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The Journal of Neuroscience, January 1, 1999, 19(1):193-205

NMDA Receptor-Mediated Control of Presynaptic Calcium and Neurotransmitter Release

Amanda J. Cochilla and Simon Alford

Department of Physiology and Northwestern University Institute for Neuroscience, Northwestern University Medical School, Chicago, Illinois 60611

Before action potential-evoked Ca2+ transients, basal presynaptic Ca2+ concentration may profoundly affect the amplitude of subsequent neurotransmitter release. Reticulospinal axons of the lamprey spinal cord receive glutamatergic synaptic input. We have investigated the effect of this input on presynaptic Ca2+ concentrations and evoked release of neurotransmitter. Paired recordings were made between reticulospinal axons and the neurons that make axo-axonic synapses onto those axons. Both excitatory and inhibitory paired-cell responses were recorded in the axons. Excitatory synaptic inputs were blocked by the AMPA receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX; 10 µM) and by the NMDA receptor antagonist 2-amino-5-phosphonopentanoate (AP-5; 50 µM). Application of NMDA evoked an increase in presynaptic Ca2+ in reticulospinal axons. Extracellular stimulation evoked Ca2+ transients in axons when applied either directly over the axon or lateral to the axons. Transients evoked by the two types of stimulation differed in magnitude and sensitivity to AP-5. Simultaneous microelectrode recordings from the axons during Ca2+ imaging revealed that stimulation of synaptic inputs directed to the axons evoked Ca2+ entry. By the use of paired-cell recordings between reticulospinal axons and their postsynaptic targets, NMDA receptor activation was shown to enhance evoked release of transmitter from the axons that received axoaxonic inputs. When the synaptic input to the axon was stimulated before eliciting an action potential in the axon, transmitter release from the axon was enhanced. We conclude that NMDA receptor-mediated input to reticulospinal axons increases basal Ca2+ within the axons and that this Ca2+ is sufficient to enhance release from the axons.

Key words: presynaptic calcium; glutamate receptor; NMDA receptor; non-NMDA receptor; transmitter release; presynaptic modulation

Copyright © 1999 Society for Neuroscience  0270-6474/99/191193-13$05.00/0


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