Development of glutamatergic innervation during maturation of adult-born neurons

doi:10.1007/s11515-015-1362-2

Front. Biol.

2015, Vol. 10

Issue (4) : 310-320 https://doi.org/10.1007/s11515-015-1362-2

REVIEW

Development of glutamatergic innervation during maturation of adult-born neurons

Cristina V. Dieni(

),Adam J. Wieckert,Linda Overstreet-Wadiche

Department of Neurobiology and Evelyn McKnight Brain Institute, University of Alabama at Birmingham, Birmingham, AL 35294,USA

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Abstract

The dentate gyrus is the entrance of the hippocampal formation and a primary target of excitatory afferents from the entorhinal cortex that carry spatial and sensory information. Mounting evidence suggests that continual adult neurogenesis contributes to appropriate processing of cortical information. The ongoing integration of adult born neurons dynamically modulates connectivity of the network, potentially contributing to dentate cognitive function. Here we review the current understanding of how glutamatergic innervation develops during the progression of adult-born neuron maturation. Summarizing the developmental stages of dentate neurogenesis, we also demonstrate that new neurons at an immature stage of maturation begin to process afferent activity from both medial and lateral entorhinal cortices.

Keywords dentate gyrus adult neurogenesis glutamatergic innervation granule cell neuroprogenitor

Corresponding Author(s): Cristina V. Dieni

Just Accepted Date: 07 May 2015 Online First Date: 14 July 2015 Issue Date: 14 August 2015

Cite this article:

Cristina V. Dieni,Adam J. Wieckert,Linda Overstreet-Wadiche. Development of glutamatergic innervation during maturation of adult-born neurons[J]. Front. Biol., 2015, 10(4): 310-320.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-015-1362-2
https://academic.hep.com.cn/fib/EN/Y2015/V10/I4/310

Fig.1 Initial silent synapses on adult born GCs arise from hilar mossy cells. (A) Left, diagram of recording from newborn GCs expressing POMC-GFP. Stimulation in the IML evokes NMDAR-only EPSCs (top right, pre-pairing) that undergo rapid incorporation of AMPARs after pairing synaptic stimulation with postsynaptic depolarization (top right, post-pairing). Ten traces overlaid (gray) with averages (black). Right bottom, plot of EPSC amplitude versus time at -70 mV (black) and+ 40 mV (blue). Adapted from Chancey et al., 2013. (B) Left, a mossy cell filled with biocytin (white) in a DG injected with ChR2-mCherry (red). Insets, mossy cell spiking in response to 455 nm light (blue bars). Scale bar, 100 μm. GCL, granule cell layer. Right, ChR2-mCherry-labeled commissural axons in the hilus and IML of the contralateral DG. Inset, example of light-evoked NMDAR EPSC in a POMC-GFP newborn GC that is blocked by CB1R agonist WIN 55 212-2. Scale bar, 100 μm. Adapted from Chancey et al., 2014.

Fig.2 Immature GCs are innervated by medial and lateral enthorinal cortex. (A) Left, cartoon showing AAV-ChR2-EGFP injection sites in LEnt or MEnt. Right, the MEnt injection site results in axonal projections expressing ChR2-GFP in the MML of the DG. (B) Left, confocal image showing ChR2-EGFP expression in the MPP and a recorded GC (white) in acute slice. Right, blue light pulses evoke AMPAR-mediated EPSCs that are blocked by CNQX (gray trace). Approximately 80% of 21-day old retroviral labeled immature GCs exhibit EPSCs evoked by selective MEnt or LEnt optogenetic stimulation. Adapted from Kumamoto et al. (2012) with permission from Nature Publishing Group. (C) Left, focal stimulation in the MEnt and LEnt also evokes AMPAR EPSCs in dentate GCs. Right, confocal image of TdTomato-labeled immature GCs in Nestin-CreER mice at 4 weeks post-tamoxifen injection (PTI). (D) Example of EPSCs in mature (left) and immature (right) GCs in response to paired-pulse stimulation of the MEnt (top) or LEnt (bottom) pathways. Adapted from Dieni et al., 2013.

Fig.3 EPSCs in ~3 week-old GCs show pharmacology of medial perforant path. (A) Immunostaining for mGluR2/3 shows selective expression in axons of MPP. (B) Percentage of GCs exhibiting EPSCs during focal MPP and LPP stimulation (*p = 0.045 Fisher’s exact test). Immature GCs were identified in GAD67-GFP reporter mice. The total number of cells recorded is indicated in the bars. (C) Left, DCG-IV (1μM) decreased EPSCs in mature GCs during MPP and LPP stimulation by 73% and 27% respectively (n = 6 each pathway, p = 0.0004 unpaired t-test). Right, examples of EPSCs recorded in mature GCs in the absence and presence of DCG-IV. (D) Left, DCG-IV decreased EPSCs in GAD67-GFP labeled immature GCs by 56% (n = 5, p = 0.0035, paired t-test). A representative time plot of EPSCs in an immature GC (left) and representative EPSCs (right).

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