The neurophysiology of sexual arousal

Best Practice and Research: Clinical Endocrinology and Metabolism

Volumn 21, Issue 3, 2007, Pages 445-461

  Schober, Justine M ^a,b   Pfaff, Donald ^b  

^a HAMOT MEDICAL CENTER   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

estrogen; hormones; nervous system neurotransmitters; sensory; sexual arousal; spinal cord

Indexed keywords

ACETYLCHOLINE; ANDROGEN; ANDROGEN RECEPTOR; CELL NUCLEUS RECEPTOR; DOPAMINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GESTAGEN; GONADORELIN; HISTAMINE; NITRIC OXIDE SYNTHASE; NORADRENALIN; PHOSPHODIESTERASE V; PHOSPHODIESTERASE V INHIBITOR; PROGESTERONE RECEPTOR; SEROTONIN; SEROTONIN RECEPTOR; SEX HORMONE;

BRAIN DEVELOPMENT; CENTRAL NERVOUS SYSTEM FUNCTION; COGNITION; CULTURAL FACTOR; ERECTILE DYSFUNCTION; GENOMICS; HEREDITY; HORMONE SYNTHESIS; HUMAN; HYPOGONADISM; HYPOTHALAMUS; NERVE ENDING; NEUROPHYSIOLOGY; NONHUMAN; PENIS ERECTION; PERIPHERAL NERVE; PROTEIN EXPRESSION; REVIEW; SEXUAL AROUSAL; SEXUAL BEHAVIOR; SOCIAL ASPECT; SOMATOSENSORY CORTEX; SPINAL CORD;

ANIMALS; AROUSAL; BRAIN; FEMALE; GENE EXPRESSION REGULATION; GENETICS, BEHAVIORAL; GENITALIA; GONADAL STEROID HORMONES; HUMANS; MALE; NEURAL PATHWAYS; NEUROTRANSMITTER AGENTS; PHYSICAL STIMULATION; RECEPTORS, SENSORY; SENSATION; SEX DIFFERENTIATION DISORDERS; SEXUAL BEHAVIOR; SEXUAL BEHAVIOR, ANIMAL; SEXUAL DYSFUNCTION, PHYSIOLOGICAL; SEXUAL DYSFUNCTIONS, PSYCHOLOGICAL; SIGNAL TRANSDUCTION;

EID: 34548566940     PISSN: 1521690X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.beem.2007.04.006     Document Type: Review

References (79)

1. Pfaff D.W. Brain Arousal and Information Theory: Neural and Genetic Mechanisms (2006), Harvard University Press, Cambridge, Mass
2. Giuliano F., Rampin O., and Allard J. Neurophysiology and pharmacology of female genital sexual response. Journal of Sex & Marital Therapy 28 supplement 1 (2002) 101-121
3. Schultz W.W., van Andel P., Sabelis I., et al. Magnetic resonance imaging of male and female genitals during coitus and female sexual arousal. BMJ (Clinical Research Ed.) 319 (1999) 1596-1600
4. Yucel S., De Souza Jr. A., and Baskin L.S. Neuroanatomy of the human female lower urogenital tract. The Journal of Urology 172 1 (2004) 191-195
5. O'Connell H.E., and DeLancey J.O. Clitoral anatomy in nulliparous, healthy, premenopausal volunteers using unenhanced magnetic resonance imaging. The Journal of Urology 173 (2005) 2060-2063
6. Hoang N.M., Smadja A., and Herve de Sigalony J.P. The reality and usefulness of Halban's fascia [French]. Journal de Gynécologie, Obstétrique et Biologie de la Reproduction 20 (1991) 51-59
7. Martin-Alguacil N., Schober J., Kow L.M., et al. Arousing properties of the vulvar epithelium. The Journal of Urology 176 (2006) 456-462
8. Kow L.M., and Pfaff D.W. Effects of estrogen treatment on the size of receptive field and response threshold of pudendal nerve in the female rat. Neuroendocrinology 13 (1973-1974) 299-313
9. Kow L.M., Malsbury C., and Pfaff D.W. Effects of progesterone on female reproductive behavior in rats: Possible modes of action and role in behavioral sex differences. In: Montagna W., and Sadler W. (Eds). Reproductive Behavior (1974), Plenum, New York 179-210
10. Komisaruk B.R., Adler N.T., and Hutchison J. Genital sensory field: enlargement by estrogen treatment in female rats. Science 178 (1972) 1295-1298
11. Pfaff D.W. Estrogens and Brain Function: Neural Analysis of a Hormone-Controlled Mammalian Reproductive Behavior (1980), Springer-Verlag, New York
12. Winkelmann R.K. The erogenous zones: their nerve supply and significance. Mayo Clinic Proceedings 34 (1959) 39-47
13. Halata Z., and Munger B.L. The neuroanatomical basis for the protopathic sensibility of the human glans penis. Brain Research 371 (1986) 205-230
14. Malinovsky L., Sommerova J., and Martincik J. Quantitative evaluation of sensory nerve endings in hypertrophy of labia minora pudendi in women. Acta Anatomica 92 (1975) 129-144
15. Pfaff D.W. Drive: Neurobiological and Molecular Mechanisms of Sexual Motivation (1999), The M.I.T. Press, Cambridge
16. Bonica J.J. Principles and Practices of Obstetric Analgesia and Anesthesia (1967), F.A. Davis, Philadelphia
17. Berkley K.J., Hotta H., Robbins A., et al. Functional properties of afferent fibers supplying reproductive and other pelvic organs in pelvic nerve of female rat. Journal of Neurophysiology 63 (1990) 256-272
18. Koeman M., van Driel M.F., Schultz W.C., et al. Orgasm after radical prostatectomy. British Journal of Urology 77 (1996) 861-864
19. Hoyt R.F. Innervation of the vagina and vulva: neurophysiology of female genital response. In: Goldstein I., Meston C.M., Davis S.R., and Traish A. (Eds). Women's Sexual Function and Dysfunction: Study, Diagnosis and Treatment (2006), Taylor & Francis, London
20. Giuliano F., and Julia-Guilloteau V. Neurophysiology of female genital response. In: Goldstein I., Meston C.M., Davis S.R., and Traish A. (Eds). Women's Sexual Function and Dysfunction: Study, Diagnosis and Treatment (2006), Taylor & Francis, London
21. Komisaruk B.R., and Whipple B. Complete spinal cord injury does not block perceptual responses to vaginal or cervical self-stimulation in women. Society for Neuroscience Abstracts 20 (1994) 961
22. Berkley K.J., Hubscher C.H., and Wall P.D. Neuronal responses to stimulation of the cervix, uterus, colon, and skin in the rat spinal cord. Journal of Neurophysiology 69 (1993) 545-556
23. Kawatani M., Takeshige C., and de Groat W.C. Central distribution of afferent pathways from the uterus of the cat. The Journal of Comparative Neurology 302 (1990) 294-304
24. Komisaruk B.R., Whipple B., Crawford A., et al. Brain activation during vaginocervical self-stimulation and orgasm in women with complete spinal cord injury: fMRI evidence of mediation by the vagus nerves. Brain Research 1024 (2004) 77-88
25. Wall P.D., and Lidierth M. Five sources of a dorsal root potential: their interactions and origins in the superficial dorsal horn. Journal of Neurophysiology 78 (1997) 860-871
26. Wall P.D., Kerr B.J., and Ramer M.S. Primary afferent input to and receptive field properties of cells in rat lumbar area X. The Journal of Comparative Neurology 449 (2002) 298-306
27. Komisaruk B.R., Gerdes C.A., and Whipple B. 'Complete' spinal cord injury does not block perceptual responses to genital self-stimulation in women. Archives of Neurology 54 (1997) 1513-1520
28. Komisaruk B.R., and Larsson K. Suppression of a spinal and a cranial nerve reflex by vaginal or rectal probing in rats. Brain Research 35 (1971) 231-235
29. Komisaruk B.R., and Sansone G. Neural pathways mediating vaginal function: the vagus nerves and spinal cord oxytocin. Scandinavian Journal of Psychology 44 (2003) 241-250
30. Hubscher CH, Johnson RD. Inputs from spinal and vagal sources converge of individual medullary reticular formation neurons. 2002 Society For Neuroscience Abstract Viewer/Itinerary Planner, 2002. 271.2.
31. McKenna K.E. Neural circuitry involved in sexual function. The Journal of Spinal Cord Medicine 24 (2001) 148-154
32. Marson L., and McKenna K.E. The identification of a brainstem site controlling spinal sexual reflexes in male rats. Brain Research 515 (1990) 303-308
33. McMahon S.B., and Wall P.D. Descending excitation and inhibition of spinal cord lamina I projection neurons. Journal of Neurophysiology 59 (1988) 1204-1219
34. Shimura T., Yamamoto T., and Shimokochi M. The medial preoptic area is involved in both sexual arousal and performance in male rats: re-evaluation of neuron activity in freely moving animals. Brain Research 640 (1994) 215-222
35. Hamann S., Herman R.A., Nolan C.L., et al. Men and women differ in amygdala response to visual sexual stimuli. Nature Neuroscience 7 (2004) 411-416
36. Holstege G., Georgiadis J.R., Paans A.M., et al. Brain activation during human male ejaculation. The Journal of Neuroscience 23 (2003) 9185-9193
37. Komisaruk B.R., and Whipple B. Functional MRI of the brain during orgasm in women. Annual Review of Sex Research 16 (2005) 62-86
38. Erlandson B.E., Fall M., and Carlsson C.A. The effect of intravaginal electrical stimulation on the feline urethra and urinary bladder. Electrical parameters. Scandinavian Journal of Urology and Nephrology. Supplementum 44 (1977) 5-18
39. Lindstrom S., Fall M., Carlsson C.A., et al. The neurophysiological basis of bladder inhibition in response to intravaginal electrical stimulation. The Journal of Urology 129 (1983) 405-410
40. Conrad L.C., and Pfaff D.W. Efferents from medial basal forebrain and hypothalamus in the rat. I. An autoradiographic study of the medial preoptic area. The Journal of Comparative Neurology 169 (1976) 185-219
41. Krieger M.S., Conrad L.C., and Pfaff D.W. An autoradiographic study of the efferent connections of the ventromedial nucleus of the hypothalamus. The Journal of Comparative Neurology 183 (1979) 785-815
42. Cottingham S.L., Femano P.A., and Pfaff D.W. Vestibulospinal and reticulospinal interactions in the activation of back muscle EMG in the rat. Experimental Brain Research 73 (1988) 198-208
43. Cottingham S.L., Femano P.A., and Pfaff D.W. Electrical stimulation of the midbrain central gray facilitates reticulospinal activation of axial muscle EMG. Experimental Neurology 97 (1987) 704-724
44. Cottingham S.L., and Pfaff D.W. Electrical stimulation of the midbrain central gray facilitates lateral vestibulospinal activation of back muscle EMG in the rat. Brain Research 421 (1987) 397-400
45. Kapp B., and Cain M. The neural basis of arousal. In: Smelser N., and Baltes P. (Eds). The International Encyclopedia of Social and Behavioral Sciences (2001), Elsevier Science Ltd, Oxford 1463-1466
46. Mallick H.N., and Kumar V.M. Gating of the dorsal penile nerve inputs by norepinephrine at the medial preoptic area in rats. Indian Journal of Physiology and Pharmacology 49 (2005) 325-330
47. Giuliano F., and Allard J. Dopamine and male sexual function. European Urology 40 (2001) 601-608
48. Hull E.M., Du J., Lorrain D.S., et al. Testosterone, preoptic dopamine, and copulation in male rats. Brain Research Bulletin 44 (1997) 327-333
49. Hull E.M., Muschamp J.W., and Sato S. Dopamine and serotonin: influences on male sexual behavior. Physiology & Behavior 83 (2004) 291-307
50. Frye C.A., and DeBold J.F. 3 alpha-OH-DHP and 5 alpha-THDOC implants to the ventral tegmental area facilitate sexual receptivity in hamsters after progesterone priming to the ventral medial hypothalamus. Brain Research 612 (1993) 130-137
51. Frye C.A., and Leadbetter E.A. 5α-reduced progesterone metabolites are essential in hamster VTA for sexual receptivity. Life Sciences 54 (1994) 653-659
52. Becker J.B., Rudick C.N., and Jenkins W.J. The role of dopamine in the nucleus accumbens and striatum during sexual behavior in the female rat. The Journal of Neuroscience 21 (2001) 3236-3241
53. Alves S.E., McEwen B.S., Hayashi S., et al. Estrogen-regulated progestin receptors are found in the midbrain raphe but not hippocampus of estrogen receptor alpha (ER alpha) gene-disrupted mice. The Journal of Comparative Neurology 427 (2000) 185-195
54. Uphouse L., Colon L., Cox A., et al. Effects of mianserin and ketanserin on lordosis behavior after systemic treatment or infusion into the ventromedial nucleus of the hypothalamus. Brain Research 718 (1996) 46-52
55. Maswood N., Caldarola-Pastuszka M., and Uphouse L. 5-HT3 receptors in the ventromedial nucleus of the hypothalamus and female sexual behavior. Brain Research 769 (1997) 13-20
56. Trevino A., Wolf A., Jackson A., et al. Reduced efficacy of 8-OH-DPAT's inhibition of lordosis behavior by prior estrogen treatment. Hormones and Behavior 35 (1999) 215-223
57. Gangestad S.W., Thornhill R., and Garver-Apgar C.E. Women's sexual interests across the ovulatory cycle depend on primary partner developmental instability. Proceedings. Biological Sciences 272 (2005) 2023-2027
58. Pfaff D., Montgomery M., and Lewis C. Somatosensory determinants of lordosis in female rats: behavioral definition of the estrogen effect. Journal of Comparative and Physiological Psychology 91 (1977) 134-145
59. Kow L.M., Montgomery M.O., and Pfaff D.W. Triggering of lordosis reflex in female rats with somatosensory stimulation: quantitative determination of stimulus parameters. Journal of Neurophysiology 42 (1979) 195-202
60. Kane D.D., Kerns J.M., Lin D.L., et al. Early structural effects of oestrogen on pudendal nerve regeneration in the rat. BJU International 93 (2004) 870-878
61. Ting A.Y., Blacklock A.D., and Smith P.G. Estrogen regulates vaginal sensory and autonomic nerve density in the rat. Biology of Reproduction 71 (2004) 1397-1404
62. Ogawa S., Olazabal U.E., Parhar I.S., et al. Effects of intrahypothalamic administration of antisense DNA for progesterone receptor mRNA on reproductive behavior and progesterone receptor immunoreactivity in female rat. The Journal of Neuroscience 14 (1994) 1766-1774
63. Lydon J.P., DeMayo F.J., Funk C.R., et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes & Development 9 (1995) 2266-2278
64. Pfaff D., Frohlich J., and Morgan M. Hormonal and genetic influences on arousal-sexual and otherwise. Trends in Neurosciences 25 (2002) 45-50
65. Kudwa A.E., Gustafsson J.A., and Rissman E.F. Estrogen receptor beta modulates estradiol induction of progestin receptor immunoreactivity in male, but not in female, mouse medial preoptic area. Endocrinology 145 (2004) 4500-4506
66. Mong J.A., and Pfaff D.W. Hormonal and genetic influences underlying arousal as it drives sex and aggression in animal and human brains. Neurobiology of Aging 24 supplement 1 (2003) S83-S88 discussion S91-2
67. Gooren L.J., and Saad F. Recent insights into androgen action on the anatomical and physiological substrate of penile erection. Asian Journal of Andrology 8 (2006) 3-9
68. Traish A.M., and Guay A.T. Are androgens critical for penile erections in humans? Examining the clinical and preclinical evidence. The Journal of Sexual Medicine 3 (2006) 382-404 discussion 404-407
69. Argiolas A., and Melis M.R. Central control of penile erection: role of the paraventricular nucleus of the hypothalamus. Progress in Neurobiology 76 (2005) 1-21
70. Shabsigh R. The effects of testosterone on the cavernous tissue and erectile function. World Journal of Urology 15 (1997) 21-26
71. Papka R.E., Srinivasan B., Miller K.E., et al. Localization of estrogen receptor protein and estrogen receptor messenger RNA in peripheral autonomic and sensory neurons. Neuroscience 79 (1997) 1153-1163
72. Zoubina E.V., and Smith P.G. Expression of estrogen receptors alpha and beta by sympathetic ganglion neurons projecting to the proximal urethra of female rats. The Journal of Urology 169 (2003) 382-385
73. Mendelsohn M.E., and Karas R.H. The protective effects of estrogen on the cardiovascular system. The New England Journal of Medicine 340 (1999) 1801-1811
74. Jankowski M., Rachelska G., Donghao W., et al. Estrogen receptors activate atrial natriuretic peptide in the rat heart. Proceedings of the National Academy of Sciences of the United States of America 98 (2001) 11765-11770
75. Nickenig G., Strehlow K., Wassmann S., et al. Differential effects of estrogen and progesterone on AT(1) receptor gene expression in vascular smooth muscle cells. Circulation 102 (2000) 1828-1833
76. Ciriello J, de Oliveira CVR, Masoumeh M, et al. Estrogen alters the cardiovascular responses to activation of rostral ventrolateral medulla in the female. 2002 Society For Neuroscience Abstract Viewer/Itinerary Planner, 2002. 768.6.
77. Rhodes C.H., Morrell J.I., and Pfaff D.W. Estrogen-concentrating neurophysin-containing hypothalamic magnocellular neurons in the vasopressin-deficient (Brattleboro) rat: a study combining steroid autoradiography and immunocytochemistry. The Journal of Neuroscience 2 (1982) 1718-1724
78. Meston C.M., Moe I.V., and Gorzalka B.B. Effects of sympathetic inhibition on receptive, proceptive, and rejection behaviors in the female rat. Physiology & Behavior 59 (1996) 537-542
79. Zucker K.J., Bradley S.J., Oliver G., et al. Hood J Self-reported arousability in women with congenital adrenal hyperplasia. Journal of Sex & Marital Therapy 30 5 (2004 Oct-Dec) 343-355