Analysis of evoked and spontaneous quantal release at high pressure in crustacean excitatory synapses

Abstract

The cellular mechanisms underlying the effect of high pressure on synaptic transmission were studied in the opener muscle of the lobster walking leg. Excitatory postsynaptic currents (EPSCs) were recorded using a loose macropatch-clamp technique at normal pressure and 3.5, 6.9 MPa helium pressure. Responses of the single excitatory axon could be grouped into two types: low-yield (L) synapses exhibiting small EPSCs with a considerable number of failures, and high-yield (H) synapses having larger EPSCs with very few failures. High pressure reduced the average EPSC amplitude in all synapses and shifted their amplitude histograms to the left by decreasing the quantal content (m) without changing their quantum current (q). A binomial distribution fit of EPSC amplitudes revealed that high pressure greatly decreased n, the number of available active zones, but the effect on p, the probability of release for each zone, was not consistent. Many of the spontaneous miniature EPSCs (mEPSCs), observed only in L-type synapses, were "giant" (size = 2-5 q). High pressure increased the frequency of the giant mEPSCs but had little effect on their amplitude histogram. High pressure depressed evoked synaptic transmission by modulating the presynaptic quantal release parameters, but concomitantly enhanced spontaneous quantal release by an unknown mechanism.

Enduring Medial Perforant Path Short-Term Synaptic Depression at High Pressure

“…Raising [Ca 2+ ] o at HP enhanced synaptic release, but its maximal effect only partially restored synaptic transmission (Grossman and Kendig, 1990; Golan and Grossman, 1992; Golan et al, 1994, 1995, 1996). Thus, synaptic release was saturated but at a subnormal level, i.e., reduced RRP (which represents the presynaptic component of the SR), and exhibited exponential FDD during stimulation at 50 Hz.…”

“…Various lines of evidence suggest that HP impairs Ca 2+ -entry in protozoa (Otter and Salmon, 1979, 1985), brain synaptosomes (Gilman et al, 1986), and presynaptic terminals of crustacean synapses (Grossman and Kendig, 1990). Furthermore, detailed quantal analysis of crustacean neuromuscular synapses revealed that in all types of synapses HP depressed release (i.e., decreased quantal content, m ) by reducing the number of active release sites ( n ) with variable small effect on the probability of release ( p ) depending on the type of the synapses (Golan et al, 1994, 1995, 1996). Similar quantal analysis for CNS and MPP synapses are not available.…”

“…High pressure (HP) of 10.1 MPa decreases single fEPSP by about 50% (Fagni et al, 1987; Talpalar and Grossman, 2003; Etzion et al, 2009), but the effect on SR dynamics is still unclear. Quantal analysis of crustacean neuromuscular synapses revealed reduction of quantal content and number of available release sites and spared quantal size and release probability at HP (Golan et al, 1994, 1995). HP-induced reduction of synaptic inputs was relieved by increasing [Ca 2+ ] o , and mimicked by lowering [Ca 2+ ] o in both, brain and crustacean preparations.…”

Pressure‐induced depression of synaptic transmission in the cerebellar parallel fibre synapse involves suppression of presynaptic N‐type Ca2+ channels

“…1979; Grossman & Kendig, 1988), which results from a decrease in transmitter release from the presynaptic terminal (Campenot, 1975; Ashford et al . 1982; Golan et al . 1995).…”

“…However, apart from decreased slow after-hyperpolarization in hippocampal neurons (Southan & Wann, 1996) and a shift in the concentration±response curve of glycine receptors (Roberts et al, 1996), pressure does not seem to affect neuronal properties in a manner consistent with hyperexcitability (Southan & Wann, 1996;Etzion & Grossman, 1999). In contrast, a signi®cant depression of synaptic transmission is consistently demonstrated (Campenot, 1975;Wann et al, 1979;Grossman & Kendig, 1988), which results from a decrease in transmitter release from the presynaptic terminal (Campenot, 1975;Ashford et al, 1982;Golan et al, 1995). This depressant effect is attributed to a reduction of calcium in¯ux into the presynaptic terminal (Gilman et al, 1986;Grossman & Kendig, 1990;Golan & Grossman, 1992;Golan et al, 1994).…”