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The Journal of Neuroscience, January 9, 2008, 28(2):385-394; doi:10.1523/JNEUROSCI.5198-07.2008

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Cellular/Molecular
Oxytocin-Induced Postinhibitory Rebound Firing Facilitates Bursting Activity in Oxytocin Neurons

Jean-Marc Israel,^1,2 Dominique A. Poulain,^1,2 and Stéphane H. R. Oliet^1,2

¹Neuroscience Research Center, Inserm U862, Bordeaux, France; ²Université Victor Segalen Bordeaux 2, Bordeaux, France

Correspondence should be addressed to Jean-Marc Israel, Inserm U862, 146 rue Léo-Saignat, 33077 Bordeaux, France. Email: jean-marc.israel{at}bordeaux.inserm.fr

During parturition and lactation, neurosecretory oxytocin (OT) neurons in the hypothalamus achieve pulsatile hormone secretion by coordinated bursts of firing that occur throughout the neuronal population. This activity is partly controlled by somatodendritic release of OT, which facilitates the onset and recurrence of synchronized bursting. To further investigate the cellular mechanisms underlying the control exerted by OT on the activity of its own neurons, we studied the effects of the peptide on membrane potential and synaptic activity in OT neurons in hypothalamic organotypic slice cultures. Bath application of low concentrations of OT (<100 nM) facilitated GABA_A receptor-mediated inhibitory transmission through a presynaptic mechanism without affecting membrane potential and excitatory glutamatergic synaptic activity. The facilitatory action of OT on GABAergic transmission was dose-dependent, starting at 25 nM and disappearing at concentrations >100 nM. As shown previously, higher concentrations of OT (>500 nM) had the opposite effect, inhibiting GABA_A receptors via a postsynaptic mechanism. Surprisingly, OT-mediated facilitation of GABAergic transmission promoted action potential firing in 40% of the neurons. Each action potential occurred at the end of the repolarizing phase of an inhibitory potential. Pharmacological dissection revealed that this firing involved the activation of low-threshold activated calcium channels. Detailed statistical analysis showed that OT-mediated firing upregulated bursting activity in OT neurons. It is thus likely to optimize OT secretion and, as a consequence, facilitate delivery and milk ejection in mammals.

Key words: hypothalamus; supraoptic; GABA; calcium current; neuroendocrine; lactation

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Received July 25, 2005; accepted Nov. 26, 2007.

Correspondence should be addressed to Jean-Marc Israel, Inserm U862, 146 rue Léo-Saignat, 33077 Bordeaux, France. Email: jean-marc.israel{at}bordeaux.inserm.fr

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