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

Abstract

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 2Ј,3Ј-cyclic nucleotide 3Ј-phosphodiesterase (CNP)-enhanced green fluorescent protein transgenic mouse, we were able to target and physiologically characterize Dlx2 ϩ 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.

Postnatal development of the hippocampal formation in male albino rats

“…This finding was consistent with other researchers [23], who observed that the DG underwent continued reorganization and lamination during early postnatal development in the mouse. This finding was consistent with other researchers [23], who observed that the DG underwent continued reorganization and lamination during early postnatal development in the mouse.…”

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

“…EGFP + cells were identified as described previously (Chittajallu et al, 2004 and 2007). The present study targeted faint EGFP + interneurons and associated (“satellite”) bright EGFP + NG2 + cells in the hilus of the dentate gyrus (Figure 1).…”

“…In this mouse, NG2 + cells can be readily identified based on their higher levels of EGFP fluorescence (Chittajallu et al, 2004; Chittajallu et al, 2005), their unique stellate morphology, and their electrophysiological membrane properties (Chittajallu et al, 2004). Conversely, in the same mouse strain, a subpopulation of interneurons express lower levels of EGFP and all the electrophysiological features typical of GABAergic interneurons (Belachew et al, 2003; Aguirre et al, 2004; Chittajallu et al, 2007). Therefore, this transgenic mouse strain enabled us to identify NG2 + progenitors and GABAergic interneurons, and to perform simultaneous electrophysiological recordings from these cells in the hilus of the dentate gyrus.…”

Is Plasticity of GABAergic Mechanisms Relevant to Epileptogenesis?

“…The other major subtype of DG interneuron is hilar HIPP cells, which co-express GABA and NPY or somatostatin (for reviews see [55, 81]. However, many other types of DG inter-neurons exist: MOPP cells [28], ivy cells and neurogliaform cells [3] and hilar neurons that innervate the inner molecular layer (HICAP cells; [51, 52]).…”