Role of prediction error and the cholinergic system on memory reconsolidation processes in mice
•Prediction Error (PE) is a boundary condition for memory to reconsolidate.•ACh receptors are involved in post-retrieval processes only when a PE is detected.•When evaluating positive and negative PE outcomes behavior response is sex-dependent. The ability to make predictions based on stored informa...
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Veröffentlicht in: | Neurobiology of learning and memory 2021-11, Vol.185, p.107534-107534, Article 107534 |
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creator | Krawczyk, M.C. Millan, J. Blake, M.G. Boccia, M.M. |
description | •Prediction Error (PE) is a boundary condition for memory to reconsolidate.•ACh receptors are involved in post-retrieval processes only when a PE is detected.•When evaluating positive and negative PE outcomes behavior response is sex-dependent.
The ability to make predictions based on stored information is a general coding strategy. A prediction error (PE) is a mismatch between expected and current events. Our memories, like ourselves, are subject to change. Thus, an acquired memory can become active and update its content or strength by a labilization-reconsolidation process. Within the reconsolidation framework, PE drives the updating of consolidated memories. In the past our lab has made key progresses showing that a blockade in the central cholinergic system during reconsolidation can cause memory impairment, while reinforcement of cholinergic activity enhances it. In the present work we determined that PE is a necessary condition for memory to reconsolidate in an inhibitory avoidance task using both male and female mice. Depending on the intensity of the unconditioned stimulus (US) used during training, a negative (higher US intensity) or positive (lower US intensity/no US) PE on a retrieval session modified the behavioral response on a subsequent testing session. Furthermore, we demonstrated that the cholinergic system modulates memory reconsolidation only when PE is detected. In this scenario administration of oxotremorine, scopolamine or nicotine after memory reactivation either enhanced or impaired memory reconsolidation in a sex-specific manner. |
doi_str_mv | 10.1016/j.nlm.2021.107534 |
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The ability to make predictions based on stored information is a general coding strategy. A prediction error (PE) is a mismatch between expected and current events. Our memories, like ourselves, are subject to change. Thus, an acquired memory can become active and update its content or strength by a labilization-reconsolidation process. Within the reconsolidation framework, PE drives the updating of consolidated memories. In the past our lab has made key progresses showing that a blockade in the central cholinergic system during reconsolidation can cause memory impairment, while reinforcement of cholinergic activity enhances it. In the present work we determined that PE is a necessary condition for memory to reconsolidate in an inhibitory avoidance task using both male and female mice. Depending on the intensity of the unconditioned stimulus (US) used during training, a negative (higher US intensity) or positive (lower US intensity/no US) PE on a retrieval session modified the behavioral response on a subsequent testing session. Furthermore, we demonstrated that the cholinergic system modulates memory reconsolidation only when PE is detected. In this scenario administration of oxotremorine, scopolamine or nicotine after memory reactivation either enhanced or impaired memory reconsolidation in a sex-specific manner.</description><identifier>ISSN: 1074-7427</identifier><identifier>EISSN: 1095-9564</identifier><identifier>DOI: 10.1016/j.nlm.2021.107534</identifier><identifier>PMID: 34619364</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Acetylcholine ; Animals ; Avoidance Learning - physiology ; Cholinergic Neurons - drug effects ; Cholinergic Neurons - physiology ; Conditioning, Classical - physiology ; Female ; Inhibitory avoidance ; Male ; Memory Consolidation - drug effects ; Memory Consolidation - physiology ; Mice ; Muscarinic receptor ; Negative outcome ; Nicotine - pharmacology ; Nicotinic receptor ; Oxotremorine - analogs & derivatives ; Oxotremorine - pharmacology ; Positive outcome ; Receptors, Cholinergic - drug effects ; Receptors, Cholinergic - physiology ; Scopolamine - pharmacology</subject><ispartof>Neurobiology of learning and memory, 2021-11, Vol.185, p.107534-107534, Article 107534</ispartof><rights>2021 Elsevier Inc.</rights><rights>Copyright © 2021 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c353t-f9bd4c371fb0790d2f4be5b12e422b0c2419f7f77754e1e1e92ee780f6e3ad463</citedby><cites>FETCH-LOGICAL-c353t-f9bd4c371fb0790d2f4be5b12e422b0c2419f7f77754e1e1e92ee780f6e3ad463</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.nlm.2021.107534$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34619364$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Krawczyk, M.C.</creatorcontrib><creatorcontrib>Millan, J.</creatorcontrib><creatorcontrib>Blake, M.G.</creatorcontrib><creatorcontrib>Boccia, M.M.</creatorcontrib><title>Role of prediction error and the cholinergic system on memory reconsolidation processes in mice</title><title>Neurobiology of learning and memory</title><addtitle>Neurobiol Learn Mem</addtitle><description>•Prediction Error (PE) is a boundary condition for memory to reconsolidate.•ACh receptors are involved in post-retrieval processes only when a PE is detected.•When evaluating positive and negative PE outcomes behavior response is sex-dependent.
The ability to make predictions based on stored information is a general coding strategy. A prediction error (PE) is a mismatch between expected and current events. Our memories, like ourselves, are subject to change. Thus, an acquired memory can become active and update its content or strength by a labilization-reconsolidation process. Within the reconsolidation framework, PE drives the updating of consolidated memories. In the past our lab has made key progresses showing that a blockade in the central cholinergic system during reconsolidation can cause memory impairment, while reinforcement of cholinergic activity enhances it. In the present work we determined that PE is a necessary condition for memory to reconsolidate in an inhibitory avoidance task using both male and female mice. Depending on the intensity of the unconditioned stimulus (US) used during training, a negative (higher US intensity) or positive (lower US intensity/no US) PE on a retrieval session modified the behavioral response on a subsequent testing session. Furthermore, we demonstrated that the cholinergic system modulates memory reconsolidation only when PE is detected. In this scenario administration of oxotremorine, scopolamine or nicotine after memory reactivation either enhanced or impaired memory reconsolidation in a sex-specific manner.</description><subject>Acetylcholine</subject><subject>Animals</subject><subject>Avoidance Learning - physiology</subject><subject>Cholinergic Neurons - drug effects</subject><subject>Cholinergic Neurons - physiology</subject><subject>Conditioning, Classical - physiology</subject><subject>Female</subject><subject>Inhibitory avoidance</subject><subject>Male</subject><subject>Memory Consolidation - drug effects</subject><subject>Memory Consolidation - physiology</subject><subject>Mice</subject><subject>Muscarinic receptor</subject><subject>Negative outcome</subject><subject>Nicotine - pharmacology</subject><subject>Nicotinic receptor</subject><subject>Oxotremorine - analogs & derivatives</subject><subject>Oxotremorine - pharmacology</subject><subject>Positive outcome</subject><subject>Receptors, Cholinergic - drug effects</subject><subject>Receptors, Cholinergic - physiology</subject><subject>Scopolamine - pharmacology</subject><issn>1074-7427</issn><issn>1095-9564</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE1LAzEURYMotlZ_gBvJ0s3UfM2kwZUUv6AgiK7DTPJiU2YmNZkK_femtrqULF4enHtJDkKXlEwpodXNatq33ZQRRvMuSy6O0JgSVRaqrMTx7i5FIQWTI3SW0ooQSks1O0UjLiqqeCXGSL-GFnBweB3BejP40GOIMURc9xYPS8BmGVrfQ_zwBqdtGqDDmemgC3GLI5jQpwzY-ie6jsFASpCwz4w3cI5OXN0muDjMCXp_uH-bPxWLl8fn-d2iMLzkQ-FUY4XhkrqGSEUsc6KBsqEMBGMNMUxQ5aSTUpYCaD6KAcgZcRXw2oqKT9D1vje_4HMDadCdTwbatu4hbJJm5YxUquKEZ5TuURNDShGcXkff1XGrKdE7r3qls1e986r3XnPm6lC_aTqwf4lfkRm43QOQP_nlIepkPPQmS82OBm2D_6f-G-1viaI</recordid><startdate>202111</startdate><enddate>202111</enddate><creator>Krawczyk, M.C.</creator><creator>Millan, J.</creator><creator>Blake, M.G.</creator><creator>Boccia, M.M.</creator><general>Elsevier Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>202111</creationdate><title>Role of prediction error and the cholinergic system on memory reconsolidation processes in mice</title><author>Krawczyk, M.C. ; Millan, J. ; Blake, M.G. ; Boccia, M.M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c353t-f9bd4c371fb0790d2f4be5b12e422b0c2419f7f77754e1e1e92ee780f6e3ad463</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Acetylcholine</topic><topic>Animals</topic><topic>Avoidance Learning - physiology</topic><topic>Cholinergic Neurons - drug effects</topic><topic>Cholinergic Neurons - physiology</topic><topic>Conditioning, Classical - physiology</topic><topic>Female</topic><topic>Inhibitory avoidance</topic><topic>Male</topic><topic>Memory Consolidation - drug effects</topic><topic>Memory Consolidation - physiology</topic><topic>Mice</topic><topic>Muscarinic receptor</topic><topic>Negative outcome</topic><topic>Nicotine - pharmacology</topic><topic>Nicotinic receptor</topic><topic>Oxotremorine - analogs & derivatives</topic><topic>Oxotremorine - pharmacology</topic><topic>Positive outcome</topic><topic>Receptors, Cholinergic - drug effects</topic><topic>Receptors, Cholinergic - physiology</topic><topic>Scopolamine - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Krawczyk, M.C.</creatorcontrib><creatorcontrib>Millan, J.</creatorcontrib><creatorcontrib>Blake, M.G.</creatorcontrib><creatorcontrib>Boccia, M.M.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Neurobiology of learning and memory</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Krawczyk, M.C.</au><au>Millan, J.</au><au>Blake, M.G.</au><au>Boccia, M.M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Role of prediction error and the cholinergic system on memory reconsolidation processes in mice</atitle><jtitle>Neurobiology of learning and memory</jtitle><addtitle>Neurobiol Learn Mem</addtitle><date>2021-11</date><risdate>2021</risdate><volume>185</volume><spage>107534</spage><epage>107534</epage><pages>107534-107534</pages><artnum>107534</artnum><issn>1074-7427</issn><eissn>1095-9564</eissn><abstract>•Prediction Error (PE) is a boundary condition for memory to reconsolidate.•ACh receptors are involved in post-retrieval processes only when a PE is detected.•When evaluating positive and negative PE outcomes behavior response is sex-dependent.
The ability to make predictions based on stored information is a general coding strategy. A prediction error (PE) is a mismatch between expected and current events. Our memories, like ourselves, are subject to change. Thus, an acquired memory can become active and update its content or strength by a labilization-reconsolidation process. Within the reconsolidation framework, PE drives the updating of consolidated memories. In the past our lab has made key progresses showing that a blockade in the central cholinergic system during reconsolidation can cause memory impairment, while reinforcement of cholinergic activity enhances it. In the present work we determined that PE is a necessary condition for memory to reconsolidate in an inhibitory avoidance task using both male and female mice. Depending on the intensity of the unconditioned stimulus (US) used during training, a negative (higher US intensity) or positive (lower US intensity/no US) PE on a retrieval session modified the behavioral response on a subsequent testing session. Furthermore, we demonstrated that the cholinergic system modulates memory reconsolidation only when PE is detected. In this scenario administration of oxotremorine, scopolamine or nicotine after memory reactivation either enhanced or impaired memory reconsolidation in a sex-specific manner.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>34619364</pmid><doi>10.1016/j.nlm.2021.107534</doi><tpages>1</tpages></addata></record> |
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subjects | Acetylcholine Animals Avoidance Learning - physiology Cholinergic Neurons - drug effects Cholinergic Neurons - physiology Conditioning, Classical - physiology Female Inhibitory avoidance Male Memory Consolidation - drug effects Memory Consolidation - physiology Mice Muscarinic receptor Negative outcome Nicotine - pharmacology Nicotinic receptor Oxotremorine - analogs & derivatives Oxotremorine - pharmacology Positive outcome Receptors, Cholinergic - drug effects Receptors, Cholinergic - physiology Scopolamine - pharmacology |
title | Role of prediction error and the cholinergic system on memory reconsolidation processes in mice |
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