The Journal of Neurophysiology Vol. 77 No. 2 February 1997, pp. 749-760
Copyright ©1997 The American Physiological Society

Transmitter Release Differs at Snake Twitch and Tonic Endplates During Potassium-Induced Nerve Terminal Depolarization

Elizabeth A. Connor¹, Anna Dunaevsky¹, David J. G. Griffiths², Jean C. Hardwick², and Rodney L. Parsons²

¹ Department of Biology, Neuroscience and Behavior Graduate Program, University of Massachusetts, Amherst, Massachusetts 01003; and ² Department of Anatomy and Neurobiology, University of Vermont, Burlington, Vermont 05405

Connor, Elizabeth A., Anna Dunaevsky, David J. G. Griffiths, Jean C. Hardwick, and Rodney L. Parsons. Transmitter release differs at snake twitch and tonic endplates during potassium-induced nerve terminal depolarization. J. Neurophysiol. 77: 749-760, 1997. Twitch and tonic muscle fibers of snake skeletal muscle differ in their synpatic as well as mechanical properties. These experiments were aimed at detemining the basis of the difference in vesicular release properties of nerve terminals at twitch and tonic endplates. Miniature endplate currents (MEPCs) were recorded from voltage-clamped garter snake muscle fibers depolarized by high K⁺ in either a control Ca²⁺ or high-Ca²⁺ solution. MEPC frequency increased at twitch and tonic endplates and remained elevated for 8 h during depolarization in control Ca²⁺. At twitch endplates depolarized in the presence of high Ca²⁺, an increase in MEPC frequency was followed by a progressive decline. In contrast, MEPC frequency remained elevated in high Ca²⁺ at tonic endplates. The observed decrease in MEPC freqency at depolarized twitch endplates in high Ca²⁺ was not a function of the level of depolarization or initial MEPC frequency, nor was it due to a reduction in MEPC amplitude and loss of MEPCs in baseline noise. An optical assay of presynaptic function in which the activity-dependent dye FM1-43 was used confired that quantal reslease differs at twitch and tonic endplates. Most twitch nerve terminals were labeled by FM1-43 during prolonged depolarization with control Ca²⁺ or after brief depolarization with high Ca²⁺. In contrast, the number of twitch nerve terminals and the degree to which they were stained was greatly reduced after prolonged exposure to high K⁺ and high Ca²⁺, whereas depolarized tonic endplates were well stained by FM1-43 during brief and prolonged exposure to high Ca²⁺. FM1-43 staining also revealed variable levels of quantal release between individual boutons at twitch endplates after prolonged depolarization in high-Ca²⁺ solution. The observed reduction in presynaptic function at twitch nerve terminals after prolonged depolarization in high-Ca²⁺ solution was reversible and therefore not due to irreversible damage to terminal boutons. MEPC frequency increased at both twitch and tonic endplates when either Sr²⁺ or Ba²⁺ was substituted for high Ca²⁺ during K⁺-induced depolarization. Over time, in Sr²⁺ or Ba²⁺ solutions, MEPC frequency remained elevated at tonic endplates but declined at twitch endplates with a time course similar to that observed in high Ca²⁺. MEPC amplitudes at both endplates remained constant. We conclude that the regulation of quantal release differs in nerve terminals innervating twitch and tonic endplates and postulate that differential intraterminal accumulation of Ca²⁺ may underlie the observed difference in presynaptic function.

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