Developmental regulation and maintenance of inwardly and outwardly rectifying K+ currents in sheep parotid cells

Sheep parotid secretory cells contain an inwardly rectifying K+ conductance not seen in nonruminants. The channels underlying this conductance are highly active in unstimulated cells and, in consequence, have been implicated in spontaneous secretion (secretion in the absence of neural and hormonal stimulation), an unusual phenomenon seen conspicuously in ruminant parotid glands. Since spontaneous secretion by the sheep parotid first appears after weaning, at the same time that the parasympathetic secretomotor innervation becomes functional, and since parasympathetic denervation of the adult parotid causes spontaneous secretion to abate over a period of weeks, it might be expected that the activity of the inwardly rectifying K+ conductance would be similarly related to parasympathetic innervation if it plays an important role in spontaneous secretion. To test this hypothesis, we used whole cell patch-clamp techniques to study the inwardly rectifying K+ conductance in secretory cells from the parotid glands of unweaned lambs and normal adult sheep studied 6 wk after unilateral parotid parasympathectomy. The secretory cells from unweaned lambs showed almost no inwardly rectifying current, and the cells from parasympathectomized glands in adults showed a reduced current compared with the contralateral control glands. Our results thus provide evidence that the inwardly rectifying current is somehow enabled by the development of a functional parasympathetic innervation.