Experience-Specific Functional Modification of the Dentate Gyrus through Adult Neurogenesis: A Critical Period during an Immature Stage

By A. Tashiro, Hiroshi Makino, Fred H. Gage. 2007

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Neural circuits in the dentate gyrus are continuously modified by adult neurogenesis, whose level is affected by the animal's experience. However, it is not known whether this experience-dependent anatomical modification alters the functional properties of the dentate gyrus. Here, using the expression of immediate early gene products, c-fos and Zif268, as indicators of recently activated neurons, we show that previous exposure to an enriched environment increases the total number of new neurons and the number of new neurons responding to reexposure to the same environment. The increase in the density of activated new neurons occurred specifically in response to exposure to the same environment but not to a different experience. Furthermore, we found that these experience-specific modifications are affected exclusively by previous exposure around the second week after neuronal birth but not later than 3 weeks. Thus, the animal's experience within a critical period during an immature stage of new neurons determines the survival and population response of the new neurons and may affect later neural representation of the experience in the dentate gyrus. This experience-specific functional modification through adult neurogenesis could be a mechanism by which new neurons exert a long-term influence on the function of the dentate gyrus related to learning and memory.

Subfields: Cell Biology, Cellular and Molecular Neuroscience, Developmental Neuroscience

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Citations in the corpus

New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? (2010, background): “Environmental enrichment for as little as 1 week is sufficient to increase the survival of the adult-born DGCs that are younger than 3 weeks of age but not of older ones, suggesting that the environmental-enrichment effect is dependent on the maturation state of adult-born DGC”
Re-evaluating circuit mechanisms underlying pattern separation (2019, positive): “In the dentate gyrus, ultra-sparse granule cell population activity (2-5%) over long timescales was originally inferred from immediate-early gene expression (Chawla et al., 2005; Tashiro et al., 2007; Alme et al., 2010).”
Recruitment of adult-generated neurons into functional hippocampal networks contributes to updating and strengthening of spatial memory (2009, background): “Activation of new granular neurons specifically in response to exposure to the same environment, but not to a different experience, has been reported recently (6).”
Stress, Depression, and Neuroplasticity: A Convergence of Mechanisms (2008, background): “It is interesting to speculate that this increased potential for plasticity in the dentate could result from an increased number of newborn granule cells, which are known to have greater potential for neuroplasticity (Toni et al, 2007; Tashiro et al, 2007).”
GABA-CREB signalling regulates maturation and survival of newly generated neurons in the adult hippocampus (2009, background): “The rate of survival can be strongly modulated by complex behavioral stimuli, such as exposure to an enriched environment (van Praag et al., 1999; Tashiro et al., 2007) and hippocampus-dependent learning paradigms (Gould et al., 1999; Dupret et al., 2007; Kee et al., 2007; Aimone et al., 2009), all…”
Effects of adult-generated granule cells on coordinated network activity in the dentate gyrus (2010, background): “Consequently, the notion has arisen that the enhanced plasticity and excitability of young neurons makes them a preferential substrate for new memories or representations (Aimone et al., 2006; Aimone et al., 2009; Doetsch and Hen, 2005; Kee et al., 2007; Tashiro et al., 2007).”
Spatial Learning Depends on Both the Addition and Removal of New Hippocampal Neurons (2007, background): “to experience-specific modifications of adult-born neurons occur at a critical period during an immature stage [29,30].”
Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation (2011, background): “Second, this immature state of GCs represents a critical developmental period in which they encode significant features of their environments (Kee et al., 2007; Tashiro et al., 2007).”
Adult neurogenesis and the plasticity of the dentate gyrus network (2011, background): “In vivo studies have interrogated firing of newborn cells using the expression of immediate-early genes as indicators of neuronal activity after spatial learning and exploration (Jessberger & Kempermann, 2003; Ramirez-Amaya et al., 2006; Kee et al., 2007; Tashiro et al., 2007).”
Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain (2009, background): “Furthermore, this immature stage corresponds to a “critical period,” when the experiences of the animals could modulate the survival and subsequent experience-specific responsiveness of adult-born DGCs (Tashiro et al., 2006, 2007).”
Synaptic integration and plasticity of new neurons in the adult hippocampus (2008, background): “…of the immediate early genes c-Fos and Arc suggest a selective incorporation of adult-born neurons into behaviourally relevant neuronal circuitry and preferential reactivation of these neurons in response to the same stimulation (Ramirez-Amaya et al. 2006; Kee et al. 2007; Tashiro et al. 2007).”
The role of adult hippocampal neurogenesis in brain health and disease (2018, background): “The increase in surviving and integrating immature neurons based on environmental inputs could be crucial, as the surviving adult-born DGCs could potentially be tuned to respond to future occurrences of the same experiences that they experience during their maturation periods [15, 23] (see also the ”
Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. (2012, unknown): “…may be compensated by the greater excitability and synaptic plasticity of young GCs (Schmidt-Hieber et al., 2004; Ge et al., 2007; Kee et al., 2007; Tashiro et al., 2007), and there may be additional unknown mechanisms that may favor the output of these cells (e.g., differential connection with…”
A Critical Time Window for the Recruitment of Bulbar Newborn Neurons by Olfactory Discrimination Learning (2011, methodology): “Recruitment of newborn neurons by odor stimulation By imaging the activation of 2-, 5-, and 9-week-old neurons using a classical functional anatomical approach (Jessberger and Kempermann, 2003; Ramirez-Amaya et al., 2006; Kee et al., 2007; Tashiro et al., 2007; Trouche et al., 2009), we found that o”
Experience dictates stem cell fate in the adult hippocampus. (2011, unknown): “Environmental enrichment was previously demonstrated to increase neuronal activity in the dentate gyrus (Tashiro et al., 2007) while social isolation was recently demonstrated to decrease it (Ibi et al.”
Mechanisms and functional implications of adult neurogenesis. (2008, unknown): “However, the animals’ experience during this time window can affect the expression of activity-dependent immediate early genes in newborn neurons when they are 6 weeks old or older (Kee et al., 2007; Tashiro et al., 2007).”
A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. (2007, unknown): “One potential mechanism for such biased recruitment is selective survival of overproduced immature neurons at the cell age of around 2 weeks in response to experience (Kee et al., 2007; Tashiro et al., 2006, 2007).”