Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1981 Jul;316:327–346. doi: 10.1113/jphysiol.1981.sp013791

Electrophysiological analysis of inhibitory synaptic mechanisms in the preoptic area of the rat.

M L Mayer
PMCID: PMC1248151  PMID: 7320870

Abstract

1. Extracellular recordings were made from single neurones in the medial preoptic-anterior hypothalamus of rats anaesthetized with urethane or pentobarbitone 2. Stimulation of the arcuate--ventromedial area evoked inhibition in 76% of neurones; inhibition occurred as the initial response in 26% of neurones, followed orthodromic excitation in 26% and antidromic excitation in 24%. Stimulation of the periaqueductal grey evoked inhibition as the initial response in 63% of neurones. 3. Stimulation of both the arcuate--ventromedial area and the periaqueductal grey generated synaptically evoked high-frequency discharges in a few neurones. 4. Short ionophoretic pulses of beta-alanine, gamma-aminobutyric acid (GABA), glycine and taurine inhibited the discharge of most preoptic-anterior hypothalamic neurones. Bicuculline methochloride and picrotoxin antagonized both GABA responses and synaptic inhibition. Strychnine antagonized beta-alanine, glycine and taurine responses without altering synaptic inhibition. 5. Reduction of hypothalamic serotonin (5-HT) levels to about 40% of control values by micro-injection of 5,7-dihydroxytryptamine into the ventral tegmental area, or parenteral injection of parachlorophenylalanine, did not alter the profile of responses evoked by either arcuate-ventromedial or periaqueductal grey stimulation. Micro-injection of tetanus toxin (100-200 MLD) into the preoptic-anterior hypothalamus significantly reduced the frequency of occurrence of inhibition evoked from both sites. 6. Pentobarbitone administered acutely or as the sole anaesthetic increased both the duration and frequency of occurrence of inhibitory responses evoked from the arcuate-ventromedial nuclei. 7. It is suggested that a GABA-linked inhibitory synaptic mechanism, activated by arcuate-ventromedial and periaqueductal grey stimulation, operates in the preoptic-anterior hypothalamus. Such convergent inhibition may be a result of activity in local interneurone circuitry.

Full text

PDF
327

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ANDERSEN P., ECCLES J. C., LOYNING Y. Recurrent inhibition in the hippocampus with identification of the inhibitory cell and its synapses. Nature. 1963 May 11;198:540–542. doi: 10.1038/198540a0. [DOI] [PubMed] [Google Scholar]
  2. ANDERSEN P., ECCLES J. C., SEARS T. A. THE VENTRO-BASAL COMPLEX OF THE THALAMUS: TYPES OF CELLS, THEIR RESPONSES AND THEIR FUNCTIONAL ORGANIZATION. J Physiol. 1964 Nov;174:370–399. doi: 10.1113/jphysiol.1964.sp007493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Azmitia E. C., Segal M. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol. 1978 Jun 1;179(3):641–667. doi: 10.1002/cne.901790311. [DOI] [PubMed] [Google Scholar]
  4. Barker J. L., McBurney R. N. Phenobarbitone modulation of postsynaptic GABA receptor function on cultured mammalian neurons. Proc R Soc Lond B Biol Sci. 1979 Dec 31;206(1164):319–327. doi: 10.1098/rspb.1979.0108. [DOI] [PubMed] [Google Scholar]
  5. Björklund A., Baumgarten H. G., Rensch A. 5,7-Dihydroxytryptamine: improvement of its selectivity for serotonin neurons in the CNS by pretreatment with desipramine. J Neurochem. 1975 Apr;24(4):833–835. [PubMed] [Google Scholar]
  6. Brown D. A., Constanti A. Interaction of pentobarbitone and gamma-aminobutyric acid on mammalian sympathetic ganglion cells. Br J Pharmacol. 1978 May;63(1):217–224. doi: 10.1111/j.1476-5381.1978.tb07791.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brownstein M. Neurotransmitters and hypothalamic hormones in the central nervous system. Fed Proc. 1977 Jun;36(7):1960–1963. [PubMed] [Google Scholar]
  8. Collins J. F., Hill R. G. Plus and minus-bicuculline methochloride as optical isomers of a GABA antagonist. Nature. 1974 Jun 28;249(460):845–847. doi: 10.1038/249845a0. [DOI] [PubMed] [Google Scholar]
  9. Curtis D. R., De Groat W. C. Tetanus toxin and spinal inhibition. Brain Res. 1968 Aug 26;10(2):208–212. doi: 10.1016/0006-8993(68)90123-6. [DOI] [PubMed] [Google Scholar]
  10. Curtis D. R., Felix D., Game C. J., McCulloch R. M. Tetanus toxin and the synaptic release of GABA. Brain Res. 1973 Mar 15;51:358–362. doi: 10.1016/0006-8993(73)90389-2. [DOI] [PubMed] [Google Scholar]
  11. Curtis D. R., Johnston G. A. Amino acid transmitters in the mammalian central nervous system. Ergeb Physiol. 1974;69(0):97–188. doi: 10.1007/3-540-06498-2_3. [DOI] [PubMed] [Google Scholar]
  12. Curzon G., Green A. R. Rapid method for the determination of 5-hydroxytryptamine and 5-hydroxyindoleacetic acid in small regions of rat brain. Br J Pharmacol. 1970 Jul;39(3):653–655. doi: 10.1111/j.1476-5381.1970.tb10373.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Davies J., Tongroach P. Tetanus toxin and synaptic inhibition in the substantia nigra and striatum of the rat. J Physiol. 1979 May;290(2):23–36. doi: 10.1113/jphysiol.1979.sp012756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dyer R. G. An electrophysiological dissection of the hypothalamic regions which regulate the pre-ovulatory secretion of luteinizing hormone in the rat. J Physiol. 1973 Oct;234(2):421–442. doi: 10.1113/jphysiol.1973.sp010352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dyer R. G., Ellendorff F., MacLeod N. K. Non-random distribution of cell types in the preoptic and anterior hypothalamic areas. J Physiol. 1976 Oct;261(2):495–504. doi: 10.1113/jphysiol.1976.sp011570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dyer R. G., MacLeod N. K., Ellendorff F. Electrophysiological evidence for sexual dimorphism and synaptic convergence in the preoptic and anterior hypothalamic areas of the rat. Proc R Soc Lond B Biol Sci. 1976 Jun 30;193(1113):421–440. doi: 10.1098/rspb.1976.0055. [DOI] [PubMed] [Google Scholar]
  17. ECCLES J. C., FATT P., KOKETSU K. Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J Physiol. 1954 Dec 10;126(3):524–562. doi: 10.1113/jphysiol.1954.sp005226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. EVERETT J. W., SAWYER C. H. A 24-hour periodicity in the "LH-release apparatus" of female rats, disclosed by barbiturate sedation. Endocrinology. 1950 Sep;47(3):198–218. doi: 10.1210/endo-47-3-198. [DOI] [PubMed] [Google Scholar]
  19. Eccles J. C., Llinás R., Sasaki K. The inhibitory interneurones within the cerebellar cortex. Exp Brain Res. 1966;1(1):1–16. doi: 10.1007/BF00235206. [DOI] [PubMed] [Google Scholar]
  20. Evans R. H. Potentiation of the effects of GABA by pentobarbitone. Brain Res. 1979 Jul 27;171(1):113–120. doi: 10.1016/0006-8993(79)90736-4. [DOI] [PubMed] [Google Scholar]
  21. Fenske M., Ellendorff F., Wuttke W. Response of medial preoptic neurons to electrical stimulation of the mediobasal hypothalamus, amygdala and mesencephalon in normal, serotonin or catecholamine deprived female rats. Exp Brain Res. 1975 May 22;22(5):495–507. doi: 10.1007/BF00237350. [DOI] [PubMed] [Google Scholar]
  22. Gardner C. R., Phillips S. W. Neuronal circuitry in the basal septum and preoptic area of the rat. Brain Res. 1977 Sep 9;133(1):95–106. doi: 10.1016/0006-8993(77)90051-8. [DOI] [PubMed] [Google Scholar]
  23. Gardner C. R., Phillips S. W. The influence of the amygdala on the basal septum and preoptic area of the rat. Exp Brain Res. 1977 Aug 31;29(2):249–263. doi: 10.1007/BF00237045. [DOI] [PubMed] [Google Scholar]
  24. Hellon R. F. The marking of electrode tip positions in nervous tissue. J Physiol. 1971;214 (Suppl):12P–12P. [PubMed] [Google Scholar]
  25. Johnston G. A., Beart P. M., Curtis D. R., Game C. J., McCulloch R. M., Maclachlan R. M. Bicuculline methochloride as a GABA antagonist. Nat New Biol. 1972 Dec 13;240(102):219–220. doi: 10.1038/newbio240219a0. [DOI] [PubMed] [Google Scholar]
  26. Krnjević K., Randić M., Straughan D. W. Nature of a cortical inhibitory process. J Physiol. 1966 May;184(1):49–77. doi: 10.1113/jphysiol.1966.sp007903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Köves K., Halász B. Location of the neural structures triggering ovulation in the rat. Neuroendocrinology. 1970;6(3):180–193. doi: 10.1159/000121922. [DOI] [PubMed] [Google Scholar]
  28. MacLeod N. K., Mayer M. L. Electrophysiological analysis of pathways connecting the medial preoptic area with the mesencephalic central grey matter in rats. J Physiol. 1980 Jan;298:53–70. doi: 10.1113/jphysiol.1980.sp013066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. MacLeod N. K., Mayer M. L. Electrophysiological analysis of pathways connecting the medial preoptic area with the mesencephalic central grey matter in rats. J Physiol. 1980 Jan;298:53–70. doi: 10.1113/jphysiol.1980.sp013066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Marco L. A., Brown T. S., Rouse M. E. Unitary responses in ventrolateral thalamus upon intranuclear stimulation. J Neurophysiol. 1967 May;30(3):482–493. doi: 10.1152/jn.1967.30.3.482. [DOI] [PubMed] [Google Scholar]
  31. Mayer M. L. Inhibitory amino acid receptors in the rostral hypothalamus: a microiontophoretic study [proceedings]. J Physiol. 1979 Nov;296:67P–67P. [PubMed] [Google Scholar]
  32. Mellanby J., Thompson P. A. The effect of tetanus toxin at the neuromuscular junction in the goldfish. J Physiol. 1972 Jul;224(2):407–419. doi: 10.1113/jphysiol.1972.sp009902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Miller F. P., Cox R. H., Jr, Snodgrass W. R., Maickel R. P. Comparative effects of p-chloroamphetamine and p-chloro-N-methylamphetamine on rat brain norepinephrine, serotonin and 5-hydroxyindole-3-acetic acid. Biochem Pharmacol. 1970 Feb;19(2):435–442. doi: 10.1016/0006-2952(70)90199-1. [DOI] [PubMed] [Google Scholar]
  34. Moss R. L., Kelly M. J., Dudley C. A. Chemosensitivity of hypophysiotropic neurons to the microelectrophoresis of biogenic amines. Brain Res. 1978 Jan 6;139(1):141–152. doi: 10.1016/0006-8993(78)90066-5. [DOI] [PubMed] [Google Scholar]
  35. Murphy J. T., Renaud L. P. Mechanisms of inhibition in the ventromedial nucleus of the hypothalamus. J Neurophysiol. 1969 Jan;32(1):85–102. doi: 10.1152/jn.1969.32.1.85. [DOI] [PubMed] [Google Scholar]
  36. Nicoll R. A., Eccles J. C., Oshima T., Rubia F. Prolongation of hippocampal inhibitory postsynaptic potentials by barbiturates. Nature. 1975 Dec 18;258(5536):625–627. doi: 10.1038/258625a0. [DOI] [PubMed] [Google Scholar]
  37. Nicoll R. A. Pentobarbital: action on frog motoneurons. Brain Res. 1975 Oct 10;96(1):119–123. doi: 10.1016/0006-8993(75)90582-x. [DOI] [PubMed] [Google Scholar]
  38. Ondo J. G. Gamma-aminobutyric acid effects on pituitary gonadotropin secretion. Science. 1974 Nov 22;186(4165):738–739. doi: 10.1126/science.186.4165.738. [DOI] [PubMed] [Google Scholar]
  39. Osborne R. H., Bradford H. F., Jones D. G. Patterns of amino acid release from nerve-endings isolated from spinal cord and medulla. J Neurochem. 1973 Aug;21(2):407–419. doi: 10.1111/j.1471-4159.1973.tb04260.x. [DOI] [PubMed] [Google Scholar]
  40. Tappaz M. L., Brownstein M. J., Kopin I. J. Glutamate decarboxylase (GAD) and gamma-aminobutyric acid (GABA) in discrete nuclei of hypothalamus and substantia nigra. Brain Res. 1977 Apr 8;125(1):109–121. doi: 10.1016/0006-8993(77)90363-8. [DOI] [PubMed] [Google Scholar]
  41. Vijayan E., McCann S. M. The effects of intraventricular injection of gamma-aminobutyric acid (GABA) on prolactin and gonadotropin release in conscious female rats. Brain Res. 1978 Oct 20;155(1):35–43. doi: 10.1016/0006-8993(78)90303-7. [DOI] [PubMed] [Google Scholar]
  42. Wang R. Y., Aghajanian G. K. Inhibiton of neurons in the amygdala by dorsal raphe stimulation: mediation through a direct serotonergic pathway. Brain Res. 1977 Jan 14;120(1):85–102. doi: 10.1016/0006-8993(77)90499-1. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES