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Journal of Neuroscience, Vol 14, 3156-3165, Copyright © 1994 by Society for Neuroscience
Target tissues and innervation regulate the characteristics of K+ currents in chick ciliary ganglion neurons developing in situ
MM Dourado, C Brumwell, ME Wisgirda, MH Jacob and SE Dryer
Department of Biological Science, Florida State University, Tallahassee, 32306-4075.
The expression of appropriate ensembles of ionic channels is necessary for
the differentiation and normal function of vertebrate neurons. Cell- cell
interactions may regulate the expression and properties of ionic channels
in embryonic neurons. Previous studies have shown that the expression of
A-type K+ channels (IA) and Ca2+-activated K+ channels (lK[Ca]) is abnormal
in chick ciliary ganglion neurons developing in vitro in the absence of
normal cell-cell interactions. Other voltage- activated currents develop
normally under these conditions. The present studies were designed to
establish the role of the target tissues and the preganglionic innervation
in regulating the expression of these currents in embryonic chick ciliary
ganglion neurons developing in situ. Surgical manipulations were used to
remove the developing optic vesicle, which contains the target tissues, the
mid-dorsal region of the midbrain primordium, which contains the
preganglionic nucleus, or both, all prior to the formation of the ciliary
ganglion. IA and IK[Ca] were then examined in acutely isolated neurons that
developed in ovo in the presence (OV+) or absence (OV-) of the normal
target tissues, in the presence (MB+) or absence (MB-) of preganglionic
innervation, and in the absence of both preganglionic innervation and
target tissues (OV- /MB-). The amplitude of IA was unaffected by the
operations. However, the activation and inactivation kinetics of IA were
two- to threefold faster in OV- or OV-/MB- cells compared to neurons
isolated from control OV+ ganglia at embryonic days 11-14 (E11-E14). There
were no changes in the voltage dependence of activation or steady-state
inactivation, or in the time course of recovery from inactivation. By
contrast, neurons isolated from MB- ganglia expressed an IA with amplitude,
voltage dependence, and kinetics that were indistinguishable from those of
control MB+ and OV+ ganglia. Therefore, interactions with target tissues in
the eye play a role in determining the characteristics of IA in developing
ciliary ganglion neurons, whereas preganglionic innervation does not.
Furthermore, the amplitude of IK[Ca] was reduced by 90-100% in OV-, MB-,
and OV-/MB- neurons isolated at E12-E14 as compared to MB+ and OV+
controls. Voltage-activated Ca2+ currents were present at normal amplitudes
in all of these neurons. Thus, the expression of IK[Ca] in chick ciliary
ganglion neurons is regulated by both target tissue interactions and
preganglionic innervation. Therefore, cell-cell interactions are necessary
for the expression of a normal ensemble of ionic channels in chick ciliary
ganglion neurons developing in situ.
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