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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...

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Autores principales: Fuchsberger, Tanja, Clopath, Claudia, Jarzebowski, Przemyslaw, Brzosko, Zuzanna, Wang, Hongbing, Paulsen, Ole
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
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.
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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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