BK-Type K-Ca channels in two parasympathetic cell types: Differences in kinetic properties and developmental expression

The intrinsic electrical properties of identified choroid and ciliary neuro ns of the chick ciliary ganglion were examined by patch-clamp recording met hods. These neurons are derived from a common pool of mesencephalic neural crest precursor cells but innervate different target tissues and have marke dly different action potential waveforms and intrinsic patterns of repetiti ve spike discharge. Therefore it is important to determine whether these ce ll types express different types of plasma membrane ionic channels, and to ascertain the developmental stages at which these cell types begin to diver ge. This study has focused on large-conductance Ca2+-activated K+ channels (K-Ca), 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 K- Ca carried by a kinetically homogeneous population of large-conductance (BK -type) K-Ca channels. However, the kinetic properties of these channels are different in the two cell types. Steady-state fluctuation analyses of macr oscopic K-Ca produced power spectra that could be fitted with a single Lore ntzian curve in both cell types. However, the resulting corner frequency wa s significantly lower in choroid neurons than in ciliary neurons, suggestin g that the underlying K-Ca channels have a longer mean open-time in choroid neurons. Consistent with fluctuation analyses, significantly slower gating of K-Ca channels in choroid neurons was also observed during macroscopic a ctivation and deactivation at membrane potentials positive to -30 mV. Diffe rences in the kinetic properties of K-Ca channels could also be observed di rectly in single-channel recordings from identified embryonic day 13 choroi d and ciliary neurons. The mean open-time of large-conductance K-Ca channel s was significantly greater in choroid neurons than in ciliary neurons in e xcised inside-out patches. The developmental expression of functional K-Ca channels appears to be regulated differently in the two cell types. Althoug h both cell types acquire functional K-Ca at the same developmental stages (embryonic days 9-13), functional expression of these channels in ciliary n eurons requires target-derived trophic factors. In contrast, expression of functional K-Ca channels proceeds normally in choroid neurons developing in vitro in the absence of target-derived trophic factors. Consistent with th is, extracts of ciliary neuron target tissues (striated muscle of the iris/ ciliary body) contain K-Ca stimulatory activity. However, K-Ca stimulatory activity cannot be detected in extracts of the smooth muscle targets of cho roid neurons.