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Self-directed exploration provides a Ncs1-dependent learning bonus

Understanding the mechanisms of memory formation is fundamental to establishing optimal educational practices and restoring cognitive function in brain disease. Here, we show for the first time in a non-primate species, that spatial learning receives a special bonus from self-directed exploration. I...

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Autores principales: Mun, Ho-Suk, Saab, Bechara J., Ng, Enoch, McGirr, Alexander, Lipina, Tatiana V., Gondo, Yoichi, Georgiou, John, Roder, John C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4671055/
https://www.ncbi.nlm.nih.gov/pubmed/26639399
http://dx.doi.org/10.1038/srep17697
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author Mun, Ho-Suk
Saab, Bechara J.
Ng, Enoch
McGirr, Alexander
Lipina, Tatiana V.
Gondo, Yoichi
Georgiou, John
Roder, John C.
author_facet Mun, Ho-Suk
Saab, Bechara J.
Ng, Enoch
McGirr, Alexander
Lipina, Tatiana V.
Gondo, Yoichi
Georgiou, John
Roder, John C.
author_sort Mun, Ho-Suk
collection PubMed
description Understanding the mechanisms of memory formation is fundamental to establishing optimal educational practices and restoring cognitive function in brain disease. Here, we show for the first time in a non-primate species, that spatial learning receives a special bonus from self-directed exploration. In contrast, when exploration is escape-oriented, or when the full repertoire of exploratory behaviors is reduced, no learning bonus occurs. These findings permitted the first molecular and cellular examinations into the coupling of exploration to learning. We found elevated expression of neuronal calcium sensor 1 (Ncs1) and dopamine type-2 receptors upon self-directed exploration, in concert with increased neuronal activity in the hippocampal dentate gyrus and area CA3, as well as the nucleus accumbens. We probed further into the learning bonus by developing a point mutant mouse (Ncs1(P144S/P144S)) harboring a destabilized NCS-1 protein, and found this line lacked the equivalent self-directed exploration learning bonus. Acute knock-down of Ncs1 in the hippocampus also decoupled exploration from efficient learning. These results are potentially relevant for augmenting learning and memory in health and disease, and provide the basis for further molecular and circuit analyses in this direction.
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spelling pubmed-46710552015-12-11 Self-directed exploration provides a Ncs1-dependent learning bonus Mun, Ho-Suk Saab, Bechara J. Ng, Enoch McGirr, Alexander Lipina, Tatiana V. Gondo, Yoichi Georgiou, John Roder, John C. Sci Rep Article Understanding the mechanisms of memory formation is fundamental to establishing optimal educational practices and restoring cognitive function in brain disease. Here, we show for the first time in a non-primate species, that spatial learning receives a special bonus from self-directed exploration. In contrast, when exploration is escape-oriented, or when the full repertoire of exploratory behaviors is reduced, no learning bonus occurs. These findings permitted the first molecular and cellular examinations into the coupling of exploration to learning. We found elevated expression of neuronal calcium sensor 1 (Ncs1) and dopamine type-2 receptors upon self-directed exploration, in concert with increased neuronal activity in the hippocampal dentate gyrus and area CA3, as well as the nucleus accumbens. We probed further into the learning bonus by developing a point mutant mouse (Ncs1(P144S/P144S)) harboring a destabilized NCS-1 protein, and found this line lacked the equivalent self-directed exploration learning bonus. Acute knock-down of Ncs1 in the hippocampus also decoupled exploration from efficient learning. These results are potentially relevant for augmenting learning and memory in health and disease, and provide the basis for further molecular and circuit analyses in this direction. Nature Publishing Group 2015-12-07 /pmc/articles/PMC4671055/ /pubmed/26639399 http://dx.doi.org/10.1038/srep17697 Text en Copyright © 2015, Macmillan Publishers Limited http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Mun, Ho-Suk
Saab, Bechara J.
Ng, Enoch
McGirr, Alexander
Lipina, Tatiana V.
Gondo, Yoichi
Georgiou, John
Roder, John C.
Self-directed exploration provides a Ncs1-dependent learning bonus
title Self-directed exploration provides a Ncs1-dependent learning bonus
title_full Self-directed exploration provides a Ncs1-dependent learning bonus
title_fullStr Self-directed exploration provides a Ncs1-dependent learning bonus
title_full_unstemmed Self-directed exploration provides a Ncs1-dependent learning bonus
title_short Self-directed exploration provides a Ncs1-dependent learning bonus
title_sort self-directed exploration provides a ncs1-dependent learning bonus
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4671055/
https://www.ncbi.nlm.nih.gov/pubmed/26639399
http://dx.doi.org/10.1038/srep17697
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