Correlation of Transmitter Release with Membrane Properties of the Presynaptic Fiber of the Squid Giant Synapse

Abstract

A B S TR A C T Depolarization of the presynaptic terminal by current produced a postsynaptic potential (PSP) which increased with increasing presynaptic polarization and then reached a plateau. Iontophoretic injection of tetraethylammonium ions (TEA) into the presynaptic axon near the terminal produced a prolonged presynaptic spike. The resulting PSP is increased in size and its time course closely followed that of the presynaptic spike. The presynaptic fiber no longer exhibited rectification and strong depolarizations revealed that the PSP reached a maximum with about 110 mv depolarization. Further depolarization produced a decrease in PSP amplitude and finally transmission was blocked. However, a PSP then always appeared on withdrawal of the depolarizing current. Under the conditions of these experiments, the PSP could be considered a direct measure of transmitter release. Bathing the TEA-injected synapse with concentrations of tetrodotoxin (TTX) sufficient to block spike activity in both pre-and postsynaptic axons did not greatly modify postsynaptic electrogenesis. However, doubling TTX concentration reversibly blocked PSP. Thus the permeability changes to Na and K accompanying the spike do not appear necessary for transmitter release. Some other processes related to the level of presynaptic polarization must be involved to explain the data. The inhibition of transmitter release by strong depolarizations appears to be related to Ca action. A membrane Ca current may also be necessary for normal transmitter release.

Mechanisms underlying presynaptic inhibition through alpha 2‐adrenoceptors in guinea‐pig submucosal neurones.

“…Fast EPSPs were prolonged by 3-to 6-fold in the presence of 2 mM-barium or 40 mM-TEA; this prolongation was most probably due to a longer duration action potential in the presynaptic cholinergic terminals (see Kusano et al 1967) as well as to the fact that these agents produced a depolarization and 2-to 3-fold increase in input resistance. (This results largely from suppression of a calcium-activated potassium current which is active at rest; Akasu & Tokimasa, 1989.)…”

“…All of these potassium channel blockers also dramatically increase transmitter release (e.g. Koketsu, 1958;Kusano, Livengood & Werman, 1967), thus making quantitative comparisons between agonist inhibition of fast EPSPs in the presence and absence of potassium channel blockers impossible. Nevertheless, we examined whether the presence of 620 a2-MEDIATED PRESYNAPTIC INHIBITION barium or TEA might qualitatively alter the ability of a2-adrenoceptor agonists to inhibit the fast EPSP.…”

Chemically Mediated Transmission at a Giant Fiber Synapse in the Central Nervous System of a Vertebrate

“…The only previously known exception is the giant synapse of the squid (17,23,27,28,33) but considerable data have also been obtained from the neuromuscular junction (21,22), the chick ciliary ganglion (29,30), and certain electroreceptors (cf. reference 6).…”

Oral Administration of Pharmacologically Active Substances to Squid: A Methodological Description

“…Many aspects of the action potential, synaptic transmission, and fast axonal transport have been worked out in detail in the squid (Young, 1939;Bulloch, 1948;Bloedel et al, 1966;Katz and Miledi, 1967;Kusano et al, 1967;Llinas et al, 1981;Augustine et al, 1985;Serulle et al, 2007). The scale of the axon and the synaptic structures allows unparalleled access for experiments.…”