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

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.