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Nicotinic acetylcholine receptors on a cholinergic nerve terminal in the cockroach,Periplaneta americana

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Summary

Intracellular microelectrode recording and ionophoretic application of carbamylcholine (CCh) were used to compare the cholinergic sensitivity of postsynaptic dendrites of an identified neurone with that of an identified presynaptic cholinergic axon.

The axon of the lateral filiform hair sensory neurone (LFHSN) in the first-instar cockroachPeriplaneta americana was found to be as sensitive to CCh as the dendritic regions of giant interneurone 3 (GI 3). The CCh response of both neurones was unaffected by replacing Ca2+ with Mg2+, confirming that the ACh receptors are present on the neurones under test. The CCh response of both neurones was mimicked by ionophoretic application of nicotine. The responses were blocked by 10−5 M mecamylamine and 10−6 M d-tubocurarine and were not affected by muscarinic antagonists, suggesting that the ACh receptors present on GI 3 and LFHSN are predominantly nicotinic.

The muscarinic agonist oxotremorine and the antagonists atropine and quinuclidinyl benzilate had no modulatory effect on LFHSN-GI 3 synaptic transmission.

The latency of the LFHSN response to CCh was consistent with the hypothesis that ACh receptors are situated on the main axon/terminal within the neuropil of the ganglion. It has previously been shown that this region of the axon does not form output synapses (Blagburn et al. 1985a). This indirect evidence indicates that presynaptic or extrasynaptic ACh receptors are present in the membrane of a cholinergic axon.

LFHSN was depolarized by synaptically-released ACh after normal or evoked spike bursts, suggesting that the nicotinic ACh receptors act as autoreceptors. However, it was not possible to obtain direct evidence to support the hypothesis that these receptors modulate ACh release.

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Abbreviations

CCh :

carbamylcholine

GI :

giant interneurone

FHSN :

filiform hair sensory neurone

LFHSN :

lateral filiform hair sensory neurone

R in :

input resistance

ΔV :

depolarization

V m :

resting potential

References

  • Bacon JP, Altman JS (1977) A silver-intensification method for cobalt-filled neurones in wholemount preparations. Brain Res 138:359–363

    Google Scholar 

  • Blagburn JM, Sattelle DB (1987) Presynaptic depolarization mediates presynaptic inhibition at a synapse between an identified mechanosensory neurone and giant interneurone 3 in the first instar cockroach,Periplaneta americana. J Exp Biol 127:135–157

    Google Scholar 

  • Blagburn JM, Beadle DJ, Sattelle DB (1985a) Development of synapses between identified sensory neurones and giant interneurones in the cockroachPeriplaneta americana. J Embryol Exp Morphol 86:227–246

    Google Scholar 

  • Blagburn JM, Beadle DJ, Sattelle DB (1985b) Development of chemosensitivity of an identified insect interneurone. J Neurosci 5:1166–1174

    Google Scholar 

  • Blagburn JM, Beadle DJ, Sattelle DB (1986) Differential synaptic input of filiform hair sensory neurones on to giant interneurones in the first instar cockroach. J Insect Phyisol 32:591–595

    Google Scholar 

  • Breer H, Knipper M (1984) Characterization of acetylcholine release from insect synaptosomes. Insect Biochem 14:337–344

    Google Scholar 

  • Callec JJ (1974) Synaptic transmission in the central nervous system of insects. In: Treherne JE (ed) Insect neurobiology. North-Holland-American Elsevier, New York, pp 119–185

    Google Scholar 

  • Callec JJ (1985) Synaptic transmission in the central nervous system. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 5. Pergamon Press, Oxford New York Toronto Sydney Paris Frankfurt, pp 139–180

    Google Scholar 

  • Callec JJ, Guillet JC, Pichon Y, Boistel J (1971) Further studies on synaptic transmission in insects. II. Relations between sensory information and its synaptic integration at the level of a single giant axon in the cockroach. J Exp Biol 55:123–149

    Google Scholar 

  • Callec JJ, David JA, Sattelle DB (1982) Ionophoretic application of acetylcholine on to the dendrites of an identified giant interneurone (GI 1) in the cockroachPeriplaneta americana. J Insect Phyisol 28:1003–1008

    Google Scholar 

  • Daley DL, Vardi N, Appignani B, Camhi JM (1981) Morphology of the giant interneurons and cereal nerve projections of the American cockroach. J Comp Neurol 196:41–52

    Google Scholar 

  • Dionne V (1976) Characterization of drug iontophoresis with a fast microassay technique. Biophys J 16:705–717

    Google Scholar 

  • Duncan CJ, Publicover SJ (1979) Inhibitory effects of cholinergic agents on the release of transmitter at the frog neuromuscular junction. J Physiol (Lond) 294:91–103

    Google Scholar 

  • Goodman CS, Spitzer NC (1980) Embryonic development of neurotransmitter receptors in grasshoppers. In: Sattelle DB, Hall LM, Hildebrand JG (eds) Receptors for neurotransmitters, hormones, and pheromones in insects. Elsevier/North Holland Biomedical Press, Amsterdam, pp 195–207

    Google Scholar 

  • Harrow ID, Hue B, Pelhate M, Sattelle DB (1980) Cockroach giant interneurones stained by cobalt-backfilling of dissected axons. J Exp Biol 84:341–343

    Google Scholar 

  • Kilbinger H (1984) Presynaptic muscarinic receptors modulating acetylcholine release. Trends Pharmacol Sci 5:103–105

    Google Scholar 

  • Kilbinger H, Wagner B (1979) The role of presynaptic muscarine receptors in regulating acetylcholine release from peripheral cholinergic neurones. In: Langer SZ, Starke K, Dubocovich ML (eds) Presynaptic receptors (Advances in the biosciences, vol 18). Pergamon Press, Oxford New York Toronto Sydney Paris Frankfurt, pp 347–352

    Google Scholar 

  • Koketsu K, Yamada M (1982) Presynaptic muscarinic receptors inhibiting active acetylcholine release in the bullfrog sympathetic ganglion. Br J Pharmacol 77:75–82

    Google Scholar 

  • Lummis SCR, Sattelle DB (1986) [N-methyl-3H]scopolamine binding sites in the central nervous system of the cockroachPeriplaneta americana. Arch Insect Biochem Physiol 3:339–347

    Google Scholar 

  • Meyer MR, Reddy GR, Edwards JS (1986) Metabolic changes in deafferented central neurons of an insect,Acheta domesticus. I. Effects on cholinergic binding sites and acetylcholinesterase. J Neurosci 6:1676–1684

    Google Scholar 

  • Michaelson DM, Avissar S, Kloog Y, Sokolovsky M (1979) Mechanism of acetylcholine release: Possible involvement of presynaptic muscarinic receptors in regulation of acetylcholine release and protein phosphorylation. Proc Natl Acad Sci USA 76:6336–6340

    Google Scholar 

  • Miledi R, Molenar P, Polak R (1978)α-Bungarotoxin enhances transmitter released at the neuromuscular junction. Nature 272:641–642

    Google Scholar 

  • Morita K, North RA, Tokimasa T (1982) Muscarinic presynaptic inhibition of synaptic transmission in myenteric plexus of guinea-pig ileum. J Physiol (Lond) 333:141–149

    Google Scholar 

  • Nordstrom O, Bartfai T (1980) Muscarinic autoreceptor regulates acetylcholine release in rat hippocampus: in vitro evidence. Acta Physiol Scand 108:347–353

    Google Scholar 

  • Peper K, Bradley RJ, Dreyer F (1982) The acetylcholine receptor at the neuromuscular junction. Physiol Rev 62:1271–1340

    Google Scholar 

  • Purves RD (1977) The time course of cellular responses to iontophoretically applied drugs. J Theor Biol 65:327–344

    Google Scholar 

  • Purves RD (1981) Microelectrode methods for intracellular recording and ionophoresis. Academic Press, London New York Toronto Syndney San Francisco

    Google Scholar 

  • Roeder KD, Tozian L, Weiant EA (1960) Endogenous nerve activity and behaviour in the mantis and cockroach. J Insect Physiol 4:45–62

    Google Scholar 

  • Sattelle DB (1980) Acetylcholine receptors of insects. Adv Insect Physiol 15:215–315

    Google Scholar 

  • Sattelle DB, Harow ID, Hue B, Pelhate M, Gepner JI, Hall LM (1983)α-Bungarotoxin blocks excitatory synaptic transmission between cereal sensory neurones and giant interneurone 2 of the cockroachPeriplaneta americana. J Exp Biol 107:473–489

    Google Scholar 

  • Szerb JC (1979) Autoregulation of acetylcholine release. In: Langer SZ, Starke K, Dubocovich ML (eds) Presynaptic Receptors (Advances in the biosciences, vol 18). Pergamon Press, Oxford New York Toronto Syndney Paris Frankfurt, pp 293–298

    Google Scholar 

  • Westin J, Langberg JL, Camhi JM (1977) Responses of giant interneurons of the cockroachPeriplaneta americana to wind puffs of different directions and velocities. J Comp Physiol 121:307–324

    Google Scholar 

  • Wilson DF (1982) Influence of presynaptic receptors on neuromuscular transmission in the rat. Am J Physiol 242:C366-C372

    Google Scholar 

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Blagburn, J.M., Sattelle, D.B. Nicotinic acetylcholine receptors on a cholinergic nerve terminal in the cockroach,Periplaneta americana . J. Comp. Physiol. 161, 215–225 (1987). https://doi.org/10.1007/BF00615242

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