A Fear Memory Engram and Its Plasticity in the Hypothalamic Oxytocin System.


Journal

Neuron
ISSN: 1097-4199
Titre abrégé: Neuron
Pays: United States
ID NLM: 8809320

Informations de publication

Date de publication:
03 07 2019
Historique:
received: 18 05 2018
revised: 08 10 2018
accepted: 18 04 2019
pubmed: 21 5 2019
medline: 23 10 2019
entrez: 21 5 2019
Statut: ppublish

Résumé

Oxytocin (OT) release by axonal terminals onto the central nucleus of the amygdala exerts anxiolysis. To investigate which subpopulation of OT neurons contributes to this effect, we developed a novel method: virus-delivered genetic activity-induced tagging of cell ensembles (vGATE). With the vGATE method, we identified and permanently tagged a small subpopulation of OT cells, which, by optogenetic stimulation, strongly attenuated contextual fear-induced freezing, and pharmacogenetic silencing of tagged OT neurons impaired context-specific fear extinction, demonstrating that the tagged OT neurons are sufficient and necessary, respectively, to control contextual fear. Intriguingly, OT cell terminals of fear-experienced rats displayed enhanced glutamate release in the amygdala. Furthermore, rats exposed to another round of fear conditioning displayed 5-fold more activated magnocellular OT neurons in a novel environment than a familiar one, possibly for a generalized fear response. Thus, our results provide first evidence that hypothalamic OT neurons represent a fear memory engram.

Identifiants

pubmed: 31104950
pii: S0896-6273(19)30386-1
doi: 10.1016/j.neuron.2019.04.029
pii:
doi:

Substances chimiques

Glutamic Acid 3KX376GY7L
Oxytocin 50-56-6

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

133-146.e8

Informations de copyright

Copyright © 2019 Elsevier Inc. All rights reserved.

Auteurs

Mazahir T Hasan (MT)

Laboratory of Memory Circuits, Achucarro Basque Center for Neuroscience, Science Park of the UPV/EHU, Sede Building, Barrio Sarriena, 48940 Leioa, Spain; Ikerbasque-Basque Foundation for Science, 48013 Bilbao, Spain; Neurocure, Charité-Universitätsmedizin, Virchowweg 6, 10117 Berlin, Germany; Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany. Electronic address: mazahir.t.hasan@gmail.com.

Ferdinand Althammer (F)

Schaller Research Group on Neuropeptides, German Cancer Research Center, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Miriam Silva da Gouveia (M)

Schaller Research Group on Neuropeptides, German Cancer Research Center, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Stephanie Goyon (S)

Centre National de la Recherche Scientifique and University of Strasbourg, Institute of Cellular and Integrative Neurosciences, 8 Allée du Général Rouvillois, 67000 Strasbourg, France.

Marina Eliava (M)

Schaller Research Group on Neuropeptides, German Cancer Research Center, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Arthur Lefevre (A)

Schaller Research Group on Neuropeptides, German Cancer Research Center, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Damien Kerspern (D)

Centre National de la Recherche Scientifique and University of Strasbourg, Institute of Cellular and Integrative Neurosciences, 8 Allée du Général Rouvillois, 67000 Strasbourg, France.

Jonas Schimmer (J)

Schaller Research Group on Neuropeptides, German Cancer Research Center, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Androniki Raftogianni (A)

Schaller Research Group on Neuropeptides, German Cancer Research Center, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Jerome Wahis (J)

Centre National de la Recherche Scientifique and University of Strasbourg, Institute of Cellular and Integrative Neurosciences, 8 Allée du Général Rouvillois, 67000 Strasbourg, France.

H Sophie Knobloch-Bollmann (HS)

Schaller Research Group on Neuropeptides, German Cancer Research Center, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Yan Tang (Y)

Schaller Research Group on Neuropeptides, German Cancer Research Center, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Xinying Liu (X)

Schaller Research Group on Neuropeptides, German Cancer Research Center, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Apar Jain (A)

Schaller Research Group on Neuropeptides, German Cancer Research Center, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Virginie Chavant (V)

Centre National de la Recherche Scientifique and University of Strasbourg, Institute of Cellular and Integrative Neurosciences, 8 Allée du Général Rouvillois, 67000 Strasbourg, France.

Yannick Goumon (Y)

Centre National de la Recherche Scientifique and University of Strasbourg, Institute of Cellular and Integrative Neurosciences, 8 Allée du Général Rouvillois, 67000 Strasbourg, France.

Jan-Marek Weislogel (JM)

Department of Neurobiology, Heidelberg University, Im Neuenheimer Feld 364, 69120 Heidelberg, Germany.

René Hurlemann (R)

Department of Psychiatry and Division of Medical Psychology, University of Bonn Medical Center, Sigmund-Freud-Strasse 25, 53105 Bonn, Germany.

Sabine C Herpertz (SC)

Department of General Psychiatry, Center of Psychosocial Medicine, Heidelberg University, Voßstraße 4, 69115 Heidelberg, Germany.

Claudia Pitzer (C)

Interdisciplinary Neurobehavioral Core (INBC), Heidelberg University, Im Neuenheimer Feld 515, 69120 Heidelberg, Germany.

Pascal Darbon (P)

Centre National de la Recherche Scientifique and University of Strasbourg, Institute of Cellular and Integrative Neurosciences, 8 Allée du Général Rouvillois, 67000 Strasbourg, France.

Godwin K Dogbevia (GK)

Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany.

Ilaria Bertocchi (I)

Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany; Max Planck Research Group at the Institute for Anatomy and Cell Biology, Heidelberg University, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Matthew E Larkum (ME)

Neurocure, Charité-Universitätsmedizin, Virchowweg 6, 10117 Berlin, Germany.

Rolf Sprengel (R)

Max Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany; Max Planck Research Group at the Institute for Anatomy and Cell Biology, Heidelberg University, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany.

Hilmar Bading (H)

Department of Neurobiology, Heidelberg University, Im Neuenheimer Feld 364, 69120 Heidelberg, Germany.

Alexandre Charlet (A)

Centre National de la Recherche Scientifique and University of Strasbourg, Institute of Cellular and Integrative Neurosciences, 8 Allée du Général Rouvillois, 67000 Strasbourg, France; University of Strasbourg Institute for Advanced Study (USIAS), Strasbourg, France. Electronic address: acharlet@unistra.fr.

Valery Grinevich (V)

Schaller Research Group on Neuropeptides, German Cancer Research Center, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany; Department of Neuropeptide Research for Psychiatry, Central Institute of Mental Health, Heidelberg University, J5, 68159 Mannheim, Germany. Electronic address: v.grinevich@dkfz-heidelberg.de.

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