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Nicotinic Receptors Concentrated in the Subsynaptic Membrane Do Not Contribute Significantly to Synaptic Currents at an Embryonic Synapse in the Chicken Ciliary Ganglion

Rapid synaptic transmission at the calyciform synapse in the embryonic chicken ciliary ganglion is mediated by two classes of nicotinic receptors: those containing α3 subunits [α3-nicotinic ACh receptors (nAChRs)] and those containing α7 subunits (α7-nAChRs). α3-nAChRs and α7-nAChRs are differentially distributed on the cell surface; α3-nAChRs are concentrated at postsynaptic densities, whereas both α7-nAChRs and α3-nAChRs are found extrasynaptically on somatic spines. I explored the contribution of α3-nAChRs and α7-nAChRs to uniquantal responses, measured as mEPSCs, or as evoked responses under low release probability conditions. The contribution that each nAChR makes to uniquantal response shape was determined by blocking one nAChR type; pharmacologically isolated α7-nAChR responses were kinetically fast (rise time, 0.32 ± 0.02 ms; decay time, 1.66 ± 0.18 ms; mean ± SD; n = 6 cells), whereas pharmacologically isolated α3-nAChR responses were slow (rise time, 1.28 ± 0.35 ms; decay time, 6.71 ± 1.46 ms; n = 8 cells). In the absence of antagonists, most cells (11 of 14) showed heterogeneity in the kinetics of uniquantal responses, with ∼25% of events exhibiting fast, α7-nAChR-like kinetics and ∼75% of events exhibiting the kinetics expected of coactivation of α7-nAChRs and α3-nAChRs. Cells rarely showed significant numbers of uniquantal responses with slow, α3-nAChR-like kinetics, which was unexpected given that α3-nAChRs alone are concentrated at postsynaptic densities. The only site where ACh quanta can activate both α3-nAChRs and α7-nAChRs readily is on the somatic spines, where α7-nAChRs and α3-nAChRs are present extrasynaptically. At the calyciform synapse, rapid synaptic transmission is mediated apparently without participation of ionotropic receptors concentrated at postsynaptic densities.