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The Journal of Neuroscience, July 23, 2008, 28(30):7610-7623; doi:10.1523/JNEUROSCI.1355-08.2008

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Cellular/Molecular
Satellite NG2 Progenitor Cells Share Common Glutamatergic Inputs with Associated Interneurons in the Mouse Dentate Gyrus

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

¹Center for Neuroscience Research, Children's National Medical Center, Washington, DC 20010, and ²Department of Neurology, Friedrich Schiller University, D-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

Several studies have provided evidence that NG2-expressing (NG2⁺) progenitor cells are anatomically associated to neurons in gray matter areas. By analyzing the spatial distribution of NG2⁺ cells in the hilus of the mouse dentate gyrus, we demonstrate that NG2⁺ cells are indeed closely associated to interneurons. To define whether this anatomical proximity reflected a specific physiological interaction, we performed patch-clamp recordings on hilar NG2⁺ cells and interneurons between 3 and 21 postnatal days. We first observed that hilar NG2⁺ cells exhibit spontaneous glutamatergic EPSCs (sEPSCs) whose frequency and amplitude increase during the first 3 postnatal weeks. At the same time, the rise time and decay time of sEPSCs significantly decreased, suggesting that glutamatergic synapses in NG2⁺ cells undergo a maturation process that is reminiscent of what has been reported in neurons during the same time period. We also observed that hilar interneurons and associated NG2⁺ cells are similarly integrated into the local network, receiving excitatory inputs from both granule cells and CA3 pyramidal neurons. By performing pair recordings, we found that bursts of activity induced by GABAergic antagonists were strongly synchronized between both cell types and that the amplitude of these bursts was positively correlated. Finally, by applying carbachol to increase EPSC activity, we observed that closely apposed cells were more likely to exhibit synchronized EPSCs than cells separated by >200 µm. The finding that NG2⁺ cells are sensing patterns of activity arising in closely associated neurons suggests that NG2⁺ cell function is finely regulated by the local network.

Key words: neural progenitor cells; dentate gyrus; synaptic transmission; glutamate receptors; synchrony; oligodendrocyte; oligodendroglia

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Received March 29, 2008; revised May 21, 2008; accepted June 6, 2008.

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

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