Long-lasting depression and the depletion hypothesis at crayfish neuromuscular junctions
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Synaptic depression was studied at the neuromuscular junctions of the crayfish giant motoneurone onto the abdominal fast flexor muscles. The kinetics of depression were compared quantitatively to predictions of the depletion hypothesis of synaptic depression.
Synaptic transmission was depressed about 71% following a single motoneurone impulse. Transmission recovered to normal along an exponential time course with an average time constant of 285 s (Fig. 1).
This recovery curve was used to predict the depression that repeated responses would be expected to suffer. Even after correction for a superimposed facilitation (Fig. 2) and non-linear postsynaptic summation, the response to repeated stimulation at frequencies at or above once per minute were less depressed than expected (Figs. 3, 4). Increasing the frequency above this rate did not enhance depression, contrary to predictions. The discrepancy was not due to a mobilization of transmitter into a releasable store (Fig. 5).
The depression caused by each stimulus in a train was much less than that following a single impulse. This contradicts the depletion hypothesis and suggests that depression is accompanied by a large change in the fraction of the releasable transmitter store liberated by an impulse, with very little accompanying depletion.
When transmitter release is reduced in high magnesium solution, there is no change in the depression observed to repeated stimulation, contrary to the depletion hypothesis (Fig. 6).
This discrepancy could be due to an effect of magnesium on mobilization. However, no difference was found in the slow recovery rates following an impulse in different magnesium concentrations (Fig. 7).
It is concluded that the depletion hypothesis is untenable as a basis for depression at this neuromuscular junction.
KeywordsDepression Neuromuscular Junction Transmitter Release Flexor Muscle Recovery Curve
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- Betz, W.J.: Depression of transmitter release at the neuromuscular junction of the frog. J. Physiol.206, 629–644 (1970)Google Scholar
- Birks, R., Macintosh, F.C.: Acetylcholine metabolism of a sympathetic ganglion. Canad. Biochem. Physiol.39, 787–827 (1961)Google Scholar
- Bruner, J., Kennedy, D.: Habituation: occurrence at a neuromuscular junction. Science169, 92–94 (1970)Google Scholar
- Castellucci, V.F., Kandel, E.R.: A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex inAplysia. Proc. nat. Acad. Sci. (Wash.)71, 5004–5008 (1974)Google Scholar
- Castellucci, V.F., Kandel, E.R.: Further analysis of the synaptic decrement underlying habituation of the gill-withdrawal reflex inAplysia. Fourth Annual Meeting, Society of Neuroscience, p. 164 (1974)Google Scholar
- Christensen, B.N., Martin, A.R.: Estimates of probability of transmitter release at the mammalian neuromuscular junction. J. Physiol.210, 933–945 (1970)Google Scholar
- Czternasty, G., Bruner, J.: Dépressions à court et à long terme de la transmission neuromusculaire chez l'Ecrevisse. C.R. Acad. Sci. Paris281, 1493–1496 (1975)Google Scholar
- Elmqvist, D., Quastel, D.M.J.: A quantitative study of end-plate potentials in isolated human muscle. J. Physiol.178, 505–529 (1965)Google Scholar
- Friesen, W.O.: Antifacilitation and facilitation in the cardiac ganglion of the spiny lobsterPanulirus interrupts. J. comp. Physiol.101, 207–224 (1975)Google Scholar
- Hubbard, J.I.: Repetitive stimulation at the mammalian neuromuscular junction and the mobilization of transmitter. J. Physiol.169, 641–662 (1963)Google Scholar
- Hubbard, J.I., Jones, S.F., Landau, E.M.: The effect of temperature change upon transmitter release, facilitation and post-tetanic potentiation. J. Physiol.216, 591–609 (1971)Google Scholar
- Jack, J.J.B., Noble, O., Tsien, R.W.: Electric current flow flow in excitable cells, pp. 64–66. Oxford: University Press 1975Google Scholar
- Kandel, E.R., Castellucci, V., Pinsker, H., Kupfermann, I.: The role of synaptic plasticity in the short-term modification of behaviour. In: Short-term changes in neural activity and behaviour (ed. G. Horn, R.A. Hinde), pp. 281–322. Cambridge: University Press 1975Google Scholar
- Kennedy, D., Takeda, K.: Reflex control of abdominal flexor muscles in the crayfish. I. The twitch system. J. exp. Biol.43, 211–227 (1965)Google Scholar
- Kusano, K., Landau, E.M.: Depression and recovery of transmission at the squid giant synapse. J. Physiol.245, 13–32 (1975)Google Scholar
- Lass, Y., Halevi, Y., Landau, E.M., Gitter, S.: A new model for transmitter mobilization in the frog neuromuscular junction. Pflügers Arch. ges. Physiol.343, 157–163 (1973)Google Scholar
- Liley, A.W., North, K.A.K.: An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction. J. Neurophysiol.16, 509–527 (1953)Google Scholar
- Linder, T.M.: The accumulative properties of facilitation at crayfish neuromuscular synapses. J. Physiol.238, 223–234 (1974)Google Scholar
- Lowagie, C., Gerschenfeld, H.M.: Glutamate antagonists at the crayfish neuromuscular junction. Nature (Lond.)248, 533–535 (1974)Google Scholar
- Lundberg, A., Quilish, H.: On the effect of calcium on presynaptic potentiation and depression of neuromuscular transmission in frog and rat. Acta Physiol. Scand.30, Suppl.111, 121–129 (1953)Google Scholar
- Magleby, K.L.: The effect of repetitive stimulation on facilitation of transmitter release at the frog neuromuscular junction. J. Physiol.234, 327–352 (1973)Google Scholar
- Magleby, K.L., Zengel, J.E.: A quantitative description of tetanic and post-tetanic potentiation of transmitter release at the frog neuromuscular junction. J. Physiol.245, 183–208 (1975)Google Scholar
- Mallart, A., Martin, A.R.: An analysis of facilitation of transmitter release at the neuromuscular junction of the frog. J. Physiol.193, 679–694 (1967)Google Scholar
- Martin, A.R.: A further study of the statistical composition of the end-plate potential. J. Physiol.130, 114–122 (1955)Google Scholar
- Nicholls, J.G., Purves, D.: A comparison of chemical and electrical synaptic transmission between single sensory cells and a motoneurone in the central nervous system of the leech. J. Physiol.225, 637–656 (1972)Google Scholar
- Otsuka, M., Endo, M., Nonomura, Y.: Presynaptic nature of neuromuscular transmission. Jap. J. Physiol.12, 573–584 (1962)Google Scholar
- Papir, D.: The effect of glycerol treatment on crab muscle fibres. J. Physiol.230, 313–330 (1973)Google Scholar
- Richards, C.D.: Potentiation and depression of synaptic transmission in the olfactory cortex of the guinea-pig. J. Physiol.222, 209–231 (1972)Google Scholar
- Schlapfer, W.T., Woodson, P.B.J., Tremblay, J.P., Barondes, S.H.: Depression and frequency facilitation at a synapse inAplysia californica: evidence for regulation by availability of transmitter. Brain Res.76, 267–280 (1974)Google Scholar
- Selverston, A.I., Remler, M.P.: Neural geometry and activation of crayfish fast flexor motoneurones. J. Neurophysiol.35, 797–814 (1972)Google Scholar
- Sevcik, C., Narahashi, T.: Electrical properties and excitation-contraction coupling in skeletal muscle treated with ethylene glycol. J. gen Physiol.60, 221–236 (1972)Google Scholar
- Takeuchi, A.: The long-lasting depression in neuromuscular transmission of frog. Jap. J. Physiol.8, 102–113 (1958)Google Scholar
- Takeuchi, A., Onodera, K.: Reversal potentials of the excitatory transmitter and L-glutamate at the crayfish neuromuscular junction. Nature New Biol.242, 124–126 (1973)Google Scholar
- Taraskevich, P.S.: Reversal potentials of L-glutamate and the excitatory transmitter at the neuromuscular junction of the crayfish. Biochim. biophys. Acta241, 700–704 (1971)Google Scholar
- Thies, R.E.: Neuromuscular depression and the apparent depletion of transmitter in mammalian muscle. J. Neurophysiol.28, 427–442 (1965)Google Scholar
- Wernig, A.: The effects of calcium and magnesium on statistical release parameters at the crayfish neuromuscular junction. J. Physiol.226, 761–768 (1972)Google Scholar
- Zucker, R.S.: Crayfish escape behavior and central synapses. I. Neural circuit exciting lateral giant fiber. J. Neuphysiol.35, 599–620 (1972a)Google Scholar
- Zucker, R.S.: Crayfish escape behavior and central synapses. II. Physiological mechanisms underlying behavioral habituation. J. Neurophysiol.35, 621–637 (1972b)Google Scholar
- Zucker, R.S.: Changes in the statistics of transmitter release during facilitation. J. Physiol.229, 787–810 (1973)Google Scholar
- Zucker, R.S.: Crayfish neuromuscular facilitation activated by constant presynaptic action potentials and depolarizing pulses. J. Physiol.241, 69–89 (1974a)Google Scholar
- Zucker, R.S.: Characteristics of crayfish neuromuscular facilitation and their calcium dependence. J. Physiol.241, 91–110 (1974b)Google Scholar
- Zucker, R.S.: Excitability changes in crayfish motor neurone terminals. J. Physiol.241, 111–126 (1974c)Google Scholar
- Zucker, R.S.: Synaptic plasticity at crayfish neuromuscular junctions. In: Identified neurons and Behavior of Arthropods (ed. G. Hoyle), pp. 49–65. New York: Plenum Press 1977Google Scholar