Neurons born in the adult dentate gyrus form functional synapses with target cells

By N. Toni, Diego A. Laplagne, Chunmei Zhao, G. Lombardi, C. Ribak, Fred H. Gage, A. F. Schinder. 2008

779 citations recorded by the source corpus.

Adult neurogenesis occurs in the hippocampus and the olfactory bulb of the mammalian CNS. Recent studies have demonstrated that newborn granule cells of the adult hippocampus are postsynaptic targets of excitatory and inhibitory neurons, but evidence of synapse formation by the axons of these cells is still lacking. By combining retroviral expression of green fluorescent protein in adult-born neurons of the mouse dentate gyrus with immuno-electron microscopy, we found output synapses that were formed by labeled terminals on appropriate target cells in the CA3 area and the hilus. Furthermore, retroviral expression of channelrhodopsin-2 allowed us to light-stimulate newborn granule cells and identify postsynaptic target neurons by whole-cell recordings in acute slices. Our structural and functional evidence indicates that axons of adult-born granule cells establish synapses with hilar interneurons, mossy cells and CA3 pyramidal cells and release glutamate as their main neurotransmitter.

Subfields: Cellular and Molecular Neuroscience, Developmental Neuroscience, Neurology

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Citations in the corpus

New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? (2010, background): “Similarly, the mossy fibre boutons of adult-born DGCs initially form synapses either with the dendritic shaft of CA3 pyramidal neurons in a region near existing thorny excrescences or directly with existing thorny excrescences that already contain a bouto”
The effects of exercise and stress on the survival and maturation of adult-generated granule cells (2009, positive): “The increased survival and more rapid functional maturation observed in runners are particularly important to consider in light of the large number of studies of adult neurogenesis that use running wheels as a standard housing feature (Laplagne et al., 2006; Laplagne et al., 2007; Toni et al., 2008;”
GABA-CREB signalling regulates maturation and survival of newly generated neurons in the adult hippocampus (2009, background): “Survival, maturation, and integration of new neurons into the hippocampal circuit are closely connected in time (van Praag et al., 2002; Schmidt-Hieber et al., 2004; Espósito et al., 2005; Zhao et al., 2006; Tashiro et al., 2007; Toni et al., 2008).”
Retrograde monosynaptic tracing reveals the temporal evolution of inputs onto new neurons in the adult dentate gyrus and olfactory bulb (2013, background): “, presumable formation of excitatory synapses) (34, 35) and the functional maturation of axonal terminals of young granule neurons (6), two morphological correlates of successful neuronal integration.”
Distinct Contribution of Adult-Born Hippocampal Granule Cells to Context Encoding (2016, positive): “Alternatively, the abGC population may modulate local excitatory/inhibitory tone in the DG and CA3 (Gu et al., 2012; Restivo et al., 2015; Toni et al., 2008) and could consequently shape spatial and contextual representations.”
The problem of pseudoreplication in neuroscientific studies: is it affecting your analysis? (2010, background): “examined how new dentate gyrus neurons integrate and form functional synapses with cells in the hilus and CA3 region of the hippocampus [30].”
Modeling new neuron function: a history of using computational neuroscience to study adult neurogenesis (2011, background): “One feature of new neuron maturation that requires further exploration is the relationship of new neurons to their targets in the CA3 and hilus (Toni et al. , 2008).”
Adult neurogenesis and the plasticity of the dentate gyrus network (2011, background): “obtained by immuno-electron microscopy and serial sectioning of retrovirally labeled neurons (Faulkner et al., 2008; Toni et al., 2008).”
Dopaminergic Modulation of Cortical Inputs during Maturation of Adult-born Dentate Granule Cells (2011, background): “, 2006) and form functional synapses with interneurons and CA3 pyramidal cells (Toni et al., 2008).”
Ablation of Fmrp in adult neural stem cells disrupts hippocampus-dependent learning (2011, positive): “Synaptic competition between old and new neurons is known to occur when newborn neurons form synaptic connections with preexisting boutons in the dentate gyru”
Computational influence of adult neurogenesis on memory encoding. (2009, positive): “…were not formed immediately but rather gradually as the neuron matured within the network according to the rate of connectivity seen biologically (Toni et al., 2008; Zhao et al., 2006 ), and these synapses were the only plastic synapses in the model, experiencing LTP and long-term depression…”
Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain (2009, background): “During this time, newborn DGCs project their axons to CA3 and grow dendrites into the molecular layer, starting to form both afferent and efferent synapses (Hastings and Gould, 1999; Zhao et al., 2006; Toni et al., 2007, 2008; Faulkner et al., 2008).”
Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. (2012, neutral): “In practice, MF boutons from young and old GCs were found to share the same spines of CA3 cells in some cases but synapse separately on different spines from CA3 cells in other cases, suggesting a competition for their targets (Toni et al., 2008).”