Peripheral and central CB1 cannabinoid receptors control stress-induced impairment of memory consolidation

Stressful events can generate emotional memories linked to the traumatic incident, but they also can impair the formation of nonemotional memories. Although the impact of stress on emotional memories is well studied, much less is known about the influence of the emotional state on the formation of n...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 113; no. 35; pp. 9904 - 9909
Main Authors Busquets-Garcia, Arnau, Gomis-González, Maria, Srivastava, Raj Kamal, Cutando, Laura, Ortega-Alvaro, Antonio, Ruehle, Sabine, Remmers, Floortje, Bindila, Laura, Bellocchio, Luigi, Marsicano, Giovanni, Lutz, Beat, Maldonado, Rafael, Ozaita, Andrés
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 30.08.2016
Subjects
Animals
Anisomycin - pharmacology
Biological Sciences
Cannabinoides
Cells
Dopamine beta-Hydroxylase - metabolism
Electroshock - adverse effects
Emotions
Estrès
Hindlimb Suspension - adverse effects
Indoles - pharmacology
Male
Memory
Memory Consolidation - drug effects
Memory Consolidation - physiology
Memory Disorders - etiology
Memory Disorders - physiopathology
Memòria
Mice, Knockout
Neurons - drug effects
Neurons - metabolism
Neurons - physiology
Piperidines - pharmacology
Proteins
Pyrazoles - pharmacology
Receptor, Cannabinoid, CB1 - genetics
Receptor, Cannabinoid, CB1 - metabolism
Receptor, Cannabinoid, CB1 - physiology
Receptors
Recognition
Rimonabant
Stress
Stress, Psychological - etiology
Stress, Psychological - physiopathology
endocannabinoid system
noradrenergic signaling
stress response
cannabinoid receptor
memory consolidation
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Abstract Stressful events can generate emotional memories linked to the traumatic incident, but they also can impair the formation of nonemotional memories. Although the impact of stress on emotional memories is well studied, much less is known about the influence of the emotional state on the formation of nonemotional memories. We used the novel object-recognition task as a model of nonemotional memory in mice to investigate the underlying mechanism of the deleterious effect of stress on memory consolidation. Systemic, hippocampal, and peripheral blockade of cannabinoid type-1 (CB1) receptors abolished the stress-induced memory impairment. Genetic deletion and rescue of CB1 receptors in specific cell types revealed that the CB1 receptor population specifically in dopamine β-hydroxylase (DBH)-expressing cells is both necessary and sufficient for stress-induced impairment of memory consolidation, but CB1 receptors present in other neuronal populations are not involved. Strikingly, pharmacological manipulations in mice expressing CB1 receptors exclusively in DBH⁺ cells revealed that both hippocampal and peripheral receptors mediate the impact of stress on memory consolidation. Thus, CB1 receptors on adrenergic and noradrenergic cells provide previously unrecognized cross-talk between central and peripheral mechanisms in the stress-dependent regulation of nonemotional memory consolidation, suggesting new potential avenues for the treatment of cognitive aspects on stress-related disorders.
AbstractList This study discloses specific central and peripheral mechanisms involving cannabinoid type-1 (CB1) receptors in impairing the effect of acute stress on the consolidation of nonemotional memory in rodents. Both hippocampal and peripheral CB1 receptors in dopamine β-hydroxylase–expressing cells (i.e., in adrenergic/noradrenergic cells) are identified as necessary and sufficient for stress-induced memory impairment. Our study provides the foundation for the development of novel potential approaches to tackle cognitive alterations in stress-related disorders. Stressful events can generate emotional memories linked to the traumatic incident, but they also can impair the formation of nonemotional memories. Although the impact of stress on emotional memories is well studied, much less is known about the influence of the emotional state on the formation of nonemotional memories. We used the novel object-recognition task as a model of nonemotional memory in mice to investigate the underlying mechanism of the deleterious effect of stress on memory consolidation. Systemic, hippocampal, and peripheral blockade of cannabinoid type-1 (CB1) receptors abolished the stress-induced memory impairment. Genetic deletion and rescue of CB1 receptors in specific cell types revealed that the CB1 receptor population specifically in dopamine β-hydroxylase (DBH)-expressing cells is both necessary and sufficient for stress-induced impairment of memory consolidation, but CB1 receptors present in other neuronal populations are not involved. Strikingly, pharmacological manipulations in mice expressing CB1 receptors exclusively in DBH + cells revealed that both hippocampal and peripheral receptors mediate the impact of stress on memory consolidation. Thus, CB1 receptors on adrenergic and noradrenergic cells provide previously unrecognized cross-talk between central and peripheral mechanisms in the stress-dependent regulation of nonemotional memory consolidation, suggesting new potential avenues for the treatment of cognitive aspects on stress-related disorders.
Significance This study discloses specific central and peripheral mechanisms involving cannabinoid type-1 (CB1) receptors in impairing the effect of acute stress on the consolidation of nonemotional memory in rodents. Both hippocampal and peripheral CB1 receptors in dopamine β-hydroxylase–expressing cells (i.e., in adrenergic/noradrenergic cells) are identified as necessary and sufficient for stress-induced memory impairment. Our study provides the foundation for the development of novel potential approaches to tackle cognitive alterations in stress-related disorders. Stressful events can generate emotional memories linked to the traumatic incident, but they also can impair the formation of nonemotional memories. Although the impact of stress on emotional memories is well studied, much less is known about the influence of the emotional state on the formation of nonemotional memories. We used the novel object-recognition task as a model of nonemotional memory in mice to investigate the underlying mechanism of the deleterious effect of stress on memory consolidation. Systemic, hippocampal, and peripheral blockade of cannabinoid type-1 (CB1) receptors abolished the stress-induced memory impairment. Genetic deletion and rescue of CB1 receptors in specific cell types revealed that the CB1 receptor population specifically in dopamine β-hydroxylase (DBH)-expressing cells is both necessary and sufficient for stress-induced impairment of memory consolidation, but CB1 receptors present in other neuronal populations are not involved. Strikingly, pharmacological manipulations in mice expressing CB1 receptors exclusively in DBH + cells revealed that both hippocampal and peripheral receptors mediate the impact of stress on memory consolidation. Thus, CB1 receptors on adrenergic and noradrenergic cells provide previously unrecognized cross-talk between central and peripheral mechanisms in the stress-dependent regulation of nonemotional memory consolidation, suggesting new potential avenues for the treatment of cognitive aspects on stress-related disorders.
Stressful events can generate emotional memories linked to the traumatic incident, but they also can impair the formation of nonemotional memories. Although the impact of stress on emotional memories is well studied, much less is known about the influence of the emotional state on the formation of nonemotional memories. We used the novel object-recognition task as a model of nonemotional memory in mice to investigate the underlying mechanism of the deleterious effect of stress on memory consolidation. Systemic, hippocampal, and peripheral blockade of cannabinoid type-1 (CB1) receptors abolished the stress-induced memory impairment. Genetic deletion and rescue of CB1 receptors in specific cell types revealed that the CB1 receptor population specifically in dopamine beta -hydroxylase (DBH)-expressing cells is both necessary and sufficient for stress-induced impairment of memory consolidation, but CB1 receptors present in other neuronal populations are not involved. Strikingly, pharmacological manipulations in mice expressing CB1 receptors exclusively in DBH+ cells revealed that both hippocampal and peripheral receptors mediate the impact of stress on memory consolidation. Thus, CB1 receptors on adrenergic and noradrenergic cells provide previously unrecognized cross-talk between central and peripheral mechanisms in the stress-dependent regulation of nonemotional memory consolidation, suggesting new potential avenues for the treatment of cognitive aspects on stress-related disorders.
Stressful events can generate emotional memories linked to the traumatic incident, but they also can impair the formation of nonemotional memories. Although the impact of stress on emotional memories is well studied, much less is known about the influence of the emotional state on the formation of nonemotional memories. We used the novel object-recognition task as a model of nonemotional memory in mice to investigate the underlying mechanism of the deleterious effect of stress on memory consolidation. Systemic, hippocampal, and peripheral blockade of cannabinoid type-1 (CB1) receptors abolished the stress-induced memory impairment. Genetic deletion and rescue of CB1 receptors in specific cell types revealed that the CB1 receptor population specifically in dopamine ...-hydroxylase (DBH)-expressing cells is both necessary and sufficient for stress-induced impairment of memory consolidation, but CB1 receptors present in other neuronal populations are not involved. Strikingly, pharmacological manipulations in mice expressing CB1 receptors exclusively in DBH+ cells revealed that both hippocampal and peripheral receptors mediate the impact of stress on memory consolidation. Thus, CB1 receptors on adrenergic and noradrenergic cells provide previously unrecognized cross-talk between central and peripheral mechanisms in the stress-dependent regulation of nonemotional memory consolidation, suggesting new potential avenues for the treatment of cognitive aspects on stress-related disorders. (ProQuest: ... denotes formulae/symbols omitted.)
Stressful events can generate emotional memories linked to the traumatic incident, but they also can impair the formation of nonemotional memories. Although the impact of stress on emotional memories is well studied, much less is known about the influence of the emotional state on the formation of nonemotional memories. We used the novel object-recognition task as a model of nonemotional memory in mice to investigate the underlying mechanism of the deleterious effect of stress on memory consolidation. Systemic, hippocampal, and peripheral blockade of cannabinoid type-1 (CB1) receptors abolished the stress-induced memory impairment. Genetic deletion and rescue of CB1 receptors in specific cell types revealed that the CB1 receptor population specifically in dopamine β-hydroxylase (DBH)-expressing cells is both necessary and sufficient for stress-induced impairment of memory consolidation, but CB1 receptors present in other neuronal populations are not involved. Strikingly, pharmacological manipulations in mice expressing CB1 receptors exclusively in DBH(+) cells revealed that both hippocampal and peripheral receptors mediate the impact of stress on memory consolidation. Thus, CB1 receptors on adrenergic and noradrenergic cells provide previously unrecognized cross-talk between central and peripheral mechanisms in the stress-dependent regulation of nonemotional memory consolidation, suggesting new potential avenues for the treatment of cognitive aspects on stress-related disorders. We acknowledge a predoctoral fellowship from the Spanish Ministry of Education and a postdoctoral fellowship from the Investments for the Future Programme, Initiative of Excellence Bordeaux, ANR-10-IDEX-03-02 (to A.B.-G.); a postdoctoral fellowship from the Marie Curie action Seventh Framework Programme for Research and Technological Development, FP7-PEOPLE-2013 (to A.B.-G.); the partial support by FRAXA Research Foundation (M.G.-G.); a European Molecular Biology Organization postdoctoral fellowship (to L. Bellocchio); grants from Ministerio de Ciencia e Innovación [BFU2012-33500 and BFU2015-68568P (to A.O.), and SAF2014-59648-P (to R.M.) (MINECO/FEDER, UE)]; Instituto de Salud Carlos III Grant RD06/0001/0001 (to R.M.); Generalitat de Catalunya Grant SGR-2014-1547 (to R.M.); ICREA (Institució Catalana de Recerca i Estudis Avançats) Academia (R.M.); the German Research Council DFG Grants FOR926 (Core Unit Endocannabinoid Measurements) (to B.L.), CRC-TRR58 (to B.L.), and CRC1080 (to B.L.); EU-FP7 Grant REPROBESITY, HEALTH-F2-2008-223713 (to B.L. and G.M.); PainCage Grant HEALTH-2013-INNOVATION-1-603191 (to G.M.); INSERM (G.M.); European Research Council Grant ENDOFOOD, ERC–2010–StG–260515 (to G.M.); Fondation pour la Recherche Medicale (G.M.); Region Aquitaine (G.M.); and LABEX BRAIN Grant ANR-10-LABX-43 (to G.M.)
Stressful events can generate emotional memories linked to the traumatic incident, but they also can impair the formation of nonemotional memories. Although the impact of stress on emotional memories is well studied, much less is known about the influence of the emotional state on the formation of nonemotional memories. We used the novel object-recognition task as a model of nonemotional memory in mice to investigate the underlying mechanism of the deleterious effect of stress on memory consolidation. Systemic, hippocampal, and peripheral blockade of cannabinoid type-1 (CB1) receptors abolished the stress-induced memory impairment. Genetic deletion and rescue of CB1 receptors in specific cell types revealed that the CB1 receptor population specifically in dopamine β-hydroxylase (DBH)-expressing cells is both necessary and sufficient for stress-induced impairment of memory consolidation, but CB1 receptors present in other neuronal populations are not involved. Strikingly, pharmacological manipulations in mice expressing CB1 receptors exclusively in DBH⁺ cells revealed that both hippocampal and peripheral receptors mediate the impact of stress on memory consolidation. Thus, CB1 receptors on adrenergic and noradrenergic cells provide previously unrecognized cross-talk between central and peripheral mechanisms in the stress-dependent regulation of nonemotional memory consolidation, suggesting new potential avenues for the treatment of cognitive aspects on stress-related disorders.
Stressful events can generate emotional memories linked to the traumatic incident, but they also can impair the formation of nonemotional memories. Although the impact of stress on emotional memories is well studied, much less is known about the influence of the emotional state on the formation of nonemotional memories. We used the novel object-recognition task as a model of nonemotional memory in mice to investigate the underlying mechanism of the deleterious effect of stress on memory consolidation. Systemic, hippocampal, and peripheral blockade of cannabinoid type-1 (CB1) receptors abolished the stress-induced memory impairment. Genetic deletion and rescue of CB1 receptors in specific cell types revealed that the CB1 receptor population specifically in dopamine β-hydroxylase (DBH)-expressing cells is both necessary and sufficient for stress-induced impairment of memory consolidation, but CB1 receptors present in other neuronal populations are not involved. Strikingly, pharmacological manipulations in mice expressing CB1 receptors exclusively in DBH(+) cells revealed that both hippocampal and peripheral receptors mediate the impact of stress on memory consolidation. Thus, CB1 receptors on adrenergic and noradrenergic cells provide previously unrecognized cross-talk between central and peripheral mechanisms in the stress-dependent regulation of nonemotional memory consolidation, suggesting new potential avenues for the treatment of cognitive aspects on stress-related disorders.
Author Ozaita, Andrés
Srivastava, Raj Kamal
Bellocchio, Luigi
Marsicano, Giovanni
Bindila, Laura
Cutando, Laura
Busquets-Garcia, Arnau
Maldonado, Rafael
Ortega-Alvaro, Antonio
Lutz, Beat
Ruehle, Sabine
Gomis-González, Maria
Remmers, Floortje
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  fullname: Bindila, Laura
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– sequence: 10
  givenname: Giovanni
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  fullname: Marsicano, Giovanni
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– sequence: 11
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  surname: Lutz
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  givenname: Rafael
  surname: Maldonado
  fullname: Maldonado, Rafael
  organization: Laboratory of Neuropharmacology-NeuroPhar, Department of Experimental and Health Sciences, University Pompeu Fabra, 08003 Barcelona, Spain
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  surname: Ozaita
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  organization: Laboratory of Neuropharmacology-NeuroPhar, Department of Experimental and Health Sciences, University Pompeu Fabra, 08003 Barcelona, Spain
BackLink https://www.ncbi.nlm.nih.gov/pubmed/27528659$$D View this record in MEDLINE/PubMed
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Issue 35
Keywords endocannabinoid system
noradrenergic signaling
stress response
cannabinoid receptor
memory consolidation
Language English
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content type line 23
Edited by Jean-Pierre Changeux, CNRS, Institut Pasteur, Paris, France, and approved July 6, 2016 (received for review January 5, 2016)
Author contributions: A.B.-G., M.G.-G., R.K.S., L.C., F.R., L. Bellocchio, G.M., B.L., R.M., and A.O. designed research; A.B.-G., M.G.-G., R.K.S., L.C., A.O.-A., F.R., L. Bindila, L. Bellocchio, and A.O. performed research; R.K.S., S.R., F.R., G.M., B.L., and R.M. contributed new reagents/analytic tools; A.B.-G., M.G.-G., R.K.S., L.C., F.R., L. Bindila, and A.O. analyzed data; and A.B.-G., M.G.-G., R.K.S., L.C., F.R., L. Bindila, G.M., B.L., R.M., and A.O. wrote the paper.
2B.L., R.M., and A.O. contributed equally to this work.
1A.B.-G., M.G.-G., and R.K.S. contributed equally to this work.
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Snippet Stressful events can generate emotional memories linked to the traumatic incident, but they also can impair the formation of nonemotional memories. Although...
Significance This study discloses specific central and peripheral mechanisms involving cannabinoid type-1 (CB1) receptors in impairing the effect of acute...
This study discloses specific central and peripheral mechanisms involving cannabinoid type-1 (CB1) receptors in impairing the effect of acute stress on the...
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StartPage 9904
SubjectTerms Animals
Anisomycin - pharmacology
Biological Sciences
Cannabinoides
Cells
Dopamine beta-Hydroxylase - metabolism
Electroshock - adverse effects
Emotions
Estrès
Hindlimb Suspension - adverse effects
Indoles - pharmacology
Male
Memory
Memory Consolidation - drug effects
Memory Consolidation - physiology
Memory Disorders - etiology
Memory Disorders - physiopathology
Memòria
Mice, Knockout
Neurons - drug effects
Neurons - metabolism
Neurons - physiology
Piperidines - pharmacology
Proteins
Pyrazoles - pharmacology
Receptor, Cannabinoid, CB1 - genetics
Receptor, Cannabinoid, CB1 - metabolism
Receptor, Cannabinoid, CB1 - physiology
Receptors
Recognition
Rimonabant
Stress
Stress, Psychological - etiology
Stress, Psychological - physiopathology
Title Peripheral and central CB1 cannabinoid receptors control stress-induced impairment of memory consolidation
URI https://www.jstor.org/stable/26471724
https://www.ncbi.nlm.nih.gov/pubmed/27528659
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