Pre- and postsynaptic N-methyl-D-aspartate receptors are required for sequential printing of fear memory engrams
Summary: The organization of fear memory involves the participation of multiple brain regions. However, it is largely unknown how fear memory is formed, which circuit pathways are used for “printing” memory engrams across brain regions, and the role of identified brain circuits in memory retrieval....
Main Authors: | , , , , , , , , , , , , , , |
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Format: | Article |
Language: | English |
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Elsevier
2023-11-01
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Series: | iScience |
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Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004223021272 |
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author | Ilaria Bertocchi Florbela Rocha-Almeida María Teresa Romero-Barragán Marco Cambiaghi Alejandro Carretero-Guillén Paolo Botta Godwin K. Dogbevia Mario Treviño Paolo Mele Alessandra Oberto Matthew E. Larkum Agnes Gruart Rolf Sprengel José Maria Delgado-García Mazahir T. Hasan |
author_facet | Ilaria Bertocchi Florbela Rocha-Almeida María Teresa Romero-Barragán Marco Cambiaghi Alejandro Carretero-Guillén Paolo Botta Godwin K. Dogbevia Mario Treviño Paolo Mele Alessandra Oberto Matthew E. Larkum Agnes Gruart Rolf Sprengel José Maria Delgado-García Mazahir T. Hasan |
author_sort | Ilaria Bertocchi |
collection | DOAJ |
description | Summary: The organization of fear memory involves the participation of multiple brain regions. However, it is largely unknown how fear memory is formed, which circuit pathways are used for “printing” memory engrams across brain regions, and the role of identified brain circuits in memory retrieval. With advanced genetic methods, we combinatorially blocked presynaptic output and manipulated N-methyl-D-aspartate receptor (NMDAR) in the basolateral amygdala (BLA) and medial prefrontal cortex (mPFC) before and after cued fear conditioning. Further, we tagged fear-activated neurons during associative learning for optogenetic memory recall. We found that presynaptic mPFC and postsynaptic BLA NMDARs are required for fear memory formation, but not expression. Our results provide strong evidence that NMDAR-dependent synaptic plasticity drives multi-trace systems consolidation for the sequential printing of fear memory engrams from BLA to mPFC and, subsequently, to the other regions, for flexible memory retrieval. |
first_indexed | 2024-03-11T18:22:40Z |
format | Article |
id | doaj.art-eef971ec2bee4393bdea89beefd17a00 |
institution | Directory Open Access Journal |
issn | 2589-0042 |
language | English |
last_indexed | 2024-03-11T18:22:40Z |
publishDate | 2023-11-01 |
publisher | Elsevier |
record_format | Article |
series | iScience |
spelling | doaj.art-eef971ec2bee4393bdea89beefd17a002023-10-15T04:38:04ZengElsevieriScience2589-00422023-11-012611108050Pre- and postsynaptic N-methyl-D-aspartate receptors are required for sequential printing of fear memory engramsIlaria Bertocchi0Florbela Rocha-Almeida1María Teresa Romero-Barragán2Marco Cambiaghi3Alejandro Carretero-Guillén4Paolo Botta5Godwin K. Dogbevia6Mario Treviño7Paolo Mele8Alessandra Oberto9Matthew E. Larkum10Agnes Gruart11Rolf Sprengel12José Maria Delgado-García13Mazahir T. Hasan14Department of Molecular Neurobiology, Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany; Department of Neuroscience ''Rita Levi Montalcini'', Neuroscience Institute Cavalieri Ottolenghi (NICO), University of Turin, 10043 Turin, Italy; Corresponding authorDivision of Neurosciences, University Pablo de Olavide, Ctra. de Utrera, km. 1 41013 Seville, SpainDivision of Neurosciences, University Pablo de Olavide, Ctra. de Utrera, km. 1 41013 Seville, SpainDepartment of Neurosciences, Biomedicine and Movement Sciences, University of Verona, Strada le Grazie 8, Verona, ItalyLaboratory of Brain Circuits Therapeutics, Achucarro Basque Center for Neuroscience, Science Park of the UPV/EHU, Sede Building, Barrio Sarriena, s/n, 48940 Leioa, SpainCNS drug development, Copenhagen, Capital Region, DenmarkDepartment of Molecular Neurobiology, Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany; Health Canada, 70 Colombine Driveway, Ottawa, ON K1A0K9, CanadaDepartment of Molecular Neurobiology, Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany; Laboratorio de Plasticidad Cortical y Aprendizaje Perceptual, Instituto de Neurociencias, Universidad de Guadalajara, Guadalajara, MexicoDepartment of Neuroscience ''Rita Levi Montalcini'', Neuroscience Institute Cavalieri Ottolenghi (NICO), University of Turin, 10043 Turin, ItalyDepartment of Neuroscience ''Rita Levi Montalcini'', Neuroscience Institute Cavalieri Ottolenghi (NICO), University of Turin, 10043 Turin, ItalyNeuroCure, Charité-Universitatsmedizin, Virchowweg 6, 10117 Berlin, GermanyDivision of Neurosciences, University Pablo de Olavide, Ctra. de Utrera, km. 1 41013 Seville, SpainDepartment of Molecular Neurobiology, Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, GermanyDivision of Neurosciences, University Pablo de Olavide, Ctra. de Utrera, km. 1 41013 Seville, Spain; Corresponding authorDepartment of Molecular Neurobiology, Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany; Laboratory of Brain Circuits Therapeutics, Achucarro Basque Center for Neuroscience, Science Park of the UPV/EHU, Sede Building, Barrio Sarriena, s/n, 48940 Leioa, Spain; Ikerbasque – Basque Foundation for Science, Bilbao, Spain; Corresponding authorSummary: The organization of fear memory involves the participation of multiple brain regions. However, it is largely unknown how fear memory is formed, which circuit pathways are used for “printing” memory engrams across brain regions, and the role of identified brain circuits in memory retrieval. With advanced genetic methods, we combinatorially blocked presynaptic output and manipulated N-methyl-D-aspartate receptor (NMDAR) in the basolateral amygdala (BLA) and medial prefrontal cortex (mPFC) before and after cued fear conditioning. Further, we tagged fear-activated neurons during associative learning for optogenetic memory recall. We found that presynaptic mPFC and postsynaptic BLA NMDARs are required for fear memory formation, but not expression. Our results provide strong evidence that NMDAR-dependent synaptic plasticity drives multi-trace systems consolidation for the sequential printing of fear memory engrams from BLA to mPFC and, subsequently, to the other regions, for flexible memory retrieval.http://www.sciencedirect.com/science/article/pii/S2589004223021272Behavioral neuroscienceCellular neuroscience |
spellingShingle | Ilaria Bertocchi Florbela Rocha-Almeida María Teresa Romero-Barragán Marco Cambiaghi Alejandro Carretero-Guillén Paolo Botta Godwin K. Dogbevia Mario Treviño Paolo Mele Alessandra Oberto Matthew E. Larkum Agnes Gruart Rolf Sprengel José Maria Delgado-García Mazahir T. Hasan Pre- and postsynaptic N-methyl-D-aspartate receptors are required for sequential printing of fear memory engrams iScience Behavioral neuroscience Cellular neuroscience |
title | Pre- and postsynaptic N-methyl-D-aspartate receptors are required for sequential printing of fear memory engrams |
title_full | Pre- and postsynaptic N-methyl-D-aspartate receptors are required for sequential printing of fear memory engrams |
title_fullStr | Pre- and postsynaptic N-methyl-D-aspartate receptors are required for sequential printing of fear memory engrams |
title_full_unstemmed | Pre- and postsynaptic N-methyl-D-aspartate receptors are required for sequential printing of fear memory engrams |
title_short | Pre- and postsynaptic N-methyl-D-aspartate receptors are required for sequential printing of fear memory engrams |
title_sort | pre and postsynaptic n methyl d aspartate receptors are required for sequential printing of fear memory engrams |
topic | Behavioral neuroscience Cellular neuroscience |
url | http://www.sciencedirect.com/science/article/pii/S2589004223021272 |
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