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Control of aversion by glycine-gated GluN1/GluN3A NMDA receptors in the adult medial habenula

Otsu, Y. and Darcq, E. and Pietrajtis, K. and Mátyás, Ferenc and Schwartz, E. and Acsády, László (2019) Control of aversion by glycine-gated GluN1/GluN3A NMDA receptors in the adult medial habenula. SCIENCE, 366 (6462). pp. 250-254. ISSN 0036-8075

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Abstract

The unconventional N-methyl-d-aspartate (NMDA) receptor subunits GluN3A and GluN3B can, when associated with the other glycine-binding subunit GluN1, generate excitatory conductances purely activated by glycine. However, functional GluN1/GluN3 receptors have not been identified in native adult tissues. We discovered that GluN1/GluN3A receptors are operational in neurons of the mouse adult medial habenula (MHb), an epithalamic area controlling aversive physiological states. In the absence of glycinergic neuronal specializations in the MHb, glial cells tuned neuronal activity via GluN1/GluN3A receptors. Reducing GluN1/GluN3A receptor levels in the MHb prevented place-aversion conditioning. Our study extends the physiological and behavioral implications of glycine by demonstrating its control of negatively valued emotional associations via excitatory glycinergic NMDA receptors.

Item Type: Article
Additional Information: Institut de Biologie de l’École Normale Supérieure (IBENS), INSERM U1024, CNRS UMR8197, École Normale Supérieure, Université PSL, Paris, 75005, France Department of Psychiatry, School of Medicine, Douglas Hospital Research Center, McGill University, Montreal, QC H4H 1R3, Canada Sorbonne Université, CNRS, INSERM, Neurosciences Paris Seine – Institut de Biologie Paris Seine (NPS-IBPS), Paris, 75005, France Laboratory of Thalamus Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, 1083, Hungary Research Centre for Natural Sciences Institute of Cognitive Neuroscience and Psychology, Budapest, 1117, Hungary Department of Anatomy and Histology, University of Veterinary Medicine, Budapest, 1078, Hungary Integrative Neuroscience and Cognition Center, CNRS UMR8002, Glia-Glia and Glia-Neuron Interactions Group, Paris Descartes University, Paris, 75006, France Pain Management Research Institute, Kolling Institute of Medical Research, Northern Clinical School, University of Sydney, Royal North Shore Hospital, St. Leonards, NSW 2065, Australia Neural Circuit Dynamics and Decision Making, Pasteur Institute, Paris, 75015, France Cited By :1 Export Date: 6 March 2020 CODEN: SCIEA Correspondence Address: Diana, M.A.; Sorbonne Université, CNRS, INSERM, Neurosciences Paris Seine – Institut de Biologie Paris Seine (NPS-IBPS)France; email: marco.diana@upmc.fr Chemicals/CAS: glycine, 56-40-6, 6000-43-7, 6000-44-8 Institut de Biologie de l’École Normale Supérieure (IBENS), INSERM U1024, CNRS UMR8197, École Normale Supérieure, Université PSL, Paris, 75005, France Department of Psychiatry, School of Medicine, Douglas Hospital Research Center, McGill University, Montreal, QC H4H 1R3, Canada Sorbonne Université, CNRS, INSERM, Neurosciences Paris Seine – Institut de Biologie Paris Seine (NPS-IBPS), Paris, 75005, France Laboratory of Thalamus Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, 1083, Hungary Research Centre for Natural Sciences Institute of Cognitive Neuroscience and Psychology, Budapest, 1117, Hungary Department of Anatomy and Histology, University of Veterinary Medicine, Budapest, 1078, Hungary Integrative Neuroscience and Cognition Center, CNRS UMR8002, Glia-Glia and Glia-Neuron Interactions Group, Paris Descartes University, Paris, 75006, France Pain Management Research Institute, Kolling Institute of Medical Research, Northern Clinical School, University of Sydney, Royal North Shore Hospital, St. Leonards, NSW 2065, Australia Neural Circuit Dynamics and Decision Making, Pasteur Institute, Paris, 75015, France Cited By :1 Export Date: 13 May 2020 CODEN: SCIEA Correspondence Address: Diana, M.A.; Sorbonne Université, CNRS, INSERM, Neurosciences Paris Seine – Institut de Biologie Paris Seine (NPS-IBPS)France; email: marco.diana@upmc.fr Chemicals/CAS: glycine, 56-40-6, 6000-43-7, 6000-44-8 Funding details: University of Tokyo Funding details: Hokkaido University, HU Funding details: Nemzeti Kutatási és Technológiai Hivatal, NKTH, ANR-09-BLAN-0401, S17JRSU003, ANR-17-CE16-0014 Funding details: European Research Council, ERC, 693021 Funding details: National Institute on Drug Abuse, NIDA, 05010 Funding details: 2017-1.2.1-NKP-2017-00002, 742595, FK124434 Funding details: National Institute on Alcohol Abuse and Alcoholism, NIAAA, 16658 Funding details: Fondation pour la Recherche Médicale, FRM, FDT20100919977 Funding details: Centre National de la Recherche Scientifique, CNRS, PICS 7415 Funding text 1: We thank M. Galante, R. Lambert, and N. Leresche for criticall reading the manuscript; M. McNicholas and S. Kirchherr for assistance during behavioral experiments; and B. Mathieu at the IBENS Imaging Facility. N. Nakanishi and S. Lipton (Scintillon Institute) provided the GluN3AKO mice and M. Mishina (Tokyo University) provided the GluN2AKO line. The anti-GluN3A antibody was a gift from M. Watanabe (Hokkaido University). We thank C. Bellone (Geneva University) for the scr/shRNA-expressing viruses. Funding: This study was supported by fellowships (NKTH-)ANR-09-BLAN-0401 to S.D., M.A.D., and L.A., and ANR-17-CE16-0014 to P.P., S.D., B.L.K., and M.A.D.; by Emergence Sorbonne (S17JRSU003) and CNRS (PICS 7415) to M.A.D.; by the European Research Council (693021) to P.P.; by ERC-FRONTHAL (742595) to L.A.; by grants FK124434 and 2017-1.2.1-NKP-2017-00002 to F.M.; and by the National Institute of Drug Abuse (05010) and the National Institute on Alcohol Abuse and Alcoholism (16658) to B.L.K. C.V.R. was supported by FRM grant FDT20100919977. C.A. Institut de Biologie de l’École Normale Supérieure (IBENS), INSERM U1024, CNRS UMR8197, École Normale Supérieure, Université PSL, Paris, 75005, France Department of Psychiatry, School of Medicine, Douglas Hospital Research Center, McGill University, Montreal, QC H4H 1R3, Canada Sorbonne Université, CNRS, INSERM, Neurosciences Paris Seine – Institut de Biologie Paris Seine (NPS-IBPS), Paris, 75005, France Laboratory of Thalamus Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, 1083, Hungary Research Centre for Natural Sciences Institute of Cognitive Neuroscience and Psychology, Budapest, 1117, Hungary Department of Anatomy and Histology, University of Veterinary Medicine, Budapest, 1078, Hungary Integrative Neuroscience and Cognition Center, CNRS UMR8002, Glia-Glia and Glia-Neuron Interactions Group, Paris Descartes University, Paris, 75006, France Pain Management Research Institute, Kolling Institute of Medical Research, Northern Clinical School, University of Sydney, Royal North Shore Hospital, St. Leonards, NSW 2065, Australia Neural Circuit Dynamics and Decision Making, Pasteur Institute, Paris, 75015, France Cited By :1 Export Date: 23 May 2020 CODEN: SCIEA Correspondence Address: Diana, M.A.; Sorbonne Université, CNRS, INSERM, Neurosciences Paris Seine – Institut de Biologie Paris Seine (NPS-IBPS)France; email: marco.diana@upmc.fr Chemicals/CAS: glycine, 56-40-6, 6000-43-7, 6000-44-8 Funding details: University of Tokyo Funding details: Hokkaido University, HU Funding details: Nemzeti Kutatási és Technológiai Hivatal, NKTH, ANR-09-BLAN-0401, S17JRSU003, ANR-17-CE16-0014 Funding details: European Research Council, ERC, 693021 Funding details: National Institute on Drug Abuse, NIDA, 05010 Funding details: 2017-1.2.1-NKP-2017-00002, 742595, FK124434 Funding details: National Institute on Alcohol Abuse and Alcoholism, NIAAA, 16658 Funding details: Fondation pour la Recherche Médicale, FRM, FDT20100919977 Funding details: Centre National de la Recherche Scientifique, CNRS, PICS 7415 Funding text 1: We thank M. Galante, R. Lambert, and N. Leresche for criticall reading the manuscript; M. McNicholas and S. Kirchherr for assistance during behavioral experiments; and B. Mathieu at the IBENS Imaging Facility. N. Nakanishi and S. Lipton (Scintillon Institute) provided the GluN3AKO mice and M. Mishina (Tokyo University) provided the GluN2AKO line. The anti-GluN3A antibody was a gift from M. Watanabe (Hokkaido University). We thank C. Bellone (Geneva University) for the scr/shRNA-expressing viruses. Funding: This study was supported by fellowships (NKTH-)ANR-09-BLAN-0401 to S.D., M.A.D., and L.A., and ANR-17-CE16-0014 to P.P., S.D., B.L.K., and M.A.D.; by Emergence Sorbonne (S17JRSU003) and CNRS (PICS 7415) to M.A.D.; by the European Research Council (693021) to P.P.; by ERC-FRONTHAL (742595) to L.A.; by grants FK124434 and 2017-1.2.1-NKP-2017-00002 to F.M.; and by the National Institute of Drug Abuse (05010) and the National Institute on Alcohol Abuse and Alcoholism (16658) to B.L.K. C.V.R. was supported by FRM grant FDT20100919977. C.A. Institut de Biologie de l’École Normale Supérieure (IBENS), INSERM U1024, CNRS UMR8197, École Normale Supérieure, Université PSL, Paris, 75005, France Department of Psychiatry, School of Medicine, Douglas Hospital Research Center, McGill University, Montreal, QC H4H 1R3, Canada Sorbonne Université, CNRS, INSERM, Neurosciences Paris Seine – Institut de Biologie Paris Seine (NPS-IBPS), Paris, 75005, France Laboratory of Thalamus Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, 1083, Hungary Research Centre for Natural Sciences Institute of Cognitive Neuroscience and Psychology, Budapest, 1117, Hungary Department of Anatomy and Histology, University of Veterinary Medicine, Budapest, 1078, Hungary Integrative Neuroscience and Cognition Center, CNRS UMR8002, Glia-Glia and Glia-Neuron Interactions Group, Paris Descartes University, Paris, 75006, France Pain Management Research Institute, Kolling Institute of Medical Research, Northern Clinical School, University of Sydney, Royal North Shore Hospital, St. Leonards, NSW 2065, Australia Neural Circuit Dynamics and Decision Making, Pasteur Institute, Paris, 75015, France Cited By :1 Export Date: 28 May 2020 CODEN: SCIEA Correspondence Address: Diana, M.A.; Sorbonne Université, CNRS, INSERM, Neurosciences Paris Seine – Institut de Biologie Paris Seine (NPS-IBPS)France; email: marco.diana@upmc.fr Chemicals/CAS: glycine, 56-40-6, 6000-43-7, 6000-44-8 Funding details: University of Tokyo Funding details: Hokkaido University, HU Funding details: Nemzeti Kutatási és Technológiai Hivatal, NKTH, ANR-09-BLAN-0401, S17JRSU003, ANR-17-CE16-0014 Funding details: European Research Council, ERC, 693021 Funding details: National Institute on Drug Abuse, NIDA, 05010 Funding details: 2017-1.2.1-NKP-2017-00002, 742595, FK124434 Funding details: National Institute on Alcohol Abuse and Alcoholism, NIAAA, 16658 Funding details: Fondation pour la Recherche Médicale, FRM, FDT20100919977 Funding details: Centre National de la Recherche Scientifique, CNRS, PICS 7415 Funding text 1: We thank M. Galante, R. Lambert, and N. Leresche for criticall reading the manuscript; M. McNicholas and S. Kirchherr for assistance during behavioral experiments; and B. Mathieu at the IBENS Imaging Facility. N. Nakanishi and S. Lipton (Scintillon Institute) provided the GluN3AKO mice and M. Mishina (Tokyo University) provided the GluN2AKO line. The anti-GluN3A antibody was a gift from M. Watanabe (Hokkaido University). We thank C. Bellone (Geneva University) for the scr/shRNA-expressing viruses. Funding: This study was supported by fellowships (NKTH-)ANR-09-BLAN-0401 to S.D., M.A.D., and L.A., and ANR-17-CE16-0014 to P.P., S.D., B.L.K., and M.A.D.; by Emergence Sorbonne (S17JRSU003) and CNRS (PICS 7415) to M.A.D.; by the European Research Council (693021) to P.P.; by ERC-FRONTHAL (742595) to L.A.; by grants FK124434 and 2017-1.2.1-NKP-2017-00002 to F.M.; and by the National Institute of Drug Abuse (05010) and the National Institute on Alcohol Abuse and Alcoholism (16658) to B.L.K. C.V.R. was supported by FRM grant FDT20100919977. C.A.
Subjects: R Medicine / orvostudomány > R1 Medicine (General) / orvostudomány általában > R850-854 Experimental medicine / kisérleti orvostudomány
SWORD Depositor: MTMT SWORD
Depositing User: MTMT SWORD
Date Deposited: 05 Oct 2020 14:15
Last Modified: 05 Oct 2020 14:15
URI: http://real.mtak.hu/id/eprint/115674

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