Somatic genital reflexes in rats with a nod to humans: Anatomy, physiology, and the role of the social neuropeptides

Hormones and Behavior

Volumn 59, Issue 5, 2011, Pages 656-665

  Normandin, Joseph J ^a,b   Murphy, Anne Z ^b,c  

^a Department of Biology ^*  (United States)

^b Georgia State University   (United States)

^c GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Anorgasmia; Clitoris; Copulation; Delayed ejaculation; Genitalia; Lordosis; Penis; Sexual behavior; Sexual dysfunction; Vagina

Indexed keywords

NEUROPEPTIDE; OXYTOCIN; VASOPRESSIN;

ARTICLE; EJACULATION; HUMAN; LUMBAR SPINAL CORD; MOTONEURON; MOTOR SYSTEM; NERVE CELL STIMULATION; NONHUMAN; PARAVENTRICULAR THALAMIC NUCLEUS; PRIORITY JOURNAL; REFLEX; SENSORY SYSTEM; SEXUAL DYSFUNCTION; SOMATIC GENITAL REFLEX; THALAMUS; UTERUS CONTRACTION;

ANIMALS; EJACULATION; FEMALE; GENITALIA; HUMANS; MALE; MEDULLA OBLONGATA; MOTOR NEURONS; NEUROPEPTIDES; RATS; REFLEX; SPINAL CORD;

EID: 79957608731     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2011.02.006     Document Type: Article

References (133)

1. Ackerman A.E., Lange G.M., Clemens L.G. Effects of paraventricular lesions on sex behavior and seminal emission in male rats. Physiol. Behav. 1997, 63:49-53.
2. Allard J., Truitt W.A., McKenna K.E., Coolen L.M. Spinal cord control of ejaculation. World J. Urol. 2005, 23:119-126.
3. Arakawa T., Hayashi S., et al. Development of the external anal sphincter with special reference to intergender difference: observations of mid-term fetuses (15-30 weeks of gestation). Okajimas Folia Anat. Jpn. 2010, 87(2):49-58.
4. Argiolas A., Collu M., Gessa G.L., Melis M.R., Serra G. The oxytocin antagonist d(CH2)5Tyr(Me)-Orn8-vasotocin inhibits male copulatory behaviour in rats. Eur. J. Pharmacol. 1988, 149:389-392.
5. Argiolas A., Melis M.R. The neurophysiology of the sexual cycle. J. Endocrinol. Invest. 2003, 26:20-22.
6. Arletti R., Bazzani C., Castelli M., Bertolini A. Oxytocin improves male copulatory performance in rats. Horm. Behav. 1985, 19:14-20.
7. Arletti R., Benelli A., Bertolini A. Sexual behavior of aging male rats is stimulated by oxytocin. Eur. J. Pharmacol. 1990, 179:377-381.
8. Balthazart J., Ball G.F. Topography in the preoptic region: differential regulation of appetitive and consummatory male sexual behaviors. Front. Neuroendocrinol. 2007, 28:161-178.
9. Baskerville T.A., Douglas A.J. Interactions between dopamine and oxytocin in the control of sexual behaviour. Prog. Brain Res. 2008, 170:277-290.
10. Blaivas J.G., Zayed A.A., Labib K.B. The bulbocavernosus reflex in urology: a prospective study of 299 patients. J. Urol. 1981, 126:197-199.
11. Borgdorff A.J., Bernabe J., Denys P., Alexandre L., Giuliano F. Ejaculation elicited by microstimulation of lumbar spinothalamic neurons. Eur. Urol. 2008, 54:449-456.
12. Breedlove S.M., Arnold A.P. Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord. Science 1980, 210:564-566.
13. Breiner S.J. Male sexual dysfunction. JAMA 2004, 292:2722. author reply 2722-2723.
14. Byrne M.M., Rolf C., Depenbusch M., Cooper T.G., Nieschlag E. Lack of effect of a single i.v. dose of oxytocin on sperm output in severely oligozoospermic men. Hum. Reprod. 2003, 18:2098-2102.
15. Cantor J.M., Binik Y.M., Pfaus J.G. Chronic fluoxetine inhibits sexual behavior in the male rat: reversal with oxytocin. Psychopharmacol. (Berl.) 1999, 144:355-362.
16. Carmichael M.S., Humbert R., Dixen J., Palmisano G., Greenleaf W., Davidson J.M. Plasma oxytocin increases in the human sexual response. J. Clin. Endocrinol. Metab. 1987, 64:27-31.
17. Carro-Juarez M., Rodriguez-Manzo G. Evidence for the presence of the spinal pattern generator involved in the control of the genital ejaculatory pattern in the female rat. Brain Res. 2006, 1084:54-60.
18. Castro-Vasquez A., Carreno N.B. A study of the sensory requirements for eliciting the pseudopregnancy response. Brain Res. 1981, 230:205-220.
19. Chen K.K., Chan S.H., Chang L.S., Chan J.Y. Participation of paraventricular nucleus of hypothalamus in central regulation of penile erection in the rat. J. Urol. 1997, 158:238-244.
20. Clement P., Bernabe J., Gengo P., Denys P., Laurin M., Alexandre L., Giuliano F. Supraspinal site of action for the inhibition of ejaculatory reflex by dapoxetine. Eur. Urol. 2007, 51:825-832.
21. Clement P., Peeters M., Bernabe J., Denys P., Alexandre L., Giuliano F. Brain oxytocin receptors mediate ejaculation elicited by 7-hydroxy-2-(di-N-propylamino) tetralin (7-OH-DPAT) in anaesthetized rats. Br. J. Pharmacol. 2008, 154:1150-1159.
22. Collins W.F., Erichsen J.T., Rose R.D. Pudendal motor and premotor neurons in the male rat: a WGA transneuronal study. J. Comp. Neurol. 1991, 308:28-41.
23. Consiglio A.R., Lucion A.B. Lesion of hypothalamic paraventricular nucleus and maternal aggressive behavior in female rats. Physiol. Behav. 1996, 59:591-596.
24. Coolen L.M. Neural control of ejaculation. J. Comp. Neurol. 2005, 493:39-45.
25. Coolen L.M., Veening J.G., Petersen D.W., Shipley M.T. Parvocellular subparafascicular thalamic nucleus in the rat: anatomical and functional compartmentalization. J. Comp. Neurol. 2003, 463:117-131.
26. Coolen L.M., Veening J.G., Wells A.B., Shipley M.T. Afferent connections of the parvocellular subparafascicular thalamic nucleus in the rat: evidence for functional subdivisions. J. Comp. Neurol. 2003, 463:132-156.
27. Dail W.G., Manzanares K., Moll M.A., Minorsky N. The hypogastric nerve innervates a population of penile neurons in the pelvic plexus. Neuroscience 1985, 16:1041-1046.
28. de Araujo C.G., Schmidt R.A., Tanagho E.A. Neural pathways to lower urinary tract identified by retrograde axonal transport of horseradish peroxidase. Urology 1982, 19:290-295.
29. de Geest K., Thiery M., Piron-Possuyt G., Vanden Driessche R. Plasma oxytocin in human pregnancy and parturition. J. Perinat. Med. 1985, 13:3-13.
30. deGroat W.C., Booth A.M. Physiology of male sexual function. Ann. Intern. Med. 1980, 92:329-331.
31. Donaldson Z.R., Young L.J. Oxytocin, vasopressin, and the neurogenetics of sociality. Science 2008, 322:900-904.
32. Eaton R.C., Markowski V.P., Lumley L.A., Thompson J.T., Moses J., Hull E.M. D2 receptors in the paraventricular nucleus regulate genital responses and copulation in male rats. Pharmacol. Biochem. Behav. 1991, 39:177-181.
33. Ertekin C., Reel F. Bulbocavernosus reflex in normal men and in patients with neurogenic bladder and/or impotence. J. Neurol. Sci. 1976, 28:1-15.
34. Fishman R.B., Breedlove S.M. Neonatal androgen maintains sexually dimorphic muscles in the absence of innervation. Muscle Nerve 1988, 11(6):553-560.
35. Forger N.G., Breedlove S.M. Sexual dimorphism in human and canine spinal cord: role of early androgen. Proc. Natl Acad. Sci. USA 1986, 83:7527-7531.
36. Freeman L.M., Padgett B.A., Prins G.S., Breedlove S.M. Distribution of androgen receptor immunoreactivity in the spinal cord of wild-type, androgen-insensitive and gonadectomized male rats. J. Neurobiol. 1995, 27:51-59.
37. Freund-Mercier M.J., Moos F., Poulain D.A., Richard P., Rodriguez F., Theodosis D.T., Vincent J.D. Role of central oxytocin in the control of the milk ejection reflex. Brain Res. Bull. 1988, 20:737-741.
38. Garner J.A., LaVail J.H. Differential anterograde transport of HSV type 1 viral strains in the murine optic pathway. J. Neurovirol. 1999, 5:140-150.
39. Gerstenberg T.C., Levin R.J., Wagner G. Erection and ejaculation in man. Assessment of the electromyographic activity of the bulbocavernosus and ischiocavernosus muscles. Br. J. Urol. 1990, 65:395-402.
40. Giraldi A., Marson L., Nappi R., Pfaus J., Traish A.M., Vardi Y., Goldstein I. Physiology of female sexual function: animal models. J. Sex. Med. 2004, 1:237-253.
41. Giuliano F., Bernabe J., Gengo P., Alexandre L., Clement P. Effect of acute dapoxetine administration on the pudendal motoneuron reflex in anesthetized rats: comparison with paroxetine. J. Urol. 2007, 177:386-389.
42. Giuliano F., Clement P. Neuroanatomy and physiology of ejaculation. Annu. Rev. Sex Res. 2005, 16:190-216.
43. Gobrogge K.L., Liu Y., Young L.J., Wang Z. Anterior hypothalamic vasopressin regulates pair-bonding and drug-induced aggression in a monogamous rodent. Proc. Natl Acad. Sci. USA 2009, 106:19144-19149.
44. Hammock E.A., Young L.J. Oxytocin, vasopressin and pair bonding: implications for autism. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361:2187-2198.
45. Hamson D.K., Jones B.A., Watson N.V. Distribution of androgen receptor immunoreactivity in the brainstem of male rats. Neuroscience 2004, 127:797-803.
46. Hart B.L., Melese-D'Hospital P.Y. Penile mechanisms and the role of the striated penile muscles in penile reflexes. Physiol. Behav. 1983, 31:807-813.
47. Hawthorn J., Ang V.T., Jenkins J.S. Effects of lesions in the hypothalamic paraventricular, supraoptic and suprachiasmatic nuclei on vasopressin and oxytocin in rat brain and spinal cord. Brain Res. 1985, 346:51-57.
48. Heinrichs M., von Dawans B., Domes G. Oxytocin, vasopressin, and human social behavior. Front. Neuroendocrinol. 2009, 30:548-557.
49. Hermann G.E., Holmes G.M., Rogers R.C., Beattie M.S., Bresnahan J.C. Descending spinal projections from the rostral gigantocellular reticular nuclei complex. J. Comp. Neurol. 2003, 455:210-221.
50. Holmes G.M., Chapple W.D., Leipheimer R.E., Sachs B.D. Electromyographic analysis of male rat perineal muscles during copulation and reflexive erections. Physiol. Behav. 1991, 49:1235-1246.
51. Holstege G. The emotional motor system. Eur. J. Morphol. 1992, 30:67-79.
52. Holstege G., Georgiadis J.R. The emotional brain: neural correlates of cat sexual behavior and human male ejaculation. Prog. Brain Res. 2004, 143:39-45.
53. Holstege G., Georgiadis J.R., Paans A.M., Meiners L.C., van der Graaf F.H., Reinders A.A. Brain activation during human male ejaculation. J. Neurosci. 2003, 23:9185-9193.
54. Hu S.H., Wei N., Wang Q.D., Yan L.Q., Wei E.Q., Zhang M.M., Hu J.B., Huang M.L., Zhou W.H., Xu Y. Patterns of brain activation during visually evoked sexual arousal differ between homosexual and heterosexual men. AJNR Am. J. Neuroradiol. 2008, 29:1890-1896.
55. Hubscher C.H., Johnson R.D. Responses of medullary reticular formation neurons to input from the male genitalia. J. Neurophysiol. 1996, 76:2474-2482.
56. 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. 2010, 588:1073-1083.
57. Hull E.M., Du J., Lorrain D.S., Matuszewich L. Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation. J. Neurosci. 1995, 15:7465-7471.
58. Ishak W.W., Berman D.S., Peters A. Male anorgasmia treated with oxytocin. J. Sex. Med. 2008, 5:1022-1024.
59. Ivell R., Balvers M., Rust W., Bathgate R., Einspanier A. Oxytocin and male reproductive function. Adv. Exp. Med. Biol. 1997, 424:253-264.
60. Jard S., Butlen D., Cantau B., Guillon G., Marie J., Roy C. The mechanisms of action of antidiuretic hormone. Adv. Nephrol. Necker Hosp. 1984, 13:163-177.
61. Johnson R.D. Descending pathways modulating the spinal circuitry for ejaculation: effects of chronic spinal cord injury. Prog. Brain Res. 2006, 152:415-426.
62. Johnson R.D., Hubscher C.H. Brainstem microstimulation differentially inhibits pudendal motoneuron reflex inputs. NeuroReport 1998, 9:341-345.
63. Karama S., Lecours A.R., Leroux J.M., Bourgouin P., Beaudoin G., Joubert S., Beauregard M. Areas of brain activation in males and females during viewing of erotic film excerpts. Hum. Brain Mapp. 2002, 16:1-13.
64. Katagiri T., Gibson S.J., Su H.C., Polak J.M. Composition and central projections of the pudendal nerve in the rat investigated by combined peptide immunocytochemistry and retrograde fluorescent labelling. Brain Res. 1986, 372:313-322.
65. Laumann E.O., Paik A., Rosen R.C. Sexual dysfunction in the United States: prevalence and predictors. JAMA 1999, 281:537-544.
66. Lee J.W., Erskine M.S. Pseudorabies virus tracing of neural pathways between the uterine cervix and CNS: effects of survival time, estrogen treatment, rhizotomy, and pelvic nerve transection. J. Comp. Neurol. 2000, 418:484-503.
67. Levin R.J. Sex and the human female reproductive tract-what really happens during and after coitus. Int. J. Impot. Res. 1998, 10(Suppl 1):S14-S21.
68. Liu Y., Curtis J.T., Wang Z. Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). Behav. Neurosci. 2001, 115:910-919.
69. Liu Y., Wang Z.X. Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 2003, 121:537-544.
70. Liu Y.C., Salamone J.D., Sachs B.D. Impaired sexual response after lesions of the paraventricular nucleus of the hypothalamus in male rats. Behav. Neurosci. 1997, 111:1361-1367.
71. Macdonald K., Macdonald T.M. The peptide that binds: a systematic review of oxytocin and its prosocial effects in humans. Harv. Rev. Psychiatry 2010, 18:1-21.
72. Marson L., Carson C.C. Central nervous system innervation of the penis, prostate, and perineal muscles: a transneuronal tracing study. Mol. Urol. 1999, 3:43-50.
73. Marson L., Foley K.A. Identification of neural pathways involved in genital reflexes in the female: a combined anterograde and retrograde tracing study. Neuroscience 2004, 127:723-736.
74. Marson L., List M.S., McKenna K.E. Lesions of the nucleus paragigantocellularis alter ex copula penile reflexes. Brain Res. 1992, 592:187-192.
75. Marson L., McKenna K.E. The identification of a brainstem site controlling spinal sexual reflexes in male rats. Brain Res. 1990, 515:303-308.
76. 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. 1996, 374:161-179.
77. Marson L., Murphy A.Z. Identification of neural circuits involved in female genital responses in the rat: a dual virus and anterograde tracing study. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 291:R419-R428.
78. Martin-Alguacil N., Schober J.M., Sengelaub D.R., Pfaff D.W., Shelley D.N. Clitoral sexual arousal: neuronal tracing study from the clitoris through the spinal tracts. J. Urol. 2008, 180:1241-1248.
79. McEwen B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 2007, 87:873-904.
80. McKenna K.E. The neurophysiology of female sexual function. World J. Urol. 2002, 20:93-100.
81. McKenna K.E., Nadelhaft I. The organization of the pudendal nerve in the male and female rat. J. Comp. Neurol. 1986, 248:532-549.
82. McKenna K.E., Nadelhaft I. The pudendo-pudendal reflex in male and female rats. J. Auton. Nerv. Syst. 1989, 27:67-77.
83. 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.
84. Murphy A.Z., Hoffman G.E. Distribution of gonadal steroid receptor-containing neurons in the preoptic-periaqueductal gray-brainstem pathway: a potential circuit for the initiation of male sexual behavior. J. Comp. Neurol. 2001, 438:191-212.
85. Murphy A.Z., Rizvi T.A., Ennis M., Shipley M.T. The organization of preoptic-medullary circuits in the male rat: evidence for interconnectivity of neural structures involved in reproductive behavior, antinociception and cardiovascular regulation. Neuroscience 1999, 91:1103-1116.
86. Newton B.W. Galanin immunoreactivity in rat spinal lamina IX: emphasis on sexually dimorphic regions. Peptides 1993, 14:955-969.
87. Nilaver G., Zimmerman E.A., Wilkins J., Michaels J., Hoffman D., Silverman A.J. Magnocellular hypothalamic projections to the lower brain stem and spinal cord of the rat. Immunocytochemical evidence for predominance of the oxytocin-neurophysin system compared to the vasopressin-neurophysin system. Neuroendocrinology 1980, 30:150-158.
88. Normandin J.J., Murphy A.Z. Nucleus paragigantocellularis afferents in male and female rats: organization, gonadal steroid receptor expression, and activation during sexual behavior. J. Comp. Neurol. 2008, 508:771-794.
89. Normandin J.J., Murphy A.Z. Excitotoxic lesions of the nucleus paragigantocellularis facilitate male sexual behavior but attenuate female sexual behavior in rats. Neuroscience 2011, 175:212-223.
90. Nunez R., Gross G.H., Sachs B.D. Origin and central projections of rat dorsal penile nerve: possible direct projection to autonomic and somatic neurons by primary afferents of nonmuscle origin. J. Comp. Neurol. 1986, 247:417-429.
91. Pacheco P., Martinez-Gomez M., Whipple B., Beyer C., Komisaruk B.R. Somato-motor components of the pelvic and pudendal nerves of the female rat. Brain Res. 1989, 490:85-94.
92. Pastelin C.F., Zempoalteca R., Pacheco P., Downie J.W., Cruz Y. Sensory and somatomotor components of the "sensory branch" of the pudendal nerve in the male rat. Brain Res. 2008, 1222:149-155.
93. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1997, Academic Press, San Diego. 3rd ed.
94. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2005, Elsevier Academic Press, Amsterdam, Boston. 5th ed.
95. Peshori K.R., Erichsen J.T., Collins W.F. Differences in the connectivity of rat pudendal motor nuclei as revealed by retrograde transneuronal transport of wheat germ agglutinin. J. Comp. Neurol. 1995, 353:119-128.
96. Peters L.C., Kristal M.B., Komisaruk B.R. Sensory innervation of the external and internal genitalia of the female rat. Brain Res. 1987, 408:199-204.
97. 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.
98. Pfaus J.G., Manitt C., Coopersmith C.B. Effects of pelvic, pudendal, or hypogastric nerve cuts on Fos induction in the rat brain following vaginocervical stimulation. Physiol. Behav. 2006, 89:627-636.
99. Phelps S.M., Campbell P., Zheng D.J., Ophir A.G. Beating the boojum: comparative approaches to the neurobiology of social behavior. Neuropharmacology 2010, 58:17-28.
100. Purinton P.T., Fletcher T.F., Bradley W.E. Innervation of pelvic viscera in the rat. Evoked potentials in nerves to bladder and penis (clitoris). Invest Urol. 1976, 14:28-32.
101. Rand M.N., Breedlove S.M. Ontogeny of functional innervation of bulbocavernosus muscles in male and female rats. Brain Res. 1987, 430:150-152.
102. Roppolo J.R., Nadelhaft I., de Groat W.C. The organization of pudendal motoneurons and primary afferent projections in the spinal cord of the rhesus monkey revealed by horseradish peroxidase. J. Comp. Neurol. 1985, 234:475-488.
103. Ross H.E., Cole C.D., Smith Y., Neumann I.D., Landgraf R., Murphy A.Z., Young L.J. Characterization of the oxytocin system regulating affiliative behavior in female prairie voles. Neuroscience 2009, 162:892-903.
104. Ross H.E., Young L.J. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front. Neuroendocrinol. 2009, 30:534-547.
105. Rowe D.W., Erskine M.S. c-Fos proto-oncogene activity induced by mating in the preoptic area, hypothalamus and amygdala in the female rat: role of afferent input via the pelvic nerve. Brain Res. 1993, 621:25-34.
106. Sachs B.D. Role of striated penile muscles in penile reflexes, copulation, and induction of pregnancy in the rat. J. Reprod. Fertil. 1982, 66:433-443.
107. Sakuma Y. Neural substrates for sexual preference and motivation in the female and male rat. Ann. NY Acad. Sci. 2008, 1129:55-60.
108. Schroder H.D. Organization of the motoneurons innervating the pelvic muscles of the male rat. J. Comp. Neurol. 1980, 192:567-587.
109. Schroder H.D. Onuf's nucleus X: a morphological study of a human spinal nucleus. Anat. Embryol. (Berl.) 1981, 162:443-453.
110. Sofroniew M.V. Projections from vasopressin, oxytocin, and neurophysin neurons to neural targets in the rat and human. J. Histochem. Cytochem. 1980, 28:475-478.
111. Stoneham M.D., Everitt B.J., Hansen S., Lightman S.L., Todd K. Oxytocin and sexual behaviour in the male rat and rabbit. J. Endocrinol. 1985, 107:97-106.
112. Swaab D.F., Pool C.W., Nijveldt F. Immunofluorescence of vasopressin and oxytocin in the rat hypothalamo-neurohypophyseal system. J. Neural Transm. 1975, 36:195-215.
113. Swanson L.W., Sawchenko P.E. Paraventricular nucleus: a site for the integration of neuroendocrine and autonomic mechanisms. Neuroendocrinology 1980, 31:410-417.
114. Tang Y., Rampin O., Calas A., Facchinetti P., Giuliano F. Oxytocinergic and serotonergic innervation of identified lumbosacral nuclei controlling penile erection in the male rat. Neuroscience 1998, 82:241-254.
115. Tang Y., Rampin O., Giuliano F., Ugolini G. Spinal and brain circuits to motoneurons of the bulbospongiosus muscle: retrograde transneuronal tracing with rabies virus. J. Comp. Neurol. 1999, 414:167-192.
116. Temel Y., Hafizi S., Beuls E., Visser-Vandewalle V. The supraspinal network in the control of erection. Expert Opin. Ther. Targets 2005, 9:941-954.
117. Truitt W.A., Coolen L.M. Identification of a potential ejaculation generator in the spinal cord. Science 2002, 297:1566-1569.
118. Truitt W.A., Shipley M.T., Veening J.G., Coolen L.M. Activation of a subset of lumbar spinothalamic neurons after copulatory behavior in male but not female rats. J. Neurosci. 2003, 23:325-331.
119. Vanderhorst V.G., Holstege G. Caudal medullary pathways to lumbosacral motoneuronal cell groups in the cat: evidence for direct projections possibly representing the final common pathway for lordosis. J. Comp. Neurol. 1995, 359:457-475.
120. Veenema A.H., Neumann I.D. Central vasopressin and oxytocin release: regulation of complex social behaviours. Prog. Brain Res. 2008, 170:261-276.
121. Vodusek D.B., Janko M., Lokar J. Direct and reflex responses in perineal muscles on electrical stimulation. J. Neurol. Neurosurg. Psychiatry 1983, 46:67-71.
122. Wagner C.K., Clemens L.G. Projections of the paraventricular nucleus of the hypothalamus to the sexually dimorphic lumbosacral region of the spinal cord. Brain Res. 1991, 539:254-262.
123. Walch K., Eder R., Schindler A., Feichtinger W. The effect of single-dose oxytocin application on time to ejaculation and seminal parameters in men. J. Assist. Reprod. Genet. 2001, 18:655-659.
124. Walter M., Bermpohl F., Mouras H., Schiltz K., Tempelmann C., Rotte M., Heinze H.J., Bogerts B., Northoff G. Distinguishing specific sexual and general emotional effects in fMRI-subcortical and cortical arousal during erotic picture viewing. Neuroimage 2008, 40:1482-1494.
125. Wiedey J., Alexander M.S., Marson L. Spinal neurons activated in response to pudendal or pelvic nerve stimulation in female rats. Brain Res. 2008, 1197:106-114.
126. Witt D.M., Insel T.R. Increased Fos expression in oxytocin neurons following masculine sexual behavior. J. Neuroendocrinol. 1994, 6:13-18.
127. Xu C., Giuliano F., Yaici E.D., Conrath M., Trassard O., Benoit G., Verge D. Identification of lumbar spinal neurons controlling simultaneously the prostate and the bulbospongiosus muscles in the rat. Neuroscience 2006, 138:561-573.
128. Yang C.C., Jiang X. Clinical autonomic neurophysiology and the male sexual response: an overview. J. Sex. Med. 2009, 6(Suppl 3):221-228.
129. Yells D.P., Hendricks S.E., Prendergast M.A. Lesions of the nucleus paragigantocellularis: effects on mating behavior in male rats. Brain Res. 1992, 596:73-79.
130. Yells D.P., Prendergast M.A., Hendricks S.E., Nakamura M. Fluoxetine-induced inhibition of male rat copulatory behavior: modification by lesions of the nucleus paragigantocellularis. Pharmacol. Biochem. Behav. 1994, 49:121-127.
131. Young L.J., Murphy Young A.Z., Hammock E.A. Anatomy and neurochemistry of the pair bond. J. Comp. Neurol. 2005, 493:51-57.
132. Zec N., Kinney H.C. Anatomic relationships of the human nucleus paragigantocellularis lateralis: a DiI labeling study. Auton. Neurosci. 2001, 89:110-124.
133. Zemanick M.C., Strick P.L., Dix R.D. Direction of transneuronal transport of herpes simplex virus 1 in the primate motor system is strain-dependent. Proc. Natl Acad. Sci. USA 1991, 88:8048-8051.