Skip to main content
SpringerLink
Log in

Cholinergic mechanisms and the response to ATP in the systemic vasculature of the rainbow trout

  • Published:
Journal of comparative physiology Aims and scope Submit manuscript

Summary

  1. 1.

    Cholinergic mechanisms in the systemic vasculature of the rainbow trout have been pharmacologically analysed using an isolated trunk preparation perfused at constant flow.

  2. 2.

    Acetylcholine (ACh) causes a two component vasoconstriction comprising a rapid initial peak (response A) and a long-lasting tail on the initial peak (response B). Skeletal muscle contraction is not involved in either response.

  3. 3.

    Response B has a high dose threshold, is nicotinic in nature, and is blocked by α-adrenoreceptor antagonists, procaine, and 0 mM Ca++ plus 20 mM Mg++, indicating a classical indirect action of ACh on sympathetic neurons or chromaffin tissue to cause the release of an adrenergic transmitter.

  4. 4.

    Response A has a lower dose threshold, is nicotinic in nature, is resistant to α-adrenergic, muscarinic cholinergic, and adrenergic neuron blockade, is insensitive to tetrotoxin and 0 mM Ca++ plus 20 mM Mg++, but is blocked with some specificity by procaine.

  5. 5.

    The properties of the nicotinic receptors of response A differ from those of the traditional ganglionic and skeletal muscle types of higher vertebrates.

  6. 6.

    Response A is mimicked by ATP, which appears to act by a direct mechanism in the preparation.

  7. 7.

    It is concluded that response A reflects either direct stimulation of nicotinic receptors on vascular tissue or an indirect nicotinic effect resulting in the release of a non-adrenergic, non-cholinergic transmitter such as ATP.

  8. 8.

    Unlike the situation in higher vertebrates, no muscarinic dilatory responses to ACh occur in the preparation.

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

Access this article

Log in via an institution

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

  • Abrahamsson, T., Nilsson, S.: Effects of nerve sectioning and drugs on the catecholamine content in the spleen of the cod,Gadus morhua. Comp. Biochem. Physiol.51 C, 231–233 (1975)

    Google Scholar 

  • Abrahamsson, T., Nilsson, S.: Phenylethanolamine-N-methyl transferase (PNMT) activity and catecholamine content in chromaffin tissue and sympathetic neurons in the cod,Gadus morhua. Acta Physiol. Scand.96, 94–99 (1976)

    Google Scholar 

  • Ariens, E.J.: Molecular pharmacology. New York: Academic Press Inc. 1964

    Google Scholar 

  • Augustinsson, K.-B., Fänge, R., Johnels, A., Östlund, E.: Histological, physiological and biochemical studies on the heart of two cyclostomes, hagfish (Myxine) and lamprey (Lampetra). J. Physiol.131, 257–276 (1956)

    Google Scholar 

  • Belaud, A., Peyraud-Waitzenegger, M., Peyraud, C.: Étude comparée des réactions vasomotrices des branchies perfusées de deux Teleosteens: la Carpe et le Congre. C. R. Soc. Biol. (Paris)165, 1114–1118 (1971)

    Google Scholar 

  • Bowman, W.C., Webb, S.N.: Neuromuscular blocking and ganglion blocking activities of some acetylcholine antagonists in the cat. J. Pharm. Pharmacol.24, 762–772 (1972)

    Google Scholar 

  • Boyd, H.: ATP as a nerve transmitter substance. J. theor. Biol.42, 49–53 (1973)

    Google Scholar 

  • Burnstock, G.: Evolution of the autonomic innervation of visceral and cardiovascular systems in vertebrates. Pharmacol. Rev.21, 247–324 (1969)

    Google Scholar 

  • Burnstock, G.: Purinergic nerves. Pharmacol. Rev.24, 509–581 (1972)

    Google Scholar 

  • Burnstock, G.: Comparative studies of purinergic nerves. J. exp. Zool.194, 103–134 (1975)

    Google Scholar 

  • Burnstock, G., Campbell, G., Satchell, D., Smythe, A.: Evidence that adenosine triphosphate or a related nucleotide is the transmitter substance released by non-adrenergic inhibitory nerves in the gut. Brit. J. Pharmacol.40, 668–688 (1970)

    Google Scholar 

  • Burnstock, G., Dumsday, B., Smythe, A.: Atropine resistant excitation of the urinary bladder: the possibility of transmission via nerves releasing a purine nucleotide. Brit. J. Pharmacol.44, 451–461 (1972)

    Google Scholar 

  • Campbell, G.: Autonomic nervous systems. In: Fish physiology, Vol. IV (eds. W.S. Hoar, D.J. Randall) New York: Academic Press Inc. 1970

    Google Scholar 

  • Carter, R.H.: Resistance to tetrodotoxin in toad sympathetic nerves. J. Pharm. Pharmacol.21, 394–395 (1969)

    Google Scholar 

  • Chan, D.K.O., Chow, P.H.: The effects of acetylcholine, biogenic amines and other vasoactive agents on the cardiovascular functions of the eel,Anguilla japonica. J. exp. Zool.196, 13–26 (1976)

    Google Scholar 

  • Comroe, J.H. Jr., Mortimer, L.: The respiratory and cardiovascular responses of temporally separated aortic and carotid bodies to cyanide, nicotine, phenyldiguanide, and serotonin. J. Pharmacol. exp. Ther.146, 33–41 (1964)

    Google Scholar 

  • Crossland, J.: Lewis's pharmacology, 4th ed. London: E. and S. Livingstone 1970

    Google Scholar 

  • Douglas, W.W.: Histamine and anti-histamines; 5-hydroxytryptamine and antagonists. In: The pharmacological basis of therapeutics, 5th ed. (eds. L.S. Goodman, A. Gilman). New York: MacMillan 1975

    Google Scholar 

  • Falck, B., Mecklenburg, C. von, Myhrberg, H., Persson, H.: Studies on adrenergic and cholinergic receptors in the isolated hearts ofLampetra fluviatilis (Cyclostomata) andPleuronectes platessa (Teleostei). Acta Physiol. Scand.68, 64–71 (1966)

    Google Scholar 

  • Goldberg, L.I.: Cardiovascular and renal actions of dopamine: potential clinical applications. Pharmacol. Rev.24, 1–29 (1972)

    Google Scholar 

  • Hanson, K.M., Moore, F.T.: Effects of intraluminal pressure in the colon on its vascular pressureflow relationships. Proc. Soc. Exp. Biol. Med.131, 373–376 (1969)

    Google Scholar 

  • Hidaka, T., Kuriyama, H.: Responses of the smooth muscle cell membrane of the guinea pig jejunum elicited by field stimulation. J. gen. Physiol.53, 471–486 (1969)

    Google Scholar 

  • Holmgren, S., Nilsson, S.: Drug effects in isolated artery strips from two teleosts,Gadus morhua andSalmo gairdneri. Acta. Physiol. Scand.90, 431–437 (1974)

    Google Scholar 

  • Holmgren, S., Nilsson, S.: Effects of some adrenergic and cholinergic drugs on isolated spleen strips from the cod,Gadus morhua. Europ. J. Pharmacol.32, 163–169 (1975)

    Google Scholar 

  • Innes, I.R., Nickerson, M.: Atropine, scopolamine, and related antimuscarinic drugs. In: The pharmacological basis of therapeutics, 5th ed. (eds. L.S. Goodman, A. Gilman). New York: MacMillan 1975

    Google Scholar 

  • Kirby, S., Burnstock, G.: Comparative pharmacological studies of isolated spiral strips of large arteries from lower vertebrates. Comp. Biochem. Physiol.28, 307–319 (1969)

    Google Scholar 

  • Klaverkamp, J.F., Dyer, D.C.: Autonomic receptors in isolated rainbow trout vasculature. European J. Pharmacol.28, 25–34 (1974)

    Google Scholar 

  • Koelle, G.B.: Neurohumoral transmission and the autonomic nervous system. In: The pharmacologyical basis of therapeutics, 5th ed. (eds. L.S. Goodman, A. Gilman). New York: MacMillan 1975a

    Google Scholar 

  • Koelle, G.B.: Parasympathomimetic agents. In: The pharmacological basis of therapeutics, 5th ed. (eds. L.S. Goodman, A. Gilman) New York: MacMillan 1975b

    Google Scholar 

  • Koelle, G.B.: Neuromuscular blocking agents. In: The pharmacological basis of therapeutics, 5th ed. (eds. L.S. Goodman, A. Gilman) New York: MacMillan 1975c

    Google Scholar 

  • Koppanyi, T., MacFarlane, M.D.: The cholinergic receptor systems of atria. Ann. N.Y. Acad. Sci.144, 543–557 (1967)

    Google Scholar 

  • Krnjevic, K.: Chemical nature of synaptic transmission in vertebrates. Physiol. Rev.54, 418–540 (1974)

    Google Scholar 

  • Lukomskaya, N.J., Michelson, M.J.: Pharmacology of the isolated heart of the lampreyLampetra fluviatilis. Comp. Gen. Pharmacol.3, 213–225 (1972)

    Google Scholar 

  • Maxwell, R.A.: Concerning the mode of action of guanethidine and some derivatives in augmenting the vasomotor action of adrenergic amines in vascular tissues of the rabbit. J. Pharmacol. exp. Ther.148, 320–328 (1965)

    Google Scholar 

  • Nickerson, M., Collier, B.: Drugs inhibiting adrenergic nerves and structures innervated by them. In: The pharmacological basis of therapeutics, 5th ed. (eds. L.S. Goodman, A. Gilman). New York: MacMillan 1975

    Google Scholar 

  • Nilsson, S.: Autonomic vasomotor innervation in the gas gland of the swim bladder of a teleost (Gadus morhua). Comp. Gen. Pharmacol.3, 371–375 (1972)

    Google Scholar 

  • Nilsson, S., Grove, D.J.: Adrenergic and cholinergic innervation of the spleen of the cod:Gadus morhua. Europ. J. Pharmacol.28, 135–143 (1974)

    Google Scholar 

  • Östlund, E., Fänge, R.: Vasodilation by adrenaline and noradrenaline and the effects of some other substances on perfused fish gills. Comp. Biochem. Physiol.5, 307–309 (1962)

    Google Scholar 

  • Rang, H.P., Ritter, J.M.: On the mechanism of desensitization at cholinergic receptors. Mol. Pharmacol.6, 357–382 (1970)

    Google Scholar 

  • Reite, O.B.: The evolution of vascular smooth muscle responses to histamine and 5-hydroxytryptamine. I. Occurrence of stimulatory actions in fish. Acta physiol. Scand.75, 221–239 (1969)

    Google Scholar 

  • Reite, O.B.: Comparative physiology of histamine. Physiol. Rev.52, 778–819 (1972)

    Google Scholar 

  • Richards, B.D., Fromm, P.O.: Patterns of blood flow through filaments and lamellae of isolatedperfused rainbow trout (Salmo gairdneri) gills. Comp. Biochem. Physiol.29, 1063–1070 (1969)

    Google Scholar 

  • Richards, B.D., Fromm, P.O.: Sodium uptake by isolated-perfused gills of rainbow trout (Salmo gairdneri). Comp. Biochem. Physiol.33, 303–310 (1970)

    Google Scholar 

  • Ritchie, J.M., Cohen, P.J.: Cocaine; procaine and other synthetic local anaesthetics. In: The pharmacological basis of therapeutics, 5th ed. (eds. L.S. Goodman, A. Gilman). New York: MacMillan 1975

    Google Scholar 

  • Sjöstrand, S.E., Sjogren, C., Schmiterlow, A.: Responses of the rabbit and cat urinary bladders in situ to drugs and to nerve stimulation. Acta pharmacol. toxicol.31, 241–254 (1972)

    Google Scholar 

  • Sneddon, J.D., Smythe, A., Satchell, D., Burnstock, G.: An investigation of the identity of the transmitter substance released by non-adrenergic, non-cholinergic excitatory nerves supplying the small intestine of some lower vertebrates. Comp. Gen. Pharmacol.4, 53–60 (1973)

    Google Scholar 

  • Spedding, M., Weetman, D.F.: Identification of separate receptors for adenosine and adenosine 5′-triphosphate in causing relaxations of the isolated taenia of the guinea-pig caecum. Brit. J. Pharmacol.57, 305–310 (1976)

    Google Scholar 

  • Stray-Pederson, S.: Vascular responses induced by drugs and by vagal stimulation in the swimbladder of the eel,Anguilla vulgaris. Comp. Gen. Pharmac.1, 358–364 (1970)

    Google Scholar 

  • Takata, M., Moore, J.W., Kao, C.Y., Fuhrman, F.A.: Blockage of sodium conductance increase in lobster giant axon by tarichatoxin (tetrodotoxin). J. gen. Physiol.49, 977–988 (1966)

    Google Scholar 

  • Volle, R.L., Koelle, G.B.: Ganglionic stimulating and blocking agents. In: The pharmacological basis of therapeutics, 5th ed. (eds. L.S. Goodman, A. Gilman). New York: MacMillan 1975

    Google Scholar 

  • Wilson, A., Schild, H.O., Modell, W.: Applied pharmacology, 11th ed. New York: Churchill Livingstone 1975

    Google Scholar 

  • Wolf, K.: Physiological salines for freshwater teleosts. Progr. Fish Cult.25, 135–140 (1963)

    Google Scholar 

  • Wood, C.M.: A pharmacological analysis of the adrenergic and cholinergic mechanisms regulating branchial vascular resistance in the rainbow trout (Salmo gairdneri). Canad. J. Zool.53, 1569–1577 (1975)

    Google Scholar 

  • Wood, C.M.: Pharmacological properties of the adrenergic receptors regulating systemic vascular resistance in the rainbow trout. J. comp. Physiol.107, 211–228 (1976)

    Google Scholar 

  • Wood, C.M., Shelton, G.: Physical and adrenergic factors affecting systemic vascular resistance in the rainbow trout: a comparison with branchial vascular resistance. J. exp. Biol.63, 505–523 (1975)

    Google Scholar 

Download references

Author information

Author notes

  1. Chris M. Wood

    Present address: Dept. of Biology, McMaster University, 1280 Main St. West, L8S 4K1, Hamilton, Ontario, Canada

Authors and Affiliations

  1. School of Biological Sciences, University of East Anglia, NR4 7TJ, Norwich, U.K.

    Chris M. Wood

Authors
  1. Chris M. Wood
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wood, C.M. Cholinergic mechanisms and the response to ATP in the systemic vasculature of the rainbow trout. J Comp Physiol B 122, 325–345 (1977). https://doi.org/10.1007/BF00692519

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00692519

Keywords

Search

Navigation