Optimal aeration of the lungs is dependent on an alveolar fluid clearance, a process that is governed by Na⁺ and Cl^- transport. However, the specific contribution of various ion channels in different alveolar cell types under basal or stimulated conditions is not exactly known. We established a novel functional model of rat lung slices suitable for nystatin-perforated whole-cell patch-clamp experiments. Lung slices retained a majority of live cells for up to 72 hours. Type II pneumocytes in situ had a mean capacitance of 8.8±2.5 pF and a resting membrane potential of -4.4±1.9 mV. Bath replacement of Na⁺ with NMDG⁺ decreased inward whole-cell currents by 70%, 21% and 52% of which were sensitive to 10 µM and 1 mM of amiloride, respectively. Exposure of slices to 0.5 µM dexamethasone for one hour did not affect ion currents, while chronic exposure (0.5 µM, 24-72 hours) induced an increase in both total Na⁺-entry currents and amiloride-sensitive currents. Under acute exposure to 100 µM cpt-cAMP, Type II cells in situ rapidly hyperpolarized by 25-30 mV, due to activation of whole-cell Cl^--currents sensitive to 0.1 mM of 5-Nitro-2-(3-phenylpropylamino)benzoic acid. Additionally in the presence of cpt-cAMP, total sodium currents and amiloride-sensitive currents increased by 32% and 70%, respectively. Thus, in Type II pneumocytes in situ: 1) amiloride-sensitive sodium channels contribute to only half of total Na⁺-entry and are stimulated by chronic exposure to glucocorticoids; 2) acute increase in cellular cAMP content simultaneously stimulates the entry of Cl^- and Na⁺ ions.