Neuronal Differentiation in the Adult Hippocampus Recapitulates Embryonic Development

By M. S. Esposito, Verónica C. Piatti, Diego A. Laplagne, Nicolás A. Morgenstern, C. Ferrari, F. Pitossi, A. F. Schinder. 2005

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In the adult hippocampus and olfactory bulb, neural progenitor cells generate neurons that functionally integrate into the existing circuits. To understand how neuronal differentiation occurs in the adult hippocampus, we labeled dividing progenitor cells with a retrovirus expressing green fluorescent protein and studied the morphological and functional properties of their neuronal progeny over the following weeks. During the first week neurons had an irregular shape and immature spikes and were synaptically silent. Slow GABAergic synaptic inputs first appeared during the second week, when neurons exhibited spineless dendrites and migrated into the granule cell layer. In contrast, glutamatergic afferents were detected by the fourth week in neurons displaying mature excitability and morphology. Interestingly, fast GABAergic responses were the latest to appear. It is striking that neuronal maturation in the adult hippocampus follows a precise sequence of connectivity (silent → slow GABA → glutamate → fast GABA) that resembles hippocampal development. We conclude that, unlike what is observed in the olfactory bulb, the hippocampus maintains the same developmental rules for neuronal integration through adulthood.

Subfields: Cellular and Molecular Neuroscience, Developmental Neuroscience, Neurology

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Citations in the corpus

Adult Neurogenesis in the Mammalian Brain: Significant Answers and Significant Questions (2011, background): “, 2006), followed by GABAergic synaptic inputs, and finally glutamatergic synaptic inputs (Espósito et al., 2005; Ge et al., 2006; Overstreet-Wadiche et al., 2006b) and mossy fiber synaptic outputs to hilar and CA3 neurons (Faulkner et al.”
New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? (2010, background): “Notably, these cells are tonically activated by ambient GABA (γ-aminobutyric acid”
Spatial Learning Depends on Both the Addition and Removal of New Hippocampal Neurons (2007, background): “Toward the end of the second week, GABA inputs become progressively hyperpolarizing, and the adult-born neurons begin receiving functional glutamatergic depolarizing afferents [11,29,40,41], a process that occurs in parallel with the formation of dendritic spines.”
Seizures Accelerate Functional Integration of Adult-Generated Granule Cells (2006, neutral): “Although adult-generated granule cells express functional AMPA and NMDA receptors, they first receive exclusively GABAergic synaptic input (Overstreet et al., 2004; Esposito et al., 2005; Ge et al., 2005; Overstreet-Wadiche et al., 2005; Song et al., 2005; Wang et al., 2005; Overstreet-Wadiche and W”
Effects of adult-generated granule cells on coordinated network activity in the dentate gyrus (2010, background): “From the time that they receive their first perforant-path synapses until they are almost fully mature (from 2-4 weeks postdivision), young granule cells have lower thresholds for firing action potentials and longterm potentiation (LTP) than mature neurons (Esposito et al., 2005; Ge et al., 2007; La”
Structural Plasticity and Hippocampal Function (2010, background): “…lines of evidence suggest that the maturational processes of adult-generated neurons follow stages characteristic of development even though they are maturing in the context of an adult hippocampus (Espósito et al. 2005; reviewed in Overstreet-Wadiche & Westbrook 2006, Ribak & Shapiro 2007).”
Molecular layer perforant path-associated cells contribute to feed-forward inhibition in the adult dentate gyrus (2013, result): “We found red cells in layer II of the ipsilateral entorhinal cortex, which is consistent with the time window of spine and glutamatergic synapse formation in new neurons (19, 20) (Fig.”
The effects of exercise and stress on the survival and maturation of adult-generated granule cells (2009, neutral): “Very few 14-day-old neurons expressed Arc, even after strong activation by kainate-induced seizures, consistent with electrophysiological studies showing that 14-day-old granule cells do not yet receive significant excitatory inputs (Esposito et al., 2005; but see Ge et al., 2006).”
Long-Term Potentiation Enhances Neurogenesis in the Adult Dentate Gyrus (2006, background): “Recent studies examining the maturation of newborn DGCs in adulthood suggest that 1-week-old neurons are immature, have few spines, and display depolarizing bicuculline-sensitive GABA currents before becoming sensitive to glutamatergic synaptic activation, which starts to be detected by only 2 weeks”
A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. (2007, neutral): “Significant LTP of EPSPs was reliably induced with TBS in GFP DGCs examined at 1 month postinfection (mpi; n = 7; Figure 1A), when most new DGCs are already fully integrated into the existing circuitry (Esposito et al., 2005; Ge et al., 2006).”
Computational influence of adult neurogenesis on memory encoding. (2009, positive): “, 2007), physiological dynamics (Esposito et al., 2005; Ge et al., 2006), and survival (Kempermann et al.”
Development of neural stem cell in the adult brain. (2008, background): “For new dentate granule cells, formation of dendritic GABAergic synaptic inputs (approximately one week after birth) initiates before formation of glutamatergic synaptic inputs (approximately two weeks after birth), and perisomatic GABAergic inputs appear to form last (Figure 2) [39].”
Anatomical gradients of adult neurogenesis and activity: young neurons in the ventral dentate gyrus are activated by water maze training (2009, neutral): “…evidence that these adult-born granule neurons are physiologically functional (Wang et al., 2000; Snyder et al., 2001; van Praag et al., 2002; Esposito et al., 2005; Ge et al., 2006) and contribute to hippocampus-dependent behaviors (Shors et al., 2001, 2002; Santarelli et al., 2003; Snyder…”
Constitutive and Synaptic Activation of GIRK Channels Differentiates Mature and Newborn Dentate Granule Cells (2018, background): “Newborn dentate GCs lack functional GIRK channels Resident neural stem cells in the adult DG continuously generate new GCs that gradually acquire the intrinsic and synaptic properties of mature GCs over several weeks (Espósito et al., 2005; Dieni et al., 2013b; Toni and Schinder, 2015).”