The basolateral amygdala-anterior cingulate pathway contributes to depression-like behaviors and comorbidity with chronic pain behaviors in male mice
Abstract While depression and chronic pain are frequently comorbid, underlying neuronal circuits and their psychopathological relevance remain poorly defined. Here we show in mice that hyperactivity of the neuronal pathway linking the basolateral amygdala to the anterior cingulate cortex is essentia...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-04-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-37878-y |
| _version_ | 1797840939342888960 |
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| author | Léa J. Becker Clémentine Fillinger Robin Waegaert Sarah H. Journée Pierre Hener Beyza Ayazgok Muris Humo Meltem Karatas Maxime Thouaye Mithil Gaikwad Laetitia Degiorgis Marie des Neiges Santin Mary Mondino Michel Barrot El Chérif Ibrahim Gustavo Turecki Raoul Belzeaux Pierre Veinante Laura A. Harsan Sylvain Hugel Pierre-Eric Lutz Ipek Yalcin |
| author_facet | Léa J. Becker Clémentine Fillinger Robin Waegaert Sarah H. Journée Pierre Hener Beyza Ayazgok Muris Humo Meltem Karatas Maxime Thouaye Mithil Gaikwad Laetitia Degiorgis Marie des Neiges Santin Mary Mondino Michel Barrot El Chérif Ibrahim Gustavo Turecki Raoul Belzeaux Pierre Veinante Laura A. Harsan Sylvain Hugel Pierre-Eric Lutz Ipek Yalcin |
| author_sort | Léa J. Becker |
| collection | DOAJ |
| description | Abstract While depression and chronic pain are frequently comorbid, underlying neuronal circuits and their psychopathological relevance remain poorly defined. Here we show in mice that hyperactivity of the neuronal pathway linking the basolateral amygdala to the anterior cingulate cortex is essential for chronic pain-induced depression. Moreover, activation of this pathway in naive male mice, in the absence of on-going pain, is sufficient to trigger depressive-like behaviors, as well as transcriptomic alterations that recapitulate core molecular features of depression in the human brain. These alterations notably impact gene modules related to myelination and the oligodendrocyte lineage. Among these, we show that Sema4a, which was significantly upregulated in both male mice and humans in the context of altered mood, is necessary for the emergence of emotional dysfunction. Overall, these results place the amygdalo-cingulate pathway at the core of pain and depression comorbidity, and unravel the role of Sema4a and impaired myelination in mood control. |
| first_indexed | 2024-04-09T16:22:55Z |
| format | Article |
| id | doaj.art-79edb28876214399bf2915cb6fdcd98c |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-04-09T16:22:55Z |
| publishDate | 2023-04-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-79edb28876214399bf2915cb6fdcd98c2023-04-23T11:23:11ZengNature PortfolioNature Communications2041-17232023-04-0114112310.1038/s41467-023-37878-yThe basolateral amygdala-anterior cingulate pathway contributes to depression-like behaviors and comorbidity with chronic pain behaviors in male miceLéa J. Becker0Clémentine Fillinger1Robin Waegaert2Sarah H. Journée3Pierre Hener4Beyza Ayazgok5Muris Humo6Meltem Karatas7Maxime Thouaye8Mithil Gaikwad9Laetitia Degiorgis10Marie des Neiges Santin11Mary Mondino12Michel Barrot13El Chérif Ibrahim14Gustavo Turecki15Raoul Belzeaux16Pierre Veinante17Laura A. Harsan18Sylvain Hugel19Pierre-Eric Lutz20Ipek Yalcin21Centre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesLaboratory of Engineering, Informatics and Imaging (ICube), Integrative multimodal imaging in healthcare (IMIS), CNRS, UMR 7357, University of StrasbourgLaboratory of Engineering, Informatics and Imaging (ICube), Integrative multimodal imaging in healthcare (IMIS), CNRS, UMR 7357, University of StrasbourgLaboratory of Engineering, Informatics and Imaging (ICube), Integrative multimodal imaging in healthcare (IMIS), CNRS, UMR 7357, University of StrasbourgCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesAix-Marseille Univ, CNRS, INT, Inst Neurosci TimoneDepartment of Psychiatry, McGill University and Douglas Mental Health University InstituteAix-Marseille Univ, CNRS, INT, Inst Neurosci TimoneCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesLaboratory of Engineering, Informatics and Imaging (ICube), Integrative multimodal imaging in healthcare (IMIS), CNRS, UMR 7357, University of StrasbourgCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesCentre National de la Recherche Scientifique, Université de Strasbourg, Institut des Neurosciences Cellulaires et IntégrativesAbstract While depression and chronic pain are frequently comorbid, underlying neuronal circuits and their psychopathological relevance remain poorly defined. Here we show in mice that hyperactivity of the neuronal pathway linking the basolateral amygdala to the anterior cingulate cortex is essential for chronic pain-induced depression. Moreover, activation of this pathway in naive male mice, in the absence of on-going pain, is sufficient to trigger depressive-like behaviors, as well as transcriptomic alterations that recapitulate core molecular features of depression in the human brain. These alterations notably impact gene modules related to myelination and the oligodendrocyte lineage. Among these, we show that Sema4a, which was significantly upregulated in both male mice and humans in the context of altered mood, is necessary for the emergence of emotional dysfunction. Overall, these results place the amygdalo-cingulate pathway at the core of pain and depression comorbidity, and unravel the role of Sema4a and impaired myelination in mood control.https://doi.org/10.1038/s41467-023-37878-y |
| spellingShingle | Léa J. Becker Clémentine Fillinger Robin Waegaert Sarah H. Journée Pierre Hener Beyza Ayazgok Muris Humo Meltem Karatas Maxime Thouaye Mithil Gaikwad Laetitia Degiorgis Marie des Neiges Santin Mary Mondino Michel Barrot El Chérif Ibrahim Gustavo Turecki Raoul Belzeaux Pierre Veinante Laura A. Harsan Sylvain Hugel Pierre-Eric Lutz Ipek Yalcin The basolateral amygdala-anterior cingulate pathway contributes to depression-like behaviors and comorbidity with chronic pain behaviors in male mice Nature Communications |
| title | The basolateral amygdala-anterior cingulate pathway contributes to depression-like behaviors and comorbidity with chronic pain behaviors in male mice |
| title_full | The basolateral amygdala-anterior cingulate pathway contributes to depression-like behaviors and comorbidity with chronic pain behaviors in male mice |
| title_fullStr | The basolateral amygdala-anterior cingulate pathway contributes to depression-like behaviors and comorbidity with chronic pain behaviors in male mice |
| title_full_unstemmed | The basolateral amygdala-anterior cingulate pathway contributes to depression-like behaviors and comorbidity with chronic pain behaviors in male mice |
| title_short | The basolateral amygdala-anterior cingulate pathway contributes to depression-like behaviors and comorbidity with chronic pain behaviors in male mice |
| title_sort | basolateral amygdala anterior cingulate pathway contributes to depression like behaviors and comorbidity with chronic pain behaviors in male mice |
| url | https://doi.org/10.1038/s41467-023-37878-y |
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