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.
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
Beitz AJ (1982) The organization of afferent projections to the midbrain periaqueductal gray of the rat. Neuroscience 7:133–159
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
Corodimas KP, Morrell JI (1990) Estradiol-concentrating forebrain and midbrain neurons project directly to the medulla. J Comp Neurol 291:609–620
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
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
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
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
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
Edwards MA, Adams DB (1974) Role of midbrain central gray in pain-induced defensive boxing of rats. Physiol Behav 13:113–121
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
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)
Frankfurt M, Fuchs E, Wuttke W (1984) Sex differences in gammaaminobutryic acid and glutamate concentrations in discrete brain nuclei. Neurosci Lett 50:245–250
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
Hylden JLK, Hayashi H, Dubner R, Bennett GJ (1986) Physiology and morphology of the lamina I spinomesencephalic projection. J Comp Neurol 247:505–515
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
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
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
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
McMahon SB, Wall PD (1985) Electrophysiological mapping of brainstem projections of spinal cord lamina I cells in the rat. Brain Res 333:19–26
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
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
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
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
Qureshi GA, Bednar I, Forsberg G, Sodersten P (1988) GABA inhibits sexual behavior in female rats. Neuroscience 27:169–174
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
Roberts LA, Beyer C, Komisaruk BR (1986) Nociceptive responses to altered GABAergic activity at the spinal cord. Life Sci 39:1667–1674
Sakuma Y, Pfaff DW (1979a) Facilitation of female reproductive behavior from mesencephalic central gray in the rat. Am J Physiol 237:R278-R284
Sakuma Y, Pfaff DW (1979b) Mesencephalic mechanisms for integration of female reproductive behavior in the rat. Am J Physiol 237:R285–290
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
Schumacher M, Coirini H, McEwen BS (1989) Regulation of high-affinity GABAa receptors in specific brain regions by ovarian hormones. Neuroendocrinology 50:315–320
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
Smith SS (1989) Progesterone enhances inhibitory responses of cerebellar purkinje cells mediated by the GABAA receptor subtype. Brain Res Bull 23:317–322
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
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
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
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
Yezierski RP (1988) Spinomesencephalic tract: projections from the lumbosacral spinal cord of the rat, cat and monkey. J Comp Neurol 267:131–146
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)
Author information
Authors and Affiliations
Rights 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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00231045