IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0081459.html
   My bibliography  Save this article

Voluntary Running in Young Adult Mice Reduces Anxiety-Like Behavior and Increases the Accumulation of Bioactive Lipids in the Cerebral Cortex

Author

Listed:
  • Iván J Santos-Soto
  • Nataliya Chorna
  • Néstor M Carballeira
  • José G Vélez-Bartolomei
  • Ana T Méndez-Merced
  • Anatoliy P Chornyy
  • Sandra Peña de Ortiz

Abstract

Combinatorial therapies using voluntary exercise and diet supplementation with polyunsaturated fatty acids have synergistic effects benefiting brain function and behavior. Here, we assessed the effects of voluntary exercise on anxiety-like behavior and on total FA accumulation within three brain regions: cortex, hippocampus, and cerebellum of running versus sedentary young adult male C57/BL6J mice. The running group was subjected to one month of voluntary exercise in their home cages, while the sedentary group was kept in their home cages without access to a running wheel. Elevated plus maze (EPM), several behavioral postures and two risk assessment behaviors (RABs) were then measured in both animal groups followed immediately by blood samplings for assessment of corticosterone levels. Brains were then dissected for non-targeted lipidomic analysis of selected brain regions using gas chromatography coupled to mass spectrometry (GC/MS). Results showed that mice in the running group, when examined in the EPM, displayed significantly lower anxiety-like behavior, higher exploratory and risky behaviors, compared to sedentary mice. Notably, we found no differences in blood corticosterone levels between the two groups, suggesting that the different EPM and RAB behaviors were not related to reduced physiological stress in the running mice. Lipidomics analysis revealed a region-specific cortical decrease of the saturated FA: palmitate (C16:0) and a concomitant increase of polyunsaturated FA, arachidonic acid (AA, omega 6-C20: 4) and docosahexaenoic acid (DHA, omega 3-C22: 6), in running mice compared to sedentary controls. Finally, we found that running mice, as opposed to sedentary animals, showed significantly enhanced cortical expression of phospholipase A2 (PLA2) protein, a signaling molecule required in the production of both AA and DHA. In summary, our data support the anxiolytic effects of exercise and provide insights into the molecular processes modulated by exercise that may lead to its beneficial effects on mood.

Suggested Citation

  • Iván J Santos-Soto & Nataliya Chorna & Néstor M Carballeira & José G Vélez-Bartolomei & Ana T Méndez-Merced & Anatoliy P Chornyy & Sandra Peña de Ortiz, 2013. "Voluntary Running in Young Adult Mice Reduces Anxiety-Like Behavior and Increases the Accumulation of Bioactive Lipids in the Cerebral Cortex," PLOS ONE, Public Library of Science, vol. 8(12), pages 1-15, December.
  • Handle: RePEc:plo:pone00:0081459
    DOI: 10.1371/journal.pone.0081459
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0081459
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0081459&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0081459?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Kay M. Tye & Rohit Prakash & Sung-Yon Kim & Lief E. Fenno & Logan Grosenick & Hosniya Zarabi & Kimberly R. Thompson & Viviana Gradinaru & Charu Ramakrishnan & Karl Deisseroth, 2011. "Amygdala circuitry mediating reversible and bidirectional control of anxiety," Nature, Nature, vol. 471(7338), pages 358-362, March.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Sorinel A Oprisan & Xandre Clementsmith & Tamas Tompa & Antonieta Lavin, 2019. "Dopamine receptor antagonists effects on low-dimensional attractors of local field potentials in optogenetic mice," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-39, October.
    2. Ren-Wen Han & Zi-Yi Zhang & Chen Jiao & Ze-Yu Hu & Bing-Xing Pan, 2024. "Synergism between two BLA-to-BNST pathways for appropriate expression of anxiety-like behaviors in male mice," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    3. Anna J. Bowen & Y. Waterlily Huang & Jane Y. Chen & Jordan L. Pauli & Carlos A. Campos & Richard D. Palmiter, 2023. "Topographic representation of current and future threats in the mouse nociceptive amygdala," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. C. Nicolas & A. Ju & Y. Wu & H. Eldirdiri & S. Delcasso & Y. Couderc & C. Fornari & A. Mitra & L. Supiot & A. Vérité & M. Masson & S. Rodriguez-Rozada & D. Jacky & J. S. Wiegert & A. Beyeler, 2023. "Linking emotional valence and anxiety in a mouse insula-amygdala circuit," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Masahiro Sawada & Ralph Adolphs & Brian J. Dlouhy & Rick L. Jenison & Ariane E. Rhone & Christopher K. Kovach & Jeremy, D. W. Greenlee & Matthew A. Howard III & Hiroyuki Oya, 2022. "Mapping effective connectivity of human amygdala subdivisions with intracranial stimulation," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    6. Carole Morel & Sarah E. Montgomery & Long Li & Romain Durand-de Cuttoli & Emily M. Teichman & Barbara Juarez & Nikos Tzavaras & Stacy M. Ku & Meghan E. Flanigan & Min Cai & Jessica J. Walsh & Scott J., 2022. "Midbrain projection to the basolateral amygdala encodes anxiety-like but not depression-like behaviors," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    7. Hansol Lim & Yue Zhang & Christian Peters & Tobias Straub & Johanna Luise Mayer & Rüdiger Klein, 2024. "Genetically- and spatially-defined basolateral amygdala neurons control food consumption and social interaction," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    8. Kaizhen Li & Konstantinos Koukoutselos & Masanori Sakaguchi & Stéphane Ciocchi, 2024. "Distinct ventral hippocampal inhibitory microcircuits regulating anxiety and fear behaviors," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pone00:0081459. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.