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Postsynaptic burst reactivation of hippocampal neurons enables associative plasticity of temporally discontiguous inputs
A fundamental unresolved problem in neuroscience is how the brain associates in memory events that are separated in time. Here, we propose that reactivation-induced synaptic plasticity can solve this problem. Previously, we reported that the reinforcement signal dopamine converts hippocampal spike t...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9612916/ https://www.ncbi.nlm.nih.gov/pubmed/36226826 http://dx.doi.org/10.7554/eLife.81071 |
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author | Fuchsberger, Tanja Clopath, Claudia Jarzebowski, Przemyslaw Brzosko, Zuzanna Wang, Hongbing Paulsen, Ole |
author_facet | Fuchsberger, Tanja Clopath, Claudia Jarzebowski, Przemyslaw Brzosko, Zuzanna Wang, Hongbing Paulsen, Ole |
author_sort | Fuchsberger, Tanja |
collection | PubMed |
description | A fundamental unresolved problem in neuroscience is how the brain associates in memory events that are separated in time. Here, we propose that reactivation-induced synaptic plasticity can solve this problem. Previously, we reported that the reinforcement signal dopamine converts hippocampal spike timing-dependent depression into potentiation during continued synaptic activity (Brzosko et al., 2015). Here, we report that postsynaptic bursts in the presence of dopamine produce input-specific LTP in mouse hippocampal synapses 10 min after they were primed with coincident pre- and post-synaptic activity (post-before-pre pairing; Δt = –20 ms). This priming activity induces synaptic depression and sets an NMDA receptor-dependent silent eligibility trace which, through the cAMP-PKA cascade, is rapidly converted into protein synthesis-dependent synaptic potentiation, mediated by a signaling pathway distinct from that of conventional LTP. This synaptic learning rule was incorporated into a computational model, and we found that it adds specificity to reinforcement learning by controlling memory allocation and enabling both ‘instructive’ and ‘supervised’ reinforcement learning. We predicted that this mechanism would make reactivated neurons activate more strongly and carry more spatial information than non-reactivated cells, which was confirmed in freely moving mice performing a reward-based navigation task. |
format | Online Article Text |
id | pubmed-9612916 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-96129162022-10-28 Postsynaptic burst reactivation of hippocampal neurons enables associative plasticity of temporally discontiguous inputs Fuchsberger, Tanja Clopath, Claudia Jarzebowski, Przemyslaw Brzosko, Zuzanna Wang, Hongbing Paulsen, Ole eLife Neuroscience A fundamental unresolved problem in neuroscience is how the brain associates in memory events that are separated in time. Here, we propose that reactivation-induced synaptic plasticity can solve this problem. Previously, we reported that the reinforcement signal dopamine converts hippocampal spike timing-dependent depression into potentiation during continued synaptic activity (Brzosko et al., 2015). Here, we report that postsynaptic bursts in the presence of dopamine produce input-specific LTP in mouse hippocampal synapses 10 min after they were primed with coincident pre- and post-synaptic activity (post-before-pre pairing; Δt = –20 ms). This priming activity induces synaptic depression and sets an NMDA receptor-dependent silent eligibility trace which, through the cAMP-PKA cascade, is rapidly converted into protein synthesis-dependent synaptic potentiation, mediated by a signaling pathway distinct from that of conventional LTP. This synaptic learning rule was incorporated into a computational model, and we found that it adds specificity to reinforcement learning by controlling memory allocation and enabling both ‘instructive’ and ‘supervised’ reinforcement learning. We predicted that this mechanism would make reactivated neurons activate more strongly and carry more spatial information than non-reactivated cells, which was confirmed in freely moving mice performing a reward-based navigation task. eLife Sciences Publications, Ltd 2022-10-13 /pmc/articles/PMC9612916/ /pubmed/36226826 http://dx.doi.org/10.7554/eLife.81071 Text en © 2022, Fuchsberger et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited. |
spellingShingle | Neuroscience Fuchsberger, Tanja Clopath, Claudia Jarzebowski, Przemyslaw Brzosko, Zuzanna Wang, Hongbing Paulsen, Ole Postsynaptic burst reactivation of hippocampal neurons enables associative plasticity of temporally discontiguous inputs |
title | Postsynaptic burst reactivation of hippocampal neurons enables associative plasticity of temporally discontiguous inputs |
title_full | Postsynaptic burst reactivation of hippocampal neurons enables associative plasticity of temporally discontiguous inputs |
title_fullStr | Postsynaptic burst reactivation of hippocampal neurons enables associative plasticity of temporally discontiguous inputs |
title_full_unstemmed | Postsynaptic burst reactivation of hippocampal neurons enables associative plasticity of temporally discontiguous inputs |
title_short | Postsynaptic burst reactivation of hippocampal neurons enables associative plasticity of temporally discontiguous inputs |
title_sort | postsynaptic burst reactivation of hippocampal neurons enables associative plasticity of temporally discontiguous inputs |
topic | Neuroscience |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9612916/ https://www.ncbi.nlm.nih.gov/pubmed/36226826 http://dx.doi.org/10.7554/eLife.81071 |
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