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Postactivation inhibition of spontaneously active neurosecretory neurons in the medicinal leech

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Abstract

Spontaneously active neurosecretory neurons in vertebrate and invertebrate nervous systems share similarities in firing frequencies, spike shapes, inhibition by the transmitters they themselves release and postactivation inhibition, an intensity-dependent period of suppressed spontaneous generation of action potentials following phases of high-frequency activity. High-frequency activation of spontaneously active serotonin-containing Retzius cells in isolated ganglia of the leech Hirudo medicinalis induced prolonged membrane hyperpolarisations causing periods of postactivation inhibition of up to 33 s. The duration of the inhibitory periods was directly related to both the number and rate of spikes during activation and was inversely proportional to a cell’s spontaneous firing frequency. The periods of postactivation inhibition remained unaffected by both serotonin depletion through repeated injections of 5,7-dihydroxytryptamine and suppressing the afterhyperpolarisation following each action potential with tetraethylammonium (TEA), iberiotoxin or charybdotoxin, suggesting that neither autoinhibition by synaptic release of serotonin nor calcium-activated potassium channels contribute to the underlying mechanism. In contrast, the postactivation inhibitory period was significantly affected both by differential electrical stimulation of the same Retzius cells via microelectrodes filled with molar concentrations of either Na+-acetate or K+-acetate, and by partial inhibition of Na+/K+-ATPase with ouabain. Thus, postactivation inhibition in Retzius cells results from prolonged hyperpolarising activity of Na+/K+-ATPase stimulated by the accumulation of cytosolic Na+ during phases of high-frequency spike activity.

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Abbreviations

5HT:

5-Hydroxytryptamine or serotonin

TEA:

Tetraethylammonium

5,7-DHT:

5,7-Dihydroxytryptamine

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Acknowledgments

We thank Maike Hartisch, Anja Weinrich and Thorin Jonsson for their help with electrophysiological recordings and statistical analysis. We also thank Elizabeth Dennison for correcting the English and two anonymous reviewers for their valuable suggestions for improvement of an earlier version of the manuscript. The experiments of this study comply with the “Principles of animal care”, publication No. 86–23, revised 1985 of the National Institute of Health, and also with the German law “Deutsches Tierschutzgesetz”.

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  1. Department of Neurobiology, Institute of Zoology, Berliner Strasse 28, 37073, Göttingen, Germany

    Daniela Gocht & Ralf Heinrich

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  1. Daniela Gocht
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Correspondence to Ralf Heinrich.

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Gocht, D., Heinrich, R. Postactivation inhibition of spontaneously active neurosecretory neurons in the medicinal leech. J Comp Physiol A 193, 347–361 (2007). https://doi.org/10.1007/s00359-006-0190-x

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