Summary
-
1.
The effect of the fast acting pyrethroid insecticide pentafluorbenzyl (1R,cis)-3-(2,2-dichlorovinyl)-2,2-dimethyl-cyclopropane-carboxylate (fenfluthrin) on impulse generation and on the generator potential in the slowly adapting stretch receptor neuron of the crayfish was investigated by recording intracellularly from the soma and extracellularly from the axon.
-
2.
Fenfluthrin (1 nM) caused prolonged afterdischarges at stimulus conditions which in control experiments elicited only one or a few action potentials. These afterdischarges could last for several minutes and were followed by a pronounced posttetanic hyperpolarization of the membrane, which was due to the activation of the electrogenic Na+/K+ pump.
-
3.
The repetitive activity originated in the axon (at or close to the ‘spike trigger zone’) or in the soma. The axon generated repetitive activity of a higher frequency than the soma.
-
4.
During repetitive activity the soma membrane gradually depolarized and the action potential decreased in amplitude. The falling phase of the action potential became prolonged and the hyperpolarizing afterpotential gradually changed into a depolarizing one. Fenfluthrin had no effect on the resting membrane potential. Similar effects were observed after treatment with the insecticide DDT.
-
5.
In the presence of 0.5 μM tetrodotoxin the shape, amplitude or stretch-dependence of the generator potential was not noticeably affected by fenfluthrin.
-
6.
It is concluded that fenfluthrin primarily affects the generation of action potentials and that it does not affect the transduction process. The repetitive afterdischarges are most readily explained by a prolongation of the sodium current flowing through insecticide-modified voltage-dependent sodium channels. This results in a depolarizing drive on the membrane potential following excitation.
Similar content being viewed by others
Abbreviations
- PTH :
-
post-tetanic hyperpolarization
- SSRN :
-
slowly adapting stretch receptor neuron
- TTX :
-
Tetrodotoxin
References
Akkermans LMA, van den Bercken J, Versluijs-Helder M (1975) Comparative effects of DDT, allethrin, dieldrin and aldrin-transdiol on sense organs ofXenopus laevis. Pestic Biochem Physiol 5:451–457
Albuquerque EX, Grampp W (1968) Effects of tetrodotoxin on the slowly adapting stretch receptor neurone of lobster. J Physiol 195:141–156
Alexandrowicz JS (1951) Muscle receptor organs in the abdomen ofHomarus vulgaris andPalinurus vulgaris. J Microsc Sci 92:163–199
Bercken J van den, Akkermans LMA, van der Zalm JM (1973) DDT-like action of allethrin in the sensory nervous system ofXenopus laevis. Eur J Pharmacol 21:95–106
Brown HM, Ottoson D, Rydquist B (1978) Crayfish stretch receptor: an investigation with voltage-clamp and ion-sensitive electrodes. J Physiol 284:155–179
Brown MC, Stein RB (1966) Quantitative studies on the slowly adapting stretch receptor of the crayfish. Kybernetik 3:175–185
Burkhardt D (1959) Effect of temperature on isolated stretchreceptor organ of the crayfish. Science 129:392–393
Chaplain RA (1975) Evidence for Ca2+ control of the transducer mechanism in crayfish stretch receptor. J Membrane Biol 21:335–351
Clements AN, May TE (1977) The actions of pyrethroids upon the peripheral nervous system and associated organs in the locust. Pestic Sci 8:661–680
Edwards C, Ottoson D (1958) The site of impulse initiation in a nerve cell of a crustacean stretch receptor. J Physiol 143:138–148
Eyzaguirre C, Kuffler SW (1955a) Processes of excitation in the dendrites and in the soma of single isolated sensory nerve cells of the lobster and crayfish. J Gen Physiol 39:87–119
Eyzaguirre C, Kuffler SW (1955b) Further study of soma, dendrite, and axon excitation in single neurons. J Gen Physiol 39:121–153
Fohlmeister J (1980) Electrical processes involved in the encoding of nerve impulses. Biol Cybern 36:103–108
Gammon DW, Brown MA, Casida JE (1981) Two classes of pyrethroid action in the cockroach. Pestic Biochem Physiol 15:181–191
Gestrelius S (1983) Control of impulse firing in lobster stretch receptor neurones. Acta Physiol Scand [Suppl] 513:1–55
Gestrelius S, Grampp W, Sjölin L (1981) Subthreshold and near-threshold membrane currents in lobster stretch receptor neurones. J Physiol 310:191–203
Grampp W (1966) The impulse activity in different parts of the slowly adapting stretch receptor neuron of the lobster. Acta Physiol Scand 66:3–36
Holan G, O'Keefe DF, Virgona C, Waiser R (1978) Structural and biological link between pyrethroids and DDT in new insecticides. Nature 272:734–736
Kaissling KE (1980) Action of chemicals, including (+)trans-permethrin and DDT, on insect olfactory receptors. In: Insect neurobiology and pesticide action. Soc Chem Ind., London, pp 351–358
Klie JW, Wellhöner HH (1973) Voltage clamp studies on the stretch response in the neuron of the slowly adapting crayfish stretch receptor. Pflügers Arch 342:93–104
Kugler J, Chaplain RA (1974) Origin of impulse initiation in the slowly adapting stretch receptor of the crayfish. Pflügers Arch 351:339–350
Leake LD (1977) The action of (S)-3-allyl-2-methyl-4-oxocyclopent-2-enyl-(1R)-trans-chrysanthemate, (S)-bioallethrin, on single neurones in the central nervous system of the leech,Hirudo medicinalis. Pestic Sci 8:713–721
Loewenstein WR, Terzuolo CA, Washizu Y (1963) Separation of transducer and impulse-generating processes in sensory receptors. Science 142:1180–1181
Lund AE, Narahashi T (1981a) Kinetics of sodium channel modification by the insecticide tetramethrin in squid axon membranes. J Pharmacol Exp Ther 219:464–473
Lund AE, Narahashi T (1981b) Modification of sodium channel kinetics by the insecticide tetramethrin in crayfish giant axons. Neurotox 2:213–229
Nakajima S, Takahashi K (1966) Post-tetanic hyperpolarization and electrogenic Na pump in stretch receptor neurone of crayfish. J Physiol 187:105–127
Narahashi T, Lund AE (1980) Giant axons as models for the study of the mechanism of action of insecticides. In: Insect neurobiology and pesticide action. Soc Chem Ind, London, pp 497–505
Naumann K (1981) Chemie der synthetischen Pyrethroid-Insektizide. Chemie der Pflanzenschutz- und Schädlingsbekämpfungsmittel, Bd 7. Springer, Berlin Heidelberg New York
Obara S, Grundfest H (1968) Effects of lithium on different membrane components of crayfish stretch receptor neurons. J Gen Physiol 51:635–654
Osborne MP (1980) The insect synapse: structural functional aspects in relation to insecticidal action. In: Insect neurobiology and pesticide action. Soc Chem Ind, London, pp 29–39
Osborne MP, Hart RJ (1979) Neurophysiological studies of the effects of permethrin upon pyrethroid resistant (kdr) and susceptible strains of dipteran larvae. Pestic Sci 10:407–413
Ottoson D, Swerup C (1982) Studies on the role of calcium in adaptation of the crustacean stretch receptor: Effects of intracellular injection of calcium, EGTA and TEA. Brain Res 244:337–341
Pansa MC, Natalizi GM, Bettini S (1973) Effect of scorpion venom and its fractions on the crayfish stretch receptor organ. Toxicon 11:283–286
Rathmayer W (1979) Anemone toxin discriminates between ionic channels for receptor potential and for action potential production in a sensory neuron. Neurosci Lett 13:313–318
Ringham GI (1971) Origin of nerve impulse in slowly adapting stretch receptor of crayfish. Neurophysiol 34:773–784
Ruigt GSF (1985) Pyrethroids. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 12. Pergamon Press, Oxford, pp 183–263
Ruigt GSF, van den Bercken J (1986) Action of pyrethroids on a nerve muscle preparation of the clawed frog,Xenopus laevis. Pestic Biochem Physiol 25:176–187
Rusinov VS, Ezrokhy VL (1967) Local and spreading excitation in different parts of stretch receptor neurons in crustaceans. Sechenov Physiol J USSR 7:777–783
Smith DO (1980) Mechanisms of action potential propagation failure at sites of axon branching in the crayfish. J Physiol 301:243–259
Smith DO (1983) Extracellular potassium levels and axon excitability during repetitive action potentials in crayfish. J Physiol 336:143–157
Sokolove PG, Cooke IM (1971) Inhibition of impulse activity in a sensory neuron by an electrogenic pump. J Gen Physiol 57:125–163
Terzuolo CA, Washizu Y (1962) Relation between stimulus strength, generator potential and impulse frequency in stretch receptor of Crustacea. J Neurophysiol 25:56–66
Vijverberg HPM, van den Bercken J (1979) Frequency-dependent effects of the pyrethroid insecticide decamethrin in frog myelinated nerve fibres. Eur J Pharmacol 58:501–504
Vijverberg HPM, van den Bercken J (1982a) Action of pyrethroid insecticides on the vertebrate nervous system. Neuropathol Appl Neurobiol 8:421–440
Vijverberg HPM, Ruigt GSF, Bercken van den J (1982b) Structure-related effects of pyrethroid insecticides on the lateralline sense organ and on peripheral nerves of the clawed frog,Xenopus laevis. Pestic Biochem Physiol 18:315–324
Vijverberg HPM, van der Zalm JM, van den Bercken J (1982) Similar mode of action of pyrethroids and DDT on sodium channel gating in myelinated nerves. Nature 295:601–603
Wellhöner HH (1968) Effects of aconitine on the slowly adapting stretch receptor neurone of the crayfish. Pflügers Arch 304:104–117
Wellhöner HH (1970) The action of veratridine on the membrane potential of the crayfish stretch receptor neurone. Naunyn-Schmiedebergs Arch Pharmakol 267:185–188
Wouters W, van den Bercken J (1978) Review: Action of pyrethroids. Gen Pharmacol 9:387–398
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ruigt, G.S.F., Klis, J.F.L. & van den Bercken, J. Pronounced repetitive activity induced by the pyrethroid insecticide, fenfluthrin, in the slowly adapting stretch receptor neuron of the crayfish. J. Comp. Physiol. 159, 43–53 (1986). https://doi.org/10.1007/BF00612494
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00612494