Skip to main content
Log in

Midbrain central gray GABAA receptor activation enhances, and blockade reduces, sexual behavior in the female rat

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

The inhibitory neurotransmitter, GABA, has been implicated in the control of lordosis behavior. Previous studies indicate that modulation of GABAA transmission can have dual effects on lordosis, being facilitative in the ventromedial hypothalamus and inhibitory in the preoptic area. The midbrain central gray (MCG) is also known to be an important neural site for regulating lordosis as well as defensive and escape behaviors, and plays an integral role in the control of nociception. Because of the multitude of behaviors regulated at the level of the MCG, we utilized a two-chamber testing apparatus that allowed simultaneous measurement of the females' proceptive (hopping and darting), receptive and rejection behaviors, as well as an index of nociception and general motor activity. We found that microinfusion of the GABAA antagonist, bicuculline, into the MCG of steroid-primed female rats resulted in a significant decrease in lordosis and proceptive behaviors at 5 min post-infusion. There was full recovery to pretest levels by 60 min. Furthermore, microinfusion of the GABAA agonist, muscimol, to estrogen-treated females that displayed low levels of receptivity and high levels of rejection behavior during a pretest, resulted in a significant increase in lordosis responding and a decrease in rejection behaviors. Neither drug significantly affected time spent in the vicinity of the male, motor activity or vocalizations. It is concluded that the decrease in lordosis resulting from blockade of GABA transmission is not solely due to the induction of antagonistic behaviors since there was no increase in rejections after bicuculline administration. The current findings are consistent with the interpretation that GABA facilitates lordosis in the MCG via disinhibition. When the retrograde tracer, Fluoro-gold, was infused into the same cannula sites in the MCG as the GABAA drugs it demonstrated the presence of strong projections from the ventromedial nucleus, zona incerta, medullary reticular formation and spinal cord. These projections to the MCG may be important for the integration of the diverse behaviors regulated at the level of the MCG and GABAergic transmission may play a role in this integration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bandler R, Depaulis A, Vergnes M (1985) Identification of mid brain neurons mediating defensive behavior in the rat by microinjections of excitatory amino acids. Behav Brain Res 15:107–109

    Google Scholar 

  • Beitz AJ (1982) The organization of afferent projections to the midbrain periaqueductal gray of the rat. Neuroscience 7:133–159

    Google Scholar 

  • Brandao ML, Di Scala G, Bouchet MJ, Schmitt P (1986) Escape behavior produced by the blockade of glutamic acid decarboxylase (GAD) in mesencephalic central gray or medial hypothalamus. Pharmacol Biochem Behav 24:497–501

    Google Scholar 

  • Corodimas KP, Morrell JI (1990) Estradiol-concentrating forebrain and midbrain neurons project directly to the medulla. J Comp Neurol 291:609–620

    Google Scholar 

  • Crowley WR, Jacobs R, Volpe J, Rodriguez-Sierra JF, Komisaruk BR (1976) Analgesic effect of vaginal stimulation in rats: modulation by graded stimulus intensity and hormones. Physiol Behav 16:483–488

    Google Scholar 

  • Depaulis A, Bandler R, Vergnes M (1989) Characterization of pretentorial periaqueductal gray matter neurons mediating intraspecific defensive behavior in the rat by microinjections of kainic acid. Brain Res 486:121–132

    Google Scholar 

  • Depaulis A, Vergnes M (1986) Elicitation of intraspecific defensive behaviors in the rat by microinjection of picrotoxin, a gamma-aminobutyric acid antagonist, into the midbrain periaqueductal gray matter. Brain Res 367:87–95

    Google Scholar 

  • Depaulis A, Morgan MM, Liebeskind JC (1987) GABAergic modulation of the analgesic effects of morphine microinjected in the ventral periaqueductal gray matter of the rat. Brain Res 436:223–228

    Google Scholar 

  • Dornan WA, Peterson M, Matuszewich, Malen P (1991) Ibotenic acid-induced lesions of the medial zona incerta decrease lordosis behavior in the female rat. Behav Neurosci 105:210–214

    Google Scholar 

  • Edwards MA, Adams DB (1974) Role of midbrain central gray in pain-induced defensive boxing of rats. Physiol Behav 13:113–121

    Google Scholar 

  • Fahrbach S, Morrell JI, Pfaff DW (1986) Identification of medial preoptic neurons that concentrate estradiol and project to the midbrain in the rat. J Comp Neurol 247:364–382

    Google Scholar 

  • Fanselow MS (1990) The midbrain periaqueductal grey as a coordinator of action in response to fear and anxiety. In: Depaulis A, Bandler R (eds) The midbrain periaqueductal gray matter: functional, anatomical and immunohistochemical organization. Plenum Publsh, New York (in press)

    Google Scholar 

  • Frankfurt M, Fuchs E, Wuttke W (1984) Sex differences in gammaaminobutryic acid and glutamate concentrations in discrete brain nuclei. Neurosci Lett 50:245–250

    Google Scholar 

  • Hennessey AC, Camak L, Gordon F, Edwards DA (1990) Connections between the pontine central gray and the ventromedial hypothalamus are essential for lordosis in female rats. Behav Neurosci 104:477–488

    Google Scholar 

  • Hylden JLK, Hayashi H, Dubner R, Bennett GJ (1986) Physiology and morphology of the lamina I spinomesencephalic projection. J Comp Neurol 247:505–515

    Google Scholar 

  • Kow L-M, Pfaff DW (1982) Responses of medullary reticulospinal and other reticular neurons to somatosensory and brainstem stimulation in anesthetized or freely moving rats with or without estrogen treatment. Exp Brain Res 47:191–202

    Google Scholar 

  • Lopez-Colome AM, McCarthy MM, Beyer C (1990) Enhancement of 3H-muscimol binding to brain synaptic membranes by progesterone and related pregnanes. Eur J Pharmacol 176:297–304

    Google Scholar 

  • McCarthy MM, Malik KF, Feder HH (1990) Increased GABAergic transmission in medial hypothalamus facilitates lordosis but has opposite effects in the preoptic area/anterior hypothalamus. Brain Res 507:40–44

    Google Scholar 

  • McCarthy MM, Masters DB, Fiber JM, Lopez-Colome AM, Beyer C, Komisaruk BR, Feder HH (1991) GABAergic control of receptivity in the female rat. Neuroendocrinology 53:473–479

    Google Scholar 

  • McMahon SB, Wall PD (1985) Electrophysiological mapping of brainstem projections of spinal cord lamina I cells in the rat. Brain Res 333:19–26

    Google Scholar 

  • Moreau J-L, Fields HL (1986) Evidence for GABA involvement in midbrain control of medullary neurons that modulate nociceptive transmission. Brain Res 397:37–46

    Google Scholar 

  • Morrell JI, Greenberger LM, Pfaff DW (1981) Hypothalamic, other diencephalic and telencephalic neurons that project to the dorsal midbrain. J Comp Neurol 201:589–620

    Google Scholar 

  • Pfaff DW, Keiner M (1973) Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J Comp Neurol 151:121–158

    Google Scholar 

  • Pfaff DW, Schwartz-Giblin S (1988) Cellular Mechanisms of female reproductive behaviors. In: Knobil E, Neill J et al. (eds) The physiology of reproduction. Raven Press, New York, pp 1487–1569

    Google Scholar 

  • Qureshi GA, Bednar I, Forsberg G, Sodersten P (1988) GABA inhibits sexual behavior in female rats. Neuroscience 27:169–174

    Google Scholar 

  • Robbins A, Schwartz-Giblin S, Pfaff DW (1990) Ascending and descending projections to medullary reticular formation sites which activate deep lumbar back muscles in the rat. Exp Brain Res 80:463–474

    Google Scholar 

  • Roberts LA, Beyer C, Komisaruk BR (1986) Nociceptive responses to altered GABAergic activity at the spinal cord. Life Sci 39:1667–1674

    Google Scholar 

  • Sakuma Y, Pfaff DW (1979a) Facilitation of female reproductive behavior from mesencephalic central gray in the rat. Am J Physiol 237:R278-R284

    Google Scholar 

  • Sakuma Y, Pfaff DW (1979b) Mesencephalic mechanisms for integration of female reproductive behavior in the rat. Am J Physiol 237:R285–290

    Google Scholar 

  • Sandkühler J, Willmann E, Fu Q-G (1991) Characteristics of mid-brain control of spinal nociceptive neurons and nonsomatosensory parameters in the pentobarbital-anesthetized rat. J Neurophys 65:33–48

    Google Scholar 

  • Schumacher M, Coirini H, McEwen BS (1989) Regulation of high-affinity GABAa receptors in specific brain regions by ovarian hormones. Neuroendocrinology 50:315–320

    Google Scholar 

  • Schwartz-Giblin S, Blackett JJ, Pfaff DW (1989) Estrogen and progesterone effects on reproductive behavior when the female rat can avoid socio-sexual contact. Soc Neurosci Abst no 435. 7, Vol. 15

  • Sirinathsinghji DJS (1985) Modulation of lordosis behavior in the female rat by corticotropin releasing factor, B-endorphin and gonadotropin releasing hormone in the mesencephalic central gray. Brain Res 336:45–55

    Google Scholar 

  • Smith SS (1989) Progesterone enhances inhibitory responses of cerebellar purkinje cells mediated by the GABAA receptor subtype. Brain Res Bull 23:317–322

    Google Scholar 

  • Swett JE, McMahon SB, Wall PD (1985) Long ascending projections to the midbrain from cells of lamina I and nucleus of the dorsolateral funiculus of the rat spinal cord. J Comp Neurol

  • Thorn BE, Applegate L, Johnson SW (1989) Ability of periaqueductal gray subdivisions and adjacent loci to elicit analgesia and ability of naloxone to reverse analgesia. Behav Neurosci 103:1335–1339

    Google Scholar 

  • Van Bockstaele EJ, Pieribone VA, Aston-Jones G (1989) Diverse afferents converge on the nucleus paragigantocellularis in the rat ventrolateral medulla: Retrograde and anterograde tracing studies. J Comp Neurol 290:561–584

    Google Scholar 

  • Wu F-S, Gibbs TT, Farb DH (1990) Inverse modulation of gamma-aminobutyric acid- and glycine-induced currents by progesterone. Molec Pharmacol 37:597–602

    Google Scholar 

  • Yamanouchi K, Arai Y (1983) Forebrain and lower brainstem participation in facilitatory and inhibitory regulation of the display of lordosis in female rats. Physiol Behav 30:155–159

    Google Scholar 

  • Yezierski RP (1988) Spinomesencephalic tract: projections from the lumbosacral spinal cord of the rat, cat and monkey. J Comp Neurol 267:131–146

    Google Scholar 

  • Yezierski RP (1990) Somatosensory input to the periaqueductal gray: spinal relay to a descending control center. In: Depaulis A, Bandler R (eds) The midbrain periaqueductal gray matter: functional, anatomical and immunohistochemical organization. Plenum Publsh, New York (in press)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

McCarthy, M.M., Pfaff, D.W. & Schwartz-Giblin, S. Midbrain central gray GABAA receptor activation enhances, and blockade reduces, sexual behavior in the female rat. Exp Brain Res 86, 108–116 (1991). https://doi.org/10.1007/BF00231045

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00231045

Key words

Navigation