Presynaptic quantal plasticity: Katz's original hypothesis revisited

Abstract

Changes in the amplitudes of signals conveyed at synaptic contacts between neurons underlie many brain functions and pathologies. Here we review the possible determinants of the amplitude and plasticity of the elementary postsynaptic signal, the miniature. In the absence of a definite understanding of the molecular mechanism releasing transmitters, we investigated a possible alternative interpretation. Classically, both the quantal theory and the vesicle theory predict that the amount of transmitter producing a miniature is determined presynaptically prior to release and that rapid changes in miniature amplitude reflect essentially postsynaptic alterations. However, recent data indicates that short-term and long-lasting changes in miniature amplitude are in large part due to changes in the amount of transmitter in individual released packets that show no evidence of preformation. Current representations of transmitter release derive from basic properties of neuromuscular transmission and endocrine secretion. Reexamination of overlooked properties of these two systems indicate that the amplitude of miniatures may depend as much, if not more, on the Ca(2+) signals in the presynaptic terminal than on the number of postsynaptic receptors available or on vesicle's contents. Rapid recycling of transmitter and its possible adsorption at plasma and vesicle lumenal membrane surfaces suggest that exocytosis may reflect membrane traffic rather than actual transmitter release. This led us to reconsider the disregarded hypothesis introduced by Fatt and Katz (1952; J Physiol 117:109-128) that the excitability of the release site may account for the "quantal effect" in fast synaptic transmission. In this case, changes in excitability of release sites would contribute to the presynaptic quantal plasticity that is often recorded.

Action Potential-Independent Release of Glutamate by Ca2+Entry through Presynaptic P2X Receptors Elicits Postsynaptic Firing in the Brainstem Autonomic Network

“…This synchronized multivesicular release generated largeramplitude mEPSCs than the basal minis; most of the latter occurs through mechanisms independent of Ca 2ϩ , leading to nonsynchronized monovesicular releases and smaller monoquantal mEPSCs (Vautrin and Barker, 2003). It has been demonstrated that multivesicular release at single release sites does occur in response to a single action potential (Tong and Jahr, 1994;Oertner et al, 2002).…”

Presynaptic plasticity and associative learning are impaired in a Drosophila presenilin null mutant

“…Following PTP however, the frequency of mEJPs was increased in both control and psn mutant terminals, but the amplitude was unaffected. While mEJP amplitude can be affected by both pre-and postsynaptic mechanisms (Karunanithi et al, 2002;Vautrin and Barker, 2003), regulation of the frequency of mEJPs occurs exclusively in the presynaptic compartment. Furthermore, the increase in quantal content following PTP, without any concomitant increase in quantal size indicates a presynaptic increase in the transmitter release.…”

Equilibrative Nucleoside Transporter 2 Regulates Associative Learning and Synaptic Function inDrosophila

“…The frequency of mEJPs, however, was significantly ( p Ͻ 0.001) elevated in both ent2 P124 and ent2 3 mutants relative to the control (1.2 Ϯ 0.1 Hz in control, 2.3 Ϯ 0.2 Hz in ent2 P124 , and 2.3 Ϯ 0.2 Hz in ent2 3 ). The amplitude of mEJPs may be affected by both presynaptic and postsynaptic factors (Karunanithi et al, 2002;Vautrin and Barker, 2003), whereas the frequency is affected exclusively by presynaptic factors. As such, the lack of change in the amplitude of mEJPs combined with an increase in the frequency of mEJPs is indicative of a presynaptic role for ent2 in synaptic transmission.…”