The Journal of Neuroscience, March 25, 2009, 29(12):3749-3759; doi:10.1523/JNEUROSCI.5404-08.2009
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Cellular/Molecular
Nicotinic Receptors Concentrated in the Subsynaptic Membrane Do Not Contribute Significantly to Synaptic Currents at an Embryonic Synapse in the Chicken Ciliary Ganglion
Peter B. Sargent
Department of Cell and Tissue Biology and the Neuroscience Graduate Program, University of California, San Francisco, San Francisco, California 94143-0640
Correspondence should be addressed to Dr. Peter B. Sargent, Department of Cell and Tissue Biology, Box 0640, University of California, San Francisco, San Francisco, CA 94143-0640. Email: peter.sargent{at}ucsf.edu
Rapid synaptic transmission at the calyciform synapse in the embryonic chicken ciliary ganglion is mediated by two classes of nicotinic receptors: those containing 
3 subunits [3-nicotinic ACh receptors (nAChRs)] and those containing 7 subunits (7-nAChRs). 3-nAChRs and 7-nAChRs are differentially distributed on the cell surface; 3-nAChRs are concentrated at postsynaptic densities, whereas both 7-nAChRs and 3-nAChRs are found extrasynaptically on somatic spines. I explored the contribution of 3-nAChRs and 7-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 7-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 3-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, 7-nAChR-like kinetics and 75% of events exhibiting the kinetics expected of coactivation of 7-nAChRs and 3-nAChRs. Cells rarely showed significant numbers of uniquantal responses with slow, 3-nAChR-like kinetics, which was unexpected given that 3-nAChRs alone are concentrated at postsynaptic densities. The only site where ACh quanta can activate both 3-nAChRs and 7-nAChRs readily is on the somatic spines, where 7-nAChRs and 3-nAChRs are present extrasynaptically. At the calyciform synapse, rapid synaptic transmission is mediated apparently without participation of ionotropic receptors concentrated at postsynaptic densities.
Received Oct. 23, 2008;
revised Jan. 16, 2009;
accepted Feb. 15, 2009.
Correspondence should be addressed to Dr. Peter B. Sargent, Department of Cell and Tissue Biology, Box 0640, University of California, San Francisco, San Francisco, CA 94143-0640. Email: peter.sargent{at}ucsf.edu
