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The Journal of Neurophysiology Vol. 84 No. 6 December 2000, pp. 2767-2776
Copyright ©2000 by the American Physiological Society
Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204-5513
Cameron, Jill S. and
Stuart E. Dryer.
BK-Type KCa Channels in Two Parasympathetic Cell
Types: Differences in Kinetic Properties and Developmental Expression. J. Neurophysiol. 84: 2767-2776, 2000. The intrinsic electrical properties of identified choroid and
ciliary neurons of the chick ciliary ganglion were examined by
patch-clamp recording methods. These neurons are derived from a common
pool of mesencephalic neural crest precursor cells but innervate
different target tissues and have markedly different action potential
waveforms and intrinsic patterns of repetitive spike discharge.
Therefore it is important to determine whether these cell types express
different types of plasma membrane ionic channels, and to ascertain the
developmental stages at which these cell types begin to diverge. This
study has focused on large-conductance Ca2+-activated K+ channels
(KCa), which are known to regulate spike waveform
and repetitive firing in many cell types. Both ciliary ganglion cell types, identified on the basis of size and somatostatin
immunoreactivity, express a robust macroscopic
KCa carried by a kinetically homogeneous population of large-conductance (BK-type) KCa
channels. However, the kinetic properties of these channels are
different in the two cell types. Steady-state fluctuation analyses of
macroscopic KCa produced power spectra that could
be fitted with a single Lorentzian curve in both cell types. However,
the resulting corner frequency was significantly lower in choroid
neurons than in ciliary neurons, suggesting that the underlying
KCa channels have a longer mean open-time in
choroid neurons. Consistent with fluctuation analyses, significantly
slower gating of KCa channels in choroid neurons
was also observed during macroscopic activation and deactivation at
membrane potentials positive to
30 mV. Differences in the kinetic
properties of KCa channels could also be observed
directly in single-channel recordings from identified embryonic
day 13 choroid and ciliary neurons. The mean open-time of
large-conductance KCa channels was significantly
greater in choroid neurons than in ciliary neurons in excised
inside-out patches. The developmental expression of functional
KCa channels appears to be regulated differently in the two cell types. Although both cell types
acquire functional KCa at the same developmental
stages (embryonic days 9-13), functional expression of
these channels in ciliary neurons requires target-derived trophic
factors. In contrast, expression of functional
KCa channels proceeds normally in choroid neurons developing in vitro in the absence of target-derived trophic factors. Consistent with this, extracts of ciliary neuron target tissues (striated muscle of the iris/ciliary body) contain
KCa stimulatory activity. However,
KCa stimulatory activity cannot be detected in
extracts of the smooth muscle targets of choroid neurons.
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