Chemogenetic Interrogation of a Brain-wide Fear Memory Network in Mice.
Identifieur interne : 000015 ( PubMed/Curation ); précédent : 000014; suivant : 000016Chemogenetic Interrogation of a Brain-wide Fear Memory Network in Mice.
Auteurs : Gisella Vetere [Canada] ; Justin W. Kenney [Canada] ; Lina M. Tran [Canada] ; Frances Xia [Canada] ; Patrick E. Steadman [Canada] ; John Parkinson [Canada] ; Sheena A. Josselyn [Canada] ; Paul W. Frankland [Canada]Source :
- Neuron [ 1097-4199 ] ; 2017.
Abstract
Behavior depends on coordinated activity across multiple brain regions. Within such networks, highly connected hub regions are assumed to disproportionately influence behavioral output, although this hypothesis has not been systematically evaluated. Previously, by mapping brain-wide expression of the activity-regulated gene c-fos, we identified a network of brain regions co-activated by fear memory. To test the hypothesis that hub regions are more important for network function, here, we simulated node deletion in silico in this behaviorally defined functional network. Removal of high degree nodes produced the greatest network disruption (e.g., reduction in global efficiency). To test these predictions in vivo, we examined the impact of post-training chemogenetic silencing of different network nodes on fear memory consolidation. In a series of independent experiments encompassing 25% of network nodes (i.e., 21/84 brain regions), we found that node degree accurately predicted observed deficits in memory consolidation, with silencing of highly connected hubs producing the largest impairments.
DOI: 10.1016/j.neuron.2017.03.037
PubMed: 28426969
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Steadman</name><affiliation wicri:level="1"><nlm:affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8</wicri:regionArea></affiliation></author><author><name sortKey="Parkinson, John" sort="Parkinson, John" uniqKey="Parkinson J" first="John" last="Parkinson">John Parkinson</name><affiliation wicri:level="1"><nlm:affiliation>Program in Molecular Structure and Function, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Departments of Biochemistry, Computer Science, and Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Molecular Structure and Function, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Departments of Biochemistry, Computer Science, and Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8</wicri:regionArea></affiliation></author><author><name sortKey="Josselyn, Sheena A" sort="Josselyn, Sheena A" uniqKey="Josselyn S" first="Sheena A" last="Josselyn">Sheena A. Josselyn</name><affiliation wicri:level="1"><nlm:affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada; Department of Psychology, University of Toronto, Toronto, ON M5S 3GM, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada; Department of Psychology, University of Toronto, Toronto, ON M5S 3GM</wicri:regionArea></affiliation></author><author><name sortKey="Frankland, Paul W" sort="Frankland, Paul W" uniqKey="Frankland P" first="Paul W" last="Frankland">Paul W. Frankland</name><affiliation wicri:level="1"><nlm:affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada; Department of Psychology, University of Toronto, Toronto, ON M5S 3GM, Canada. Electronic address: paul.frankland@sickkids.ca.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada; Department of Psychology, University of Toronto, Toronto, ON M5S 3GM</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2017">2017</date><idno type="RBID">pubmed:28426969</idno><idno type="pmid">28426969</idno><idno type="doi">10.1016/j.neuron.2017.03.037</idno><idno type="wicri:Area/PubMed/Corpus">000015</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">000015</idno><idno type="wicri:Area/PubMed/Curation">000015</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Curation">000015</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Chemogenetic Interrogation of a Brain-wide Fear Memory Network in Mice.</title><author><name sortKey="Vetere, Gisella" sort="Vetere, Gisella" uniqKey="Vetere G" first="Gisella" last="Vetere">Gisella Vetere</name><affiliation wicri:level="1"><nlm:affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8</wicri:regionArea></affiliation></author><author><name sortKey="Kenney, Justin W" sort="Kenney, Justin W" uniqKey="Kenney J" first="Justin W" last="Kenney">Justin W. Kenney</name><affiliation wicri:level="1"><nlm:affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8</wicri:regionArea></affiliation></author><author><name sortKey="Tran, Lina M" sort="Tran, Lina M" uniqKey="Tran L" first="Lina M" last="Tran">Lina M. Tran</name><affiliation wicri:level="1"><nlm:affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8</wicri:regionArea></affiliation></author><author><name sortKey="Xia, Frances" sort="Xia, Frances" uniqKey="Xia F" first="Frances" last="Xia">Frances Xia</name><affiliation wicri:level="1"><nlm:affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8</wicri:regionArea></affiliation></author><author><name sortKey="Steadman, Patrick E" sort="Steadman, Patrick E" uniqKey="Steadman P" first="Patrick E" last="Steadman">Patrick E. Steadman</name><affiliation wicri:level="1"><nlm:affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8</wicri:regionArea></affiliation></author><author><name sortKey="Parkinson, John" sort="Parkinson, John" uniqKey="Parkinson J" first="John" last="Parkinson">John Parkinson</name><affiliation wicri:level="1"><nlm:affiliation>Program in Molecular Structure and Function, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Departments of Biochemistry, Computer Science, and Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Molecular Structure and Function, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Departments of Biochemistry, Computer Science, and Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8</wicri:regionArea></affiliation></author><author><name sortKey="Josselyn, Sheena A" sort="Josselyn, Sheena A" uniqKey="Josselyn S" first="Sheena A" last="Josselyn">Sheena A. Josselyn</name><affiliation wicri:level="1"><nlm:affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada; Department of Psychology, University of Toronto, Toronto, ON M5S 3GM, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada; Department of Psychology, University of Toronto, Toronto, ON M5S 3GM</wicri:regionArea></affiliation></author><author><name sortKey="Frankland, Paul W" sort="Frankland, Paul W" uniqKey="Frankland P" first="Paul W" last="Frankland">Paul W. Frankland</name><affiliation wicri:level="1"><nlm:affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada; Department of Psychology, University of Toronto, Toronto, ON M5S 3GM, Canada. Electronic address: paul.frankland@sickkids.ca.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada; Department of Psychology, University of Toronto, Toronto, ON M5S 3GM</wicri:regionArea></affiliation></author></analytic><series><title level="j">Neuron</title><idno type="eISSN">1097-4199</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Behavior depends on coordinated activity across multiple brain regions. Within such networks, highly connected hub regions are assumed to disproportionately influence behavioral output, although this hypothesis has not been systematically evaluated. Previously, by mapping brain-wide expression of the activity-regulated gene c-fos, we identified a network of brain regions co-activated by fear memory. To test the hypothesis that hub regions are more important for network function, here, we simulated node deletion in silico in this behaviorally defined functional network. Removal of high degree nodes produced the greatest network disruption (e.g., reduction in global efficiency). To test these predictions in vivo, we examined the impact of post-training chemogenetic silencing of different network nodes on fear memory consolidation. In a series of independent experiments encompassing 25% of network nodes (i.e., 21/84 brain regions), we found that node degree accurately predicted observed deficits in memory consolidation, with silencing of highly connected hubs producing the largest impairments.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">28426969</PMID><DateCreated><Year>2017</Year><Month>04</Month><Day>20</Day></DateCreated><DateRevised><Year>2017</Year><Month>04</Month><Day>20</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">1097-4199</ISSN><JournalIssue CitedMedium="Internet"><Volume>94</Volume><Issue>2</Issue><PubDate><Year>2017</Year><Month>Apr</Month><Day>19</Day></PubDate></JournalIssue><Title>Neuron</Title><ISOAbbreviation>Neuron</ISOAbbreviation></Journal><ArticleTitle>Chemogenetic Interrogation of a Brain-wide Fear Memory Network in Mice.</ArticleTitle><Pagination><MedlinePgn>363-374.e4</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S0896-6273(17)30259-3</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.neuron.2017.03.037</ELocationID><Abstract><AbstractText>Behavior depends on coordinated activity across multiple brain regions. Within such networks, highly connected hub regions are assumed to disproportionately influence behavioral output, although this hypothesis has not been systematically evaluated. Previously, by mapping brain-wide expression of the activity-regulated gene c-fos, we identified a network of brain regions co-activated by fear memory. To test the hypothesis that hub regions are more important for network function, here, we simulated node deletion in silico in this behaviorally defined functional network. Removal of high degree nodes produced the greatest network disruption (e.g., reduction in global efficiency). To test these predictions in vivo, we examined the impact of post-training chemogenetic silencing of different network nodes on fear memory consolidation. In a series of independent experiments encompassing 25% of network nodes (i.e., 21/84 brain regions), we found that node degree accurately predicted observed deficits in memory consolidation, with silencing of highly connected hubs producing the largest impairments.</AbstractText><CopyrightInformation>Copyright © 2017 Elsevier Inc. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Vetere</LastName><ForeName>Gisella</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kenney</LastName><ForeName>Justin W</ForeName><Initials>JW</Initials><AffiliationInfo><Affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tran</LastName><ForeName>Lina M</ForeName><Initials>LM</Initials><AffiliationInfo><Affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xia</LastName><ForeName>Frances</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Steadman</LastName><ForeName>Patrick E</ForeName><Initials>PE</Initials><AffiliationInfo><Affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Parkinson</LastName><ForeName>John</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Program in Molecular Structure and Function, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Departments of Biochemistry, Computer Science, and Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Josselyn</LastName><ForeName>Sheena A</ForeName><Initials>SA</Initials><AffiliationInfo><Affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada; Department of Psychology, University of Toronto, Toronto, ON M5S 3GM, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Frankland</LastName><ForeName>Paul W</ForeName><Initials>PW</Initials><AffiliationInfo><Affiliation>Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Physiology, University of Toronto, Toronto, ON M5S 1A8, Canada; Institute of Medical Science, University of Toronto, Toronto, ON M5S 1A8, Canada; Department of Psychology, University of Toronto, Toronto, ON M5S 3GM, Canada. Electronic address: paul.frankland@sickkids.ca.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Neuron</MedlineTA><NlmUniqueID>8809320</NlmUniqueID><ISSNLinking>0896-6273</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">CA1</Keyword><Keyword MajorTopicYN="N">DREADDS</Keyword><Keyword MajorTopicYN="N">contextual fear conditioning</Keyword><Keyword MajorTopicYN="N">functional connectivity</Keyword><Keyword MajorTopicYN="N">graph theory</Keyword><Keyword MajorTopicYN="N">hippocampus</Keyword><Keyword MajorTopicYN="N">lateral septal nucleus</Keyword><Keyword MajorTopicYN="N">laterodorsal thalamic nucleus</Keyword><Keyword MajorTopicYN="N">neocortex</Keyword><Keyword MajorTopicYN="N">reuniens thalamic nucleus</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2016</Year><Month>09</Month><Day>06</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2017</Year><Month>01</Month><Day>26</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2017</Year><Month>03</Month><Day>27</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2017</Year><Month>4</Month><Day>21</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2017</Year><Month>4</Month><Day>21</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2017</Year><Month>4</Month><Day>21</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">28426969</ArticleId><ArticleId IdType="pii">S0896-6273(17)30259-3</ArticleId><ArticleId IdType="doi">10.1016/j.neuron.2017.03.037</ArticleId></ArticleIdList></PubmedData></pubmed></record>Pour manipuler ce document sous Unix (Dilib)
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