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The Journal of Neuroscience, January 15, 2000, 20(2):696-708

Intermediate Zone Cells Express Calcium-Permeable AMPA Receptors and Establish Close Contact with Growing Axons

Christine Métin¹, Jean-Pierre Denizot², and Nicole Ropert²

¹ Equipe Régionalisation Nerveuse, Centre National de la Recherche Scientifique (CNRS) Unité Mixte de Recherche 8542, Niveau 8, Ecole Normale Supérieure, 75230 Paris Cédex 05, France, and ² Institut Alfred Fessard, CNRS Unité Propre de Recherche 2212, 91198 Gif sur Yvette, France

Recent studies have shown that cells in the intermediate zone (IZ) of the embryonic neocortex originate in the basal telencephalon and migrate tangentially in the cortical wall (Anderson et al., 1997; Tamamaki et al., 1997; Wichterle et al., 1999). We had previously observed growing cortical axons closely apposed to calbindin-positive, tangentially oriented cells in the IZ (Métin and Godement, 1996), and it has been shown that neurites in the IZ express a glutamate transporter (Furuta et al., 1997). To test if glutamate released by corticofugal growth cones could influence the tangential IZ cells, we characterized the glutamate receptors expressed by IZ cells using patch-clamp techniques, histochemical labeling, and immunostaining on slices of embryonic mice forebrain. We show that tangential IZ cells express inwardly rectifying kainate responses, but not NMDA responses, and accumulate cobalt after AMPA receptor activation. We conclude that IZ cells express calcium-permeable AMPA receptors. This property correlates with our observation that the GluR2 subunit is not expressed in the IZ.

AMPA receptors are activated by a millimolar concentration of glutamate. To know whether this high level of glutamate could occur at the surface of IZ cells, we examined contacts made by corticofugal growth cones and calbindin-positive IZ cells using electron microscopy. We show vesicle-containing neurites tightly apposed to calbindin-positive IZ cells over remarkably long length. This suggests that glutamate released by growing corticofugal axons could reach high concentrations close to AMPA receptors of tangential IZ cells and efficiently activate them to control the intracellular calcium in embryonic IZ cells.

Key words: cortex; development; tangential migration; cortical plate; glutamate; calcium permeability; cyclothiazide; LY303070; GYKI 53784; GABA; GABA_A receptors; mouse

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Copyright © 2000 Society for Neuroscience  0270-6474/00/202696-13$05.00/0

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