et al. Brain processing of visual sexual stimuli in treated and untreated hypogonadal patients. Psychoneuroendocrinology 30, 461-482 (2005). (Pubitemid 40249812)
33. Ossewaarde, L. et al. Changes in functioning of mesolimbic incentive processing circuits during the premenstrual phase. Soc. Cogn. Affect. Neurosci. 6, 612-620 (2010).
34. Hermans, E.J. et al. Effects of exogenous testosterone on the ventral striatal BOLD response during reward anticipation in healthy women. Neuroimage 52, 277-283 (2010).
35. Roozendaal, B., McEwen, B.S. & Chattarji, S. Stress, memory and the amygdala. Nat. Rev. Neurosci. 10, 423-433 (2009).
36. Hamann, S.B., Ely, T.D., Grafton, S.T. & Kilts, C.D. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nat. Neurosci. 2, 289-293 (1999). (Pubitemid 30491302)
37. Both, S. et al. Unconscious classical conditioning of sexual arousal: evidence for the conditioning of female genital arousal to subliminally presented sexual stimuli. J. Sex. Med. 5, 100-109 (2008).
38. Both, S. et al. Appetitive and aversive classical conditioning of female sexual response. J. Sex. Med. 5, 1386-1401 (2008). (Pubitemid 351803104)
39. Both, S., Brauer, M. & Laan, E. Classical conditioning of sexual response in women: a replication study. J. Sex. Med. 8, 3116-3131 (2011).
40. Klucken, T. et al. Neural activations of the acquisition of conditioned sexual arousal: effects of contingency awareness and sex. J. Sex. Med. 6, 3071-3085 (2009).
41. Sescousse, G., Redoute, J. & Dreher, J.C. The architecture of reward value coding in the human orbitofrontal cortex. J. Neurosci. 30, 13095-13104 (2010).
42. Pfaus, J.G. & Gorzalka, B.B. Opioids and sexual behavior. Neurosci. Biobehav. Rev. 11, 1-34 (1987). (Pubitemid 17042718)
43. Chessick, R.D. The "pharmacogenic orgasm" in the drug addict. Arch. Gen. Psychiatry 3, 545-556 (1960).
44. Whipple, B. & Komisaruk, B.R. Elevation of pain threshold by vaginal stimulation in women. Pain 21, 357-367 (1985). (Pubitemid 15093085)
45. Szechtman, H., Hershkowitz, M. & Simantov, R. Sexual behavior decreases pain sensitivity and stimulated endogenous opioids in male rats. Eur. J. Pharmacol. 70, 279-285 (1981). (Pubitemid 11149320)
46. Komisaruk, B.R. & Whipple, B. Non-genital orgasms. Sex. Relat. Ther. 26, 356-372 (2011).
47. Komisaruk, B.R., Beyer, C. & Whipple, B. The Science of Orgasm (JHU Press, Baltimore, 2006).
48. Carson, C. & Wyllie, M. Improved ejaculatory latency, control and sexual satisfaction when PSD502 is applied topically in men with premature ejaculation: results of a phase III, double-blind, placebo-controlled study. J. Sex. Med. 7, 3179-3189 (2010).
49. Kinsey A.C., Pomeroy W., Martin C., Gebhard P.H. Sexual behavior in the human female (W. B. Saunders Philadelphia 1953).
50. Williams-Ashman, H.G. Enigmatic features of penile development and functions. Perspect. Biol. Med. 33, 335-374 (1990). (Pubitemid 20163340)
51. Marson, L. Central nervous system neurons identified after injection of pseudorabies virus into the rat clitoris. Neurosci. Lett. 190, 41-44 (1995).
52. Marson, L. & McKenna, K.E. CNS cell groups involved in the control of the ischiocavernosus and bulbospongiosus muscles: a transneuronal tracing study using pseudorabies virus. J. Comp. Neurol. 374, 161-179 (1996). (Pubitemid 26357183)
53. Moszkowicz, D. et al. Neural supply to the clitoris: immunohistochemical study with three-dimensional reconstruction of cavernous nerve, spongious nerve, and dorsal clitoris nerve in human fetus. J. Sex. Med. 8, 1112-1122 (2011).
54. Andrews, A.H., Blowey, R.W., Boyd, H. & Eddy, R.G. Bovine Medicine (Blackwell Scientific Publications, Oxford, 1992).
55. Rowland, D.L. Penile sensitivity in men: a composite of recent findings. Urology 52, 1101-1105 (1998). (Pubitemid 28533385)
56. Johnson, R.D. & Halata, Z. Topography and ultrastructure of sensory nerve endings in the glans penis of the rat. J. Comp. Neurol. 312, 299-310 (1991).
57. Halata, Z. & Munger, B.L. The neuroanatomical basis for the protopathic sensibility of the human glans penis. Brain Res. 371, 205-230 (1986). (Pubitemid 16082898)
58. Vallbo, A., Olausson, H., Wessberg, J. & Norrsell, U. A system of unmyelinated afferents for innocuous mechanoreception in the human skin. Brain Res. 628, 301-304 (1993). (Pubitemid 23331622)
59. Bjornsdotter, M., Morrison, I. & Olausson, H. Feeling good: on the role of C fiber mediated touch in interoception. Exp. Brain Res. 207, 149-155 (2010).
60. Levin, R. & Meston, C. Nipple/breast stimulation and sexual arousal in young men and women. J. Sex. Med. 3, 450-454 (2006).
61. Hubscher, C.H., Reed, W.R., Kaddumi, E.G., Armstrong, J.E. & Johnson, R.D. Select spinal lesions reveal multiple ascending pathways in the rat conveying input from the male genitalia. J. Physiol. 588, 1073-1083 (2010).
62. Beric, A. & Light, J.K. Anorgasmia in anterior spinal cord syndrome. J. Neurol. Neurosurg. Psychiatry 56, 548-551 (1993). (Pubitemid 23171789)
63. 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. 96, 201-208 (2009).
64. Kippin, T.E. & Pfaus, J.G. The nature of the conditioned response mediating olfactory conditioned ejaculatory preference in the male rat. Behav. Brain Res. 122, 11-24 (2001). (Pubitemid 32238171)
65. Agmo, A. & Berenfeld, R. Reinforcing properties of ejaculation in the male rat: role of opioids and dopamine. Behav. Neurosci. 104, 177-182 (1990). (Pubitemid 20138274)
66. Rodriguez-Manzo, G. & Fernandez-Guasti, A. Opioid antagonists and the sexual satiation phenomenon. Psychopharmacology (Berl.) 122, 131-136 (1995). (Pubitemid 26019149)
67. Coria-Avila, G.A., Ouimet, A.J., Pacheco, P., Manzo, J. & Pfaus, J.G. Olfactory conditioned partner preference in the female rat. Behav. Neurosci. 119, 716-725 (2005). (Pubitemid 40934362)
68. Coria-Avila, G.A. et al. Neurochemical basis of conditioned partner preference in the female rat: I. Disruption by naloxone. Behav. Neurosci. 122, 385-395 (2008). (Pubitemid 351672329)
69. Paredes, R.G. & Vazquez, B. What do female rats like about sex? Paced mating. Behav. Brain Res. 105, 117-127 (1999). (Pubitemid 29447617)
70. Paredes, R.G. & Martinez, I. Naloxone blocks place preference conditioning after paced mating in female rats. Behav. Neurosci. 115, 1363-1367 (2001). (Pubitemid 33139144)
71. Kippin, T.E., Sotiropoulos, V., Badih, J. & Pfaus, J.G. Opposing roles of the nucleus accumbens and anterior lateral hypothalamic area in the control of sexual behaviour in the male rat. Eur. J. Neurosci. 19, 698-704 (2004). (Pubitemid 38241309)
72. Cibrian-Llanderal, T. et al. Clitoral stimulation modulates appetitive sexual behavior and facilitates reproduction in rats. Physiol. Behav. 100, 148-153 (2010).
73. Meerts, S.H. & Clark, A.S. Artificial vaginocervical stimulation induces a conditioned place preference in female rats. Horm. Behav. 55, 128-132 (2009).
74. 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. 59, 520-527 (2011).
75. Ismail, N., Zhao, Y. & Pfaus, J.G. Context-dependent acquisition of copulatory behavior in the male rat: role of female availability. Behav. Neurosci. 122, 991-997 (2008).
76. Tenk, C.M., Wilson, H., Zhang, Q., Pitchers, K.K. & Coolen, L.M. Sexual reward in male rats: effects of sexual experience on conditioned place preferences associated with ejaculation and intromissions. Horm. Behav. 55, 93-97 (2009).
77. 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. 44, 397-407 (1997). (Pubitemid 27467285)
78. Georgiadis, J.R. et al. Dynamic subcortical blood flow during male sexual activity with ecological validity: a perfusion fMRI study. Neuroimage 50, 208-216 (2010).
79. Redouté, J. et al. Brain processing of visual sexual stimuli in human males. Hum. Brain Mapp. 11, 162-177 (2000).
80. Arnow, B.A. et al. Women with hypoactive sexual desire disorder compared to normal females: a functional magnetic resonance imaging study. Neuroscience 158, 484-502 (2009).
81. Robinson, T.E. & Berridge, K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Brain Res. Rev. 18, 247-291 (1993). (Pubitemid 23219500)
82. Blackburn, J.R., Pfaus, J.G. & Phillips, A.G. Dopamine functions in appetitive and defensive behaviours. Prog. Neurobiol. 39, 247-279 (1992).
83. Matsumoto, J. et al. Neuronal responses in the nucleus accumbens shell during sexual behavior in male rats. J. Neurosci. 32, 1672-1686 (2012).
84. Georgiadis, J.R. Exposing orgasm in the brain: a critical eye. Sex. Rel. Ther. 26, 342-355 (2011).
85. Whipple, B. & Komisaruk, B.R. Brain (PET) responses to vaginal-cervical self-stimulation in women with complete spinal cord injury: preliminary findings. J. Sex Marital Ther. 28, 79-86 (2002). (Pubitemid 34008317)
86. Liu, W.C. et al. fMRI study of acupuncture-induced periaqueductal gray activity in humans. Neuroreport 15, 1937-1940 (2004).
87. Komisaruk, B.R. et al. Women's clitoris, vagina, and cervix mapped on the sensory cortex: fMRI evidence. J. Sex. Med. 8, 2822-2830 (2011).
88. Georgiadis, J.R. et al. Regional cerebral blood flow changes associated with clitorally induced orgasm in healthy women. Eur. J. Neurosci. 24, 3305-3316 (2006). (Pubitemid 44952662)
89. Georgiadis, J.R., Reinders, A.A., Paans, A.M., Renken, R. & Kortekaas, R. Men versus women on sexual brain function: prominent differences during tactile genital stimulation, but not during orgasm. Hum. Brain Mapp. 30, 3089-3101 (2009).
90. Kell, C.A., von Kriegstein, K., Rosler, A., Kleinschmidt, A. & Laufs, H. The sensory cortical representation of the human penis: revisiting somatotopy in the male homunculus. J. Neurosci. 25, 5984-5987 (2005). (Pubitemid 40911429)
91. Michels, L., Mehnert, U., Boy, S., Schurch, B. & Kollias, S. The somatosensory representation of the human clitoris: an fMRI study. Neuroimage 49, 177-184 (2010).
92. Mehnert, U. et al. Brain activation in response to bladder filling and simultaneous stimulation of the dorsal clitoral nerve-an fMRI study in healthy women. Neuroimage 41, 682-689 (2008).
93. Georgiadis, J.R. & Holstege, G. Human brain activation during sexual stimulation of the penis. J. Comp. Neurol. 493, 33-38 (2005). (Pubitemid 41636183)
94. Mäkelä, J.P. et al. Dorsal penile nerve stimulation elicits left-hemisphere dominant activation in the second somatosensory cortex. Hum. Brain Mapp. 18, 90-99 (2003). (Pubitemid 36150929)
95. Mouras, H. et al. Activation of mirror-neuron system by erotic video clips predicts degree of induced erection: an fMRI study. Neuroimage 42, 1142-1150 (2008).
96. Moulier, V. et al. Neuroanatomical correlates of penile erection evoked by photographic stimuli in human males. Neuroimage 33, 689-699 (2006). (Pubitemid 44508666)
97. Berridge, K.C. Food reward: brain substrates of wanting and liking. Neurosci. Biobehav. Rev. 20, 1-25 (1996). (Pubitemid 126682107)
98. Smith, K.S. & Berridge, K.C. The ventral pallidum and hedonic reward: neurochemical maps of sucrose "liking" and food intake. J. Neurosci. 25, 8637-8649 (2005). (Pubitemid 41362040)
99. Weil, Z.M., Zhang, Q., Hornung, A., Blizard, D. & Pfaff, D.W. Impact of generalized brain arousal on sexual behavior. Proc. Natl Acad. Sci. USA 107, 2265-2270 (2010).
100. Pfaff, D.W., Kieffer, B.L. & Swanson, L.W. Mechanisms for the regulation of state changes in the central nervous system: an introduction. Ann. NY Acad. Sci. 1129, 1-7 (2008). (Pubitemid 351990299)
101. Hamann, S., Herman, R.A., Nolan, C.L. & Wallen, K. Men and women differ in amygdala response to visual sexual stimuli. Nat. Neurosci. 7, 411-416 (2004). (Pubitemid 38429182)
102. Beauregard, M., Levesque, J. & Bourgouin, P. Neural correlates of conscious self-regulation of emotion. J. Neurosci. 21, RC165 (2001).
103. Davis, M. & Whalen, P.J. The amygdala: vigilance and emotion. Mol. Psychiatry 6, 13-34 (2001). (Pubitemid 32096061)
104. Rauch, S.L. et al. Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol. Psychiatry 47, 769-776 (2000). (Pubitemid 30254049)
105. Koukounas, E. & McCabe, M.P. Sexual and emotional variables influencing sexual response to erotica: a psychophysiological investigation. Arch. Sex. Behav. 30, 393-408 (2001). (Pubitemid 39592018)
106. Georgiadis, J.R., Reinders, A.A., van der Graaf, F.H., Paans, A.M. & Kortekaas, R. Brain activation during human male ejaculation revisited. Neuroreport 18, 553-557 (2007). (Pubitemid 46594914)
107. Forbes, C.E. & Grafman, J. The role of the human prefrontal cortex in social cognition and moral judgment. Annu. Rev. Neurosci. 33, 299-324 (2010).
108. van Netten, J.J., Georgiadis, J.R., Nieuwenburg, A. & Kortekaas, R. 8-13 Hz fluctuations in rectal pressure are an objective marker of clitorally-induced orgasm in women. Arch. Sex. Behav. 37, 279-285 (2008). (Pubitemid 351423074)
109. Bohlen, J.G., Held, J.P., Sanderson, M.O. & Ahlgren, A. The female orgasm: pelvic contractions. Arch. Sex. Behav. 11, 367-386 (1982). (Pubitemid 13215893)
110. Bohlen, J.G., Held, J.P. & Sanderson, M.O. The male orgasm: pelvic contractions measured by anal probe. Arch. Sex. Behav. 9, 503-521 (1980). (Pubitemid 11180004)
111. Bechara, A. Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat. Neurosci. 8, 1458-1463 (2005). (Pubitemid 41573656)
112. Bancroft, J. & Janssen, E. The dual control model of male sexual response: a theoretical approach to centrally mediated erectile dysfunction. Neurosci. Biobehav. Rev. 24, 571-579 (2000). (Pubitemid 30398517)
113. 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. 99, 151-161 (1985). (Pubitemid 15173442)
114. Rodriguez-Manzo, G. & Fernandez-Guasti, A. Participation of the central noradrenergic system in the reestablishment of copulatory behavior of sexually exhausted rats by yohimbine, naloxone, and 8-OH-DPAT. Brain Res. Bull. 38, 399-404 (1995).
115. Pfaus, J.G. & Wilkins, M.F. A novel environment disrupts copulation in sexually naive but not experienced male rats: reversal with naloxone. Physiol. Behav. 57, 1045-1049 (1995).
116. Fiorino, D.F. & Phillips, A.G. Facilitation of sexual behavior in male rats following d-amphetamine-induced behavioral sensitization. Psychopharmacology (Berl.) 142, 200-208 (1999). (Pubitemid 29190856)
117. Pfaus, J.G. & Pinel, J.P. Alcohol inhibits and disinhibits sexual behavior in the male rat. Psychobiology 17, 195-201 (1989). (Pubitemid 19145026)
118. Pfaus, J.G. et al. Inhibitory and disinhibitory effects of psychomotor stimulants and depressants on the sexual behavior of male and female rats. Horm. Behav. 58, 163-176 (2010).
119. Germé, K. et al. Differential pattern of brain activation by an olfactory cue associated with sexual excitation or inhibition in the male rat. Presented at Neuroscience 2011.
120. Garcia-Horsman, S.P., Agmo, A. & Paredes, R.G. Infusions of naloxone into the medial preoptic area, ventromedial nucleus of the hypothalamus, and amygdala block conditioned place preference induced by paced mating behavior. Horm. Behav. 54, 709-716 (2008).
121. Cera, N. et al. The role of left superior parietal lobe in male sexual behavior: dynamics of distinct components revealed by fMRI. J. Sex. Med. 9, 1602-1612 (2012).
122. Bianchi-Demicheli, F. et al. Neural bases of hypoactive sexual desire disorder in women: an event-related FMRI study. J. Sex. Med. 8, 2546-2559 (2011).
123. Fisk, G.D. & Wyss, J.M. Descending projections of infralimbic cortex that mediate stimulation-evoked changes in arterial pressure. Brain Res. 859, 83-95 (2000). (Pubitemid 30138195)
124. LeDoux, J. Rethinking the emotional brain. Neuron 73, 653-676 (2012).
125. Georgiadis, J.R. Doing it... wild? On the role of the cerebral cortex in human sexual activity. Sociaffective Neuroscience & Psychology 2, 17337 (2012).
126. Mostafa, T., Khouly, G.E. & Hassan, A. Pheromones in sex and reproduction: do they have a role in humans? J. Adv. Res. 3, 1-9 (2012).
127. Mast, T.G. & Samuelsen, C.L. Human pheromone detection by the vomeronasal organ: unnecessary for mate selection? Chem. Senses 34, 529-531 (2009).
128. Wallen, K. Sex and context: hormones and primate sexual motivation. Horm. Behav. 40, 339-357 (2001). (Pubitemid 32846365)
129. Johnson, K.L. & Tassinary, L.G. Compatibility of basic social perceptions determines perceived attractiveness. Proc. Natl Acad. Sci. USA 104, 5246-5251 (2007). (Pubitemid 47186207)
130. Berridge, K.C. & Robinson, T.E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Brain Res. Rev. 28, 309-369 (1998). (Pubitemid 29012677)
131. Raichle, M.E. & Mintun, M.A. Brain work and brain imaging. Ann. Rev. Neurosci. 29, 449-476 (2006). (Pubitemid 44476853)