Skip to main content
Log in

Angiotensin excites hippocampal pyramidal cells by two mechanisms

  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Summary

  1. 1.

    The mechanism of action of angiotensins was studied on CA 1 pyramidal cells in hippocampal slices of the rat. Extracellular field potentials, single-cell action potentials, and intracellular excitatory and inhibitory postsynaptic potentials (epsps and ipsps) were recorded.

  2. 2.

    Angiotensin II and Des-Asp1-angiotensin II added to the perfusion fluid caused a dose-dependent increase in extracellularly recorded epsps and synaptically evoked population spikes. Either the neurons were depolarized by angiotensins and their firing frequency of action potentials increased or the membrane potential was unaffected.

  3. 3.

    Local application of angiotensins caused a depolarization associated with a conductance increase which was resistant to synaptic isolation.

  4. 4.

    Evoked and spontaneous inhibitory postsynaptic potentials were reduced by angiotensins, but the effects ofγ-aminobutyric acid (GABA) on soma and dendrites were unchanged.

  5. 5.

    All angiotensin effects were blocked by the specific antagonist Sar1, Ala8-angiotensin II (saralasin).

  6. 6.

    It is concluded that angiotensins excite CA 1 pyramidal cells by a direct and a disinhibitory mechanism.

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.

Similar content being viewed by others

References

  • Alger, B. E., and Nicoll, R. A. (1980). Spontaneous inhibitory postsynaptic potentials in hippocampus: Mechanism for tonic inhibition.Brain Res. 200195–200.

    Google Scholar 

  • Andersen, P. (1975). Organization of hippocampal neurons and their interconnections. InThe Hippocampus (L. Isaacson and K. H. Pribram, Eds.), Plenum Press, New York, pp. 155–175.

    Google Scholar 

  • Andersen, P., Sundberg, S. H., Sveen, O., and Wigström, H. (1977). Specific and long-lasting potentiation of synaptic transmission in hippocampal slices.Nature 266736–737.

    Google Scholar 

  • Andersen, P., Dingledine, R., Gjerstad, L., Langmoen, I. A., and Mosfeldt-Laursen, A. (1980). Two different responses of hippocampal pyramidal cells to application of gamma-amino butyric acid.J. Physiol. (Lond.) 305279–296.

    Google Scholar 

  • Buckle, P. J., and Haas, H. L. (1982). Enhancement of synaptic transmission by 4-aminopyridine in hippocampal slices of the rat.J. Physiol. (Lond.) 326(in press).

  • Celio, M. R., Clemens, D. L., and Inagami, T. (1980). Renin in anterior pituitary, pineal and neuronal cells of mouse brain: Immunohistochemical localization.Biomed. Res. 1427–431.

    Google Scholar 

  • Changaris, D. G., Keil, L. C., and Severs, W. B. (1978). Angiotensin II immunohistochemistry of the rat brain.Neuroendocrinology 25257–274.

    Google Scholar 

  • Curtis, D. R., and Johnston, G. A. R. (1974). Amino acid transmitters in the mammalian central nervous system.Ergeb. Physiol. 6997–188.

    Google Scholar 

  • Dingledine, R., and Gjerstad, L. (1980). Reduced inhibition during epileptiform activity in the in vitro hippocampal slice.J. Physiol. (Lond.) 305297–313.

    Google Scholar 

  • Epstein, A. N., Fitzsimons, J. T., and Rolls, B. J. (1970). Drinking induced by injection of angiotensin II into the brain of the rat.J. Physiol. (Lond.) 210457–474.

    Google Scholar 

  • Felix, D. (1976). Peptide and acetylcholine action on neurons of the cat subfornical organ.Naunyn Schmiedebergs Arch. Pharmacol. 29215–20.

    Google Scholar 

  • Felix, D., and Schlegel, W. (1978). Angiotensin receptive neurones in the subfornical organ. Structureactivity relations.Brain Res. 149107–116.

    Google Scholar 

  • Fischer-Ferraro, C., Nahmod, V. E., Goldstein, D. J., and Finkielman, S. (1971). Angiotensin and renin in rat and dog brain.J. Exp. Med. 133353–361.

    Google Scholar 

  • Fitzsimons, J. T. (1972). Thirst.Physiol. Rev. 52468–561.

    Google Scholar 

  • Fuxe, K., Ganten, D., Hökfelt, T. M., and Bolme, P. (1976). Immunohistochemical evidence for the existence of angiotensin II-containing nerve terminals in the brain and spinal cord in the rat.Neurosci. Lett. 2229–234.

    Google Scholar 

  • Gähwiler, B. H. (1980). Excitatory action of opioid peptides and opiates on cultured hippocampal pyramidal cells.Brain Res. 194193–203.

    Google Scholar 

  • Gähwiler, B. H., and Dreifuss, J. J. (1980). Transition from random to phasic firing induced in neurons cultured from the hypothalamic supraoptic area.Brain Res. 193415–425.

    Google Scholar 

  • Ganten, D., Minnich, J. E., Granger, P., Hayduk, K., Brecht, H. M., Barbeau, A., Boucher, R., and Genest, J. (1971). Angiotensin-forming enzyme in brain tissue.Science 17364–65.

    Google Scholar 

  • Ganten, D., Hutchinson, J. S., Schelling, P., Ganten, U., and Fischer, H. (1976). The iso-renin angiotensin systems in extrarenal tissue.Clin. Exp. Pharmacol. Physiol. 3103–126.

    Google Scholar 

  • Haas, H. L. (1982). Cholinergic disinhibition in hippocampal slices of the rat.Brain Res. 233200–204.

    Google Scholar 

  • Haas, H. L., and Ryall, R. W. (1980). Is excitation by enkephalines of hippocampal neurones in the rat due to presynaptic facilitation or to disinhibition?J. Physiol. (Lond.) 308315–330.

    Google Scholar 

  • Haas, H. L., Schaerer, B., and Vosmansky, M. (1979). A simple perfusion chamber for the study of nervous tissue slices in vitro.J. Neurosci. Methods 1323–325.

    Google Scholar 

  • Haas, H. L., Felix, D., Celio, M. R., and Inagami, T. (1980). Angiotensin II in the hippocampus. A histochemical and electrophysiological study.Experientia 361394–1395.

    Google Scholar 

  • Hesse, G. W., and Teyler, T. J. (1976). Reversible loss of hippocampal long term potentiation following electroconvulsive seizures.Nature (Lond.) 264562–564.

    Google Scholar 

  • Hirose, S., Yokosawa, H., Inagami, T., and Workman, R. J. (1980). Renin and prorenin in hog brain: Ubiquitous distribution and high concentration in the pituitary and pineal.Brain Res. 191489–499.

    Google Scholar 

  • Huwyler, T., and Felix, D. (1980). Angiotensin II-sensitive neurons in septal areas of the rat.Brain Res. 195187–195.

    Google Scholar 

  • Inagami, T., Clemens, D. L., Celio, M. R., Brown, A., Sandru, L., Herschkowitz, N., Hoffman, L. H., and Kasselberg, A. G. (1980). Inflammatory peptide in spinal cord: Evidence that the mediator of antidromic vasodilatation is not substance P.Neurosci. Lett. 1891–98.

    Google Scholar 

  • Köller, M., Krause, H. P., Hoffmeister, F., and Ganten, D. (1979). Endogenous brain angiotensin II disrupts passive avoidance behavior in rats.Neurosci. Lett. 1471–75.

    Google Scholar 

  • Morgan, J. M., and Routtenberg, A. (1977). Angiotensin injected into the neostriatum after learning disrupts retention performance.Science 19687–89.

    Google Scholar 

  • Nicoll, R. A., and Barker, J. L. (1971). Excitation of supraoptic neurosecretory cells by angiotensin II.Nature New Biol. (Lond.) 233172–173.

    Google Scholar 

  • Nicoll, R. A., Alger, B. E., and Jahr, C. E. (1980). Enkephalin blocks inhibitory pathways in the vertebrate CNS.Nature (Lond.) 28722–25.

    Google Scholar 

  • Peach, M. J. (1977). Renin-angiotensin system: Biochemistry and mechanisms of action.Physiol. Rev. 57313–370.

    Google Scholar 

  • Phillips, M. I., and Felix, D. (1976). Specific angiotensin II receptive neurons in the cat subfornical organ.Brain Res. 109531–540.

    Google Scholar 

  • Phillips, M. I., Felix, D., Hoffman, W. E., and Ganten, D. (1977). Angiotensin-sensitive sites in the brain ventricular system. InSociety for Neuroscience Symposia, Vol. 2 Soc. Neurosci. Bethesda, Md., pp. 308–339.

    Google Scholar 

  • Phillips, M. I., Weihenmeyer, J., Felix, D., Ganten, D., and Hoffman, W. E. (1979). Evidence for an endogenous brain reninangiotensin system.Fed. Proc. 382260–2266.

    Google Scholar 

  • Ramsay, D. J. (1979). The brain renin angiotensin system: A reevaluation.Neuroscience 4313–321.

    Google Scholar 

  • Reid, I. A., (1977). Is there a brain renin-angiotensin system?Circ. Res. 41147–153.

    Google Scholar 

  • Schelling, P., Speck, G., Unger, T., and Ganten, D. (1980). The brain renin-angiotensin system: Biochemistry, localization and functional aspects. InAdvances in Experimental Medicine: A Centenary Tribute to Claude Bernard, (H. Parvez and S. Parvez, Eds.), Elsevier, Amsterdam, pp. 243–288.

    Google Scholar 

  • Schwartzkroin, P. A., and Prince, D. A. (1980). Changes in excitatory and inhibitory synaptic potentials leading to epileptogenic activity.Brain Res. 18361–76.

    Google Scholar 

  • Severs, W. B., and Daniels-Severs, A. E. (1973). Effects of angiotensin on the central nervous system.Pharmacol. Rev. 25415–449.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haas, H.L., Felix, D. & Davis, M.D. Angiotensin excites hippocampal pyramidal cells by two mechanisms. Cell Mol Neurobiol 2, 21–32 (1982). https://doi.org/10.1007/BF00735064

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00735064

Key words

Navigation