The Journal of Neurophysiology Vol. 78 No. 5 November 1997, pp. 2246-2253
Copyright ©1997 The American Physiological Society

Contribution of Outward Currents to Spike-Frequency Adaptation in Hypoglossal Motoneurons of the Rat

Andrea Sawczuk, Randall K. Powers, and Marc D. Binder

Department of Physiology and Biophysics, University of Washington, School of Medicine, Seattle, Washington 98195

Sawczuk, Andrea, Randall K. Powers, and Marc D. Binder. Contribution of outward currents to spike-frequency adaptation in hypoglossal motoneurons of the rat. J. Neurophysiol. 78: 2246-2253, 1997. Spike-frequency adaptation has been attributed to the actions of several different membrane currents. In this study, we assess the contributions of two of these currents: the net outward current generated by the electrogenic Na⁺-K⁺ pump and the outward current that flows through Ca²⁺-activated K⁺ channels. In recordings made from hypoglossal motoneurons in slices of rat brain stem, we found that bath application of a 4-20 µM ouabain solution produced a partial block of Na⁺-K⁺ pump activity as evidenced by a marked reduction in the postdischarge hyperpolarization that follows a period of sustained discharge. However, we observed no significant change in either the initial, early, or late phases of spike-frequency adaptation in the presence of ouabain. Adaptation also has been related to increases in the duration and magnitude of the medium-duration afterhyperpolarization (mAHP) mediated by Ca²⁺-activated K⁺ channels. When we replaced the 2 mM Ca²⁺ in the bathing solution with Mn²⁺, there was a significant decrease in the amplitude of the mAHP after a spike. The decrease in mAHP amplitude resulted in a decrease in the magnitude of the initial phase of spike-frequency adaptation as has been reported previously by others. However, quite unexpectedly we also found that reducing the mAHP resulted in a dramatic increase in the magnitude of both the early and late phases of adaptation. These changes could be reversed by restoring the normal Ca²⁺ concentration in the bath. Our results with ouabain indicate that the Na⁺-K⁺ pump plays little, if any, role in the three phases of adaptation in rat hypoglossal motoneurons. Our results with Ca²⁺ channel blockade support the hypothesis that initial adaptation is, in part, controlled by conductances underlying the mAHP. However, our failure to eliminate initial adaptation completely by blocking Ca²⁺ channels suggests that other membrane mechanisms also contribute. Finally, the increase in both the early and late phases of adaptation in the presence of Mn²⁺ block of Ca²⁺ channels lends further support to the hypothesis that the initial and later (i.e., early and late) phases of spike-frequency adaptation are mediated by different cellular mechanisms.

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