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The Journal of Neuroscience, August 1, 2007, 27(31):8219-8225; doi:10.1523/JNEUROSCI.2476-07.2007

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Brief Communications
Differential Synaptic Integration of Interneurons in the Outer and Inner Molecular Layers of the Developing Dentate Gyrus

Ramesh Chittajallu,¹ Albrecht Kunze,^1,2 Jean-Marie Mangin,¹ and Vittorio Gallo¹

¹Center for Neuroscience Research, Children's National Medical Center, Washington, DC 20010, and ²Department of Neurology, University of Jena, 07747 Jena, Germany

Correspondence should be addressed to Vittorio Gallo, Center for Neuroscience Research, Children's Research Institute, Children's National Medical Center, Washington, DC 20010. Email: vgallo{at}cnmcresearch.org

The dentate gyrus (DG) undergoes continued reorganization and lamination during early postnatal development. Interneurons with anatomically identified synaptic contacts migrate from the outer to the inner regions of the molecular layer (ML) of the DG. By using the 2',3'-cyclic nucleotide 3'-phosphodiesterase (CNP)-enhanced green fluorescent protein transgenic mouse, we were able to target and physiologically characterize Dlx2⁺ developing ML interneurons. We investigated whether synapses on migrating ML interneurons were functional and defined properties of synaptic inputs onto interneurons that were located in the outer ML (OML) or inner ML (IML). Consistent with ongoing maturation, IML interneurons displayed lower input resistances and more hyperpolarized resting membrane potentials than OML interneurons. Both OML and IML interneurons received a direct excitatory monosynaptic input from the entorhinal cortex via the perforant paths, but this input was differentially sensitive to activation of presynaptic group II and III metabotropic glutamate receptors. Furthermore, only IML interneurons also received significant synaptic input from the CA3/hilar region, especially under conditions of experimentally induced disinhibition. These changes are attributed to a significant reorganization of dendritic fields. GABA_A receptor-mediated innervation of OML and IML interneurons also displayed significant differences in miniature IPSC amplitude, frequency, and decay kinetics. Finally, cell-attached recordings indicated that GABA_A receptor activation was depolarizing in OML interneurons but predominantly shunting in IML interneurons. Our data provide evidence that developing ML interneurons receive functional glutamatergic and GABAergic inputs and undergo significant changes in synaptic integration during migration from the OML to the IML.

Key words: CNP-expressing progenitors; cell migration; hippocampus; synaptic transmission; GABA_A receptors; presynaptic regulation

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Received April 16, 2007; accepted June 20, 2007.

Correspondence should be addressed to Vittorio Gallo, Center for Neuroscience Research, Children's Research Institute, Children's National Medical Center, Washington, DC 20010. Email: vgallo{at}cnmcresearch.org

This article has been cited by other articles:

				V. Gallo, J.-M. Mangin, M. Kukley, and D. Dietrich Synapses on NG2-expressing progenitors in the brain: multiple functions? J. Physiol., August 15, 2008; 586(16): 3767 - 3781. [Abstract] [Full Text] [PDF]

				J.-M. Mangin, A. Kunze, R. Chittajallu, and V. Gallo Satellite NG2 Progenitor Cells Share Common Glutamatergic Inputs with Associated Interneurons in the Mouse Dentate Gyrus J. Neurosci., July 23, 2008; 28(30): 7610 - 7623. [Abstract] [Full Text] [PDF]

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