A role for preoptic glutamate in the regulation of male reproductive behavior

Neuroscientist

Volumn 15, Issue 1, 2009, Pages 11-19

  Dominguez, Juan M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Endocrine; Glutamate; Limbic; NMDA receptor; Preoptic area; Reproduction

Indexed keywords

GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN FOS;

BRAIN CELL; COPULATION; EJACULATION; EVENING DOSAGE; HISTOLOGY; HUMAN; MATING; MEDIAL PREOPTIC AREA; MICRODIALYSIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SEXUAL BEHAVIOR;

ANIMALS; GLUTAMIC ACID; HUMANS; MALE; PREOPTIC AREA; REPRODUCTION; SEXUAL BEHAVIOR; SEXUAL BEHAVIOR, ANIMAL;

EID: 59149091939     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858408322679     Document Type: Review

References (117)

1. Arendash GW, Gorski RA 1983. Effects of discrete lesions of the sexually dimorphic nucleus of the preoptic area or other medial preoptic regions on the sexual behavior of male rats. Brain Res Bull 10: 147-54.
2. Ball GF, Balthazart J. 2007. How useful is the appetitive and consummatory distinction for our understanding of the neuroendocrine control of sexual behavior ? Horm Behav 51: 569-78.
3. Balthazart J., Baillien M., Ball GF 2001. Rapid and reversible inhibition of brain aromatase activity. J Neuroendocrinol 13: 63-73.
4. Balthazart J., Baillien M., Ball GF 2006. Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinology 147: 359-66.
5. Balthazart J., Baillien M., Charlier TD, Ball GF 2003. Calcium-dependent phosphorylation processes control brain aromatase in quail. Eur J Neurosci 17: 1591-606.
6. Balthazart J., Ball GF 2006. Is brain estradiol a hormone or a neurotransmitter ? Trends Neurosci 29: 241-9.
7. Balthazart J., Ball GF 2007. Topography in the preoptic region: differential regulation of appetitive and consummatory male sexual behaviors. Front Neuroendocrinol 28: 161-78 ; Epub 2007 Jun 8.
8. Baum MJ, Everitt BJ 1992. 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: 627-46.
9. Beach FA 1944. Relative effects of androgen upon the mating behavior of male rats subjected to forebrain injury or castration. J Exp Zool 97: 249-85.
10. Beach FA, Holz-Tucker A. 1949. Effects of different concentrations of androgens upon sexual behavior in castrated male rats. J Comp Physiol Psychol 42: 433-53.
11. Bialy M., Rydz M., Kaczmarek L. 2000. Precontact 50-kHz vocalizations in male rats during acquisition of sexual experience. Behav Neurosci 114: 983-90.
12. Bressler SC, Baum MJ 1996. Sex comparison of neuronal Fos immunoreactivity in the rat vomeronasal projection circuit after chemosensory stimulation. Neuroscience 71: 1063-72.
13. Brudzynski SM, Pniak A. 2002. Social contacts and production of 50-kHz short ultrasonic calls in adult rats. J Comp Psychol 116: 73-82.
14. Can A., Domjan M., Delville Y. 2007. Sexual experience modulates neuronal activity in male Japanese quail. Horm Behav 52: 590-9.
15. Cantor JM, Binik YM, Pfaus JG 1999. Chronic fluoxetine inhibits sexual behavior in the male rat: reversal with oxytocin. Psychopharmacology (Berl) 144: 355-62.
16. Carey RJ, Dai H., Gui J. 1998. Effects of dizocilpine (MK-801) on motor activity and memory. Psychopharmacology (Berl) 137: 241-6.
17. Carlsson ML, Carlsson A., Nilsson M. 2004. Schizophrenia: from dopamine to glutamate and back. Curr Med Chem 11: 267-77.
18. Chen L., Huang LY 1992. Protein kinase C reduces Mg2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356: 521-3.
19. Choi DW 1988. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1: 623-34.
20. Coolen LM, Peters HJ, Veening JG 1996. Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison. Brain Res 738: 67-82.
21. Cornil CA, Taziaux M., Baillien M., Ball GF, Balthazart J. 2006. Rapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail. Horm Behav 49: 45-67.
22. Curtis DR, Watkins JC 1960. The excitation and depression of spinal neurones by structurally related amino acids. J Neurochem 6: 117-41.
23. Danbolt NC 2001. Glutamate uptake. Prog Neurobiol 65: 1-105.
24. Davidson JM 1966. Characteristics of sex behaviour in male rats following castration. Anim Behav 14: 266-72.
25. Davidson JM, Camargo CA, Smith ER 1979. Effects of androgen on sexual behavior in hypogonadal men. J Clin Endocrinol Metab 48: 955-8.
26. Davidson JM, Kwan M., Greenleaf WJ 1982. Hormonal replacement and sexuality in men. Clin Endocrinol Metab 11: 599-623.
27. de Bartolomeis A., Fiore G., Iasevoli F. 2005. Dopamineglutamate interaction and antipsychotics mechanism of action: implication for new pharmacological strategies in psychosis. Curr Pharm Des 11: 3561-94.
28. Dewsbury DA 1969. Copulatory behaviour of rats (Rattus norvegicus) as a function of prior copulatory experience. Anim Behav 17: 217-23.
29. Dingledine R., Borges K., Bowie D., Traynelis SF 1999. The glutamate receptor ion channels. Pharmacol Rev 51: 7-61.
30. Dominguez J., Riolo JV, Xu Z., Hull EM 2001. Regulation by the medial amygdala of copulation and medial preoptic dopamine release. J Neurosci 21: 349-55.
31. Dominguez JM, Balfour ME, Coolen LM 2003. Copulation-induced activation of NMDA receptor containing neurons in the medial preoptic nucleus. Horm Behav 44: 46.
32. Dominguez JM, Balfour ME, Lee HS, Brown JL, Davis BA, Coolen LM 2007. Mating activates NMDA receptors in the medial preoptic area of male rats. Behav Neurosci 121: 1023-31.
33. Dominguez JM, Brann JH, Gil M., Hull EM 2006. Sexual experience increases nitric oxide synthase in the medial preoptic area of male rats. Behav Neurosci 120: 1389-94.
34. Dominguez JM, Gil M., Brann JH, Hull EM 2005. Serotonin inhibits mating-induced glutamate activity in the medial preoptic area: implications for impaired libido resulting from SSRIs [abstract]. Neuropsychopharmacology 30 (Suppl): S106.
35. Dominguez JM, Gil M., Hull EM 2006. Preoptic glutamate facilitates male sexual behavior. J Neurosci 26: 1699-703.
36. Dominguez JM, Hull EM 2001. Stimulation of the medial amygdala enhances medial preoptic dopamine release: implications for male rat sexual behavior. Brain Res 917: 225-9.
37. Dominguez JM, Hull EM 2005. Dopamine, the medial preoptic area, and male sexual behavior. Physiol Behav 86: 356-68.
38. Dominguez JM, Muschamp JW, Schmich JM, Hull EM 2004. Nitric oxide mediates glutamate-evoked dopamine release in the medial preoptic area. Neuroscience 125: 203-10.
39. Fisher AE 1956. Maternal and sexual behavior induced by intracranial chemical stimulation. Science 124: 228-9.
40. Forrest D., Yuzaki M., Soares HD, Ng L., Luk DC, Sheng M., and others. 1994. Targeted disruption of NMDA receptor 1 gene abolishes NMDA response and results in neonatal death. Neuron 13: 325-38.
41. Ghosh A., Ginty DD, Bading H., Greenberg ME 1994. Calcium regulation of gene expression in neuronal cells. J Neurobiol 25: 294-303.
42. Gill CJ, Wersinger SR, Veney SL, Rissman EF 1998. Induction of fos-like immunoreactivity in musk shrews after mating. Brain Res 811: 21-8.
43. Giuliano F. 2007. 5-Hydroxytryptamine in premature ejaculation: opportunities for therapeutic intervention. Trends Neurosci 30: 79-84.
44. Giuliano F., Rampin O., Brown K., Courtois F., Benoit G., Jardin A. 1996. Stimulation of the medial preoptic area of the hypothalamus in the rat elicits increases in intracavernous pressure. Neurosci Lett 209: 1-4.
45. Hamed S., Mohamed K., El- Taher A., Hamed E., Omar H. 2006. The sexual and reproductive health in men with generalized epilepsy: a multidisciplinary evaluation. Int J Impot Res 18: 287-95.
46. Heeb MM, Yahr P. 1996. 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: 1049-71.
47. Heimer L., Larsson K. 1966 /67. Impairment of mating behavior in male rats following lesions in the preoptic-anterior hypothalamic continuum. Brain Res 3: 248-63.
48. Hull EM, Bitran D., Pehek EA, Warner RK, Band LC, Holmes GM 1986. Dopaminergic control of male sex behavior in rats: effects of an intracerebrally-infused agonist. Brain Res 370: 73-81.
49. Hull EM, Dominguez JM 2003. Sex behavior. In: Gallagher M, Nelson RJ, Weiner IB, editors. Handbook of psychology, biological psychology. Hoboken: Wiley. p 321-53.
50. Hull EM, Dominguez JM 2006. Getting his act together: roles of glutamate, nitric oxide, and dopamine in the medial preoptic area. Brain Res 1126: 66-75.
51. Hull EM, Dominguez JM, Muschamp JW 2007. Neurochemical mediators of male sexual behavior. In: Lajtha A, Blaustein J, editors. Handbook of neurochemistry and molecular biology. 3 rd ed. New York: Springer. p 37-94.
52. Hull EM, Du J., Lorrain DS, Matuszewich L. 1995. Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation. J Neurosci 15: 7465-71.
53. Hull EM, Lorrain DS, Du J., Matuszewich L., Lumley LA, Putnam SK, and others. 1999. Hormone-neurotransmitter interactions in the control of sexual behavior. Behav Brain Res 105: 105-16.
54. Hull EM, Meisel RL, Sachs BD 2002. Male sexual behavior. In: Rubin RT, editor. Hormones, brain and behavior. San Diego: Academic Press. p 3-137.
55. Hull EM, Muschamp JW, Sato S. 2004. Dopamine and serotonin: influences on male sexual behavior. Physiol Behav 83: 291-307.
56. Hull EM, Wood RI, McKenna KE 2006. The neurobiology of male sexual behavior. In: Neill J, Pfaff, D, editors. The physiology of reproduction. New York: Elsevier. p 1729-824.
57. Kelliher KR, Liu YC, Baum MJ, Sachs BD 1999. Neuronal Fos activation in olfactory bulb and forebrain of male rats having erections in the presence of inaccessible estrous females. Neuroscience 92: 1025-33.
58. Kendrick KM, Drewett RF 1979. Testosterone reduces refractory period of stria terminalis neurons in the rat brain. Science 204 (4395). 877-9.
59. Kocsis K., Kiss J., Csaki A., Halasz B. 2003. Location of putative glutamatergic neurons projecting to the medial preoptic area of the rat hypothalamus. Brain Res Bull 61: 459-68.
60. Kollack-Walker S., Newman SW 1997. Mating-induced expression of c-fos in the male Syrian hamster brain: role of experience, pheromones, and ejaculations. J Neurobiol 32: 481-501.
61. Lange KW, Kornhuber J., Riederer P. 1997. Dopamine/glutamate interactions in Parkinson's disease. Neurosci Biobehav Rev 21: 393-400.
62. Larsson K. 1959. Experience and maturation in the development of sexual behavior in the male puberty rat. Behaviour 14: 101-7.
63. Larsson K. 1978. Experiential factors in the development of sexual behavior. In: Hutchison JB, editor. Biological determinants of sexual behaviour. New York: Wiley & Sons. p 55-86.
64. Larsson K., Heimer L. 1964. Mating behaviour of male rats after lesions in the preoptic area. Nature 202: 413-4.
65. LeDoux JE 2000. Emotion circuits in the brain. Annu Rev Neurosci 23: 155-84.
66. Lorrain DS, Riolo JV, Matuszewich L., Hull EM 1999. Lateral hypothalamic serotonin inhibits nucleus accumbens dopamine: implications for sexual satiety. J Neurosci 19: 7648-52.
67. Lumley LA, Hull EM 1999. Effects of a D1 antagonist and of sexual experience on copulation-induced Fos-like immunoreactivity in the medial preoptic nucleus. Brain Res 829: 55-68.
68. Mahesh VB, Brann DW 2005. Regulatory role of excitatory amino acids in reproduction. Endocrine 28: 271-80.
69. Malenka RC, Nicoll RA 1999. Long-term potentiation-a decade of progress ? Science 285: 1870-4.
70. Malsbury CW 1971. Facilitation of male rat copulatory behavior by electrical stimulation of the medial preoptic area. Physiol Behav 7: 797-805.
71. Markowski VP, Eaton RC, Lumley LA, Moses J., Hull EM 1994. A D1 agonist in the MPOA facilitates copulation in male rats. Pharmacol Biochem Behav 47: 483-6.
72. Marson L., McKenna KE 1994. Stimulation of the hypothalamus initiates the urethrogenital reflex in male rats. Brain Res 638: 103-8.
73. Martin SJ, Grimwood PD, Morris RG 2000. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23: 649-711.
74. McEwen BS, Davis PG, Parsons B., Pfaff DW 1979. The brain as a target for steroid hormone action. Annu Rev Neurosci 2: 65-112.
75. Meltzer LT, Christoffersen CL, Serpa KA 1997. Modulation of dopamine neuronal activity by glutamate receptor subtypes. Neurosci Biobehav Rev 21: 511-8.
76. Miserendino MJ, Sananes CB, Melia KR, Davis M. 1990. Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature 345: 716-8.
77. Moghaddam B., Wolf ME 2003. Glutamate and disorders of cognition and motivation. New York: New York Academy of Sciences.
78. Montouris G., Morris GL 3rd. 2005. Reproductive and sexual dysfunction in men with epilepsy. Epilepsy Behav 7 (Suppl 2). S7-14.
79. Morelli M. 1997. Dopamine/glutamate interaction as studied by combining turning behaviour and c-Fos expression. Neurosci Biobehav Rev 21: 505-9.
80. Nordeen KW 1997. Neural correlates of sensitive periods in avian song learning. Ann N Y Acad Sci 807: 386-400.
81. Oomura Y., Aou S., Koyama Y., Fujita I., Yoshimatsu H. 1988. Central control of sexual behavior. Brain Res Bull 20: 863-70.
82. Ozawa S., Kamiya H., Tsuzuki K. 1998. Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54: 581-618.
83. Pehek EA, Thompson JT, Eaton RC, Bazzett TJ, Hull EM 1988. Apomorphine and haloperidol, but not domperidone, affect penile reflexes in rats. Pharmacol Biochem Behav 31: 201-8.
84. Pehek EA, Warner RK, Bazzett TJ, Bitran D., Band LC, Eaton RC, and others. 1988. Microinjection of cis-flupenthixol, a dopamine antagonist, into the medial preoptic area impairs sexual behavior of male rats. Brain Res 443: 70-6.
85. Pfaus JG 1999. Revisiting the concept of sexual motivation. Annu Rev Sex Res 10: 120-56.
86. Pfaus JG, Heeb MM 1997. Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Res Bull 44: 397-407.
87. Pfaus JG, Mendelson SD, Phillips AG 1990. A correlational and factor analysis of anticipatory and consummatory measures of sexual behavior in the male rat. Psychoneuroendocrinology 15: 329-40.
88. Powell WS, Dominguez JM, Hull EM 2003. An NMDA antagonist impairs copulation and the experience-induced enhancement of male sexual behavior in the rat. Behav Neurosci 117: 69-75.
89. Robertson GS, Pfaus JG, Atkinson LJ, Matsumura H., Phillips AG, Fibiger HC 1991. Sexual behavior increases c-fos expression in the forebrain of the male rat. Brain Res 564: 352-7.
90. Rodriguez-Manzo G., Pellicer F., Larsson K., Fernandez-Guasti A. 2000. Stimulation of the medical preoptic area facilitates sexual behavior but does not reverse sexual satiation. Behav Neurosci 114: 553-60.
91. Sachs BD 2007 a. A contextual definition of male sexual arousal. Horm Behav 51: 569-78.
92. Sachs BD 2007 b. The appetitive-consummatory distinction: is this 100-year-old baby worth saving? Reply to Ball and Balthazart. Horm Behav 2007 ; Epub ahead of print Dec 4.
93. Scaletta LL, Hull EM 1990. Systemic or intracranial apomorphine increases copulation in long-term castrated male rats. Pharmacol Biochem Behav 37: 471-5.
94. Schmidt WJ 1998. Dopamine-glutamate interactions in the basal ganglia. Amino Acids 14: 5-10.
95. Segraves RT 2007. Sexual dysfunction associated with antidepressant therapy. Urol Clin North Am 34: 575-9, vii.
96. Sesack SR, Carr DB, Omelchenko N., Pinto A. 2003. Anatomical substrates for glutamate-dopamine interactions: evidence for specificity of connections and extrasynaptic actions. Ann N Y Acad Sci 1003: 36-52.
97. Shimura T., Yamamoto T., Shimokochi M. 1994. 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 Res 640: 215-22.
98. Simerly RB, Swanson LW 1986. The organization of neural inputs to the medial preoptic nucleus of the rat. J Comp Neurol 246: 312-42.
99. Simerly RB, Swanson LW 1988. Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterograde tract-tracing study in the rat. J Comp Neurol 270: 209-42.
100. Simmons DA, Yahr P. 2003. GABA and glutamate in mating-activated cells in the preoptic area and medial amygdala of male gerbils. J Comp Neurol 459: 290-300.
101. Smaldone M., Sukkarieh T., Reda A., Khan A. 2004. Epilepsy and erectile dysfunction: a review. Seizure 13: 453-9.
102. Stone CP 1939. Copulatory activity in adult male rats following castration and injection of testosterone proprionate. Endocrinology 69: 373-380.
103. Sukoff Rizzo SJ, Schechter LE, Rosenzweig-Lipson S. 2008. A novel approach for predicting antidepressant-induced sexual dysfunction in rats. Psychopharmacology (Berl) 195: 459-67.
104. Swanson LW 2004. Brain maps: structure of the rat brain. San Diego: Elsevier.
105. Taziaux M., Cornil CA, Dejace C., Arckens L., Ball GF, Balthazart J. 2006. Neuroanatomical specificity in the expression of the immediate early gene c-fos following expression of appetitive and consummatory male sexual behaviour in Japanese quail. Eur J Neurosci 23: 1869-87.
106. Tingley WG, Ehlers MD, Kameyama K., Doherty C., Ptak JB, Riley CT, and others. 1997. Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J Biol Chem 272: 5157-66.
107. Van De Poll NE, Van Dis H. 1979. The effect of medial preoptic-anterior hypothalamic lesions on bisexual behavior of the male rat. Brain Res Bull 4: 505-11.
108. Vaughan E., Fisher AE 1962. Male sexual behavior induced by intracranial electrical stimulation. Science 137: 758-60.
109. Veening JG, Coolen LM 1998. Neural activation following sexual behavior in the male and female rat brain. Behav Brain Res 92: 181-93.
110. Warner RK, Thompson JT, Markowski VP, Loucks JA, Bazzett TJ, Eaton RC, and others. 1991. Microinjection of the dopamine antagonist cis-flupenthixol into the MPOA impairs copulation, penile reflexes and sexual motivation in male rats. Brain Res 540: 177-82.
111. Watkins JC 1986. Twenty-five years of excitatory amino acid research. The end of the beginning? In: Roberts PJ, Storm-Mathisen J, Bradford HF, editors. Excitatory amino acids. London: Macmillan. p 1-39.
112. Westerman AT, Roma PG, Dominguez JM 2007. The antiepileptic primidone impairs male sexual behavior. Poster session presented at the 37th Annual Meeting of the Society for Neuroscience, San Diego, CA.
113. Wood RI 1997. Thinking about networks in the control of male hamster sexual behavior. Horm Behav 32: 40-5.
114. Wood RI, Newman SW 1993. Mating activates androgen receptor-containing neurons in chemosensory pathways of the male Syrian hamster brain. Brain Res 614: 65-77.
115. Wood RI, Newman SW 1995. Hormonal influence on neurons of the mating behavior pathway in male hamsters. In: Micevych PE, Hammer RPJ, editors. Neurobiological effects of sex steroid hormones. Cambridge: Cambridge University Press. p 3-39.
116. Woodrum ST, Brown CS 1998. Management of SSRI-induced sexual dysfunction. Ann Pharmacother 32: 1209-15.
117. Zheng F., Gingrich MB, Traynelis SF, Conn PJ 1998. Tyrosine kinase potentiates NMDA receptor currents by reducing tonic zinc inhibition. Nat Neurosci 1: 185-91.