Inverse relationship between adult hippocampal cell proliferation and synaptic rewiring in the dentate gyrus

Butz, Markus; Teuchert-Noodt, Gertraud; Grafen, Keren; Ooyen, Arjen van

doi:10.1002/hipo.20445

Cited by 43 publications

(48 citation statements)

References 147 publications

(157 reference statements)

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“…Instead, "homeostatic-like" changes within mature dentate gyrus networks may restore the balance of inhibition and excitation in the absence of immature DCGs. Indeed, the level of neurogenesis correlates inversely with rates of synaptic turnover under certain conditions (36).…”

Section: Discussionmentioning

confidence: 99%

Compensatory network changes in the dentate gyrus restore long-term potentiation following ablation of neurogenesis in young-adult mice

Singer

Gamelli

Fuller

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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It is now well established that neurogenesis in the rodent subgranular zone of the hippocampal dentate gyrus continues throughout adulthood. Neuroblasts born in the dentate subgranular zone migrate into the granule cell layer, where they differentiate into neurons known as dentate granule cells. Suppression of neurogenesis by irradiation or genetic ablation has been shown to disrupt synaptic plasticity in the dentate gyrus and impair some forms of hippocampus-dependent learning and memory. Using a recently developed transgenic mouse model for suppressing neurogenesis, we sought to determine the long-term impact of ablating neurogenesis on synaptic plasticity in young-adult mice. Consistent with previous reports, we found that ablation of neurogenesis resulted in significant deficits in dentate gyrus long-term potentiation (LTP) when examined at a time proximal to the ablation. However, the observed deficits in LTP were not permanent. LTP in the dentate gyrus was restored within 6 wk and this recovery occurred in the complete absence of neurogenesis. The recovery in LTP was accompanied by prominent changes within the dentate gyrus, including an increase in the survival rate of newborn cells that were proliferating just before the ablation and a reduction in inhibitory input to the granule cells of the dentate gyrus. These findings suggest that prolonged suppression of neurogenesis in young-adult mice results in wide-ranging compensatory changes in the structure and dynamics of the dentate gyrus that function to restore plasticity.adult neurogenesis | thymidine kinase | metaplasticity | miniature inhibitory postsynaptic currents F orebrain neurogenesis persists into adulthood in the subgranular zone (SGZ) of the hippocampal dentate gyrus in rodents (1-4). Under normal conditions (i.e., in the absence of overt pathology) neuroblasts that arise in the SGZ migrate a short distance into the dentate granule cell layer (GCL) and differentiate into dentate granule cells (DGCs), where they subsequently reach functional maturity (5, 6). The birth, integration, and survival of DGCs are modulated by environmental enrichment (7), exercise (8), stress (9, 10), hippocampus-dependent learning (11), and direct manipulation of neuronal activity (12, 13). In addition, adult-born DGCs respond preferentially in hippocampus-dependent memory tasks (14) and display increased synaptic plasticity relative to mature DGCs (15,16).The correlation of increased DGC neurogenesis with cognitively demanding tasks has led to the hypothesis that adult-born neurons are integral participants in hippocampus-dependent memory processing and behavior. The role of adult-born DGCs in hippocampal function has been studied at the behavioral level in rodents after suppressing neurogenesis with antimitotic agents (17, 18), radiation (19), or genetic targeting (19)(20)(21)(22). These studies indicate that adult-born DGCs are necessary for some hippocampus-dependent tasks, although results have been inconsistent and vary by rodent species and strain, behavioral ...

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Section: Discussionmentioning

confidence: 99%

Compensatory network changes in the dentate gyrus restore long-term potentiation following ablation of neurogenesis in young-adult mice

Singer

Gamelli

Fuller

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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“…Aiming to bridge structure and function at the theoretical level, recently developed computational models started implementing rules for anatomical modifications at the cellular level to look for dynamic network property changes over time (Butz et al, 2008). …”

Section: Brain Plasticity—cellular Mechanismsmentioning

confidence: 99%

Computational anatomy for studying use-dependant brain plasticity

Draganski

Kherif

Lutti

2014

Front. Hum. Neurosci.

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In this article we provide a comprehensive literature review on the in vivo assessment of use-dependant brain structure changes in humans using magnetic resonance imaging (MRI) and computational anatomy. We highlight the recent findings in this field that allow the uncovering of the basic principles behind brain plasticity in light of the existing theoretical models at various scales of observation. Given the current lack of in-depth understanding of the neurobiological basis of brain structure changes we emphasize the necessity of a paradigm shift in the investigation and interpretation of use-dependent brain plasticity. Novel quantitative MRI acquisition techniques provide access to brain tissue microstructural properties (e.g., myelin, iron, and water content) in-vivo, thereby allowing unprecedented specific insights into the mechanisms underlying brain plasticity. These quantitative MRI techniques require novel methods for image processing and analysis of longitudinal data allowing for straightforward interpretation and causality inferences.

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“…The focal retinal lesion is modeled as a circumscribed removal of the vertical input stream. To model structural changes of the neuron, we created a novel model formalism in which each neuron has a number of axonal elements (representing boutons) and dendritic elements (representing spines) [1,3]. Synapses are formed by merging axonal and dendritic elements.…”

mentioning

confidence: 99%

Need for homeostasis in electrical activity may account for cortical network rewiring

Butz¹,

Ooyen²

2011

BMC Neurosci

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Inverse relationship between adult hippocampal cell proliferation and synaptic rewiring in the dentate gyrus

Cited by 43 publications

References 147 publications

Compensatory network changes in the dentate gyrus restore long-term potentiation following ablation of neurogenesis in young-adult mice

Compensatory network changes in the dentate gyrus restore long-term potentiation following ablation of neurogenesis in young-adult mice

Computational anatomy for studying use-dependant brain plasticity

Need for homeostasis in electrical activity may account for cortical network rewiring

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