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Intraterminal Ca²⁺ concentration and asynchronous transmitter release at single GABAergic boutons in rat collicular cultures

Sergei Kirischuk and Rosemarie Grantyn

Neurotransmitter release in response to a single action potential has a precise time course. A significant fraction of the releasable vesicles is exocytosed synchronously, within a few milliseconds after the arrival of an action potential. If repeatedly activated, stimulus-locked phasic synchronous release declines, but synaptic transmission can be maintained through tonic asynchronous transmitter release. The desynchronisation of release during repetitive activation is generally attributed to a build-up of intraterminal Ca²⁺ concentration. However, the precise relationship between presynaptic Ca²⁺ level and asynchronous release rate at small central synapses has remained unclear. Here we characterise this relationship for single GABAergic terminals in rat collicular cultures. In the presence of tetrodotoxin, inhibitory postsynaptic currents (IPSCs) and presynaptic Ca²⁺ transients were recorded in response to direct presynaptic depolarisation of individual boutons. Repetitive stimulation indeed resulted in a shift from phasic to asynchronous neurotransmitter release. A clear dominance of the asynchronous release mode was observed after 10 pulses. The steady-state asynchronous release rate showed a third-power dependency on the presynaptic Ca²⁺ concentration, which is similar to that of evoked release. The Ca²⁺ sensor for asynchronous release exhibited a high affinity for Ca²⁺ and was far from saturation. These properties of the Ca²⁺ sensor should make the asynchronous release very sensitive to any modification of presynaptic Ca²⁺ concentration, including those resulting from changes in presynaptic activity patterns. Thus, asynchronous release represents a powerful but delicately regulated mechanism that ensures the maintenance of appropriate inhibition when the readily releasable pool of vesicles is depleted.

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