IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36643-5.html
   My bibliography  Save this article

Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport

Author

Listed:
  • Laura Bojarskaite

    (University of Oslo
    Oslo University Hospital)

  • Alexandra Vallet

    (University of Oslo)

  • Daniel M. Bjørnstad

    (University of Oslo)

  • Kristin M. Gullestad Binder

    (University of Oslo)

  • Céline Cunen

    (University of Oslo
    Norwegian Computing Center)

  • Kjell Heuser

    (Oslo University Hospital)

  • Miroslav Kuchta

    (Simula Research Laboratory)

  • Kent-Andre Mardal

    (University of Oslo
    Simula Research Laboratory)

  • Rune Enger

    (University of Oslo)

Abstract

Perivascular spaces are important highways for fluid and solute transport in the brain enabling efficient waste clearance during sleep. However, the underlying mechanisms augmenting perivascular flow in sleep are unknown. Using two-photon imaging of naturally sleeping male mice we demonstrate sleep cycle-dependent vascular dynamics of pial arteries and penetrating arterioles: slow, large-amplitude oscillations in NREM sleep, a vasodilation in REM sleep, and a vasoconstriction upon awakening at the end of a sleep cycle and microarousals in NREM and intermediate sleep. These vascular dynamics are mirrored by changes in the size of the perivascular spaces of the penetrating arterioles: slow fluctuations in NREM sleep, reduction in REM sleep and an enlargement upon awakening after REM sleep and during microarousals in NREM and intermediate sleep. By biomechanical modeling we demonstrate that these sleep cycle-dependent perivascular dynamics likely enhance fluid flow and solute transport in perivascular spaces to levels comparable to cardiac pulsation-driven oscillations.

Suggested Citation

  • Laura Bojarskaite & Alexandra Vallet & Daniel M. Bjørnstad & Kristin M. Gullestad Binder & Céline Cunen & Kjell Heuser & Miroslav Kuchta & Kent-Andre Mardal & Rune Enger, 2023. "Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36643-5
    DOI: 10.1038/s41467-023-36643-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36643-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-36643-5?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. Antoine Bergel & Thomas Deffieux & Charlie Demené & Mickaël Tanter & Ivan Cohen, 2018. "Local hippocampal fast gamma rhythms precede brain-wide hyperemic patterns during spontaneous rodent REM sleep," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    2. Antoine Louveau & Igor Smirnov & Timothy J. Keyes & Jacob D. Eccles & Sherin J. Rouhani & J. David Peske & Noel C. Derecki & David Castle & James W. Mandell & Kevin S. Lee & Tajie H. Harris & Jonathan, 2015. "Structural and functional features of central nervous system lymphatic vessels," Nature, Nature, vol. 523(7560), pages 337-341, July.
    3. Laura Bojarskaite & Daniel M. Bjørnstad & Klas H. Pettersen & Céline Cunen & Gudmund Horn Hermansen & Knut Sindre Åbjørsbråten & Anna R. Chambers & Rolf Sprengel & Koen Vervaeke & Wannan Tang & Rune E, 2020. "Astrocytic Ca2+ signaling is reduced during sleep and is involved in the regulation of slow wave sleep," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    4. Julie Seibt & Clément J. Richard & Johanna Sigl-Glöckner & Naoya Takahashi & David I. Kaplan & Guy Doron & Denis Limoges & Christina Bocklisch & Matthew E. Larkum, 2017. "Cortical dendritic activity correlates with spindle-rich oscillations during sleep in rodents," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    5. Humberto Mestre & Natasha Verma & Thom D. Greene & LiJing A. Lin & Antonio Ladron-de-Guevara & Amanda M. Sweeney & Guojun Liu & V. Kaye Thomas & Chad A. Galloway & Karen L. Mesy Bentley & Maiken Neder, 2022. "Periarteriolar spaces modulate cerebrospinal fluid transport into brain and demonstrate altered morphology in aging and Alzheimer’s disease," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. Julie Seibt & Clément J. Richard & Johanna Sigl-Glöckner & Naoya Takahashi & David I. Kaplan & Guy Doron & Denis Limoges & Christina Bocklisch & Matthew E. Larkum, 2017. "Publisher Correction: Cortical dendritic activity correlates with spindle-rich oscillations during sleep in rodents," Nature Communications, Nature, vol. 8(1), pages 1-1, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Gianina Ungurean & Mehdi Behroozi & Leonard Böger & Xavier Helluy & Paul-Antoine Libourel & Onur Güntürkün & Niels C. Rattenborg, 2023. "Wide-spread brain activation and reduced CSF flow during avian REM sleep," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

    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. Thomas Schreiner & Benjamin J. Griffiths & Merve Kutlu & Christian Vollmar & Elisabeth Kaufmann & Stefanie Quach & Jan Remi & Soheyl Noachtar & Tobias Staudigl, 2024. "Spindle-locked ripples mediate memory reactivation during human NREM sleep," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. I. Hristovska & M. Robert & K. Combet & J. Honnorat & J-C Comte & O. Pascual, 2022. "Sleep decreases neuronal activity control of microglial dynamics in mice," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Shelei Pan & Peter H. Yang & Dakota DeFreitas & Sruthi Ramagiri & Peter O. Bayguinov & Carl D. Hacker & Abraham Z. Snyder & Jackson Wilborn & Hengbo Huang & Gretchen M. Koller & Dhvanii K. Raval & Gra, 2023. "Gold nanoparticle-enhanced X-ray microtomography of the rodent reveals region-specific cerebrospinal fluid circulation in the brain," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Yung-Tian A. Gau & Eric T. Hsu & Richard J. Cha & Rebecca W. Pak & Loren L. Looger & Jin U. Kang & Dwight E. Bergles, 2024. "Multicore fiber optic imaging reveals that astrocyte calcium activity in the mouse cerebral cortex is modulated by internal motivational state," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    5. Per Kristian Eide & Aslan Lashkarivand & Are Pripp & Lars Magnus Valnes & Markus Herberg Hovd & Geir Ringstad & Kaj Blennow & Henrik Zetterberg, 2023. "Plasma neurodegeneration biomarker concentrations associate with glymphatic and meningeal lymphatic measures in neurological disorders," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    6. Xiang He & Daiqin Xiong & Lei Zhao & Jialong Fu & Lingfei Luo, 2024. "Meningeal lymphatic supporting cells govern the formation and maintenance of zebrafish mural lymphatic endothelial cells," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Carolin Beuker & David Schafflick & Jan-Kolja Strecker & Michael Heming & Xiaolin Li & Jolien Wolbert & Antje Schmidt-Pogoda & Christian Thomas & Tanja Kuhlmann & Irene Aranda-Pardos & Noelia A-Gonzal, 2022. "Stroke induces disease-specific myeloid cells in the brain parenchyma and pia," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Chou, Dean & Chen, Po-Yen, 2024. "A machine learning method to explore the glymphatic system via poroelastodynamics," Chaos, Solitons & Fractals, Elsevier, vol. 178(C).
    9. Nicola A. Kearns & Artemis Iatrou & Daniel J. Flood & Sashini Tissera & Zachary M. Mullaney & Jishu Xu & Chris Gaiteri & David A. Bennett & Yanling Wang, 2023. "Dissecting the human leptomeninges at single-cell resolution," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    10. Miao Wang & Congcong Yan & Xi Li & Tianhao Yang & Shengnan Wu & Qian Liu & Qingming Luo & Feifan Zhou, 2024. "Non-invasive modulation of meningeal lymphatics ameliorates ageing and Alzheimer’s disease-associated pathology and cognition in mice," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    11. Gianina Ungurean & Mehdi Behroozi & Leonard Böger & Xavier Helluy & Paul-Antoine Libourel & Onur Güntürkün & Niels C. Rattenborg, 2023. "Wide-spread brain activation and reduced CSF flow during avian REM sleep," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    12. Fushun Wang & Wei Wang & Simeng Gu & Dan Qi & Nathan A. Smith & Weiguo Peng & Wei Dong & Jiajin Yuan & Binbin Zhao & Ying Mao & Peng Cao & Qing Richard Lu & Lee A. Shapiro & S. Stephen Yi & Erxi Wu & , 2023. "Distinct astrocytic modulatory roles in sensory transmission during sleep, wakefulness, and arousal states in freely moving mice," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    13. Hadi Abou-El-Hassan & Rafael M. Rezende & Saef Izzy & Galina Gabriely & Taha Yahya & Bruna K. Tatematsu & Karl J. Habashy & Juliana R. Lopes & Gislane L. V. Oliveira & Amir-Hadi Maghzi & Zhuoran Yin &, 2023. "Vγ1 and Vγ4 gamma-delta T cells play opposing roles in the immunopathology of traumatic brain injury in males," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    14. Shinnosuke Nomura & Shin-Ichiro Terada & Teppei Ebina & Masato Uemura & Yoshito Masamizu & Kenichi Ohki & Masanori Matsuzaki, 2024. "ARViS: a bleed-free multi-site automated injection robot for accurate, fast, and dense delivery of virus to mouse and marmoset cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    15. Josephine A. Mapunda & Javier Pareja & Mykhailo Vladymyrov & Elisa Bouillet & Pauline Hélie & Petr Pleskač & Sara Barcos & Johanna Andrae & Dietmar Vestweber & Donald M. McDonald & Christer Betsholtz , 2023. "VE-cadherin in arachnoid and pia mater cells serves as a suitable landmark for in vivo imaging of CNS immune surveillance and inflammation," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    16. Geir Ringstad & Per Kristian Eide, 2023. "The pitfalls of interpreting hyperintense FLAIR signal as lymph outside the human brain," Nature Communications, Nature, vol. 14(1), pages 1-3, December.
    17. Anastasia Mozokhina & Rostislav Savinkov, 2020. "Mathematical Modelling of the Structure and Function of the Lymphatic System," Mathematics, MDPI, vol. 8(9), pages 1-18, September.
    18. Shinji Naganawa & Yutaka Kato & Tadao Yoshida & Michihiko Sone, 2023. "Fluid signal suppression characteristics of 3D-FLAIR with a T2 selective inversion pulse in the skull base," Nature Communications, Nature, vol. 14(1), pages 1-3, December.
    19. Dongyu Li & Shaojun Liu & Tingting Yu & Zhang Liu & Silin Sun & Denis Bragin & Alexander Shirokov & Nikita Navolokin & Olga Bragina & Zhengwu Hu & Jürgen Kurths & Ivan Fedosov & Inna Blokhina & Alexan, 2023. "Photostimulation of brain lymphatics in male newborn and adult rodents for therapy of intraventricular hemorrhage," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    20. Weiping Dai & Mengqian Yang & Pei Xia & Chuan Xiao & Shuying Huang & Zhan Zhang & Xin Cheng & Wenchang Li & Jian Jin & Jingyun Zhang & Binghuo Wu & Yingying Zhang & Pei-hui Wu & Yangyang Lin & Wen Wu , 2022. "A functional role of meningeal lymphatics in sex difference of stress susceptibility in mice," Nature Communications, Nature, vol. 13(1), pages 1-21, 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:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36643-5. 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: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    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.