Journal of Neuroscience, Vol 7, 3813-3826, Copyright © 1987 by Society for Neuroscience
Muscarinic and nicotinic synaptic activation of the developing chicken iris
G Pilar, R Nunez, IS McLennan and SD Meriney
Department of Physiology and Neurobiology, University of Connecticut, Storrs 06268.
The development of the mechanical characteristics of contraction and the
pharmacology of synaptic activation in chick iris and ciliary body were
examined from embryonic day 9 through posthatching. The ciliary
ganglion-target muscle system has proven to be a useful model for both in
vivo and in vitro studies of neuron-target interactions; one such
interaction is involved in neuronal cell death, which in the ciliary
ganglion occurs from Stage (St) 34 to 40. To understand the mechanism by
which cholinergic blocking agents prevent naturally occurring neuronal
death in the chick ciliary ganglion (see the following paper, Meriney et
al., 1987), it was necessary to determine the effect of these agents on
synaptic transmission at target structures during the cell death period.
Initially (St 34-36), iris muscle contraction are synaptically mediated via
muscarinic ACh receptors (AChRs) on myoepithelial cells, which have the
contractile and structural characteristics of smooth muscle. Close
apposition of synaptic terminals, similar to that described for mature
synapses, was observed on these myoepithelial cells. Subsequently (St 37),
the striated muscle fibers that appear are activated by nicotinic
receptors, although muscarinic AChRs are also present. Mechanically, this
can be seen as gradually changing from a slow-onset contraction, elicited
only by 30 Hz stimulation, to a fast-twitch response (St 37-44). Dilator
fibers that develop later in the iris (at about St 39) also possess
nicotinic and muscarinic receptors. The ciliary body musculature, although
not extensively studied, also appears to have dual cholinergic activation
during development. The mature iris has predominately striated muscle
fibers that have both junctional nicotinic and muscarinic (mostly
extrajunctional) AChRs. The dual presence of both receptor types in the
same muscle fiber was confirmed with intracellular recordings, in which
only the initial portion of the ACh-elicited depolarization was sensitive
to alpha bungarotoxin (alpha BTX). In addition, specific muscarinic binding
sites were described in the developing, as well as in the mature, iris. The
developing chick iris was also shown to contract directly in response to
light, this response disappearing after hatching. This unique dual-receptor
pharmacology (nicotinic- muscarinic) and light response of a striated
muscle may be due to the neural crest origin of these cells.