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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
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    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
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    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.

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