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The Journal of Neuroscience, May 11, 2005, 25(19):4755-4765; doi:10.1523/JNEUROSCI.0553-05.2005

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Development/Plasticity/Repair
A Noncanonical Release of GABA and Glutamate Modulates Neuronal Migration

Jean-Bernard Manent, Michaël Demarque, Isabel Jorquera, Christophe Pellegrino, Yehezkel Ben-Ari, Laurent Aniksztejn, and Alfonso Represa

Institut de Neurobiologie de la Méditerranée, Institut National de la Santé et de la Recherche Médicale U29, Campus de Luminy BP13, 13273 Marseille, France

Immature neurons express GABA and glutamate receptors before synapse formation, and both transmitters are released at an early developmental stage. We have now tested the hypothesis that the ongoing release of GABA and glutamate modulates neuronal migration. Using 5-bromo-2'-deoxyuridine labeling and cocultures of hippocampal slices obtained from naive and green fluorescent protein-transgenic mice, we report that migration is severely affected by GABA_A or NMDA receptor antagonist treatments. These effects were also present in munc18-1 knock-out slices in which soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE)-dependent vesicular secretion of transmitters has been deleted. GABA_A antagonists were more efficient than NMDA antagonists to reduce cell migration, in keeping with the earlier maturation of GABAergic mechanisms. We conclude that GABA and, to a lesser degree, glutamate released in a SNARE-independent mechanism exert a paracrine action on neuronal migration.

Key words: neuron; migration; neurotransmitter; GABA; glutamate; hippocampus

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Received Sep 7, 2004; revised March 25, 2005; accepted March 30, 2005.

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