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Rapid Synaptic Transmission in the Avian Ciliary Ganglion Is Mediated by Two Distinct Classes of Nicotinic Receptors

We analyzed the kinetics and pharmacology of EPSCs in two kinds of neurons in the embryonic avian ciliary ganglion. Whole-cell voltage-clamp recordings revealed that the singly innervated ciliary neurons had large-amplitude (1.5–8.0 nA) EPSCs that could be classified according to the kinetics of their falling phases. Most of the neurons responded with an EPSC the falling phase of which followed a double exponential time course with time constants of ∼1 and 10 msec. The EPSCs of the remaining ciliary neurons followed a single time constant (∼8 msec). Multiple innervated choroid neurons had smaller-amplitude responses (0.2–1.5 nA when all inputs were activated) that appeared to contain only a slowly decaying component (τ = 12 msec). The fast and slow components of EPSC decay seen in most ciliary neurons could be pharmacologically isolated with two toxins against nicotinic acetylcholine receptors (AChRs). The fast component was blocked by 50 nm α-bungarotoxin (α-BuTx), which binds α7-subunit-containing AChRs. The slow component was selectively blocked by 50 nm α-conotoxin MII (α-CTx-MII), which blocks mammalian AChRs containing an α3/β2 subunit interface. A combination of both α-BuTx and α-CTx-MII abolished nearly all evoked current. Similar pharmacological results were found for ciliary neurons with monoexponentially decaying EPSCs and for choroid neurons. These results suggest that nerve-evoked transmitter acts on at least two different populations of AChRs on autonomic motor neurons in the ciliary ganglion.