Octopamine increases the excitability of neurons in the snail feeding system by modulation of inward sodium current but not outward potassium currents

Ágnes Vehovszky,Henriette Szabó,Christopher Jh Elliott

doi:10.1186/1471-2202-6-70

Ágnes Vehovszky, Henriette Szabó + Show 1 more

Open Access

https://doi.org/10.1186/1471-2202-6-70

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Abstract

BackgroundAlthough octopamine has long been known to have major roles as both transmitter and modulator in arthropods, it has only recently been shown to be functionally important in molluscs, playing a role as a neurotransmitter in the feeding network of the snail Lymnaea stagnalis. The synaptic potentials cannot explain all the effects of octopamine-containing neurons on the feeding network, and here we test the hypothesis that octopamine is also a neuromodulator.ResultsThe excitability of the B1 and B4 motoneurons in the buccal ganglia to depolarising current clamp pulses is significantly (P << 0.05) increased by (10 μM) octopamine, whereas the B2 motoneuron becomes significantly less excitable. The ionic currents evoked by voltage steps were recorded using 2-electrode voltage clamp. The outward current of B1, B2 and B4 motoneurons had two components, a transient IA current and a sustained IK delayed-rectifier current, but neither was modulated by octopamine in any of these three buccal neurons. The fast inward current was eliminated in sodium – free saline and so is likely to be carried by sodium ions. 10 μM octopamine enhanced this current by 33 and 45% in the B1 and B4 motoneurons respectively (P << 0.05), but a small reduction was seen in the B2 neuron. A Hodgkin-Huxley style simulation of the B1 motoneuron confirms that a 33% increase in the fast inward current by octopamine increases the excitability markedly.ConclusionWe conclude that octopamine is also a neuromodulator in snails, changing the excitability of the buccal neurons. This is supported by the close relationship from the voltage clamp data, through the quantitative simulation, to the action potential threshold, changing the properties of neurons in a rhythmic network. The increase in inward sodium current provides an explanation for the polycyclic modulation of the feeding system by the octopamine-containing interneurons, making feeding easier to initiate and making the feeding bursts more intense.

Highlights

Octopamine has long been known to have major roles as both transmitter and modulator in arthropods, it has only recently been shown to be functionally important in molluscs, playing a role as a neurotransmitter in the feeding network of the snail Lymnaea stagnalis
Octopamine increases the excitability of the B1 and B4, but not B2 motoneuron Excitability experiments were performed in Hi-Di to decrease spontaneous synaptic inputs on the cell under study
Simulation of B1 We have modelled the voltage-activated currents of B1 motoneuron using a Hodgkin-Huxley style simulation, with a view to confirming that the 33% increase in inward sodium current confers an increase in excitability

Summary

Introduction

Octopamine has long been known to have major roles as both transmitter and modulator in arthropods, it has only recently been shown to be functionally important in molluscs, playing a role as a neurotransmitter in the feeding network of the snail Lymnaea stagnalis. The synaptic potentials cannot explain all the effects of octopamine-containing neurons on the feeding network, and here we test the hypothesis that octopamine is a neuromodulator. With its repetitive protraction and retraction of the radula to ingest food, has provided a simple model system for the study of central pattern generator neuronal networks and of the way in which the pattern is reshaped by neuromodulators [1,2]. In the buccal ganglia (page number not for citation purposes).

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