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The Journal of Neuroscience, October 1, 1999, 19(19):8528-8541

Ca²⁺-Permeable AMPA Receptors and Spontaneous Presynaptic Transmitter Release at Developing Excitatory Spinal Synapses

Jeffrey Rohrbough and Nicholas C. Spitzer

Department of Biology and Center for Molecular Genetics, University of California, San Diego, La Jolla, California 92093

At many mature vertebrate glutamatergic synapses, excitatory transmission strength and plasticity are regulated by AMPA and NMDA receptor (AMPA-R and NMDA-R) activation and by patterns of presynaptic transmitter release. Both receptors potentially direct neuronal differentiation by mediating postsynaptic Ca²⁺ influx during early development. However, the development of synaptic receptor expression and colocalization has been examined developmentally in only a few systems, and changes in release properties at neuronal synapses have not been characterized extensively. We recorded miniature EPSCs (mEPSCs) from spinal interneurons in Xenopus embryos and larvae. In mature 5-8 d larvae, ~70% of mEPSCs in Mg²⁺-free saline are composed of both a fast AMPA-R-mediated component and a slower NMDA-R-mediated decay, indicating receptor colocalization at most synapses. By contrast, in 39-40 hr embryos ~65% of mEPSCs are exclusively fast, suggesting that these synapses initially express predominantly AMPA-R. In a physiological Mg²⁺ concentration (1 mM), mEPSCs throughout development are mainly AMPA-R-mediated at negative potentials. Embryonic synaptic AMPA-R are highly Ca²⁺-permeable, mEPSC amplitude is over twofold larger than at mature synapses, and mEPSCs frequently occur in bursts consistent with asynchronous multiquantal release. AMPA-R function in this motor pathway thus appears to be independent of previous NMDA-R activation, unlike other regions of the developing nervous system, ensuring a greater reliability for embryonic excitatory transmission. Early spontaneous excitatory activity is specialized to promote AMPA-R-mediated synaptic Ca²⁺ influx, which likely has significant roles in neuronal development.

Key words: Ca²⁺-permeable AMPA receptors; NMDA receptors; developing excitatory synapses; spontaneous transmitter release; mEPSCs; receptor colocalization; presynaptic mEPSC bursts

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Copyright © 1999 Society for Neuroscience  0270-6474/99/19198528-14$05.00/0

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