JOURNALOF NEUROPHYSIOLOGY Vol. 76, No. 1, July 1996. Printed in U.S.A. Electrogenic Pump and a Ca2+ -Dependent K+ Conductance Contribute to a Posttetanic Hyperpolarization in Lamprey Sensory Neurons DAVID PARKER, RUSSELL HILL, AND STEN GRILLNER Nobel Institute of Neurophysiology, Department of Neuroscience, Karolinska Institute, S-l 7177, Stockholm, Sweden SUMMARY AND CONCLUSIONS 1. Tetanic stimulationof lamprey sensory dorsalcells resulted in a posttetanic hyperpolarization(PTH) . The amplitude and dura- tion of the PTH were dependent on the stimulus duration and frequency. ThePTH was not reversed at membrane potentials nega- tive to - 100 mV, whereas the afterhyperpolarization following singleaction potentials reversed at approximately -85 mV. There wasalsoa biphasic effect on the input resistance during the PTH, with an early reduction that recoveredto control before the PTH had decayed. 2. The amplitudeand duration of the PTH were increased in Ringer solutioncontainingtetraethylammonium and 4-aminopyri- dine, both of which broadened single action potentials,but were reduced after intracellularinjection of Cs +. Ca2+ -free Ringer solu- tion, Cd2+,and Co2+ also reduced the PTH, suggesting the involve- ment of a Ca2+ -dependent K+ conductance. However, the PTH was not reduced in Ba2+ Ringersolution, or by the Ca2+-dependent K+ channel antagonists apamin and charybdotoxin. 3. The cardiac glycoside ouabainreduced the amplitude and duration of the PTH, as did substitution of Na+ with choline or Li +. K+ -free Ringersolutionalso reduced the PTH, whereas high- K+ Ringer solutionhad more variable effects. The amplitudeand duration of the PTH were also dependent on temperature. These results support the involvement of anouabain-sensitive Na-K pump in the PTH. 4. The PTH wasreduced by the tachykinins substance P and physalaemin, and by Shydroxytryptamine, which blocks apamin-sensitive Ca2+ -dependent K+ channelsin the lamprey. However, y-aminobutyric acid, which has been reported to re- duce a Ca2+-dependent K+ conductance in the dorsal cells, did not reduce the PTH. 5. These results suggest that a Ca2+-dependent K+ conductance and an Na-K electrogenic pump underlie the PTH. The PTH re- duces the excitability of the dorsal cells, suggesting that it may act as a mechanism to gate sensoryinformation entering the spinal cord. INTRODUCTION The pattern and frequency of action potentials are deter- mined by the conductances that a neuron possesses. An im- portant determinant of the firing frequency is the afterhyper- polarization (AHP) following single action potentials (Gus- tafsson 1974). In many cells there are early and late components to the AHP. The early component may consist of several voltage-dependent conductances (Storm 1987), whereasthe late component is often due to a Ca2+-dependent K+ conductance (Gustafsson 1974; Hill et al. 1985, 1992), which has been shown to be important for spike frequency regulation and burst termination (Gustafsson 1974; Wallen et al. 1989; Zhang and Krnjevic 1987). In addition to the AHP following single action potentials, tetanic stimulation can result in a prolonged AHP or postte- tanic hyperpolarization (PTH). A PTH in the frog sciatic nerve was abolished by tetraethylammonium (TEA), sug- gesting that a K+ conductance was responsible (Bergman et al. 1980). In hippocampal CA1 neurons, a PTH has been described that reversed at -86 mV, was dependent on the extracellular K+ concentration, and was depressed by Ba2+, suggesting that it was due to a Ca2+-dependent K+ conduc- tance ( Alger and Nicoll 1980). This PTH was associated with an increased conductance and inhibited spikes elicited by depolarizing current pulses. A PTH can also be produced by activation of an electro- genie Na-K pump as a result of changes in ion distribution following repetitive stimulation. This has been shown in the terminals of lizard motor neurons (Morita et al. 1993), mammalian nonmyelinated axons (den Hertog and Ritchie 1969), and a crayfish stretch receptor neuron (Sokolove and Cooke 1971) . Na-K pump-dependent effects are blocked by cardiac glycosides and by replacement of extracellular Na+ with Li+, are dependent on temperature and extracellular potassium, but are not markedly voltage sensitive (Morita et al. 1993; Schoepfle and Katholi 1973)) and are not associ- ated with changes in the input resistance of the cell (Morita et al. 1993). In this paper we examine the properties and underlying mechanisms of a PTH in lamprey dorsal cells. These are primary sensory neurons that have large cell bodies in the spinal cord (Rovainen 1967), which facilitates the examina- tion of their properties. There are two types of dorsal cells, rapidly adapting touch (T) and slowly adapting pressure (P) cells (Christenson et al. 1988). After single action potentials, the dorsal cells have an early AHP that is only partly TEA- sensitive (Hill et al. 1985), and a small slower AHP that may be due to a Ca2+-dependent K+ conductance (Leonard and Wickelgren 1985). Stimulation of P-type dorsal cells can increase the ventral root burst intensity ipsilaterally and decrease it contralaterally (Buchanan and Cohen 1982)) sug- gesting that dorsal cell input modulates the locomotor net- work. In this paper we show that the dorsal cells are hyperpolar- ized after tetanic stimulation. This is partly due to a Ca2’- dependent K+ conductance that does not resemble the pre- viously described lamprey Ca 2+ -dependent K + conduc- tances (Wallen et al. 1989)) and also to activation of an electrogenic Na-K pump. The PTH blocks dorsal cell action potentials, suggesting that it can gate sensory input entering the spinai”cord, possibly acting as a mechanism to prevent 540 0022-3077/96 $5.00 Copyright 0 1996 The American Physiological Society