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The Journal of Neuroscience, July 16, 2003, 23(15):6272-6279

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Segregation and Coactivation of Developing Neocortical Layer 1 Neurons

Takeshi Soda,¹ Ryo Nakashima,² Dai Watanabe,¹ Kazunori Nakajima,^3,4 Ira Pastan,⁵ and Shigetada Nakanishi^1,2

¹Department of Biological Sciences, Kyoto University Faculty of Medicine, and ²Department of Molecular and System Biology, Kyoto University Graduate School of Biostudies, Kyoto 606-8501, Japan, ³Department of Anatomy, Keio University School of Medicine, Tokyo 160-8582, Japan, ⁴Department of Molecular Neurobiology, Institute of DNA Medicine, Jikei University School of Medicine, Tokyo 105-8461, Japan, and ⁵Laboratory of Molecular Biology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, Maryland 20892

Layer 1 in the developing cerebral cortex is populated by two basic neuronal cell types, Cajal–Retzius (CR) cells and non-CR cells. We generated transgenic mice in which green fluorescent protein (GFP) was driven by the promoter of metabotropic glutamate receptor subtype 2 and expressed specifically in CR cells during cortical development. On the basis of the precise identification of CR cells with GFP fluorescence, we pursued developmental changes and synaptic mechanisms of both CR and non-CR cells during the postnatal period. Immunostaining in combination with GFP fluorescence imaging showed that GFP and reelin, a protein involved in corticogenesis, completely overlap in CR cells at postnatal day 0. At the subsequent postnatal stage, reelin-positive neurons are segregated and categorized into GFP-positive/GABA-negative CR cells and GFP-negative/GABA-positive non-CR cells. Individual and simultaneous whole-cell recordings of CR and non-CR cells in developing cerebral slices revealed that spontaneous and electrically evoked postsynaptic currents (sPSCs and ePSCs) measured in CR and non-CR cells are differentially mediated by GABA_A receptors versus GABA_A, AMPA, and NMDA receptors, respectively. Furthermore, CR and non-CR cells show synchronized repetitive barrages of sPSCs that reflect a network-driven activity in the developing cerebral cortex. These findings imply that the layer 1 neurons dynamically change and play a distinct and integral role in the postnatal developing neocortex.

Key words: Cajal–Retzius cell; transgenic mouse; green fluorescent protein; neocortex; layer 1; synaptic transmission; neural circuit; reelin

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Received Jan. 23, 2003; revised May. 8, 2003; accepted May. 13, 2003.

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