IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29622-9.html
   My bibliography  Save this article

CO2 signaling mediates neurovascular coupling in the cerebral cortex

Author

Listed:
  • Patrick S. Hosford

    (University College London)

  • Jack A. Wells

    (University College London)

  • Shereen Nizari

    (University College London)

  • Isabel N. Christie

    (University College London)

  • Shefeeq M. Theparambil

    (University College London)

  • Pablo A. Castro

    (Centro de Estudios Científicos (CECs) & Universidad San Sebastián
    Universidad Austral de Chile)

  • Anna Hadjihambi

    (University College London)

  • L. Felipe Barros

    (Centro de Estudios Científicos (CECs) & Universidad San Sebastián)

  • Iván Ruminot

    (Centro de Estudios Científicos (CECs) & Universidad San Sebastián)

  • Mark F. Lythgoe

    (University College London)

  • Alexander V. Gourine

    (University College London)

Abstract

Neurovascular coupling is a fundamental brain mechanism that regulates local cerebral blood flow (CBF) in response to changes in neuronal activity. Functional imaging techniques are commonly used to record these changes in CBF as a proxy of neuronal activity to study the human brain. However, the mechanisms of neurovascular coupling remain incompletely understood. Here we show in experimental animal models (laboratory rats and mice) that the neuronal activity-dependent increases in local CBF in the somatosensory cortex are prevented by saturation of the CO2-sensitive vasodilatory brain mechanism with surplus of exogenous CO2 or disruption of brain CO2/HCO3− transport by genetic knockdown of electrogenic sodium-bicarbonate cotransporter 1 (NBCe1) expression in astrocytes. A systematic review of the literature data shows that CO2 and increased neuronal activity recruit the same vasodilatory signaling pathways. These results and analysis suggest that CO2 mediates signaling between neurons and the cerebral vasculature to regulate brain blood flow in accord with changes in the neuronal activity.

Suggested Citation

  • Patrick S. Hosford & Jack A. Wells & Shereen Nizari & Isabel N. Christie & Shefeeq M. Theparambil & Pablo A. Castro & Anna Hadjihambi & L. Felipe Barros & Iván Ruminot & Mark F. Lythgoe & Alexander V., 2022. "CO2 signaling mediates neurovascular coupling in the cerebral cortex," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29622-9
    DOI: 10.1038/s41467-022-29622-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29622-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-29622-9?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. Y. Iturria-Medina & R. C. Sotero & P. J. Toussaint & J. M. Mateos-Pérez & A. C. Evans, 2016. "Early role of vascular dysregulation on late-onset Alzheimer’s disease based on multifactorial data-driven analysis," Nature Communications, Nature, vol. 7(1), pages 1-14, September.
    2. David Attwell & Alastair M. Buchan & Serge Charpak & Martin Lauritzen & Brian A. MacVicar & Eric A. Newman, 2010. "Glial and neuronal control of brain blood flow," Nature, Nature, vol. 468(7321), pages 232-243, November.
    3. Alexander V. Gourine & Enrique Llaudet & Nicholas Dale & K. Michael Spyer, 2005. "ATP is a mediator of chemosensory transduction in the central nervous system," Nature, Nature, vol. 436(7047), pages 108-111, July.
    4. Shefeeq M. Theparambil & Patrick S. Hosford & Iván Ruminot & Olga Kopach & James R. Reynolds & Pamela Y. Sandoval & Dmitri A. Rusakov & L. Felipe Barros & Alexander V. Gourine, 2020. "Astrocytes regulate brain extracellular pH via a neuronal activity-dependent bicarbonate shuttle," Nature Communications, Nature, vol. 11(1), pages 1-15, 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. Adam Institoris & Milène Vandal & Govind Peringod & Christy Catalano & Cam Ha Tran & Xinzhu Yu & Frank Visser & Cheryl Breiteneder & Leonardo Molina & Baljit S. Khakh & Minh Dang Nguyen & Roger J. Tho, 2022. "Astrocytes amplify neurovascular coupling to sustained activation of neocortex in awake mice," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Xin Rui Lim & Mohammad M. Abd-Alhaseeb & Michael Ippolito & Masayo Koide & Amanda J. Senatore & Curtis Plante & Ashwini Hariharan & Nick Weir & Thomas A. Longden & Kathryn A. Laprade & James M. Staffo, 2024. "Endothelial Piezo1 channel mediates mechano-feedback control of brain blood flow," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Grant R. Gordon, 2024. "Neurovascular coupling during hypercapnia in cerebral blood flow regulation," Nature Communications, Nature, vol. 15(1), pages 1-3, December.
    4. Marine Tournissac & Emmanuelle Chaigneau & Sonia Pfister & Ali-Kemal Aydin & Yannick Goulam Houssen & Philip O’Herron & Jessica Filosa & Mayeul Collot & Anne Joutel & Serge Charpak, 2024. "Neurovascular coupling and CO2 interrogate distinct vascular regulations," Nature Communications, Nature, vol. 15(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. Marine Tournissac & Emmanuelle Chaigneau & Sonia Pfister & Ali-Kemal Aydin & Yannick Goulam Houssen & Philip O’Herron & Jessica Filosa & Mayeul Collot & Anne Joutel & Serge Charpak, 2024. "Neurovascular coupling and CO2 interrogate distinct vascular regulations," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Lazaro M Sanchez-Rodriguez & Yasser Iturria-Medina & Erica A Baines & Sabela C Mallo & Mehdy Dousty & Roberto C Sotero & on behalf of The Alzheimer’s Disease Neuroimaging Initiative, 2018. "Design of optimal nonlinear network controllers for Alzheimer's disease," PLOS Computational Biology, Public Library of Science, vol. 14(5), pages 1-24, May.
    3. Daniel S. Kluger & Carina Forster & Omid Abbasi & Nikos Chalas & Arno Villringer & Joachim Gross, 2023. "Modulatory dynamics of periodic and aperiodic activity in respiration-brain coupling," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    4. Xin Rui Lim & Mohammad M. Abd-Alhaseeb & Michael Ippolito & Masayo Koide & Amanda J. Senatore & Curtis Plante & Ashwini Hariharan & Nick Weir & Thomas A. Longden & Kathryn A. Laprade & James M. Staffo, 2024. "Endothelial Piezo1 channel mediates mechano-feedback control of brain blood flow," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Minhui Ouyang & John A. Detre & Jessica L. Hyland & Kay L. Sindabizera & Emily S. Kuschner & J. Christopher Edgar & Yun Peng & Hao Huang, 2024. "Spatiotemporal cerebral blood flow dynamics underlies emergence of the limbic-sensorimotor-association cortical gradient in human infancy," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. Shashank Shekhar & Shaoxun Wang & Paige N Mims & Ezekiel Gonzalez-Fernandez & Chao Zhang & Xiaochen He & Catherine Y Liu & Wenshan Lv & Yangang Wang & Juebin Huang & Fan Fan, 2017. "Impaired Cerebral Autoregulation-A Common Neurovascular Pathway in Diabetes may Play a Critical Role in Diabetes-Related Alzheimers Disease," Current Research in Diabetes & Obesity Journal, Juniper Publishers Inc., vol. 2(3), pages 40-45, June.
    7. William A. Mills & AnnaLin M. Woo & Shan Jiang & Joelle Martin & Dayana Surendran & Matthew Bergstresser & Ian F. Kimbrough & Ukpong B. Eyo & Michael V. Sofroniew & Harald Sontheimer, 2022. "Astrocyte plasticity in mice ensures continued endfoot coverage of cerebral blood vessels following injury and declines with age," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    8. Domenic H. Cerri & Daniel L. Albaugh & Lindsay R. Walton & Brittany Katz & Tzu-Wen Wang & Tzu-Hao Harry Chao & Weiting Zhang & Randal J. Nonneman & Jing Jiang & Sung-Ho Lee & Amit Etkin & Catherine N., 2024. "Distinct neurochemical influences on fMRI response polarity in the striatum," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    9. Nicole Haack & Pavel Dublin & Christine R Rose, 2014. "Dysbalance of Astrocyte Calcium under Hyperammonemic Conditions," PLOS ONE, Public Library of Science, vol. 9(8), pages 1-11, August.
    10. E. J. Mathias & M. J. Plank & T. David, 2017. "A model of neurovascular coupling and the BOLD response PART II," Computer Methods in Biomechanics and Biomedical Engineering, Taylor & Francis Journals, vol. 20(5), pages 519-529, April.
    11. Ahmed Faraz Khan & Quadri Adewale & Sue-Jin Lin & Tobias R. Baumeister & Yashar Zeighami & Felix Carbonell & Nicola Palomero-Gallagher & Yasser Iturria-Medina, 2023. "Patient-specific models link neurotransmitter receptor mechanisms with motor and visuospatial axes of Parkinson’s disease," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Stacy A. Hussong & Andy Q. Banh & Candice E. Skike & Angela O. Dorigatti & Stephen F. Hernandez & Matthew J. Hart & Beatriz Ferran & Haneen Makhlouf & Maria Gaczynska & Pawel A. Osmulski & Salome A. M, 2023. "Soluble pathogenic tau enters brain vascular endothelial cells and drives cellular senescence and brain microvascular dysfunction in a mouse model of tauopathy," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Shashank Shekhar & Shaoxun Wang & Paige N Mims & Ezekiel Gonzalez-Fernandez & Chao Zhang & Xiaochen He & Catherine Y Liu & Wenshan Lv & Yangang Wang & Juebin Huang & Fan Fan, 2017. "Impaired Cerebral Autoregulation-A Common Neurovascular Pathway in Diabetes may Play a Critical Role in Diabetes-Related Alzheimer’s Disease," Current Research in Diabetes & Obesity Journal, Juniper Publishers Inc., vol. 2(3), pages 1-6, June.
    14. Fotios Koskeridis & Nurun Fancy & Pei Fang Tan & Devendra Meena & Evangelos Evangelou & Paul Elliott & Dennis Wang & Paul M. Matthews & Abbas Dehghan & Ioanna Tzoulaki, 2024. "Multi-trait association analysis reveals shared genetic loci between Alzheimer’s disease and cardiovascular traits," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    15. Yu, Yangyang & Yuan, Zhixuan & Li, Jiajia & Wu, Ying, 2023. "Dynamic analysis of epileptic seizures caused by energy failure after ischemic stroke," Chaos, Solitons & Fractals, Elsevier, vol. 176(C).
    16. Rita Gil & Mafalda Valente & Noam Shemesh, 2024. "Rat superior colliculus encodes the transition between static and dynamic vision modes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    17. Liza J. Severs & Nicholas E. Bush & Lely A. Quina & Skyler Hidalgo-Andrade & Nicholas J. Burgraff & Tatiana Dashevskiy & Andy Y. Shih & Nathan A. Baertsch & Jan-Marino Ramirez, 2023. "Purinergic signaling mediates neuroglial interactions to modulate sighs," Nature Communications, Nature, vol. 14(1), pages 1-14, 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:13:y:2022:i:1:d:10.1038_s41467-022-29622-9. 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.