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The Journal of Neuroscience, January 7, 2004, 24(1):183-196; doi:10.1523/JNEUROSCI.1074-03.2004

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Development/Plasticity/Repair
The Role of AMPA Receptor Gating in the Development of High-Fidelity Neurotransmission at the Calyx of Held Synapse

Indu Joshi, Shahira Shokralla, Paul Titis, and Lu-Yang Wang

The Program for Brain and Behavioral Research and Division of Neurology, The Hospital for Sick Children and Department of Physiology, University of Toronto, Toronto, Ontario, Canada M5G, 1X8

During early postnatal development of auditory synapses, the decay time course of AMPA receptor (AMPAR) EPSCs accelerates markedly, but the mechanisms underlying this process remain uncertain. Using the developing calyx of Held synapse in the mouse auditory brainstem, we have examined presynaptic and postsynaptic elements that may regulate decay kinetics of AMPAR EPSCs. We found that the decay time kinetics was voltage dependent in both immature and mature synapses, being slower at positive potentials than negative potentials. By recording evoked miniature events in extracellular Ca²⁺ or Sr²⁺, we revealed a significant decrease in decay time constants of EPSCs as maturation progresses. On the basis of internal and external polyamine block of AMPAR EPSCs and immunohistochemistry assays with subunit-specific antibodies, we demonstrated that the glutamate receptor (GluR) 2 subunit is virtually absent at all developmental ages. Antibody staining patterns suggest a gradual shift in subunit composition from GluR1- to GluR3/4-dominant phenotypes. Kinetic analyses of deactivation, desensitization, and recovery from desensitization in outside-out patches in response to ultrafast application of glutamate lend supportive evidence that such a shift in the gating phenotype likely accounts for the accelerated time course throughout development. Finally, by pharmacologically manipulating AMPAR gating and using simulated EPSCs to evoke action potentials, we demonstrated that rapid decay kinetics of AMPAR EPSCs is essential for this synapse to accommodate high-frequency firing without compromising spike amplitude. Hence, developmental alterations in the subunit composition likely dictate changes in the time course of AMPAR EPSCs and play an indispensable role in the refinement of high-fidelity neurotransmission at the calyx of Held synapse.

Key words: calyx of Held-MNTB synapse; Ca²⁺-permeable AMPA receptors; polyamine; synaptic transmission; spike firing; developmental plasticity

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Received April 10, 2003; revised October 29, 2003; accepted October 29, 2003.

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