Vaginocervical stimulation induces Fos in glutamate neurons in the ventromedial hypothalamus: Attenuation by estrogen and progesterone

Hormones and Behavior

Volumn 56, Issue 4, 2009, Pages 450-456

  Georgescu, Michaela ^a   Sabongui, Camille ^a   Del Corpo, Adina ^a   Marsan, Lina ^a   Pfaus, James G ^a  

^a and Applied Physiology   (Canada)

Author keywords

Female rat; Genitosensory stimulation; Inhibition; Sexual behavior

Indexed keywords

ESTRADIOL BENZOATE; ESTROGEN; GLUTAMATE RECEPTOR AGONIST; GLUTAMIC ACID; PROGESTERONE; PROTEIN FOS; SEX HORMONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FACILITATION; FEMALE; HORMONE ACTION; HORMONE RESPONSE; HYPOTHALAMUS; NERVE CELL; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SEXUAL BEHAVIOR; SEXUALITY;

ANIMALS; CELL COUNT; CERVIX UTERI; ESTRADIOL; ESTROGENS; FEMALE; GLUTAMIC ACID; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; NEURONS; OVARIECTOMY; PHYSICAL STIMULATION; PROGESTERONE; PROTO-ONCOGENE PROTEINS C-FOS; RANDOM ALLOCATION; RATS; RATS, LONG-EVANS; VAGINA;

EID: 70349747282     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2009.07.014     Document Type: Article

References (80)

1. Acosta-Martinez M., and Etgen A.M. The role of delta-opioid receptors in estrogen facilitation of lordosis behavior. Behav. Brain Res. 136 (2002) 93-102
2. Acosta-Martinez M., and Etgen A.M. Activation of mu-opioid receptors inhibits lordosis in estrogen and progesterone-primed female rats. Horm. Behav. 41 (2002) 88-100
3. Adamec R.E. Partial kindling of the ventral hippocampus: identification of changes in limbic physiology which accompany changes in feline aggression and defense. Physiol. Behav. 49 (1991) 443-453
4. Adler N.T., and Toner J.P. The effects of copulatory behaviour on sperm transport and fertility in rats. In: Komisaruk B.R., et al. (Ed). Reproduction: A Behavioural and Neuroendocrine Perspective (1986), New York Academy of Sciences Press, New York 21-32
5. Allen, T.O., Adler, N.T., Greenberg, J.H., Reivich, M., 1981. Vaginocervical stimulation selectively increases metabolic activity in the rat brain. Science 211, 1070-1072.
6. Auger, A.P., Blaustein, J.D., 1995. Progesterone enhances and estradiol-induced increase in Fos immunoreactivity in localized regions of the female rat forebrain. J. Neurosci. 15, 2272-2279.
7. Auger A.P., Moffatt C.A., and Blaustein J.D. Reproductively-relevant stimuli induce Fos-immunoreactivity within progestin-receptor containing neurons in localized regions of female rat forebrain. J. Neuroendocrinol. 8 (1996) 831-838
8. Ban T. Fiber connections in the hypothalamus and some autonomic functions. Pharmacol. Biochem. Behav. 3 Suppl. 1 (1975) 3-13
9. Blake, C.A., Sawyer C.H., 1972. Effects of vaginal stimulation on hypothalamic multiple-unit activity and pituitary LH release in the rat. Neuroendocrinology 10, 358-370.
10. Borszcz G.S. Contribution of the ventromedial hypothalamus to generation of the affective dimension of pain. Pain 123 (2006) 155-168
11. Bray G.A., and York D.A. The MONA LISA hypothesis in the time of leptin. Recent Prog. Horm. Res. 53 (1998) 95-117
12. Brayley K.N., and Albert D.J. Suppression of VMH-lesion-induced reactivity and aggressiveness by electrical stimulation ventral to the anterior septum in the rat. Physiol. Behav. 18 (1977) 567-571
13. Connor M., and Christie M.D. Opioid receptor signaling mechanisms. Clin. Exp. Pharmacol. Physiol. 16 (1999) 493-499
14. Coopersmith C., Candurra C., and Erskine M.S. Effects of paced mating and intromissive stimulation on feminine sexual behavior and estrus termination in the cycling rat. J. Comp. Psychol. 110 (1996) 176-186
15. Coria-Avila G.A., and Pfaus J.G. Neuronal activation by stimuli that predict sexual reward in female rats. Neuroscience 148 (2007) 623-632
16. Coria-Avila G.A., Ouimet A.J., Pacheco P., Manzo J., and Pfaus J.G. Olfactory conditioned partner preference in the female rat. Behav. Neurosci. 119 (2005) 716-725
17. Coria-Avila G.J., Jones S.L., Solomon C.E., Gavrila A.M., Jordan G.J., and Pfaus J.G. Conditioned partner preference in female rats for strain of male. Physiol. Behav. 88 (2006) 529-537
18. Dafney N., and Terkel J. Hypothalamic neuronal activity associated with onset of pseudopregnancy in the rat. Neuroendocrinology 51 (1990) 459-467
19. Dai J., Van Der Vliet J., Swaab D.F., and Buijs R.M. Postmortem anterograde tracing of intrahypothalamic projections of the human dorsomedial nucleus of the hypothalamus. J. Comp. Neurol. 401 (1998) 16-33
20. Dai Y., Moriyama T., Higashi T., Togashi K., Kobayashi K., Yamanaka H., Tominaga M., and Noguchi K. Proteinase-activated receptor 2-mediated potentiation of transient receptor potential vanilloid subfamily 1 activity reveals a mechanism for proteinase-induced inflammatory pain. J. Neurosci. 24 (2004) 4293-4299
21. Delorey T.M., and Olsen R.W. GABA and glycine. In: Siegel G.J., Agranoff B.W., Albers R.W., and Molinoff P.B. (Eds). Basic Neurochemistry. 5th ed. (1994), Raven, New York 389-399
22. Edmonds S., Zoloth S.R., and Adler N.T. Storage of copulatory stimulation in the female rat. Physiol. Behav. 8 (1972) 161-164
23. Emery D.E., and Moss R.L. Lesions confined to the ventromedial hypothalamus decrease the frequency of coital contacts in female rats. Horm. Behav. 18 (1984) 313-329
24. Erskine M.S. Effects of paced coital stimulation on estrus duration in intact cycling rats and in ovariectomized and ovariectomized-adrenalectomized hormone-primed rats. Behav. Neurosci. 99 (1985) 151-161
25. Erskine M.S., and Baum M.J. Effects of paced coital stimulation on termination of estrus and brain indoleamine levels in female rats. Pharmacol. Biochem. Behav. 17 (1982) 857-861
26. Erskine M.S., and Hanrahan S.B. Effects of paced mating on c-fos gene expression in the female rat brain. J. Neuroendocrinol. 9 (1997) 903-912
27. Etgen A.M. Inhibition of estrus behavior in rats by intrahypothalamic application of agents that disrupt nuclear binding of estrogen-receptor complexes. Horm. Behav. 21 (1987) 528-535
28. Fahrbach S.E., Morrell J.I., and Pfaff D.W. Studies of ventromedial hypothalamic afferents in the rat using three methods of HRP application. Exp. Brain Res. 77 (1989) 221-233
29. Frye C.A., and Erskine M.S. Influence of time of mating and paced copulation on induction of pseudopregnancy in cyclic female rats. J. Reprod. Fertil. 90 (1990) 375-385
30. Frye C.A., and Duncan J.E. Progesterone metabolites, effective at the GABA A receptor complex, attenuate pain sensitivity in rats. Brain Res. 643 (1994) 194-203
31. García Horsman S.P., Ågmo A., and Paredes R.G. Infusions of naloxone into the medial preoptic area, ventromedial hypothalamus, and amygdala block conditioned place preference induced by paced mating behavior. Horm. Behav. 54 (2008) 709-716
32. Georgescu M., and Pfaus J.G. Role of glutamate receptors in the ventromedial hypothalamus in the regulation of female rat sexual behaviors. I. Behavioral effects of glutamate and its selective receptor agonists AMPA, NMDA and kainate. Pharmacol. Biochem. Behav. 83 (2006) 322-332
33. Georgescu M., and Pfaus J.G. Role of glutamate receptors in the ventromedial hypothalamus in the regulation of female rat sexual behaviors. II. Behavioral effects of selective glutamate receptor antagonists AP-5, CNQX, and DNQX. Pharmacol. Biochem. Behav. 83 (2006) 333-341
34. Gold R.M., Quackenbush P.M., and Kapatos G. Obesity following combination of rostrolateral VMH cut and contralateral mammillary area lesion. J. Comp. Physiol. Psychol. 79 (1972) 210-218
35. Harlan R.E., Shivers B.D., and Pfaff D.W. Estrogenic maintenance of lordotic responsiveness: requirement for hypothalamic action potentials. Brain Res. 268 (1983) 67-78
36. Hennessey A.C., Camak L., Gordon F., and Edwards D.A. Connections between the pontine central grey and ventromedial hypothalamus are essential for lordosis in female rats. Behav. Neurosci. 104 (1990) 477-488
37. Konorski J. Integrative Activity of the Brain (1967), University of Chicago Press, Chicago
38. Kornberg E., and Erskine M.S. Effects of differential mating stimulation on the onset of prolactin surges in pseudopregnant rats. Psychoneuroendocrinology 19 (1994) 357-371
39. Kow L.M., Halan R.E., Shivers B.D., and Pfaff D.W. Inhibition of the lordosis reflex in rats by intrahypothalamic infusion of neural excitatory agents: evidence that the hypothalamus contains separate inhibitory and facilitory elements. Brain Res. 341 (1985) 26-34
40. Lauber A., Romano G.J., Mobbs C.V., Howells R.D., and Pfaff D.W. Estradiol induction of proenkephalin messenger RNA in hypothalamus: dose-response and relation to reproductive behavior in the female rat. Brain Res. Mol. Brain Res. 8 (1990) 47-54
41. Lehmann M.L., and Erskine M.J. Induction of pseudopregnancy using artificial VCS: importance of lordosis intensity and prestimulus estrous cycle length. Horm. Behav. 45 (2004) 75-83
42. Lodder J., and Zeilmaker G.H. Role of pelvic nerves in postcopulatory abbreviation of behavioral estrus in female rats. J. Comp. Physiol. Psychol. 90 (1976) 925-929
43. MacLusky N.J., and McEwen B.S. OE modulates progestin receptor concentrations in some rat brain regions but not in others. Nature 274 (1978) 276-278
44. MacLusky N.J., and McEwen B.S. Progestin receptors in rat brain: distribution and properties of cytoplasmic progestin-binding sites. Endocrinology 106 (1980) 192-202
45. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., and Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232 (1986) 1004-1007
46. Malsbury C.A., Kow L.-M., and Pfaff D.W. Effects of medial hypothalamic lesions on the lordosis response and other behaviors in female golden hamsters. Physiol. Behav. 19 (1977) 223-237
47. Martinez I., and Paredes R.G. Only self-paced mating is rewarding in rats of both sexes. Horm. Behav. 40 (2001) 510-517
48. Mathews D., and Edwards D.A. The ventromedial nucleus of the hypothalamus and the hormonal arousal of sexual behaviors in the female rat. Horm. Behav. 8 (1977) 40-51
49. Marshall N.B., Barrnett R.J., and Mayer J. Hypothalamic lesions in goldthioglucose injected mice. Proc. Soc. Exp. Biol. Med. 90 (1955) 240-244
50. McCarthy, M.M., Malik, K.F., Feder, H.H., 1990. Increased GABAergic transmission in medial hypothalamus facilitates lordosis but has the opposite effect in preoptic area. Brain Res. 507, 40-44.
51. McCarthy M.M., Curran G.H., and Feder H.H. Excitatory amino acid modulation of lordosis in the rat. Neurosci. Lett. 126 (1991) 94-97
52. McCarthy, M.M., Masters, D.B., Rimvall, K., Schwartz-Giblin, S., Pfaff, D.W., 1994. Intracerebral administration of antisense oligodeoxynucleotides to GAD65 and GAD67 mRNAs modulate reproductive behavior in the female rat. Brain Res. 636, 209-220.
53. McCarthy M.M., Kaufman L.C., Brooks P.J., and Pfaff D.W. E modulation of mRNA levels for the two forms of glutamic acid decarboxylase (GAD) in female rat brain. J. Comp. Neurol. 360 (1995) 685-697
54. Meisel R.L., and Pfaff D.W. Specificity and neural sites of action of anisomycin in the reduction of facilitation of female sexual behavior in rats. Horm. Behav. 19 (1985) 237-251
55. Paredes R.G., and Alonso A. Sexual behavior regulated (paced) by the female induces conditioned place preference. Behav. Neurosci. 111 (1997) 123-128
56. Paredes R.G., and Vazquez B. What do female rats like about sex? Paced mating. Behav. Brain Res. 105 (1999) 117-127
57. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. 4th ed. (1998), Academic Press, San Diego
58. Pfaff D.W. Estrogens and Brain Function (1980), Springer-Verlag, New York
59. Pfaff D.W. Drive: Neurobiological and Molecular Mechanisms of Sexual Motivation (1999), MIT Press, Cambridge, MA
60. Pfaff D.W., and Keiner M. Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J. Comp. Neurol. 151 (1973) 121-158
61. Pfaff D.W., Schwartz-Giblin S., McCarthy M.M., and Kow L.-M. Cellular and molecular mechanisms of female reproductive behaviors. In: Knobil E., et al. (Ed). The Physiology of Reproduction (2nd Ed) 2 (1994), Raven Press, New York 107-220
62. Pfaus J.G., Kleopoulos S.P., Mobbs C.V., Gibbs R.B., and Pfaff D.W. Sexual stimulation activates c-fos within estrogen concentrating regions of the female rat forebrain. Brain Res. 624 (1993) 253-267
63. Pfaus J.G., Marcangione C., Smith W.J., Manitt C., and Abillamaa H. Differential induction of Fos in the female rat brain following different amounts of vaginocervical stimulation: modulation by steroids hormones. Brain Res. 741 (1996) 314-330
64. Pfaus J.G., Smith W.J., and Coopersmith C.B. Appetitive and consummatory behaviors of females rats in bilevel chambers: I. A correlational and factor analysis, and the effects of ovarian steroids. Horm. Behav. 33 (1999) 224-240
65. Pfaus J.G., Smith W.J., Byrne N., and Stephens G. Appetitive and consummatory behaviors of females rats in bilevel chambers: II. Patterns of estrus termination following vaginocervical stimulation. Horm. Behav. 37 (2000) 96-107
66. Pfaus J.G., Manitt C., and Coopersmith C.B. Effects of pelvic, pudendal, or hypogastric nerve cuts on Fos induction in the rat brain following vaginocervical stimulation. Physiol. Behav. 89 (2006) 627-636
67. Powers J.B. Hormonal control of sexual receptivity during the estrous cycle of the rat. Physiol. Behav. 5 (1970) 831-835
68. Rajendren G., Dudley C.A., and Moss R.L. Role of ventromedial nucleus of hypothalamus in male-induced enhancement of lordosis in female rats. Physiol. Behav. 50 (1991) 705-710
69. Rodriguez-Sierra J.F., Crowley W.R., and Komisaruk B.R. Vaginal stimulation in rats induces prolonged lordosis responsiveness and sexual receptivity. J. Comp. Physiol. Psychol. 89 (1975) 79-85
70. Romano G.J., Mobbs C.V., Lauber A., Howells R.D., and Pfaff D.W. Differential regulation of proenkephalin gene expression by estrogen in the ventromedial hypothalamus of male and female rats: implications for the molecular basis of a sexually differentiated behavior. Brain Res. 536 (1990) 63-68
71. Sakuma Y., and Pfaff D.W. Facilitation of lordosis reflex of female rats from the ventromedial nucleus of the hypothalamus. J. Physiol. 288 (1979) 189-202
72. Steinach E. Geschlechtstrieb und echt sekundäre Geschlechtsmerkmale als Folge der innersekretorischen Funktion der Keimdrüsen (Sex instinct and genuine secondary sex characteristics as a result of internal secretion of the gonads). Zent.bl. Physiol. 24 (1910) 551
73. Sterner M.R., Meisel R.L., and Diekman M.A. Forebrain sites of estradiol-17 beta action on sexual behavior and aggression in female Syrian hamsters. Behav. Neurosci. 106 (1992) 162-171
74. Storlien L.H., and Albert D.J. The effect of VMH lesion, lateral cuts and anterior cuts on food intake, activity level, food motivation, and reactivity to taste. Physiol. Behav. 9 (1972) 191-197
75. Sun D., Vingrys A.J., and Kalloniatis M. Metabolic and functional profiling of the normal rat retina. J. Comp. Neurol. 505 (2007) 93-114
76. Swanson L.W. Brain Maps: Structure of the Rat Brain (1992), Elsevier, Amsterdam
77. Tetel M.J., Getzinger M.J., and Blaustein J.D. Fos expression in the rat brain following vaginal-cervical stimulation by mating and manual probing. J. Neuroendocrinol. 5 (1993) 397-404
78. Tetel M.J., Getzinger M.J., and Blaustein J.D. Estradiol and progesterone influence he response of ventromedial hypothalamic neurons to tactile stimuli associated with female reproduction. Brain Res. 646 (1994) 267-272
79. Wersinger S.A., Baum M.J., and Erskine M.S. Mating-induced FOS-like immunoreactivity in the rat forebrain: a sex comparison and a dimorphic effect of pelvic nerve transaction. J. Neuroendocrinol. 5 (1993) 557-568
80. Wise R.A., and Hoffman D.C. Localization of drug reward mechanisms by intracranial injections. Synapse 10 (1992) 247-263