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Olfactory bulb astrocytes link social transmission of stress to cognitive adaptation in male mice

Author

Listed:
  • Paula Gómez-Sotres

    (U1215 Neurocentre Magendie)

  • Urszula Skupio

    (U1215 Neurocentre Magendie)

  • Tommaso Dalla Tor

    (U1215 Neurocentre Magendie
    University of the Basque Country UPV/EHU)

  • Francisca Julio-Kalajzic

    (U1215 Neurocentre Magendie)

  • Astrid Cannich

    (U1215 Neurocentre Magendie)

  • Doriane Gisquet

    (U1215 Neurocentre Magendie)

  • Itziar Bonilla-Del Rio

    (University of the Basque Country UPV/EHU
    Science Park of the UPV/EHU)

  • Filippo Drago

    (University of Catania)

  • Nagore Puente

    (University of the Basque Country UPV/EHU
    Science Park of the UPV/EHU)

  • Pedro Grandes

    (University of the Basque Country UPV/EHU
    Science Park of the UPV/EHU)

  • Luigi Bellocchio

    (U1215 Neurocentre Magendie)

  • Arnau Busquets-Garcia

    (PRBB)

  • Jaideep S. Bains

    (University Health Network
    University of Calgary)

  • Giovanni Marsicano

    (U1215 Neurocentre Magendie)

Abstract

Emotions and behavior can be affected by social chemosignals from conspecifics. For instance, olfactory signals from stressed individuals induce stress-like physiological and synaptic changes in naïve partners. Direct stress also alters cognition, but the impact of socially transmitted stress on memory processes is currently unknown. Here we show that exposure to chemosignals produced by stressed individuals is sufficient to impair memory retrieval in unstressed male mice. This requires astrocyte control of information in the olfactory bulb mediated by mitochondria-associated CB1 receptors (mtCB1). Targeted genetic manipulations, in vivo Ca2+ imaging and behavioral analyses reveal that mtCB1-dependent control of mitochondrial Ca2+ dynamics is necessary to process olfactory information from stressed partners and to define their cognitive consequences. Thus, olfactory bulb astrocytes provide a link between social odors and their behavioral meaning.

Suggested Citation

  • Paula Gómez-Sotres & Urszula Skupio & Tommaso Dalla Tor & Francisca Julio-Kalajzic & Astrid Cannich & Doriane Gisquet & Itziar Bonilla-Del Rio & Filippo Drago & Nagore Puente & Pedro Grandes & Luigi B, 2024. "Olfactory bulb astrocytes link social transmission of stress to cognitive adaptation in male mice," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51416-4
    DOI: 10.1038/s41467-024-51416-4
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    References listed on IDEAS

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    1. Daniel Jimenez-Blasco & Arnau Busquets-Garcia & Etienne Hebert-Chatelain & Roman Serrat & Carlos Vicente-Gutierrez & Christina Ioannidou & Paula Gómez-Sotres & Irene Lopez-Fabuel & Monica Resch-Beushe, 2020. "Glucose metabolism links astroglial mitochondria to cannabinoid effects," Nature, Nature, vol. 583(7817), pages 603-608, July.
    2. Zhiguo Ma & Tobias Stork & Dwight E. Bergles & Marc R. Freeman, 2016. "Neuromodulators signal through astrocytes to alter neural circuit activity and behaviour," Nature, Nature, vol. 539(7629), pages 428-432, November.
    3. Tamás Füzesi & Nuria Daviu & Jaclyn I. Wamsteeker Cusulin & Robert P. Bonin & Jaideep S. Bains, 2016. "Hypothalamic CRH neurons orchestrate complex behaviours after stress," Nature Communications, Nature, vol. 7(1), pages 1-14, September.
    4. Geoffrey Terral & Evan Harrell & Gabriel Lepousez & Yohan Wards & Dinghuang Huang & Tiphaine Dolique & Giulio Casali & Antoine Nissant & Pierre-Marie Lledo & Guillaume Ferreira & Giovanni Marsicano & , 2024. "Endogenous cannabinoids in the piriform cortex tune olfactory perception," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Etienne Hebert-Chatelain & Tifany Desprez & Román Serrat & Luigi Bellocchio & Edgar Soria-Gomez & Arnau Busquets-Garcia & Antonio Christian Pagano Zottola & Anna Delamarre & Astrid Cannich & Peggy Vin, 2016. "A cannabinoid link between mitochondria and memory," Nature, Nature, vol. 539(7630), pages 555-559, November.
    6. Kevin Ung & Teng-Wei Huang & Brittney Lozzi & Junsung Woo & Elizabeth Hanson & Brandon Pekarek & Burak Tepe & Debosmita Sardar & Yi-Ting Cheng & Gary Liu & Benjamin Deneen & Benjamin R. Arenkiel, 2021. "Olfactory bulb astrocytes mediate sensory circuit processing through Sox9 in the mouse brain," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    7. Giovanni Marsicano & Carsten T. Wotjak & Shahnaz C. Azad & Tiziana Bisogno & Gerhard Rammes & Maria Grazia Cascio & Heike Hermann & Jianrong Tang & Clementine Hofmann & Walter Zieglgänsberger & Vincen, 2002. "The endogenous cannabinoid system controls extinction of aversive memories," Nature, Nature, vol. 418(6897), pages 530-534, August.
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