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The Journal of Neuroscience, May 31, 2006, 26(22):5901-5909; doi:10.1523/JNEUROSCI.1033-06.2006

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Development/Plasticity/Repair
Glutamate Acting on AMPA But Not NMDA Receptors Modulates the Migration of Hippocampal Interneurons

Jean-Bernard Manent, Isabel Jorquera, Yehezkel Ben-Ari, Laurent Aniksztejn, and Alfonso Represa

Institut de Neurobiologie de la Méditerranée, Institut National de la Santé et de la Recherche Médicale, Unité 29, 13273 Marseille, France

Correspondence should be addressed to Alfonso Represa, Institut de Neurobiologie de la Méditerranée, Institut National de la Santé et de la Recherche Médicale, Unité 29, Campus de Luminy, Boite Postale 13, 13273 Marseille, France. Email: represa{at}inmed.univ-mrs.fr

Paracrine GABA and glutamate acting, respectively, on GABA_A and NMDA receptors modulate the migration of hippocampal pyramidal cells. Using corticohippocampal organotypic explants from glutamic acid decarboxylase (GAD) 67–enhanced green fluorescent protein (EGFP) knock-in embryos, we now report that, in contrast to pyramidal neurons, the blockade of AMPA but not NMDA receptors exerts important actions on the migration of GABAergic interneurons. In addition, the blockade of GABA_A receptors fails to modify the migration rates of GABAergic interneurons. Immunohistochemical analyses of GAD67–EGFP embryos (from embryonic day 14 to birth) reveal that interneurons colonize the hippocampal primordium by embryonic day 15. At that stage, the hippocampal primordium is already composed of pioneer glutamatergic neurons, including (1) Cajal-Retzius cells, immunopositive to calretinin and reelin, and (2) other presumptive pioneer pyramidal cells that are immunopositive to III-tubulin and vesicular glutamate transporter 3 and immunonegative to GABA or GAD67. Therefore, the migrations of pyramidal neurons and GABAergic interneurons are cross-modulated: glutamate released from pioneer glutamatergic neurons facilitates the migration of GABAergic interneurons, which in turn would release GABA, facilitating the migration of glutamatergic neuroblasts. This general sequence may provide a retroactive positive loop needed to construct the hippocampal network. It might constitute a primitive homeostatic mechanism in the developing brain that acts to balance GABA–glutamate contributions to network construction and activity.

Key words: interneurons; migration; neurotransmitter; GABA; glutamate; AMPA; hippocampus

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Received Dec. 2, 2005; revised April 12, 2006; accepted April 16, 2006.

Correspondence should be addressed to Alfonso Represa, Institut de Neurobiologie de la Méditerranée, Institut National de la Santé et de la Recherche Médicale, Unité 29, Campus de Luminy, Boite Postale 13, 13273 Marseille, France. Email: represa{at}inmed.univ-mrs.fr

This article has been cited by other articles:

				Y. Ben-Ari, J.-L. Gaiarsa, R. Tyzio, and R. Khazipov GABA: A Pioneer Transmitter That Excites Immature Neurons and Generates Primitive Oscillations Physiol Rev, October 1, 2007; 87(4): 1215 - 1284. [Abstract] [Full Text] [PDF]

				J.-B. Manent and A. Represa Neurotransmitters and Brain Maturation: Early Paracrine Actions of GABA and Glutamate Modulate Neuronal Migration Neuroscientist, June 1, 2007; 13(3): 268 - 279. [Abstract] [PDF]

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