Summary
Recording from the dendrite membrane indicated a resting potential of −51.6 mV, which was reduced by inhibition of the Na+/K+ pump. Voltage clamp at rest revealed a small inward current between −50 and −80 mV and a larger outward current at clamp potentials of −40 to +30 mV. Using ramp-changes of muscle tension as stimuli a time-variant tension-induced inward current (TIC) became apparent, the amplitude of which decreased towards larger depolarizing voltages until at +18 mV the current reversed the direction. The time course of the conductance changes corresponds to similar phases in the generator potential. The outward current only responded to fast reductions in tension, decreasing transiently. A contribution of the active Na+/K+ pump to the hyperpolarizing potential response is suggested by the effects of K-removal or Na-substitution by Li+. In Na-free choline chloride media the generator potential and the TIC was depressed by 70–85%. Additional removal of Ca2+ abolished the TIC. In contrast, lowering the Ca2+ level in presence of Na+ decreased the membrane resistance and markedly enhanced the TIC (maximally eightfold at 10−5 m Ca2+) while 75–150mm Ca2+ or intracellular application of a Ca-ionophore had the reverse effect.
Similar content being viewed by others
References
Brown, H. M., Hagiwara, S., Koike, H. Meech, R. M. 1970. Membrane properties of a barnacle photoreceptor examined by the voltage clamp technique.J. Physiol. 208: 385
Carpenter, D. O., Alving, B. 1968. A contribution of an electrogenic Na+-pump to membrane potential inAplysia neurons.J. Gen. Physiol. 52:1
Case, G. D., Vanderkooi, J. M., Scarpa, A. 1974. Physical properties of biological membranes determined by the fluorescence of the calcium ionophore A 23187.Arch. Biochem. Biophys. 162:174
Chaplain, R. A., Michaelis, B., Coenen, R. 1971. Systems analysis of biological receptors. I. A quantitative description of the input-output characteristics of the slowly adapting stretch receptor of the crayfish.Kybernetik 9:85
Coenen, R., Chaplain, R. A. 1973. Systems analysis of biological receptors. II. The transfer characteristics of the frog muscle spindle.Kybernetik 13:183
Dunham, E. T., Glynn, I. M. 1961. Adenosine triphosphatase activity and the active movements of alkali metal ions.J. Physiol. 156:274
Edwards, C. C., Terzuolo, C. A., Washizu, Y. 1963. The effects of changes of the ionic environment upon an isolated crustancean sensory neuron.J. Neurophysiol. 26:948
Eimerl, S., Savion, N., Heichal, O., Selinger Z. 1974. Induction of enzyme secretion in rat pancreatic slices using the ionophore A 23187 and calcium. An experimental by-pass of the hormone receptor pathway.J. Biol. Chem. 249:3991
Eyzaguirre, C., Kuffler S. W. 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
Eyzaguirre, C., Kuffler, S. W. 1955b. Further study of soma dendrite and axon excitation in single neurons.J. Gen. Physiol. 39:121
Florey, E., Florey, E. 1955. Microanatomy of the abdominal stretch receptor of the crayfish (Astacus fluviatilis L.).J. Gen. Physiol. 39:69
Frankenhaeuser, B., Hodgkin, A. L. 1957. The action of calcium in the electrical properties of squid axons.J. Physiol. 137:218
Fulpius, B., Baumann, F. 1969. Effects of sodium, potassium, and calcium ions on slow and spike potentials in single photoreceptor cells.J. Gen. Physiol. 53:541
Geduldig, D., Junge, D. 1968. Sodium and calcium components of action potentials in theAplysia giant neurone.J. Physiol. 199:347
Gray, J. A. B., Sato, M. 1953. Properties of receptor potentials in Pacinian corpuscles.J. Physiol. 122:610
Hagins, W. A. 1972. The visual process.Annu. Rev. Biophys. Bioeng. 1:131
Harreveldt, A. van 1936. A physiological solution for freshwater crustaceans.Proc. Soc. Exp. Biol. 34:428
Hasan, Z., Houk, J. C. 1972. Non-linear behaviour of primary spindle receptors in response to small, slow ramp stretches.Brain Res. 44:680
Hendriks, Th., Daemen, F. J. M., Bonting, S. L. 1974. Biochemical aspects of the visual process. XXV. Light-induced calcium movement in isolated frog rod outer segments.Biochim. Biophys. Acta 345:468
Husmark, I., Ottoson, D. 1970. Relation between tension and sensory response of isolated frog muscle spindle during stretch.Acta Physiol. Scand. 79:321
Husmark, I., Ottoson, D. 1971a. The contribution of mechanical factors to the early adaptation of the spindle response.J. Physiol. 212:577
Husmark, I., Ottoson, D. 1971b. Ionic effects on spindle adaptation.J. Physiol. 218:257
Inoue, J., Kobatake, Y., Tasaki, J. 1973. Excitability, instability and phase transitions in squid axon membrane under internal perfusion with dilute salt solution.Biochim. Biophys. Acta 307:471
Katz, B. 1950. Depolarization of sensory terminals and the initiation of impulse in the muscle spindle.J. Physiol. 111:261
Klie, J. W., Wellhöner, H. H. 1973. Voltage clamp studies on the stretch response in the neuron of the slowly adapting crayfish stretch receptor.Pflüg. Arch. 342:93
Kugler, J., Chaplain, R. A. 1974. Origin of impulse initiation in the slowly adapting stretch receptor of the crayfish.Pflüg. Arch. 351:339
Loewenstein, W. R. 1961. Excitation and inactivation in a receptor membrane.Ann. N.Y. Acad. Sci. 94:510
Loewenstein, W. R. 1971. Mechano-electrical transduction in the Pacinian corpuscle. Initiation of sensory impulses in a mechanoreceptor.In: Handbook of Sensory Physiology. W. R. Loewenstein, editor. Vol. I, p. 260. Springer-Verlag, Berlin
Loewenstein, W. R., Terzuolo, C. A., Washizu, Y. 1963. Separation of transducer and impulse-generating processes in sensory receptors.Science 142:1180
Millecchia, R., Mauro, A. 1969. The ventral photoreceptor cells ofLimulus. III. A voltage-clamp study.J. Gen. Physiol. 54:331
Moore, L. E. 1971. Effect of temperature and calcium ions on rate constants of myelinated nerve.Amer. J. Physiol. 221:131
Nakajima, S., Onodera, K. 1969. Adaptation of the generator potential in the crayfish stretch receptors under constant length and tension.J. Physiol. 200:187
Obara, S., Grundfest, H. 1968. Effects of lithium on different membrane components of crayfish stretch receptor neurons.J. Gen. Physiol. 51:635
Ottoson, D. 1964. The effect of sodium deficiency on the response of the isolated muscle spindle.J. Physiol. 171:109
Ottoson, D. 1965. The action of calcium on the frog's isolated muscle spindle.J. Physiol. 178:68
Ottoson, D., Shepherd, G. M. 1971. Transducer properties and integrative mechanisms in the frog's muscle spindle.In: Handbook of Sensory Physiology. W. R. Loewenstein, editor. Vol. I, p. 442. Springer-Verlag, Berlin
Reuter, H. 1967. The dependence of slow inward curren in Purkinje fibres on the extracellular calcium concentration.J. Physiol. 192:479
Sokolove, P. G., Cooke, I. M. 1971. Inhibition of impulse activity in a sensory neuron by an electrogenic pump.J. Gen. Physiol. 57:125
Tasaki, I. 1968. Nerve Excitation. C. C. Thomas, Springfield, Illinois
Terzuolo, C. A., Washizu, Y. 1962. Relation between stimulus strength generator potential and impulse frequency in stretch receptor of crustacea.J. Neurophysiol. 25:56
Wendler, L. 1963. Über die Wirkungskette zwischen Reiz und Erregung (Versuche an abdominalen Streckrezeptoren dekapoder Krebse).Z. Vergl. Physiol. 47:279
Werman, R., Grundfest, H. 1961. Graded and all-or-none electrogenesis in arthropod muscle. II. The effects of alkali-earth and onium ions on lobster muscle fibers.J. Gen. Physiol. 44:997
Yamagishi, S., Grundfest, H. 1971. Contributions of various ions to the resting and action potentials of crayfish medial giant axons.J. Membrane Biol. 5:345
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Chaplain, R.A. Evidence for Ca2+ control of the transducer mechanism in crayfish stretch receptor. J. Membrain Biol. 21, 335–351 (1975). https://doi.org/10.1007/BF01941075
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01941075