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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
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    References listed on IDEAS

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    1. 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.
    2. 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.
    3. 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.
    4. 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.
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    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. Grant R. Gordon, 2024. "Neurovascular coupling during hypercapnia in cerebral blood flow regulation," Nature Communications, Nature, vol. 15(1), pages 1-3, December.
    3. 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.

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