Infusions of bicuculline to the ventral tegmental area attenuates sexual, exploratory, and anti-anxiety behavior of proestrous rats

Pharmacology Biochemistry and Behavior

Volumn 93, Issue 4, 2009, Pages 474-481

  Frye, Cheryl A ^a   Paris, Jason J ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Allopregnanolone; Behavioral estrus; Corticosterone; Hypothalamic pituitary adrenal axis; Lordosis; Progesterone; Social behavior; Stress

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID A RECEPTOR; BICUCULLINE;

ANIMAL EXPERIMENT; APPETITE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DIENCEPHALON; EXPLORATORY BEHAVIOR; FEMALE; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LORDOSIS; MAZE TEST; MESENCEPHALON; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROESTRUS; RAT; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; SOCIAL INTERACTION; STEROIDOGENESIS; TRANQUILIZING ACTIVITY; VENTRAL TEGMENTUM;

ANIMALS; ANXIETY; BICUCULLINE; CONSUMMATORY BEHAVIOR; DESOXYCORTICOSTERONE; ESTROUS CYCLE; EXPLORATORY BEHAVIOR; FEMALE; GABA ANTAGONISTS; HORMONES; INTERPERSONAL RELATIONS; MICROINJECTIONS; MOTOR ACTIVITY; NEUROSECRETORY SYSTEMS; POSTURE; RATS; RATS, LONG-EVANS; RECEPTORS, GABA-A; SEXUAL BEHAVIOR, ANIMAL; STEREOTAXIC TECHNIQUES; VENTRAL TEGMENTAL AREA;

RATTUS; RODENTIA;

EID: 67849124136     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2009.06.012     Document Type: Article

References (87)

1. Bianchi L., Ballini C., Colivicchi M.A., Della Corte L., Giovannini M.G., and Pepeu G. Investigation on acetylcholine, aspartate, glutamate and GABA extracellular levels from ventral hippocampus during repeated exploratory activity in the rat. Neurochem Res 28 (2003) 565-573
2. A receptor. Brain Res 561 (1991) 157-161
3. Bitran D., Foley M., Audette D., Leslie N., and Frye C.A. Activation of peripheral mitochondrial benzodiazepine receptors in the hippocampus stimulates allopregnanolone synthesis and produces anxiolytic-like effects in the rat. Psychopharmacology 151 (2000) 64-71
4. Blaustein J.D., Tetel M.J., Ricciardi K.H., Delville Y., and Turcotte J.C. Hypothalamic ovarian steroid hormone-sensitive neurons involved in female sexual behavior. Psychoneuroendocrinology 19 (1994) 505-516
5. Blizard D.A., Lippman H.R., and Chen J.J. Sex differences in open-field behavior in the rat: the inductive and activational role of gonadal hormones. Physiol Behav 14 (1975) 601-608
6. Choi S., and Dallman M.F. Hypothalamic obesity: multiple routes mediated by loss of function in medial cell groups. Endocrinology 140 (1999) 4081-4088
7. DeBold J.F., and Malsbury C.W. Facilitation of sexual receptivity by hypothalamic and midbrain implants of progesterone in female hamsters. Physiol Behav 46 (1989) 655-660
8. de Groote L., and Linthorst A.C. Exposure to novelty and forced swimming evoke stressor-dependent changes in extracellular GABA in the rat hippocampus. Neuroscience 148 (2007) 794-805
9. B receptors in the regulation of the nucleus accumbens dopamine response to stress. Brain Res 1150 (2007) 62-68
10. Droste SK, Collins A, Lightman SL, Linthorst AC, Reul JM. Distinct, time-dependent effects of voluntary exercise on circadian and ultradian rhythms and stress responses of free corticosterone in the rat hippocampus. Endocrinology in press. doi:10.1210/en.2009-0402.
11. Drugan R.C., Holmes P.V., Scher D.M., Luczak S., Oh H., and Ferland R.J. Environmentally induced changes in peripheral benzodiazepine receptors are stressor and tissue specific. Pharmacol Biochem Behav 50 (1995) 551-562
12. Echo J.A., Lamonte N., Ackerman T.F., and Bodnar R.J. Alterations in food intake elicited by GABA and opioid agonists and antagonists administered into the ventral tegmental area region of rats. Physiol Behav 76 (2002) 107-116
13. Erskine M.S. Effects of paced coital stimulation on estrus duration in intact cycling rats and ovariectomized and ovariectomized-adrenalectomized hormone-primed rats. Behav Neurosci 99 (1985) 151-161
14. Erskine M.S., and Kornberg E. Stress and ACTH increase circulating concentrations of 3-androstanediol in female rats. Life Sci 51 (1992) 2065-2071
15. Feder H.H. Hormones and sexual behavior. Annu Rev Psychol 35 (1984) 165-200
16. File S.E. The interplay of learning and anxiety in the elevated plus-maze. Behav Brain Res 58 (1993) 199-202
17. File S.E., and Seth P. A review of 25 years of the social interaction test. Eur J Pharmacol 463 (2003) 35-53
18. Frye C.A. The role of neurosteroids and non-genomic effects of progestins and androgens in mediating sexual receptivity of rodents. Brain Res Brain Res Rev 37 (2001) 201-222
19. Frye C.A., and Bayon L.E. Mating stimuli influence endogenous variations in the neurosteroids 3, 5-THP and 3-Diol. J Neuroendocrinol 11 (1999) 839-847
20. 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
21. Frye C.A., and Petralia S.M. Lordosis of rats is modified by neurosteroidogenic effects of membrane benzodiazepine receptors in the ventral tegmental area. Neuroendocrinology 77 (2003) 71-82
22. Frye C.A., and Rhodes M.E. Progestin concentrations are increased following paced mating in midbrain, hippocampus, diencephalon, and cortex of rats in behavioral estrus, but only in midbrain of diestrous rats. Neuroendocrinology 83 (2006) 336-347
23. Frye C.A., and Rhodes M.E. The role and mechanisms of steroid hormones in approach/avoidance behavior. In: Elliot A.J. (Ed). Handbook of approach and avoidance motivation (2008), Lawrence Erlbaum Associates, Mahwah, NJ 109-126
24. Frye C.A., and Seliga A.M. Effects of olanzapine infusions to the ventral tegmental area on lordosis and midbrain 3, 5-THP concentrations in rats. Psychopharmacology 170 (2003) 132-139
25. Frye C.A., and Seliga A.M. Olanzapine's effects to reduce fear and anxiety and enhance social interactions coincide with increased progestin concentrations of ovariectomized rats. Psychoneuroendocrinology 28 (2003) 657-673
26. 5, but not progestin receptor, antagonist and anti-sense oligonucleotide infusions to the ventral tegmental area of cycling rats and hamsters attenuate lordosis. Behav Brain Res 103 (1999) 23-34
27. Frye C.A., Mermelstein P.G., and DeBold J.F. Evidence for a non-genomic action of progestins on sexual receptivity in hamster ventral tegmental area but not hypothalamus. Brain Res 578 (1992) 87-93
28. Frye C.A., Mermelstein P.G., and DeBold J.F. Bicuculline infused into the hamster ventral tegmentum inhibits, while sodium valproate facilitates, sexual receptivity. Pharmacol Biochem Behav 46 (1993) 1-8
29. Frye C.A., Van Keuren K.R., Rao P.N., and Erskine M.S. Progesterone and 3-androstanediol conjugated to bovine serum albumin affects estrous behavior when applied to the MBH and POA. Behav Neurosci 110 (1996) 603-612
30. Frye C.A., Petralia S.M., and Rhodes M.E. Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3, 5-THP. Pharmacol Biochem Behav 67 (2000) 587-596
31. Frye C.A., Rhodes M.E., Petralia S.M., Walf A.A., Sumida K., and Edinger K.L. 3-hydroxy-5-pregnan-20-one in the midbrain ventral tegmental area mediates social, sexual, and affective behaviors. Neuroscience 138 (2006) 1007-1014
32. A receptors. Horm Behav 50 (2006) 332-337
33. Frye C.A., Paris J.J., and Rhodes M.E. Engaging in paced mating, but neither exploratory, anti-anxiety, nor social behavior, increases 5-reduced progestin concentrations in midbrain, hippocampus, striatum, and cortex. Reproduction 133 (2007) 663-674
34. Frye C.A., Paris J.J., and Rhodes M.E. Exploratory, anti-anxiety, social, and sexual behaviors of rats in behavioral estrus is attenuated with inhibition of 3, 5-THP formation in the midbrain ventral tegmental area. Behav Brain Res 193 (2008) 269-276
35. Frye C.A., Paris J.J., and Rhodes M.E. Increasing 3, 5-THP following inhibition of neurosteroid biosynthesis in the ventral tegmental area reinstates anti-anxiety, social and sexual behavior of naturally-receptive rats. Reproduction 137 (2009) 119-128
36. Gans S., and Erskine M.S. Effects of neonatal testosterone treatment on pacing behaviors and development of a conditioned place preference. Horm Behav 44 (2003) 354-364
37. Gasbarri A., Sulli A., and Packard M.G. The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuro-Psychopharmacol Biol Psychiatry 21 (1997) 1-22
38. Haefely W. Involvement of GABA in the actions of neuropsychotropic drugs. Int J Neurol 13 (1979) 53-66
39. Hardy D.F., and DeBold J.F. Effects of coital stimulation upon behavior of the female rat. J Comp Physiol Psychol 78 (1972) 400-408
40. Herman J.P., Dolgas C.M., and Carlson S.C. Ventral subiculum co-ordinates situation-specific neuroendocrine and behavioral stress responses. Neuroscience 86 (1998) 449-459
41. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., et al. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24 (2003) 151-180
42. A receptor blockade in the anterior ventral tegmental area increases extracellular levels of dopamine in the nucleus accumbens of rats. J Neurochem 69 (1997) 137-143
43. A antagonists directly into the ventral tegmental area and adjacent regions. Behav Neurosci 111 (1997) 369-380
44. Jahnsen H., and Laursen A.M. The effects of a benzodiazepine on the hyperpolarizing and the depolarizing responses of hippocampal cells to GABA. Brain Res 207 (1981) 214-217
45. 1 receptors modulate glutamate transmission in the ventral tegmental area. J Neurosci 15 (1995) 5379-5388
46. Kliewer S.A., Goodwin B., and Willson T.M. The nuclear pregnane X receptor: a key regulator of xenobiotic metabolism. Endocr Rev 23 (2002) 687-702
47. Langmade S.J., Gale S.E., Frolov A., Mohri I., Suzuki K., Mellon S.H., et al. Pregnane X receptor (PXR) activation: a mechanism for neuroprotection in a mouse model of Niemann-Pick C disease. Proc Natl Acad Sci U S A 103 (2006) 13807-13812
48. A receptors in the ventral tegmental area control bidirectional reward signalling between dopaminergic and non-dopaminergic neural motivational systems. Eur J Neurosci 13 (2001) 1009-1015
49. A receptors signal bidirectional reward transmission from the ventral tegmental area to the tegmental pedunculopontine nucleus as a function of opiate state. Eur J Neurosci 20 (2004) 2179-2187
50. Linthorst A.C., and Reul J.M. Stress and the brain: solving the puzzle using microdialysis. Pharmacol Biochem Behav 90 (2008) 163-173
51. Lisman J.E., and Grace A.A. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46 (2005) 703-713
52. Long J.A., and Evans H.M. Oestrous cycle in the rat and its associated phenomena. Mem Univ Calif 6 (1922) 1-146
53. Luine V. Sex differences in chronic stress effects on memory in rats. Stress 5 (2002) 205-216
54. 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
55. Malsbury C.W., Kow L.M., and Pfaff D.W. Effects of medial hypothalamic lesions on the lordosis response and other behaviors in remale golden hamsters. Physiol Behav 19 (1977) 223-237
56. Marshall J.F., and Teitelbaum P. Further analysis of sensory inattention following lateral hypothalamic damage in rats. J Comp Physiol Psychol 86 (1974) 375-395
57. Masuyama H., Suwaki N., Tateishi Y., Nakatsukasa H., Segawa T., and Hiramatsu Y. The pregnane X receptor regulates gene expression in a ligand- and promoter-selective fashion. Mol Endocrinol 19 (2005) 1170-1180
58. McCarthy M.M., Masters D.B., Rimvall K., Schwartz-Giblin S., and Pfaff D.W. Intracerebral administration of antisense oligodeoxynucleotides to GAD65 and GAD67 mRNAs modulate reproductive behavior in the female rat. Brain Res 636 (1994) 209-220
59. McCarthy M.M., Felzenberg E., Robbins A., Pfaff D.W., and Schwartz-Giblin S. Infusions of diazepam and allopregnanolone into the midbrain central gray facilitate open-field behavior and sexual receptivity in female rats. Horm Behav 29 (1995) 279-295
60. McClintock M.K., and Adler N.T. Induction of persistent estrus by airborne chemical communication among female rats. Horm Behav 11 (1978) 414-418
61. Meerts S.H., and Clark A.S. Female rats exhibit a conditioned place preference for nonpaced mating. Horm Behav 51 (2007) 89-94
62. Meerts S.H., and Clark A.S. Artificial vaginocervical stimulation induces a conditioned place preference in female rats. Horm Behav 55 (2009) 128-132
63. Meisel R.L., Dohanich G.P., McEwen B.S., and Pfaff D.W. Antagonism of sexual behavior in female rats by ventromedial hypothalamic implants of antiestrogen. Neuroendocrinology 45 (1987) 201-207
64. Meisel R.L., Camp D.M., and Robinson T.E. A microdialysis study of ventral striatal dopamine during sexual behavior in female Syrian hamsters. Behav Brain Res 55 (1993) 151-157
65. Mellon S.H., Gong W., and Schonemann M.D. Endogenous and synthetic neurosteroids in treatment of Niemann-Pick Type C disease. Brain Res Rev 57 (2008) 410-420
66. Miczek K.A., Yap J.J., and Covington III H.E. Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake. Pharmacol Ther 120 (2008) 102-128
67. Mora S., Dussaubat N., and Díaz-Véliz G. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 21 (1996) 609-620
68. Narang V.S., Fraga C., Kumar N., Shen J., Throm S., Stewart C.F., et al. Dexamethasone increases expression and activity of multidrug resistance transporters at the rat blood-brain barrier. Am J Physiol, Cell Physiol 295 (2008) C440-C450
69. A receptors in the anterior ventral tegmental area attenuates ethanol intake of the alcohol-preferring P rat. Psychopharmacology 139 (1998) 108-116
70. Nyakas C., De Kloet E.R., Veldhuis H.D., and Bohus B. Hippocampal corticosterone receptors and novelty-induced behavioral activity: effect of kainic acid lesion in the hippocampus. Brain Res 288 (1983) 219-228
71. Patchev V.K., Shoaib M., Holsboer F., and Almeida O.F. The neurosteroid tetrahydroprogesterone counteracts corticotropin-releasing hormone-induced anxiety and alters the release and gene expression of corticotropin-releasing hormone in the rat hypothalamus. Neuroscience 62 (1994) 265-271
72. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1986), Academic Press, New York
73. Pfaus J.G., Jakob A., Kleopoulos S.P., Gibbs R.B., and Pfaff D.W. Sexual stimulation induces Fos immunoreactivity within GnRH neurons of the female rat preoptic area: interaction with steroid hormones. Neuroendocrinology 60 (1994) 283-290
74. Pleim E.T., Lisciotto C.A., and DeBold J.F. Facilitation of sexual receptivity in hamsters by simultaneous progesterone implants into the VMH and ventral mesencephalon. Horm Behav 24 (1990) 139-151
75. Powers J.B. Facilitation of lordosis in ovariectomized rats by intracerebral progesterone implants. Brain Res 48 (1972) 311-325
76. Purdy R.H., Morrow A.L., Moore Jr. P.H., and Paul S.M. Stress-induced elevations of γ-aminobutyric acid type A receptor-active steroids in the rat brain. Proc Natl Acad Sci U S A 15 88 (1991) 4553-4557
77. Reddy D.S., and Kulkarni S.K. Sex and estrous cycle-dependent changes in neurosteroid and benzodiazepine effects on food consumption and plus-maze learning behaviors in rats. Pharmacol Biochem Behav 62 (1999) 53-60
78. Rodbard D., and Hutt D.M. Statistical analysis of radioimmunoassay and immunoradiometric assays: a generalized, weighted iterative, least squares method for logistic curve fitting. In: International Atomic Energy Agency (Ed). Symposium on Radioimmunoassay and Related Procedures in Medicine (1974), Uniput, New York 209-233
79. Steffensen S.C., Svingos A.L., Pickel V.M., and Henriksen S.J. Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J Neurosci 18 (1998) 8003-8015
80. Sutcliffe J.S., Marshall K.M., and Neill J.C. Influence of gender on working and spatial memory in the novel object recognition task in the rat. Behav Brain Res 177 (2007) 117-125
81. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9 (1982) 321-353
82. Takahashi L.K., and Lisk R.D. Diencephalic sites of progesterone action for inhibiting aggression and facilitating sexual receptivity in estrogen-primed golden hamsters. Endocrinology 116 (1985) 2393-2399
83. Takahashi L.K., and Lisk R.D. Dual progesterone action in diencephalon facilitates the induction of sexual receptivity in estrogen-primed golden hamsters. Physiol Behav 44 (1988) 741-747
84. A receptor single-channel kinetic properties of mouse spinal cord neurons in culture. J Physiol 456 (1992) 215-245
85. A receptor. J Neurosci 17 (1997) 625-634
86. 3H]R-5020 injection. Mol Cell Endocrinol 12 (1978) 67-79
87. Xi Z.X., and Stein E.A. Increased mesolimbic GABA concentration blocks heroin self-administration in the rat. J Pharmacol Exp Ther 294 (2000) 613-619