Abstract

The dynamics of different ionic currents shape the bursting activity of neurons and networks that control motor output. Despite being ubiquitous in all animal cells, the contribution of the Na(+)/K(+) pump current to such bursting activity has not been well studied. We used monensin, a Na(+)/H(+) antiporter, to examine the role of the pump on the bursting activity of oscillator heart interneurons in leeches. When we stimulated the pump with monensin, the period of these neurons decreased significantly, an effect that was prevented or reversed when the h-current was blocked by Cs(+). The decreased period could also occur if the pump was inhibited with strophanthidin or K(+)-free saline. Our monensin results were reproduced in model, which explains the pump's contributions to bursting activity based on Na(+) dynamics. Our results indicate that a dynamically oscillating pump current that interacts with the h-current can regulate the bursting activity of neurons and networks.

Highlights

  • Rhythmic behaviors such as walking, breathing, and running are controlled by central pattern generators, networks of neurons that produce rhythmic activity without sensory input (Marder and Calabrese, 1996; Marder and Bucher, 2001)

  • The rhythmic bursting activity of each constituent neuron within a central pattern generator is shaped by the dynamics of various ionic currents that are intrinsic to each neuron (Harris-Warrick, 2002)

  • We examined the role of the Na+/K+ pump in regulating the bursting activity of oscillator heart interneurons, which pace the leech heartbeat central pattern generator

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Summary

Introduction

Rhythmic behaviors such as walking, breathing, and running are controlled by central pattern generators, networks of neurons that produce rhythmic activity without sensory input (Marder and Calabrese, 1996; Marder and Bucher, 2001). Many central pattern generator neurons have a persistent Na+ current or a low-threshold Ca2+ current that supports bursting (Opdyke and Calabrese, 1994; Butera et al, 1999; Del Negro et al, 2002; Rybak et al, 2004), a hyperpolarization-activated inward current that provides recovery from inhibition to initiate bursting (Angstadt and Calabrese, 1989; Golowasch and Marder, 1992), and a transient K+ current that impedes initiations of action potentials and bursts (Simon et al, 1992) Modulation of these ionic currents can alter the timing and intensity of these neurons’ bursting activity (e.g., Tobin and Calabrese, 2005; Koizumi and Smith, 2008). In addition to maintaining internal concentrations of Na+ and K+, the pump contributes a voltage drop to the resting membrane potential (Hodgkin and Keynes, 1955; Carpenter and Alving, 1968; Smith et al, 1968; Baylor and Nicholls, 1969) and is able to generate a slow afterhyperpolarization after a train

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