Serotonin 1A receptors and sexual behavior in male rats: A review

Pharmacology Biochemistry and Behavior

Volumn 121, Issue , 2014, Pages 102-114

  Snoeren, Eelke M S ^a   Veening, Jan G ^b,c   Olivier, Berend ^b   Oosting, Ronald S ^b  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UTRECHT UNIVERSITY   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Animal models; Male; Serotonin; Sexual behavior

Indexed keywords

MONOAMINE; SEROTONIN 1A RECEPTOR; SEROTONIN AGONIST; SEROTONIN RECEPTOR; SEROTONIN TRANSPORTER; 2 DIPROPYLAMINO 8 HYDROXYTETRALIN; BIOGENIC AMINE; SEROTONIN; SEROTONIN 1 AGONIST;

BRAIN REGION; COPULATION; EJACULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEROTONINERGIC SYSTEM; SEXUAL BEHAVIOR; ANATOMY AND HISTOLOGY; ANIMAL; BIOLOGICAL MODEL; BRAIN; DRUG EFFECTS; FEMALE; MALE; NERVE TRACT; PHYSIOLOGY; RAT;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; ANIMALS; BIOGENIC MONOAMINES; BRAIN; COPULATION; EJACULATION; FEMALE; MALE; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; RATS; RECEPTOR, SEROTONIN, 5-HT1A; SEROTONIN; SEROTONIN 5-HT1 RECEPTOR AGONISTS; SEXUAL BEHAVIOR, ANIMAL;

EID: 84901194368     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2013.11.007     Document Type: Review

References (167)

1. G.K. Aghajanian Feedback regulation of central monoaminergic neurons: evidence from single cell recording studies Essays Neurochem Neuropharmacol 3 1978 1 32
2. A. Ågmo Male rat sexual behavior Brain Res Brain Res Protoc 1 1997 203 209 (Pubitemid 28281344)
3. S. Ahlenius, and K. Larsson Lisuride, LY-141865, and 8-OH-DPAT facilitate male rat sexual behavior via a non-dopaminergic mechanism Psychopharmacology (Berl) 83 1984 330 334 (Pubitemid 14057669)
4. S. Ahlenius, and K. Larsson Evidence for an involvement of 5-HT1B receptors in the inhibition of male rat ejaculatory behavior produced by 5-HTP Psychopharmacology (Berl) 137 1998 374 382 (Pubitemid 28305373)
5. S. Ahlenius, K. Larsson, and A. Wijkstrom Behavioral and biochemical effects of the 5-HT1A receptor agonists flesinoxan and 8-OH-DPAT in the rat Eur J Pharmacol 200 1991 259 266
6. G. Andersson, and K. Larsson Effects of FG 5893, a new compound with 5-HT1A receptor agonistic and 5-HT2 receptor antagonistic properties, on male rat sexual behavior Eur J Pharmacol 255 1994 131 137 (Pubitemid 24105753)
7. S. Aznar, Z. Qian, R. Shah, B. Rahbek, and G.M. Knudsen The 5-HT1A serotonin receptor is located on calbindin- and parvalbumin-containing neurons in the rat brain Brain Res 959 2003 58 67 (Pubitemid 35435406)
8. M.E. Balfour, L. Yu, and L.M. Coolen Sexual behavior and sex-associated environmental cues activate the mesolimbic system in male rats Neuropsychopharmacology 29 2004 718 730 (Pubitemid 38402479)
9. N.M. Barnes, and T. Sharp A review of central 5-HT receptors and their function Neuropharmacology 38 1999 1083 1152 (Pubitemid 29292403)
10. M.J. Baum, and B.J. Everitt Increased expression of c-fos in the medial preoptic area after mating in male rats: role of afferent inputs from the medial amygdala and midbrain central tegmental field Neuroscience 50 1992 627 646
11. F.A. Beach Sexual attractivity, proceptivity, and receptivity in female mammals Horm Behav 7 1976 105 138
12. G. Behzadi, P. Kalen, F. Parvopassu, and L. Wiklund Afferents to the median raphe nucleus of the rat: retrograde cholera toxin and wheat germ conjugated horseradish peroxidase tracing, and selective D-[3H]aspartate labelling of possible excitatory amino acid inputs Neuroscience 37 1990 77 100 (Pubitemid 20262233)
13. S. Benloucif, and M.P. Galloway Facilitation of dopamine release in vivo by serotonin agonists: studies with microdialysis Eur J Pharmacol 200 1991 1 8
14. E. Bjorkstrand, S. Ahlenius, U. Smedh, and K. Uvnas-Moberg The oxytocin receptor antagonist 1-deamino-2-D-Tyr-(OEt)-4-Thr-8-Orn-oxytocin inhibits effects of the 5-HT1A receptor agonist 8-OH-DPAT on plasma levels of insulin, cholecystokinin and somatostatin Regul Pept 63 1996 47 52
15. P. Bobillier, F. Pettijean, D. Salvert, M. Ligier, and S. Seguin Differential projections of the nucleus raphe dorsalis and nucleus raphe centralis as revealed by autoradiography Brain Res 85 1975 205 210
16. F.J. Bosker, A.A. Klompmakers, and H.G. Westenberg Effects of single and repeated oral administration of fluvoxamine on extracellular serotonin in the median raphe nucleus and dorsal hippocampus of the rat Neuropharmacology 34 1995 501 508
17. S.C. Bressler, and M.J. Baum Sex comparison of neuronal Fos immunoreactivity in the rat vomeronasal projection circuit after chemosensory stimulation Neuroscience 71 1996 1063 1072 (Pubitemid 26090019)
18. S. Campeau, and S.J. Watson Jr. Connections of some auditory-responsive posterior thalamic nuclei putatively involved in activation of the hypothalamo-pituitary-adrenocortical axis in response to audiogenic stress in rats: an anterograde and retrograde tract tracing study combined with Fos expression J Comp Neurol 423 2000 474 491 (Pubitemid 30451680)
19. C. Caquineau, G. Leng, X.M. Guan, M. Jiang, L. Van der Ploeg, and A.J. Douglas Effects of alpha-melanocyte-stimulating hormone on magnocellular oxytocin neurones and their activation at intromission in male rats J Neuroendocrinol 18 2006 685 691 (Pubitemid 44132616)
20. A. Carlsson, B. Falck, K. Fuxe, and N.A. Hillarp Cellular localization of monoamines in the spinal cord Acta Physiol Scand 60 1964 112 119
21. M. Carro-Juarez, and G. Rodriguez-Manzo Role of genital sensory information in the control of the functioning of the spinal generator for ejaculation Int J Impot Res 17 2005 114 120 (Pubitemid 40434583)
22. M. Carro-Juarez, and G. Rodriguez-Manzo The spinal pattern generator for ejaculation Brain Res Rev 58 2008 106 120
23. J.S. Chan, M.D. Waldinger, B. Olivier, and R.S. Oosting Drug-induced sexual dysfunction in rats Curr Protoc Neurosci 2010 34 Chapter 9: Unit 9
24. J.S. Chan, E.M. Snoeren, E. Cuppen, M.D. Waldinger, B. Olivier, and R.S. Oosting The serotonin transporter plays an important role in male sexual behavior: a study in serotonin transporter knockout rats J Sex Med 8 2011 97 108
25. L.M. Coolen, B. Olivier, H.J. Peters, and J.G. Veening Demonstration of ejaculation-induced neural activity in the male rat brain using 5-HT1A agonist 8-OH-DPAT Physiol Behav 62 1997 881 891 (Pubitemid 27412649)
26. L.M. Coolen, H.J. Peters, and J.G. Veening Distribution of Fos immunoreactivity following mating versus anogenital investigation in the male rat brain Neuroscience 77 1997 1151 1161 (Pubitemid 27128788)
27. L.M. Coolen, H.J. Peters, and J.G. Veening Anatomical interrelationships of the medial preoptic area and other brain regions activated following male sexual behavior: a combined fos and tract-tracing study J Comp Neurol 397 1998 421 435 (Pubitemid 28307342)
28. L.M. Coolen, J.G. Veening, D.W. Petersen, and M.T. Shipley Parvocellular subparafascicular thalamic nucleus in the rat: anatomical and functional compartmentalization J Comp Neurol 463 2003 117 131 (Pubitemid 36842388)
29. L.M. Coolen, J.G. Veening, A.B. Wells, and M.T. Shipley Afferent connections of the parvocellular subparafascicular thalamic nucleus in the rat: evidence for functional subdivisions J Comp Neurol 463 2003 132 156 (Pubitemid 36842389)
30. L.M. Coolen, J. Allard, W.A. Truitt, and K.E. McKenna Central regulation of ejaculation Physiol Behav 83 2004 203 215 (Pubitemid 39361566)
31. V. Cornea-Hebert, M. Riad, C. Wu, S.K. Singh, and L. Descarries Cellular and subcellular distribution of the serotonin 5-HT2A receptor in the central nervous system of adult rat J Comp Neurol 409 1999 187 209 (Pubitemid 29264253)
32. S.L. Cottingham, and D.W. Pfaff Electrical stimulation of the midbrain central gray facilitates lateral vestibulospinal activation of back muscle EMG in the rat Brain Res 421 1987 397 400 (Pubitemid 18021654)
33. S.L. Cottingham, P.A. Femano, and D.W. Pfaff Electrical stimulation of the midbrain central gray facilitates reticulospinal activation of axial muscle EMG Exp Neurol 97 1987 704 724 (Pubitemid 17143120)
34. J. de Castilhos, S. Marcuzzo, C.D. Forti, R.M. Frey, D. Stein, and M. Achaval et al. Further studies on the rat posterodorsal medial amygdala: dendritic spine density and effect of 8-OH-DPAT microinjection on male sexual behavior Brain Res Bull 69 2006 131 139 (Pubitemid 43375866)
35. T.R. de Jong, T. Pattij, J.G. Veening, P.J. Dederen, M.D. Waldinger, and A.R. Cools et al. Citalopram combined with WAY 100635 inhibits ejaculation and ejaculation-related Fos immunoreactivity Eur J Pharmacol 509 2005 49 59 (Pubitemid 40248785)
36. T.R. de Jong, T. Pattij, J.G. Veening, M.D. Waldinger, A.R. Cools, and B. Olivier Effects of chronic selective serotonin reuptake inhibitors on 8-OH-DPAT-induced facilitation of ejaculation in rats: comparison of fluvoxamine and paroxetine Psychopharmacology (Berl) 179 2005 509 515
37. T.R. de Jong, J.G. Veening, B. Olivier, and M.D. Waldinger Oxytocin involvement in SSRI-induced delayed ejaculation: a review of animal studies J Sex Med 4 2007 14 28 (Pubitemid 46002363)
38. L. Descarries, M. Riad, and M. Parent Ultrastructure of the serotonin innervation in the mammalian central nervous system C.P. Muller, B.L. Jacobs, Handbook of the behavioral neurobiology of serotonin 2010 Elsevier Amsterdam 65 102
39. A. Fernandez-Guasti, and A. Escalante Role of presynaptic serotonergic receptors on the mechanism of action of 5-HT1A and 5-HT1B agonists on masculine sexual behaviour: physiological and pharmacological implications J Neural Transm Gen Sect 85 1991 95 107
40. A. Fernandez-Guasti, S. Hansen, T. Archer, and G. Jonsson Noradrenaline-serotonin interactions in the control of sexual behavior in the male rat: DSP4-induced noradrenaline depletion antagonizes the facilitatory effect of serotonin receptor agonists, 5-MeODMT and lisuride Brain Res 377 1986 112 118 (Pubitemid 16063044)
41. A. Fernandez-Guasti, A. Escalante, and A. Ågmo Inhibitory action of various 5-HT1B receptor agonists on rat masculine sexual behaviour Pharmacol Biochem Behav 34 1989 811 816 (Pubitemid 20036581)
42. A. Fernandez-Guasti, A. Escalante, E. Hong, and A. Ågmo Behavioural actions of the serotonergic anxiolytic indorenate Pharmacol Biochem Behav 37 1990 83 88 (Pubitemid 20341690)
43. A. Fernandez-Guasti, A.L. Escalante, S. Ahlenius, V. Hillegaart, and K. Larsson Stimulation of 5-HT1A and 5-HT1B receptors in brain regions and its effects on male rat sexual behaviour Eur J Pharmacol 210 1992 121 129
44. L.M. Flanagan-Cato, B.J. Lee, and L.H. Calizo Co-localization of midbrain projections, progestin receptors, and mating-induced fos in the hypothalamic ventromedial nucleus of the female rat Horm Behav 50 2006 52 60 (Pubitemid 43776833)
45. G. Flugge, D. Pfender, S. Rudolph, H. Jarry, and E. Fuchs 5HT1A-receptor binding in the brain of cyclic and ovariectomized female rats J Neuroendocrinol 11 1999 243 249 (Pubitemid 29149877)
46. M.M. Foreman, R.W. Fuller, J.D. Leander, M.J. Benvenga, D.T. Wong, and D.L. Nelson et al. Preclinical studies on LY228729: a potent and selective serotonin1A agonist J Pharmacol Exp Ther 267 1993 58 71 (Pubitemid 23324989)
47. M.M. Foreman, R.W. Fuller, K. Rasmussen, D.L. Nelson, D.O. Calligaro, and L. Zhang et al. Pharmacological characterization of LY293284: a 5-HT1A receptor agonist with high potency and selectivity J Pharmacol Exp Ther 270 1994 1270 1281 (Pubitemid 24315249)
48. K.S. Frohmader, K.K. Pitchers, M.E. Balfour, and L.M. Coolen Mixing pleasures: review of the effects of drugs on sex behavior in humans and animal models Horm Behav 58 2010 149 162
49. K.S. Frohmader, J. Wiskerke, R.A. Wise, M.N. Lehman, and L.M. Coolen Methamphetamine acts on subpopulations of neurons regulating sexual behavior in male rats Neuroscience 166 2010 771 784
50. P. Gaspar, O. Cases, and L. Maroteaux The developmental role of serotonin: news from mouse molecular genetics Nat Rev Neurosci 4 2003 1002 1012 (Pubitemid 37486676)
51. M.A. Geyer, A. Puerto, W.J. Dawsey, S. Knapp, W.P. Bullard, and A.J. Mandell Histologic and enzymatic studies of the mesolimbic and mesostriatal serotonergic pathways Brain Res 106 1976 241 256
52. M. Gil, R. Bhatt, K.B. Picotte, and E.M. Hull Oxytocin in the medial preoptic area facilitates male sexual behavior in the rat Horm Behav 59 2011 435 443
53. M. Gil, R. Bhatt, K.B. Picotte, and E.M. Hull Sexual experience increases oxytocin receptor gene expression and protein in the medial preoptic area of the male rat Psychoneuroendocrinology 38 2013 1688 1697
54. M. Gothert, and G. Weinheimer Extracellular 5-hydroxytryptamine inhibits 5-hydroxytryptamine release from rat brain cortex slices Naunyn Schmiedebergs Arch Pharmacol 310 1979 93 96 (Pubitemid 10214655)
55. K.K. Gulia, V.M. Kumar, and H.N. Mallick Role of the lateral septal noradrenergic system in the elaboration of male sexual behavior in rats Pharmacol Biochem Behav 72 2002 817 823 (Pubitemid 34621308)
56. S.M. Haensel, and A.K. Slob Flesinoxan: a prosexual drug for male rats Eur J Pharmacol 330 1997 1 9 (Pubitemid 27304028)
57. M. Han, X.F. Huang, T.M. du Bois, and C. Deng The effects of antipsychotic drugs administration on 5-HT1A receptor expression in the limbic system of the rat brain Neuroscience 164 2009 1754 1763
58. S. Hansen Spinal control of sexual behavior: effects of intrathecal administration of lisuride Neurosci Lett 33 1982 329 332 (Pubitemid 13119543)
59. M.M. Heeb, and P. Yahr c-Fos immunoreactivity in the sexually dimorphic area of the hypothalamus and related brain regions of male gerbils after exposure to sex-related stimuli or performance of specific sexual behaviors Neuroscience 72 1996 1049 1071 (Pubitemid 26135585)
60. M.M. Heeb, and P. Yahr Anatomical and functional connections among cell groups in the gerbil brain that are activated with ejaculation J Comp Neurol 439 2001 248 258 (Pubitemid 32906026)
61. V. Hillegaart, and S. Ahlenius Facilitation and inhibition of male rat ejaculatory behaviour by the respective 5-HT1A and 5-HT1B receptor agonists 8-OH-DPAT and anpirtoline, as evidenced by use of the corresponding new and selective receptor antagonists NAD-299 and NAS-181 Br J Pharmacol 125 1998 1733 1743 (Pubitemid 29000820)
62. V. Hillegaart, S. Ahlenius, and K. Larsson Region-selective inhibition of male rat sexual behavior and motor performance by localized forebrain 5-HT injections: a comparison with effects produced by 8-OH-DPAT Behav Brain Res 42 1991 169 180
63. G.E. Hoffman, and D. Lyo Anatomical markers of activity in neuroendocrine systems: are we all 'fos-ed out'? J Neuroendocrinol 14 2002 259 268 (Pubitemid 34285295)
64. J.P. Hornung The neuroanatomy of the serotonergic system C.P. Muller, Handbook of the behavioral neurobiology of serotonin 2010 Elsevier Amsterdam 51 64
65. D. Hoyer, D.E. Clarke, J.R. Fozard, P.R. Hartig, G.R. Martin, and E.J. Mylecharane et al. International union of pharmacology classification of receptors for 5-hydroxytryptamine (serotonin) Pharmacol Rev 46 1994 157 203 (Pubitemid 24185150)
66. E.M. Hull, R.C. Eaton, V.P. Markowski, J. Moses, L.A. Lumley, and J.A. Loucks Opposite influence of medial preoptic D1 and D2 receptors on genital reflexes: implications for copulation Life Sci 51 1992 1705 1713
67. G.E. Hunt, I.S. McGregor, J.L. Cornish, and P.D. Callaghan MDMA-induced c-Fos expression in oxytocin-containing neurons is blocked by pretreatment with the 5-HT-1A receptor antagonist WAY 100635 Brain Res Bull 86 2011 65 73
68. H. Imai, M.R. Park, D.A. Steindler, and S.T. Kitai The morphology and divergent axonal organization of midbrain raphe projection neurons in the rat Brain Dev 8 1986 343 354 (Pubitemid 16004050)
69. H. Imai, D.A. Steindler, and S.T. Kitai The organization of divergent axonal projections from the midbrain raphe nuclei in the rat J Comp Neurol 243 1986 363 380 (Pubitemid 16179241)
70. B.L. Jacobs, and C.A. Fornal Serotonin and motor activity Curr Opin Neurobiol 7 1997 820 825 (Pubitemid 28052305)
71. C.E. Johansson, B.J. Meyerson, and U. Hacksell The novel 5-HT1A receptor antagonist (S)-UH-301 antagonizes 8-OH-DPAT-induced effects on male as well as female rat copulatory behaviour Eur J Pharmacol 202 1991 81 87
72. H. Jorgensen, M. Riis, U. Knigge, A. Kjaer, and J. Warberg Serotonin receptors involved in vasopressin and oxytocin secretion J Neuroendocrinol 15 2003 242 249 (Pubitemid 36266891)
73. H. Jovanovic, A. Perski, H. Berglund, and I. Savic Chronic stress is linked to 5-HT(1A) receptor changes and functional disintegration of the limbic networks Neuroimage 55 2011 1178 1188
74. G. Ju, X.J. Duan, and X. Zhang Serotonin-like immunoreactive fibers in the medial dorsal accessory group and the anterior fornical nucleus of the magnocellular neurosecretory system in the rat Neurosci Lett 93 1988 19 22
75. P. Kalen, and L. Wiklund Projections from the medial septum and diagonal band of Broca to the dorsal and central superior raphe nuclei: a non-cholinergic pathway Exp Brain Res 75 1989 401 416 (Pubitemid 19110677)
76. H.K. Kia, M.C. Miquel, M.J. Brisorgueil, G. Daval, M. Riad, and S. El Mestikawy et al. Immunocytochemical localization of serotonin1A receptors in the rat central nervous system J Comp Neurol 365 1996 289 305
77. J. Kievit, and H.G. Kuypers Subcortical afferents to the frontal lobe in the rhesus monkey studied by means of retrograde horseradish peroxidase transport Brain Res 85 1975 261 266
78. T.E. Kippin, V. Sotiropoulos, J. Badih, and J.G. Pfaus 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 2004 698 704 (Pubitemid 38241309)
79. V. Kiyasova, S.P. Fernandez, J. Laine, L. Stankovski, A. Muzerelle, and S. Doly et al. A genetically defined morphologically and functionally unique subset of 5-HT neurons in the mouse raphe nuclei J Neurosci 31 2011 2756 2768
80. C. Kohler, and H. Steinbusch Identification of serotonin and non-serotonin-containing neurons of the mid-brain raphe projecting to the entorhinal area and the hippocampal formation. A combined immunohistochemical and fluorescent retrograde tracing study in the rat brain Neuroscience 7 1982 951 975 (Pubitemid 12122247)
81. S. Kollack-Walker, and S.W. Newman Mating-induced expression of c-fos in the male Syrian hamster brain: role of experience, pheromones, and ejaculations J Neurobiol 32 1997 481 501 (Pubitemid 27172934)
82. Y. Kondo, A. Shinoda, K. Yamanouchi, and Y. Arai Role of septum and preoptic area in regulating masculine and feminine sexual behavior in male rats Horm Behav 24 1990 421 434 (Pubitemid 20319017)
83. B.E. Kosofsky, and M.E. Molliver The serotoninergic innervation of cerebral cortex: different classes of axon terminals arise from dorsal and median raphe nuclei Synapse 1 1987 153 168 (Pubitemid 17119662)
84. P.J. Larsen, A. Hay-Schmidt, N. Vrang, and J.D. Mikkelsen Origin of projections from the midbrain raphe nuclei to the hypothalamic paraventricular nucleus in the rat: a combined retrograde and anterograde tracing study Neuroscience 70 1996 963 988 (Pubitemid 26014860)
85. E. Le Poul, N. Laaris, E. Doucet, A.M. Laporte, M. Hamon, and L. Lanfumey Early desensitization of somato-dendritic 5-HT1A autoreceptors in rats treated with fluoxetine or paroxetine Naunyn Schmiedebergs Arch Pharmacol 352 1995 141 148
86. J.E. LeDoux, D.A. Ruggiero, and D.J. Reis Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat J Comp Neurol 242 1985 182 213 (Pubitemid 16208466)
87. J.E. LeDoux, A. Sakaguchi, J. Iwata, and D.J. Reis Auditory emotional memories: establishment by projections from the medial geniculate nucleus to the posterior neostriatum and/or dorsal amygdala Ann N Y Acad Sci 444 1985 463 464
88. J.E. LeDoux, D.A. Ruggiero, R. Forest, R. Stornetta, and D.J. Reis Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat J Comp Neurol 264 1987 123 146 (Pubitemid 17147831)
89. R.L. Lee, E.R. Smith, M. Mas, and J.M. Davidson Effects of intrathecal administration of 8-OH-DPAT on genital reflexes and mating behavior in male rats Physiol Behav 47 1990 665 669 (Pubitemid 20146751)
90. Q. Li, N.A. Muma, G. Battaglia, and L.D. Van de Kar A desensitization of hypothalamic 5-HT1A receptors by repeated injections of paroxetine: reduction in the levels of G(i) and G(o) proteins and neuroendocrine responses, but not in the density of 5-HT1A receptors J Pharmacol Exp Ther 282 1997 1581 1590 (Pubitemid 27408344)
91. C. Looney, K.B. Thor, D. Ricca, and L. Marson Differential effects of simultaneous or sequential administration of paroxetine and WAY-100,635 on ejaculatory behavior Pharmacol Biochem Behav 82 2005 427 433 (Pubitemid 41827585)
92. H.P. Lorez, and J.G. Richards Supra-ependymal serotoninergic nerves in mammalian brain: morphological, pharmacological and functional studies Brain Res Bull 9 1982 727 741 (Pubitemid 13166440)
93. D.S. Lorrain, L. Matuszewich, R.D. Friedman, and E.M. Hull Extracellular serotonin in the lateral hypothalamic area is increased during the postejaculatory interval and impairs copulation in male rats J Neurosci 17 1997 9361 9366 (Pubitemid 27498462)
94. D.S. Lorrain, L. Matuszewich, and E.M. Hull 8-OH-DPAT influences extracellular levels of serotonin and dopamine in the medial preoptic area of male rats Brain Res 790 1998 217 223 (Pubitemid 28234506)
95. R.A. Lucio, J. Manzo, M. Martinez-Gomez, B.D. Sachs, and P. Pacheco Participation of pelvic nerve branches in male rat copulatory behavior Physiol Behav 55 1994 241 246 (Pubitemid 24065230)
96. I. Malagie, A. Deslandes, and A.M. Gardier Effects of acute and chronic tianeptine administration on serotonin outflow in rats: comparison with paroxetine by using in vivo microdialysis Eur J Pharmacol 403 2000 55 65
97. L.A. Mamounas, C.A. Mullen, E. O'Hearn, and M.E. Molliver Dual serotoninergic projections to forebrain in the rat: morphologically distinct 5-HT axon terminals exhibit differential vulnerability to neurotoxic amphetamine derivatives J Comp Neurol 314 1991 558 586
98. H. Marberger The mechanisms of ejaculation Basic Life Sci 4 1974 99 110
99. M. Marcinkiewicz, D. Verge, H. Gozlan, L. Pichat, and M. Hamon Autoradiographic evidence for the heterogeneity of 5-HT1 sites in the rat brain Brain Res 291 1984 159 163 (Pubitemid 14221340)
100. L. Marson, and K. Gravitt Spinal neurons activated with the urethrogenital reflex in the male rat Brain Res 1026 2004 108 115 (Pubitemid 39336421)
101. L. Marson, and K.E. McKenna A role for 5-hydroxytryptamine in descending inhibition of spinal sexual reflexes Exp Brain Res 88 1992 313 320
102. L. Marson, and K.E. McKenna Stimulation of the hypothalamus initiates the urethrogenital reflex in male rats Brain Res 638 1994 103 108
103. L. Marson, M.S. List, and K.E. McKenna Lesions of the nucleus paragigantocellularis alter ex copula penile reflexes Brain Res 592 1992 187 192
104. E. Marvin, K. Scrogin, and B. Dudas Morphology and distribution of neurons expressing serotonin 5-HT1A receptors in the rat hypothalamus and the surrounding diencephalic and telencephalic areas J Chem Neuroanat 39 2010 235 241
105. C.W. Mathes, E.R. Smith, B.R. Popa, and J.M. Davidson Effects of intrathecal and systemic administration of buspirone on genital reflexes and mating behavior in male rats Pharmacol Biochem Behav 36 1990 63 68 (Pubitemid 20165636)
106. L. Matuszewich, D.S. Lorrain, R. Trujillo, J. Dominguez, S.K. Putnam, and E.M. Hull Partial antagonism of 8-OH-DPAT'S effects on male rat sexual behavior with a D2, but not a 5-HT1A, antagonist Brain Res 820 1999 55 62 (Pubitemid 29225478)
107. L. Maxwell, D.J. Maxwell, M. Neilson, and R. Kerr A confocal microscopic survey of serotoninergic axons in the lumbar spinal cord of the rat: co-localization with glutamate decarboxylase and neuropeptides Neuroscience 75 1996 471 480 (Pubitemid 26361337)
108. K.E. McKenna, S.K. Chung, and K.T. McVary A model for the study of sexual function in anesthetized male and female rats Am J Physiol 261 1991 R1276 R1285
109. J.H. McLean, and M.T. Shipley Serotonergic afferents to the rat olfactory bulb: I. Origins and laminar specificity of serotonergic inputs in the adult rat J Neurosci 7 1987 3016 3028
110. S.D. Mendelson, and B.B. Gorzalka 5-HT1A receptors: differential involvement in female and male sexual behavior in the rat Physiol Behav 37 1986 345 351 (Pubitemid 16047517)
111. G. Mengod, R. Cortes, M.T. Vilaro, and D. Hoyer Distribution of 5-HT receptors in the central nervous system C.P. Muller, B.L. Jacobs, Handbook of the behavioral neurobiology of serotonin 2010 Elsevier Amsterdam 123 138
112. J. Mos, J. Van Logten, K. Bloetjes, and B. Olivier The effects of idazoxan and 8-OH-DPAT on sexual behaviour and associated ultrasonic vocalizations in the rat Neurosci Biobehav Rev 15 1991 505 515
113. C.P. Muller, and B.L. Jacobs Activity of brain serotonergic neurons in relation to physiology and behavior Handbook of behavioral neurobiology of serotonin 2010 Academic Press Amsterdam 153 162
114. A.Z. Murphy, and G.E. Hoffman 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 438 2001 191 212 (Pubitemid 32801219)
115. D.L. Murphy, A. Lerner, G. Rudnick, and K.P. Lesch Serotonin transporter: gene, genetic disorders, and pharmacogenetics Mol Interv 4 2004 109 123 (Pubitemid 38584973)
116. S. Nishitani, T. Moriya, Y. Kondo, Y. Sakuma, and K. Shinohara Induction of Fos immunoreactivity in oxytocin neurons in the paraventricular nucleus after female odor exposure in male rats: effects of sexual experience Cell Mol Neurobiol 24 2004 283 291 (Pubitemid 38481023)
117. J.J. Normandin, and A.Z. Murphy Serotonergic lesions of the periaqueductal gray, a primary source of serotonin to the nucleus paragigantocellularis, facilitate sexual behavior in male rats Pharmacol Biochem Behav 98 2011 369 375
118. P. Osei-Owusu, A. James, J. Crane, and K.E. Scrogin 5-Hydroxytryptamine 1A receptors in the paraventricular nucleus of the hypothalamus mediate oxytocin and adrenocorticotropin hormone release and some behavioral components of the serotonin syndrome J Pharmacol Exp Ther 313 2005 1324 1330 (Pubitemid 40727038)
119. R.G. Paredes, E. Kica, and M.J. Baum Differential effects of the serotonin1A agonist, 8-OH-DPAT, on masculine and feminine sexual behavior of the ferret Psychopharmacology (Berl) 114 1994 591 596 (Pubitemid 24152139)
120. R.G. Paredes, J.L. Contreras, and A. Ågmo Serotonin and sexual behavior in the male rabbit J Neural Transm 107 2000 767 777 (Pubitemid 30468264)
121. A. Pazos, and J.M. Palacios Quantitative autoradiographic mapping of serotonin receptors in the rat brain. I. Serotonin-1 receptors Brain Res 346 1985 205 230 (Pubitemid 16241111)
122. A. Pazos, R. Cortes, and J.M. Palacios Quantitative autoradiographic mapping of serotonin receptors in the rat brain. II. Serotonin-2 receptors Brain Res 346 1985 231 249 (Pubitemid 16241112)
123. D.W. Pfaff, A. Korotzer, S. Schwartz-Giblin, and S.L. Cottingham Hypothalamic effects on medullary reticular activation of deep back muscle EMG Physiol Behav 47 1990 185 196 (Pubitemid 20049465)
124. J.G. Pfaus, C. Marcangione, W.J. Smith, C. Manitt, and H. Abillamaa Differential induction of Fos in the female rat brain following different amounts of vaginocervical stimulation: modulation by steroid hormones Brain Res 741 1996 314 330 (Pubitemid 26426331)
125. B.V. Phillips-Farfan, and A. Fernandez-Guasti Endocrine, neural and pharmacological aspects of sexual satiety in male rats Neurosci Biobehav Rev 33 2009 442 455
126. G. Pineyro, N. Castanon, R. Hen, and P. Blier Regulation of [3H]5-HT release in raphe, frontal cortex and hippocampus of 5-HT1B knock-out mice Neuroreport 7 1995 353 359
127. S.M. Pomerantz, B.C. Hepner, and J.M. Wertz Serotonergic influences on male sexual behavior of rhesus monkeys: effects of serotonin agonists Psychopharmacology (Berl) 111 1993 47 54 (Pubitemid 23101351)
128. M. Pompeiano, J.M. Palacios, and G. Mengod Distribution and cellular localization of mRNA coding for 5-HT1A receptor in the rat brain: correlation with receptor binding J Neurosci 12 1992 440 453
129. N.K. Popova, and T.G. Amstislavskaya Involvement of the 5-HT(1A) and 5-HT(1B) serotonergic receptor subtypes in sexual arousal in male mice Psychoneuroendocrinology 27 2002 609 618 (Pubitemid 34310622)
130. J. Prins, and A.M. Krajnc The role of monoamines in the nucleus accumbens and prefrontal cortex in relation to reward and anhedonia: an intracranial self-administration and microdialysis study in rats 2013 [submitted for publication]
131. O. Rampin, F. Giuliano, P. Dompeyre, and J.P. Rousseau Physiological evidence of neural pathways involved in reflexogenic penile erection in the rat Neurosci Lett 180 1994 138 142 (Pubitemid 24333888)
132. R.C. Rosen, R.M. Lane, and M. Menza Effects of SSRIs on sexual function: a critical review J Clin Psychopharmacol 19 1999 67 85 (Pubitemid 29047334)
133. S. Saha, F.O. Gamboa-Esteves, and T.F. Batten Differential distribution of 5-HT 1A and 5-HT 1B-like immunoreactivities in rat central nucleus of the amygdala neurones projecting to the caudal dorsomedial medulla oblongata Brain Res 1330 2010 20 30
134. P.E. Sawchenko, L.W. Swanson, H.W. Steinbusch, and A.A. Verhofstad The distribution and cells of origin of serotonergic inputs to the paraventricular and supraoptic nuclei of the rat Brain Res 277 1983 355 360 (Pubitemid 13023961)
135. S.L. Schnur, E.R. Smith, R.L. Lee, M. Mas, and J.M. Davidson A component analysis of the effects of DPAT on male rat sexual behavior Physiol Behav 45 1989 897 901 (Pubitemid 19158275)
136. T. Sharp Serotonergic feedback control C.P. Muller, B.L. Jacobs, Handbook of the behavioral neurobiology of serotonin 2010 Elsevier Amsterdam 233 248
137. T. Sharp, L. Boothman, J. Raley, and P. Queree Important messages in the 'post': recent discoveries in 5-HT neurone feedback control Trends Pharmacol Sci 28 2007 629 636 (Pubitemid 350166575)
138. H. Sijbesma, J. Schipper, J.C. Cornelissen, and E.R. de Kloet Species differences in the distribution of central 5-HT1 binding sites: a comparative autoradiographic study between rat and guinea pig Brain Res 555 1991 295 304
139. R.B. Simerly, and L.W. Swanson The organization of neural inputs to the medial preoptic nucleus of the rat J Comp Neurol 246 1986 312 342 (Pubitemid 16079501)
140. G. Skagerberg, and A. Bjorklund Topographic principles in the spinal projections of serotonergic and non-serotonergic brainstem neurons in the rat Neuroscience 15 1985 445 480 (Pubitemid 15002128)
141. E.M. Snoeren, J.G. Veening, B. Olivier, and R.S. Oosting Serotonin 1A receptors and sexual behavior in female rats: a review Pharmacol Biochem Behav 2013 [accepted]
142. M. Stavy, and J. Herbert Differential effects of beta-endorphin infused into the hypothalamic preoptic area at various phases of the male rat's sexual behaviour Neuroscience 30 1989 433 442 (Pubitemid 19168493)
143. H.W. Steinbusch, and R. Nieuwenhuys Localization of serotonin-like immunoreactivity in the central nervous system and pituitary of the rat, with special references to the innervation of the hypothalamus Adv Exp Med Biol 133 1981 7 35
144. L. Svensson, and S. Hansen Spinal monoaminergic modulation of masculine copulatory behavior in the rat Brain Res 302 1984 315 321 (Pubitemid 14077760)
145. D.R. Thomas, E.M. Soffin, C. Roberts, J.N. Kew, R.M. de la Flor, and L.A. Dawson et al. SB-699551-A (3-cyclopentyl-N-[2-(dimethylamino)ethyl]-N- [(4′-{[(2-phenylethyl)amino]me thyl}-4-biphenylyl)methyl]propanamide dihydrochloride), a novel 5-HT5A receptor-selective antagonist, enhances 5-HT neuronal function: evidence for an autoreceptor role for the 5-HT5A receptor in guinea pig brain Neuropharmacology 51 2006 566 577 (Pubitemid 44215960)
146. M. Tohyama, and K. Takatsuij Atlas of neuroactive substances and their receptors in the rat 1998 Oxford University Press Oxford 44 51
147. W.A. Truitt, and L.M. Coolen Identification of a potential ejaculation generator in the spinal cord Science 297 2002 1566 1569 (Pubitemid 34971006)
148. L. Uphouse, and J. Guptarac Serotonin and sexual behavior C.P. Muller, B.L. Jacobs, Handbook of the behavioral neurobiology of serotonin 2010 Elsevier Amsterdam 347 366
149. L.D. Van de Kar, A.D. Levy, Q. Li, and M.S. Brownfield A comparison of the oxytocin and vasopressin responses to the 5-HT1A agonist and potential
150. J.G. Veening, and L.M. Coolen Neural activation following sexual behavior in the male and female rat brain Behav Brain Res 92 1998 181 193 (Pubitemid 28223589)
151. J.G. Veening, and L.M. Coolen Neural mechanismen of sexual behavior in the male rat: emphasis on ejaculation-related circuits Pharmacol Biochem Behav 2013 [under revision]
152. J.G. Veening, L.W. Swanson, W.M. Cowan, R. Nieuwenhuys, and L.M. Geeraedts The medial forebrain bundle of the rat. II. An autoradiographic study of the topography of the major descending and ascending components J Comp Neurol 206 1982 82 108 (Pubitemid 12103432)
153. R.P. Vertes A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat J Comp Neurol 313 1991 643 668
154. R.P. Vertes Serotonergic regulation of rhythmical activity in the brain, concentrating on the hippocampus C.P. Muller, B.L. Jacobs, Handbook of the behavioral neurobiology of serotonin 2010 Elsevier Amsterdam 277 292
155. R.P. Vertes, W.J. Fortin, and A.M. Crane Projections of the median raphe nucleus in the rat J Comp Neurol 407 1999 555 582 (Pubitemid 29196671)
156. A. Vicentic, Q. Li, G. Battaglia, and L.D. Van de Kar WAY-100635 inhibits 8-OH-DPAT-stimulated oxytocin, ACTH and corticosterone, but not prolactin secretion Eur J Pharmacol 346 1998 261 266 (Pubitemid 28234327)
157. C.K. Wagner, and L.G. Clemens Neurophysin-containing pathway from the paraventricular nucleus of the hypothalamus to a sexually dimorphic motor nucleus in lumbar spinal cord J Comp Neurol 336 1993 106 116 (Pubitemid 23273959)
158. R.Y. Wang, and G.K. Aghajanian Collateral inhibition of serotonergic neurones in the rat dorsal raphe nucleus: pharmacological evidence Neuropharmacology 17 1978 819 825 (Pubitemid 9100409)
159. R.Y. Wang, and G.K. Aghajanian Correlative firing patterns of serotonergic neurons in rat dorsal raphe nucleus J Neurosci 2 1982 11 16 (Pubitemid 12146054)
160. Q.P. Wang, H. Ochiai, and Y. Nakai GABAergic innervation of serotonergic neurons in the dorsal raphe nucleus of the rat studied by electron microscopy double immunostaining Brain Res Bull 29 1992 943 948
161. S.R. Wersinger, M.J. Baum, and M.S. Erskine Mating-induced FOS-like immunoreactivity in the rat forebrain: a sex comparison and a dimorphic effect of pelvic nerve transection J Neuroendocrinol 5 1993 557 568 (Pubitemid 23306608)
162. J.O. Willoughby, and W.W. Blessing Origin of serotonin innervation of the arcuate and ventromedial hypothalamic region Brain Res 418 1987 170 173 (Pubitemid 17155597)
163. Y. Yasui, T. Kayahara, K. Nakano, and N. Mizuno The subparafascicular thalamic nucleus of the rat receives projection fibers from the inferior colliculus and auditory cortex Brain Res 537 1990 323 327
164. Y. Yasui, C.B. Saper, and D.F. Cechetto Calcitonin gene-related peptide (CGRP) immunoreactive projections from the thalamus to the striatum and amygdala in the rat J Comp Neurol 308 1991 293 310
165. Y. Yasui, K. Nakano, and N. Mizuno Descending projections from the subparafascicular thalamic nucleus to the lower brain stem in the rat Exp Brain Res 90 1992 508 518
166. D.P. Yells, S.E. Hendricks, and M.A. Prendergast Lesions of the nucleus paragigantocellularis: effects on mating behavior in male rats Brain Res 596 1992 73 79
167. Y. Zhang, T.S. Gray, D.N. D'Souza, G.A. Carrasco, K.J. Damjanoska, and B. Dudas et al. Desensitization of 5-HT1A receptors by 5-HT2A receptors in neuroendocrine neurons in vivo J Pharmacol Exp Ther 310 2004 59 66 (Pubitemid 38812695)