Conditional reduction of adult neurogenesis impairs bidirectional hippocampal synaptic plasticity

Massa, Federico; Koehl, Muriel; Wiesner, Theresa; Grosjean, Noëlle; Revest, Jean‐Michel; Piazza, Pier-Vincenzo; Abrous, Djoher Nora; Oliet, Stéphane H. R.

doi:10.1073/pnas.1016928108

Cited by 81 publications

(66 citation statements)

References 28 publications

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“…These deficits were not related to a disruption of ongoing neurogenesis since at the time of killing cell proliferation was back to normal. An alteration of synaptic plasticity can be ruled out since LTP and LTD impairments are rescued completely within 4 weeks after restoring adult neurogenesis (Massa et al, 2011). The deficits that we observed were not either due to ablation of subventricular zone progenitor cells or to nonspecific effects of AraC since animals tested for a shorter delay learned the task.…”

Section: Functional Integration Of Mature Adult-born Neuronsmentioning

confidence: 70%

Long-Lasting Plasticity of Hippocampal Adult-Born Neurons

et al. 2012

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Adult neurogenesis occurs in the dentate gyrus of the hippocampus, which is a key structure in learning and memory. It is believed that adult-born neurons exert their unique role in information processing due to their high plasticity during immature stage that renders them malleable in response to environmental demands. Here, we demonstrate that, in rats, there is no critical time window for experience-induced dendritic plasticity of adult-born neurons as spatial learning in the water maze sculpts the dendritic arbor of adult-born neurons even when they are several months of age. By ablating neurogenesis within a specific period of time, we found that learning was disrupted when the delay between ablation and learning was extended to several months. Together, these results show that mature adult-born neurons are still plastic when they are functionally integrated into dentate network. Our results suggest a new perspective with regard to the role of neo-neurons by highlighting that even mature ones can provide an additional source of plasticity to the brain to process memory information.

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Section: Functional Integration Of Mature Adult-born Neuronsmentioning

confidence: 70%

Long-Lasting Plasticity of Hippocampal Adult-Born Neurons

et al. 2012

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“…Hence, administration of the tetracycline analog, doxycycline, increases subgranular zone apoptosis. However, neurogenesis is reduced rather than ablated in this model (Dupret et al 2008;Massa et al 2011).…”

Section: Abgcs and Pattern Separationmentioning

confidence: 71%

“…Points (1), (3), and (4) are now wellreplicated findings (Saxe et al 2007;Wang et al 2008;Garthe et al 2009;Massa et al 2011) and a study in which NR2B was genetically deleted from abGCs recently found that LTP was absent in DG field recordings (Kheirbek et al 2012a). Schmidt-Hieber et al (2004) made whole-cell recordings from young abGCs (PSA-NCAM immunoreactive) and matGCs and applied three different LTP induction protocols where u-burst afferent stimulation was paired with distinct regimes of postsynaptic depolarization (all in the presence of a GABA A antagonist).…”

Section: Afferent Synaptic Plasticitymentioning

confidence: 85%

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Adult neurogenesis in the mammalian hippocampus: Why the dentate gyrus?

2013

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In the adult mammalian brain, newly generated neurons are continuously incorporated into two networks: interneurons born in the subventricular zone migrate to the olfactory bulb, whereas the dentate gyrus (DG) of the hippocampus integrates locally born principal neurons. That the rest of the mammalian brain loses significant neurogenic capacity after the perinatal period suggests that unique aspects of the structure and function of DG and olfactory bulb circuits allow them to benefit from the adult generation of neurons. In this review, we consider the distinctive features of the DG that may account for it being able to profit from this singular form of neural plasticity. Approaches to the problem of neurogenesis are grouped as “bottom-up,” where the phenotype of adult-born granule cells is contrasted to that of mature developmentally born granule cells, and “top-down,” where the impact of altering the amount of neurogenesis on behavior is examined. We end by considering the primary implications of these two approaches and future directions.

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“…These newborn neurons have biophysical characteris-tics that allow them to preferentially contribute back to synaptic plasticity, in that they have a lower threshold for the induction of LTP compared to mature neurons, due to their higher input resistance and slower membrane time constant [14,15]. Newborn neurons are also important for the induction of bidirectional hippocampal synaptic plasticity [16]. Furthermore, evidence is mounting to support the idea that adult-born neurons are integral participants in hippocampal-dependent cognitive processes, such as learning and memory formation [17][18][19], and mood regulation [20][21][22].…”

mentioning

confidence: 99%

The role of the N-methyl-d-aspartate receptor in the proliferation of adult hippocampal neural stem and precursor cells

Taylor

Bartlett

2014

Sci. China Life Sci.

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New neurons are continuously generated from resident pools of neural stem and precursor cells (NSPCs) in the adult brain. There are multiple pathways through which adult neurogenesis is regulated, and here we review the role of the N-methyl-D-aspartate receptor (NMDAR) in regulating the proliferation of NSPCs in the adult hippocampus. Hippocampal-dependent learning tasks, enriched environments, running, and activity-dependent synaptic plasticity, all potently up-regulate hippocampal NSPC proliferation. We first consider the requirement of the NMDAR in activity-dependent synaptic plasticity, and the role the induction of synaptic plasticity has in regulating NSPCs and newborn neurons. We address how specific NMDAR agonists and antagonists modulate proliferation, both in vivo and in vitro, and then review the evidence supporting the hypothesis that NMDARs are present on NSPCs. We believe it is important to understand the mechanisms underlying the activation of adult neurogenesis, given the potential that endogenous stem cell populations have for repopulating the hippocampus with functional new neurons. In conditions such as age-related memory decline, neurodegeneration and psychiatric disease, mature neurons are lost or become defective; as such, stimulating adult neurogenesis may provide a therapeutic strategy to overcome these conditions. The adult brain continuously generates new neurons throughout life. These adult-born neurons arise from endogenous neural stem and precursor cells (NSPCs), which primarily reside within two neurogenic niches: the subgranular zone (SGZ) in the dentate gyrus (DG) of the hippocampus, and the subventricular zone (SVZ) of the lateral ventricles. In the 20 years since adult mammalian neurogenesis started receiving substantial attention [1,2], scientists have made great progress in understanding the mechanisms that regulate stem cell maintenance, proliferation, differentiation, maturation and integration [3,4]. Early on, extrinsic cues from the environment, such as learning [5], physical activity [6], and enriched environments [7,8], were found to potently enhance hippocampal neurogenesis. It was not long before a link was made to synaptic plasticity [9], which is also enhanced by physical exercise [10], and is widely accepted as the synaptic mechanism underlying hippocampal learning and memory [11]. Synaptic plasticity and adult hippocampal neurogenesis are intimately linked, as long-term potentiation (LTP), an activity-dependent change in synaptic efficacy, can influence the activation and proliferation of NSPCs in the DG (e.g., [12]), as well as the survival of newborn neurons (e.g., [13]). These newborn neurons have biophysical characteris-

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Conditional reduction of adult neurogenesis impairs bidirectional hippocampal synaptic plasticity

Cited by 81 publications

References 28 publications

Long-Lasting Plasticity of Hippocampal Adult-Born Neurons

Long-Lasting Plasticity of Hippocampal Adult-Born Neurons

Adult neurogenesis in the mammalian hippocampus: Why the dentate gyrus?

The role of the N-methyl-d-aspartate receptor in the proliferation of adult hippocampal neural stem and precursor cells

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