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First published online November 1, 2006
Journal of Experimental Biology 209, 4429-4435 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02553

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Excitatory actions of GABA mediate severe-hypoxia-induced depression of neuronal activity in the pond snail (Lymnaea stagnalis)

Una Cheung, Mehrnoush Moghaddasi, Hannah L. Hall, J. J. B. Smith, Leslie T. Buck and Melanie A. Woodin^*

Department of Cell and Systems Biology, University of Toronto, Ontario, Canada

^* Author for correspondence (e-mail: m.woodin{at}utoronto.ca)

Accepted 18 September 2006

To characterize the effect of severe hypoxia on neuronal activity, long-term intracellular recordings were made from neurones in the isolated central ring ganglia of Lymnaea stagnalis. When a neurone at rest in normoxia was subjected to severe hypoxia, action potential firing frequency decreased by 38% (from 2.4-1.5 spikes s^-1), and the resting membrane potential hyperpolarized from -70.3 to -75.1 mV. Blocking GABA_A receptor-mediated synaptic transmission with the antagonist bicuculline methiodide (100 µmol l^-1) decreased neuronal activity by 36%, and prevented any further changes in response to severe hypoxia, indicating that GABAergic neurotransmission mediates the severe hypoxia-induced decrease in neuronal activity. Puffing 100 µmol l^-1 GABA onto the cell body produced an excitatory response characterized by a transient increase in action potential (AP) firing, which was significantly decreased in severe hypoxia. Perturbing intracellular chloride concentrations with the Na⁺/K⁺/Cl^- (NKCC1) cotransporter antagonist bumetanide (100 µmol l^-1) decreased AP firing by 40%, consistent with GABA being an excitatory neurotransmitter in the adult Lymnaea CNS. Taken together, these studies indicate that severe hypoxia reduces the activity of NKCC1, leading to a reduction in excitatory GABAergic transmission, which results in a hyperpolarization of the resting membrane potential (V_m) and as a result decreased AP frequency.

Key words: GABA, Lymnaea stagnalis, hypoxia

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