Stress deficits in reward behaviour are associated with and replicated by dysregulated amygdala-nucleus accumbens pathway function in mice
Abstract Reduced reward interest/learning and reward-to-effort valuation are distinct, common symptoms in neuropsychiatric disorders for which chronic stress is a major aetiological factor. Glutamate neurons in basal amygdala (BA) project to various regions including nucleus accumbens (NAc). The BA-...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-04-01
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| Series: | Communications Biology |
| Online Access: | https://doi.org/10.1038/s42003-023-04811-4 |
| _version_ | 1797845786404323328 |
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| author | Lorraine Madur Christian Ineichen Giorgio Bergamini Alexandra Greter Giulia Poggi Nagiua Cuomo-Haymour Hannes Sigrist Yaroslav Sych Jean-Charles Paterna Klaus D. Bornemann Coralie Viollet Francesc Fernandez-Albert Gregorio Alanis-Lobato Bastian Hengerer Christopher R. Pryce |
| author_facet | Lorraine Madur Christian Ineichen Giorgio Bergamini Alexandra Greter Giulia Poggi Nagiua Cuomo-Haymour Hannes Sigrist Yaroslav Sych Jean-Charles Paterna Klaus D. Bornemann Coralie Viollet Francesc Fernandez-Albert Gregorio Alanis-Lobato Bastian Hengerer Christopher R. Pryce |
| author_sort | Lorraine Madur |
| collection | DOAJ |
| description | Abstract Reduced reward interest/learning and reward-to-effort valuation are distinct, common symptoms in neuropsychiatric disorders for which chronic stress is a major aetiological factor. Glutamate neurons in basal amygdala (BA) project to various regions including nucleus accumbens (NAc). The BA-NAc neural pathway is activated by reward and aversion, with many neurons being monovalent. In adult male mice, chronic social stress (CSS) leads to reduced discriminative reward learning (DRL) associated with decreased BA-NAc activity, and to reduced reward-to-effort valuation (REV) associated, in contrast, with increased BA-NAc activity. Chronic tetanus toxin BA-NAc inhibition replicates the CSS-DRL effect and causes a mild REV reduction, whilst chronic DREADDs BA-NAc activation replicates the CSS effect on REV without affecting DRL. This study provides evidence that stress disruption of reward processing involves the BA-NAc neural pathway; the bi-directional effects implicate opposite activity changes in reward (learning) neurons and aversion (effort) neurons in the BA-NAc pathway following chronic stress. |
| first_indexed | 2024-04-09T17:44:35Z |
| format | Article |
| id | doaj.art-07210833de8e4c8cb484870cc8edadc8 |
| institution | Directory Open Access Journal |
| issn | 2399-3642 |
| language | English |
| last_indexed | 2024-04-09T17:44:35Z |
| publishDate | 2023-04-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Communications Biology |
| spelling | doaj.art-07210833de8e4c8cb484870cc8edadc82023-04-16T11:22:45ZengNature PortfolioCommunications Biology2399-36422023-04-016112010.1038/s42003-023-04811-4Stress deficits in reward behaviour are associated with and replicated by dysregulated amygdala-nucleus accumbens pathway function in miceLorraine Madur0Christian Ineichen1Giorgio Bergamini2Alexandra Greter3Giulia Poggi4Nagiua Cuomo-Haymour5Hannes Sigrist6Yaroslav Sych7Jean-Charles Paterna8Klaus D. Bornemann9Coralie Viollet10Francesc Fernandez-Albert11Gregorio Alanis-Lobato12Bastian Hengerer13Christopher R. Pryce14Preclinical Laboratory, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric University Hospital Zürich (PUK) and University of Zurich (UZH)Preclinical Laboratory, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric University Hospital Zürich (PUK) and University of Zurich (UZH)Preclinical Laboratory, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric University Hospital Zürich (PUK) and University of Zurich (UZH)Preclinical Laboratory, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric University Hospital Zürich (PUK) and University of Zurich (UZH)Preclinical Laboratory, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric University Hospital Zürich (PUK) and University of Zurich (UZH)Preclinical Laboratory, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric University Hospital Zürich (PUK) and University of Zurich (UZH)Preclinical Laboratory, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric University Hospital Zürich (PUK) and University of Zurich (UZH)Institute of Cellular and Integrative Neuroscience, University of StrasbourgViral Vector Facility, University of Zurich and ETH ZurichCNS Diseases Research, Boehringer Ingelheim Pharma GmbH & Co. KGGlobal Computational Biology and Digital Sciences, Boehringer Ingelheim Pharma GmbH & Co. KGGlobal Computational Biology and Digital Sciences, Boehringer Ingelheim Pharma GmbH & Co. KGGlobal Computational Biology and Digital Sciences, Boehringer Ingelheim Pharma GmbH & Co. KGCNS Diseases Research, Boehringer Ingelheim Pharma GmbH & Co. KGPreclinical Laboratory, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric University Hospital Zürich (PUK) and University of Zurich (UZH)Abstract Reduced reward interest/learning and reward-to-effort valuation are distinct, common symptoms in neuropsychiatric disorders for which chronic stress is a major aetiological factor. Glutamate neurons in basal amygdala (BA) project to various regions including nucleus accumbens (NAc). The BA-NAc neural pathway is activated by reward and aversion, with many neurons being monovalent. In adult male mice, chronic social stress (CSS) leads to reduced discriminative reward learning (DRL) associated with decreased BA-NAc activity, and to reduced reward-to-effort valuation (REV) associated, in contrast, with increased BA-NAc activity. Chronic tetanus toxin BA-NAc inhibition replicates the CSS-DRL effect and causes a mild REV reduction, whilst chronic DREADDs BA-NAc activation replicates the CSS effect on REV without affecting DRL. This study provides evidence that stress disruption of reward processing involves the BA-NAc neural pathway; the bi-directional effects implicate opposite activity changes in reward (learning) neurons and aversion (effort) neurons in the BA-NAc pathway following chronic stress.https://doi.org/10.1038/s42003-023-04811-4 |
| spellingShingle | Lorraine Madur Christian Ineichen Giorgio Bergamini Alexandra Greter Giulia Poggi Nagiua Cuomo-Haymour Hannes Sigrist Yaroslav Sych Jean-Charles Paterna Klaus D. Bornemann Coralie Viollet Francesc Fernandez-Albert Gregorio Alanis-Lobato Bastian Hengerer Christopher R. Pryce Stress deficits in reward behaviour are associated with and replicated by dysregulated amygdala-nucleus accumbens pathway function in mice Communications Biology |
| title | Stress deficits in reward behaviour are associated with and replicated by dysregulated amygdala-nucleus accumbens pathway function in mice |
| title_full | Stress deficits in reward behaviour are associated with and replicated by dysregulated amygdala-nucleus accumbens pathway function in mice |
| title_fullStr | Stress deficits in reward behaviour are associated with and replicated by dysregulated amygdala-nucleus accumbens pathway function in mice |
| title_full_unstemmed | Stress deficits in reward behaviour are associated with and replicated by dysregulated amygdala-nucleus accumbens pathway function in mice |
| title_short | Stress deficits in reward behaviour are associated with and replicated by dysregulated amygdala-nucleus accumbens pathway function in mice |
| title_sort | stress deficits in reward behaviour are associated with and replicated by dysregulated amygdala nucleus accumbens pathway function in mice |
| url | https://doi.org/10.1038/s42003-023-04811-4 |
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