The basolateral amygdala-anterior cingulate pathway contributes to depression-like behaviors and comorbidity with chronic pain behaviors in male mice

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 and Ipek Yalcin ()
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Léa J. Becker: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Clémentine Fillinger: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Robin Waegaert: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Sarah H. Journée: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Pierre Hener: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Beyza Ayazgok: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Muris Humo: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Meltem Karatas: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Maxime Thouaye: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Mithil Gaikwad: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Laetitia Degiorgis: University of Strasbourg
Marie des Neiges Santin: University of Strasbourg
Mary Mondino: University of Strasbourg
Michel Barrot: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
El Chérif Ibrahim: INT, Inst Neurosci Timone
Gustavo Turecki: McGill University and Douglas Mental Health University Institute
Raoul Belzeaux: INT, Inst Neurosci Timone
Pierre Veinante: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Laura A. Harsan: University of Strasbourg
Sylvain Hugel: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Pierre-Eric Lutz: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives
Ipek Yalcin: Université de Strasbourg, Institut des Neurosciences Cellulaires et Intégratives

Nature Communications, 2023, vol. 14, issue 1, 1-23

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-37878-y

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