Structure, function, and plasticity of hippocampal dentate gyrus microcircuits

The hippocampus mediates several higher brain functions, such as learning, memory, and spatial coding. The input region of the hippocampus, the dentate gyrus, plays a critical role in these processes. Several lines of evidence suggest that the dentate gyrus acts as a preprocessor of incoming informa...

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Autores principales: Peter Jonas, John Lisman
Formato: Online
Lenguaje:inglés
Publicado: Frontiers Media SA 2021
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Acceso en línea:17757
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author Peter Jonas
John Lisman
author_browse John Lisman
Peter Jonas
author_facet Peter Jonas
John Lisman
author_sort Peter Jonas
collection Directory of Open Access Books
description The hippocampus mediates several higher brain functions, such as learning, memory, and spatial coding. The input region of the hippocampus, the dentate gyrus, plays a critical role in these processes. Several lines of evidence suggest that the dentate gyrus acts as a preprocessor of incoming information, preparing it for subsequent processing in CA3. For example, the dentate gyrus converts input from the entorhinal cortex, where cells have multiple spatial fields, into the spatially more specific place cell activity characteristic of the CA3 region. Furthermore, the dentate gyrus is involved in pattern separation, transforming relatively similar input patterns into substantially different output patterns. Finally, the dentate gyrus produces a very sparse coding scheme in which only a very small fraction of neurons are active at any one time. How are these unique functions implemented at the level of cells and synapses? Dentate gyrus granule cells receive excitatory neuron input from the entorhinal cortex and send excitatory output to the hippocampal CA3 region via the mossy fibers. Furthermore, several types of GABAergic interneurons are present in this region, providing inhibitory control over granule cell activity via feedback and feedforward inhibition. Additionally, hilar mossy cells mediate an excitatory loop, receiving powerful input from a small number of granule cells and providing highly distributed excitatory output to a large number of granule cells. Finally, the dentate gyrus is one of the few brain regions exhibiting adult neurogenesis. Thus, new neurons are generated and functionally integrated throughout life. How these specific cellular and synaptic properties contribute to higher brain functions remains unclear. One way to understand these properties of the dentate gyrus is to try to integrate experimental data into models, following the famous Hopfield quote: "Build it, and you understand it." However, when trying this, one faces two major challenges. First, hard quantitative data about cellular properties, structural connectivity, and functional properties of synapses are lacking. Second, the number of individual neurons and synapses to be represented in the model is huge. For example, the dentate gyrus contains ~1 million granule cells in rodents, and ~10 million in humans. Thus, full scale models will be complex and computationally demanding. In this Frontiers Research Topic, we collect important information about cells, synapses, and microcircuit elements of the dentate gyrus. We have put together a combination of original research articles, review articles, and a methods article. We hope that the collected information will be useful for both experimentalists and modelers. We also hope that the papers will be interesting beyond the small world of "dentology", i.e., for scientists working on other brain areas. Ideally, the dentate gyrus may serve as a blueprint, helping neuroscientists to define strategies to analyze network organization of other brain regions.
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spelling doab-20.500.12854ir-601562024-04-05T12:36:12Z Structure, function, and plasticity of hippocampal dentate gyrus microcircuits Peter Jonas John Lisman RC321-571 Q1-390 Dentate Gyrus adult neurogenesis mossy fibers mossy cells granule cells mossy fiber synapses Hippocampus thema EDItEUR::P Mathematics and Science::PS Biology, life sciences::PSA Life sciences: general issues::PSAN Neurosciences The hippocampus mediates several higher brain functions, such as learning, memory, and spatial coding. The input region of the hippocampus, the dentate gyrus, plays a critical role in these processes. Several lines of evidence suggest that the dentate gyrus acts as a preprocessor of incoming information, preparing it for subsequent processing in CA3. For example, the dentate gyrus converts input from the entorhinal cortex, where cells have multiple spatial fields, into the spatially more specific place cell activity characteristic of the CA3 region. Furthermore, the dentate gyrus is involved in pattern separation, transforming relatively similar input patterns into substantially different output patterns. Finally, the dentate gyrus produces a very sparse coding scheme in which only a very small fraction of neurons are active at any one time. How are these unique functions implemented at the level of cells and synapses? Dentate gyrus granule cells receive excitatory neuron input from the entorhinal cortex and send excitatory output to the hippocampal CA3 region via the mossy fibers. Furthermore, several types of GABAergic interneurons are present in this region, providing inhibitory control over granule cell activity via feedback and feedforward inhibition. Additionally, hilar mossy cells mediate an excitatory loop, receiving powerful input from a small number of granule cells and providing highly distributed excitatory output to a large number of granule cells. Finally, the dentate gyrus is one of the few brain regions exhibiting adult neurogenesis. Thus, new neurons are generated and functionally integrated throughout life. How these specific cellular and synaptic properties contribute to higher brain functions remains unclear. One way to understand these properties of the dentate gyrus is to try to integrate experimental data into models, following the famous Hopfield quote: "Build it, and you understand it." However, when trying this, one faces two major challenges. First, hard quantitative data about cellular properties, structural connectivity, and functional properties of synapses are lacking. Second, the number of individual neurons and synapses to be represented in the model is huge. For example, the dentate gyrus contains ~1 million granule cells in rodents, and ~10 million in humans. Thus, full scale models will be complex and computationally demanding. In this Frontiers Research Topic, we collect important information about cells, synapses, and microcircuit elements of the dentate gyrus. We have put together a combination of original research articles, review articles, and a methods article. We hope that the collected information will be useful for both experimentalists and modelers. We also hope that the papers will be interesting beyond the small world of "dentology", i.e., for scientists working on other brain areas. Ideally, the dentate gyrus may serve as a blueprint, helping neuroscientists to define strategies to analyze network organization of other brain regions. 2021-02-12T04:45:02Z 2021-02-12T04:45:02Z 2015-12-03 13:02:24 2015 book 17757 16648714 9782889193875 https://directory.doabooks.org/handle/20.500.12854/60156 eng Frontiers Research Topics image/jpeg Attribution 4.0 International http://www.frontiersin.org/books/Structure_function_and_plasticity_of_hippocampal_dentate_gyrus_microcircuits/440 http://journal.frontiersin.org/researchtopic/737/structure-function-and-plasticity-of-hippocampal-dentate-gyrus-microcircuits Frontiers Media SA 10.3389/978-2-88919-387-5 10.3389/978-2-88919-387-5 bf5ce210-e72e-4860-ba9b-c305640ff3ae 9782889193875 133 open access
spellingShingle RC321-571
Q1-390
Dentate Gyrus
adult neurogenesis
mossy fibers
mossy cells
granule cells
mossy fiber synapses
Hippocampus
thema EDItEUR::P Mathematics and Science::PS Biology, life sciences::PSA Life sciences: general issues::PSAN Neurosciences
Peter Jonas
John Lisman
Structure, function, and plasticity of hippocampal dentate gyrus microcircuits
title Structure, function, and plasticity of hippocampal dentate gyrus microcircuits
title_full Structure, function, and plasticity of hippocampal dentate gyrus microcircuits
title_fullStr Structure, function, and plasticity of hippocampal dentate gyrus microcircuits
title_full_unstemmed Structure, function, and plasticity of hippocampal dentate gyrus microcircuits
title_short Structure, function, and plasticity of hippocampal dentate gyrus microcircuits
title_sort structure function and plasticity of hippocampal dentate gyrus microcircuits
topic RC321-571
Q1-390
Dentate Gyrus
adult neurogenesis
mossy fibers
mossy cells
granule cells
mossy fiber synapses
Hippocampus
thema EDItEUR::P Mathematics and Science::PS Biology, life sciences::PSA Life sciences: general issues::PSAN Neurosciences
topic_facet RC321-571
Q1-390
Dentate Gyrus
adult neurogenesis
mossy fibers
mossy cells
granule cells
mossy fiber synapses
Hippocampus
thema EDItEUR::P Mathematics and Science::PS Biology, life sciences::PSA Life sciences: general issues::PSAN Neurosciences
url 17757
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