Glial and neuronal control of brain blood flow

Attwell, David; Buchan, Alastair M.; Charpak, Serge; Lauritzen, Martin; MacVicar, Brian A.; Newman, Eric A.

doi:10.1038/nature09613

Cited by 2,511Barrier Structure and Function StudiesTraumatic Brain Injury and Neurovascular DisturbancesNeuroscience and Neuropharmacology Research

Glial and neuronal control of brain blood flow

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Attwell, David, Buchan, Alastair M., Charpak, Serge, Lauritzen, Martin, MacVicar, Brian A., Newman, Eric A.·2010·Nature

DOI 10.1038/nature09613PMC PMC3206737

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Abstract

Blood flow in the brain is regulated by neurons and astrocytes. Knowledge of how these cells control blood flow is crucial for understanding how neural computation is powered, for interpreting functional imaging scans of brains, and for developing treatments for neurological disorders. It is now recognized that neurotransmitter-mediated signalling has a key role in regulating cerebral blood flow, that much of this control is mediated by astrocytes, that oxygen modulates blood flow regulation, and that blood flow may be controlled by capillaries as well as by arterioles. These conceptual shifts in our understanding of cerebral blood flow control have important implications for the development of new therapeutic approaches.

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Delivery of energy substrates can be adjusted on demand through modulation of neurovascular coupling or via neuronal signaling to astrocytes.
“This process can be adjusted on demand either through modulation of neurovascular coupling15–17 or via neuronal signaling to astrocytes18.”
From Energy paradox in REM sleep: balancing supply and consumption in brain metabolism (2026) · cites this paper as [16]
As neural activity elevates, local oxygen consumption and demand increases, triggering vasodilation of arterioles and capillaries to increase cerebral blood flow.
“As neural activity elevates, local oxygen consumption and demand increases, triggering vasodilation of arterioles and capillaries to increase cerebral blood flow (124), which supplies oxygenated hemoglobin in excess of the metabolic rate of oxygen consumption (125).”
From Electrophysiological source imaging: A noninvasive window to brain dynamics (2018) · cites this paper as [124]
The cascade of metabolic and vascular events known as neurovascular coupling involves complex signaling among neurons, astrocytes, and the local vasculature and remains a topic of active research.
“Such a cascade of metabolic and vascular events, known as the neurovascular coupling, involves complex signaling among neurons, astrocytes, and the local vasculature (124, 126, 127), and remains a topic of active research enabled by emerging tools (128).”
From Electrophysiological source imaging: A noninvasive window to brain dynamics (2018) · cites this paper as [124]
PVMs are most abundant on pial and parenchymal vessels larger than 20 μm in diameter, especially pial arterioles, and cover 70%-80% of their length.
“PVMs were found most abundantly in association with pial and parenchymal vessels larger than 20 μm in diameter, particularly pial arterioles, a key site for flow regulation (7), the length of which was covered 70%-80% by PVMs (Supplemental Figure 1, A-E; supplemental material available online with this article; doi:10.1172/JCI86950DS1).”
From Perivascular macrophages mediate the neurovascular and cognitive dysfunction associated with hypertension (2016) · cites this paper as [7]

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Iadecola, C., & Zhang, F. (1994) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1994.266.2.r546 · Cited by 117 · see citing works
The Relationship between Blood Flow and Neuronal Activity in the Rodent Olfactory Bulb
Chaigneau, E. M., Tiret, P., Lecoq, J. A., Ducros, M. G., Knöpfel, T., & Charpak, S. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3141-06.2007 · Cited by 110 · see citing works
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Effect of stepped hypoglycemia on regional cerebral blood flow response to physiological brain activation
Powers, W. J., Hirsch, I. B., & Cryer, P. E. (1996) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1996.270.2.h554 · Cited by 103 · see citing works
Expression of COX-2 by Normal and Reactive Astrocytes in the Adult Rat Central Nervous System
Hirst, W. D., Young, K. A., Newton, R. C., Allport, V. C., Marriott, D. R., & Wilkin, G. P. (1999) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1998.0731 · Cited by 102 · see citing works
Persisting depletion of brain glucose following cortical spreading depression, despite apparent hyperaemia: evidence for risk of an adverse effect of Leao's spreading depression
Hashemi, P., Bhatia, R., Nakamura, H., Dreier, J. P., Graf, R., Strong, A. J., & Boutelle, M. G. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2008.108 · Cited by 101 · see citing works
Epoxyeicosatrienoic Acids Function as Selective, Endogenous Antagonists of Native Thromboxane Receptors: Identification of a Novel Mechanism of Vasodilation
Behm, D. J., Ogbonna, A. C., Wu, C. W., Burns-Kurtis, C. L., & Douglas, S. A. (2008) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.108.145102 · Cited by 101 · see citing works
Mechanisms involved in the cerebrovascular dilator effects of N-methyl-d-aspartate in cerebral cortex
Busija, D. W., Bari, F., Domoki, F., & Louis, T. M. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.011 · Cited by 100 · see citing works
Pathway-Specific Variations in Neurovascular and Neurometabolic Coupling in Rat Primary Somatosensory Cortex
Enager, P., Piilgaard, H., Offenhauser, N., Kocharyan, A., Fernandes, P., Hamel, É., & Lauritzen, M. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.23 · Cited by 100 · see citing works
Self-citation
Arginine-nitric oxide pathway and cerebrovascular regulation in cortical spreading depression
Fabricius, M. E., Akgören, N., & Lauritzen, M. (1995) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1995.269.1.h23 · Cited by 100 · see citing works
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Role of cGMP versus 20-HETE in the vasodilator response to nitric oxide in rat cerebral arteries
Sun, C., Falck, J. R., Okamoto, H., Harder, D. R., & Roman, R. J. (2000) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2000.279.1.h339 · Cited by 100 · see citing works
Neurovascular relationships in hippocampal slices: physiological and anatomical studies of mechanisms underlying flow-metabolism coupling in intraparenchymal microvessels
Lovick, T. A., Brown, L. A., & Key, B. J. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00737-4 · Cited by 99 · see citing works
Mechanism of CO2 response in cerebral arteries of the newborn pig: role of phospholipase, cyclooxygenase, and lipoxygenase pathways.
Wagerle, L. C., & Mishra, O. P. (1988) · Circulation Research · doi:10.1161/01.res.62.5.1019 · Cited by 97 · see citing works
Key role of tissue plasminogen activator in neurovascular coupling
Park, L., Gallo, E. F., Anrather, J., Wang, G., Norris, E. H., Paul, J., Strickland, S., & Iadecola, C. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708823105 · Cited by 96 · see citing works
Neurovascular Coupling in Rat Brain Operates Independent of Hemoglobin Deoxygenation
Lindauer, U., Leithner, C., Kaasch, H., Rohrer, B., Foddis, M., Füchtemeier, M., Offenhauser, N., Steinbrink, J. M., Royl, G., Kohl‐Bareis, M., et al. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.259 · Cited by 95 · see citing works
Neurovascular Coupling Is Not Mediated by Potassium Siphoning from Glial Cells
Metea, M. R., Kofuji, P., & Newman, E. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3204-06.2007 · Cited by 93 · see citing works
Self-citation
Mechanisms involved in the cerebrovascular dilator effects of cortical spreading depression
Busija, D. W., Bari, F., Domoki, F., Horiguchi, T., & SHIMIZU, K. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2008.09.008 · Cited by 93 · see citing works
Putative Cyclooxygenase-3 Expression in Rat Brain Cells
Kis, B., Snipes, J. A., Isse, T., Nagy, K. A., & Busija, D. W. (2003) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/01.wcb.0000090681.07515.81 · Cited by 92 · see citing works
Nitric oxide is the predominant mediator of cerebellar hyperemia during somatosensory activation in rats
Yang, G., Chen, G., Ebner, T. J., & Iadecola, C. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.277.6.r1760 · Cited by 90 · see citing works
Nitric oxide and adenosine mediate vasodilation during functional activation in cerebellar cortex
Li, J., & Iadecola, C. (1994) · Neuropharmacology · doi:10.1016/0028-3908(94)90049-3 · Cited by 89 · see citing works
Magnetic Resonance Studies of Brain Function and Neurochemistry
Uǧurbil, K., Adriany, G., Andersen, P., Chen, W., Rolf Gruetter, A., Hu, X. P., Merkle, H., Kim, D., Kim, S., Strupp, J., et al. (2000) · Annual Review of Biomedical Engineering · doi:10.1146/annurev.bioeng.2.1.633 · Cited by 88 · see citing works
Pharmacological Uncoupling of Activation Induced Increases in CBF and CMRO 2
Leithner, C., Royl, G., Offenhauser, N., Füchtemeier, M., Kohl‐Bareis, M., Villringer, A., Dirnagl, U., & Lindauer, U. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.211 · Cited by 86 · see citing works
Dependency of Cortical Functional Hyperemia to Forepaw Stimulation on Epoxygenase and Nitric Oxide Synthase Activities in Rats
Peng, X., Zhang, C., Alkayed, N. J., Harder, D. R., & Koehler, R. C. (2004) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200405000-00004 · Cited by 85 · see citing works
NADH: sensor of blood flow need in brain, muscle, and other tissues
Ido, Y., Chang, K. C., Woolsey, T. A., & Williamson, J. R. (2001) · The FASEB Journal · doi:10.1096/fj.00-0652fje · Cited by 85 · see citing works
Nonlinear Neurovascular Coupling in Rat Sensory Cortex by Activation of Transcallosal Fibers
Hoffmeyer, H. W., Enager, P., Thomsen, K. J., & Lauritzen, M. (2006) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600372 · Cited by 84 · see citing works
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Capillary Flow and Diameter Changes during Reperfusion after Global Cerebral Ischemia Studied by Intravital Video Microscopy
Hauck, E. F., Apostel, S., Hoffmann, J. F., Heimann, A., & Kempski, O. S. (2004) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200404000-00003 · Cited by 82 · see citing works
Odor-Evoked Oxygen Consumption by Action Potential and Synaptic Transmission in the Olfactory Bulb
Lecoq, J. A., Tiret, P., Najac, M., Shepherd, G. M., Greer, C. A., & Charpak, S. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4817-08.2009 · Cited by 80 · see citing works
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Role of Extracellular and Intracellular Acidosis for Hypercapnia-Induced Inhibition of Tension of Isolated Rat Cerebral Arteries
Tian, R., Vogel, P., Lassen, N. A., Mulvany, M. J., Andreasen, F., & Aalkjær, C. (1995) · Circulation Research · doi:10.1161/01.res.76.2.269 · Cited by 79 · see citing works
Change of cerebrovascular reactivity after cortical spreading depression in cats and rats
Wahl, M., Lauritzen, M., & Schilling, L. (1987) · Brain Research · doi:10.1016/0006-8993(87)90682-2 · Cited by 77 · see citing works
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Attenuation of activity-induced increases in cerebellar blood flow in mice lacking neuronal nitric oxide synthase
Yang, G., Zhang, Y., Ross, M. E., & Iadecola, C. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00043.2003 · Cited by 74 · see citing works
Cerebral circulatory responses to hypercapnia and hypoxia in the recovery period following complete and incomplete cerebral ischemia in the rat
Kågström, E., Smith, M., & Siesjö, B. K. (1983) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1983.tb07272.x · Cited by 73 · see citing works
Cerebral blood flow increases evoked by electrical stimulation of rat cerebellar cortex: relation to excitatory synaptic activity and nitric oxide synthesis
Akgören, N., Dalgaard, P., & Lauritzen, M. (1996) · Brain Research · doi:10.1016/0006-8993(95)01354-7 · Cited by 71 · see citing works
Self-citation
Rapid Rise of Extracellular pH Evoked by Neural Activity Is Generated by the Plasma Membrane Calcium ATPase
Makani, S., & Chesler, M. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00948.2009 · Cited by 69 · see citing works
Measuring the effects of indomethacin on changes in cerebral oxidative metabolism and cerebral blood flow during sensorimotor activation
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Cerebral autoregulation and gas exchange studied using a human cardiopulmonary model
Lu, K., Clark, J. W., Ghorbel, F. H., Robertson, C. S., Ware, D. L., Zwischenberger, J. B., & Bidani, A. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00594.2003 · Cited by 63 · see citing works
Effects of ischemia on brain blood flow and oxygen consumption of newborn pigs
Leffler, C. W., Busija, D. W., Mirro, R., Armstead, W. M., & Beasley, D. G. (1989) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1989.257.6.h1917 · Cited by 61 · see citing works
Evidence Against H + and K + as main Factors for the Control of Cerebral Blood Flow: A Microelectrode Study
Astrup, J., Heuser, D., Lassen, N. A., Nilsson, B., Norberg, K., & Siesjd, B. K. (1978) · Novartis Foundation symposium · doi:10.1002/9780470720370.ch16 · Cited by 61 · see citing works
Nitric Oxide and Prostanoids Participate in Cerebral Vasodilation Elicited by Electrical Stimulation of the Rostral Ventrolateral Medulla
Golanov, E. V., & Reis, D. J. (1994) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1994.61 · Cited by 59 · see citing works
AMINO ACID RELEASE FROM THE CEREBRAL CORTEX DURING SPREADING DEPRESSION AND ASPHYXIATION*
Harreveld, A. V., & Kooiman, M. (1965) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1965.tb04243.x · Cited by 54 · see citing works
Assessing the physiological concentration and targets of nitric oxide in brain tissue
Hall, C. N., & Attwell, D. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.154724 · Cited by 52 · see citing works
Self-citation
Postischemic Attenuation of Cerebral Artery Reactivity Is Increased in the Presence of Tissue Plasminogen Activator
Cipolla, M. J., Lessov, N. S., & Clark, W. M. (2000) · Stroke · doi:10.1161/01.str.31.4.940 · Cited by 50 · see citing works
The No-Reflow Phenomenon
Galiuto, L., Rebuzzi, A. G., & Crea, F. (2009) · JACC. Cardiovascular imaging · doi:10.1016/j.jcmg.2008.11.003 · Cited by 50 · see citing works
Dose dependent effects of reactive oxygen and nitrogen species on the function of neuronal nitric oxide synthase
Sun, J., Druhan, L. J., & Zweier, J. L. (2008) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2008.01.003 · Cited by 47 · see citing works
Gross Persistence of Capillary Plasma Perfusion after Middle Cerebral Artery Occlusion in the Rat Brain
Theilen, H., Schröck, H., & Kuschinsky, W. (1994) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1994.138 · Cited by 47 · see citing works
Modification of activity‐dependent increases in cerebellar blood flow by extracellular potassium in anaesthetized rats
Caesar, K., Akgören, N., Mathiesen, C., & Lauritzen, M. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.00281.x · Cited by 45 · see citing works
Self-citation
Nitric oxide synthase inhibition does not affect somatosensory evoked potentials in the rat
Lindauer, U., Megow, D., Schultze, J., Weber, J. R., & Dirnagl, U. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)13044-5 · Cited by 45 · see citing works
Effects of reactive oxygen and nitrogen species on cyclooxygenase-1 and -2 activities
Fujimoto, Y., Uno, E., & Sakuma, S. (2004) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2004.06.002 · Cited by 44 · see citing works
Affinities of various mammalian arachidonate lipoxygenases and cyclooxygenases for molecular oxygen as substrate
Juránek, I., Suzuki, H., & Yamamoto, S. (1999) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/s0005-2760(98)00159-3 · Cited by 44 · see citing works
Impaired cerebrovascular reactivity after cortical spreading depression in rats: Restoration by nitric oxide or cGMP
Scheckenbach, K. E. L., Dreier, J. P., Dirnagl, U., & Lindauer, U. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.07.007 · Cited by 34 · see citing works
The cortical energy needed for conscious perception
Schölvinck, M. L., Howarth, C., & Attwell, D. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.01.032 · Cited by 33 · see citing works
Self-citation
Laminar analysis of activity-dependent increases of CBF in rat cerebellar cortex: dependence on synaptic strength
Akgören, N., Mathiesen, C., Rubin, I., & Lauritzen, M. (1997) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1997.273.3.h1166 · Cited by 28 · see citing works
Self-citation
Adrenomedullin-induced relaxation of rat brain pericytes is related to the reduced phosphorylation of myosin light chain through the cAMP/PKA signaling pathway
Takata, F., Dohgu, S., Nishioku, T., Takahashi, H., Harada, E., Makino, I., Nakashima, M., Yamauchi, A., & Kataoka, Y. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.10.082 · Cited by 24 · see citing works
Ca2+‐ and thromboxane‐dependent distribution of MaxiK channels in cultured astrocytes: From microtubules to the plasma membrane
Ou, J. W., Kumar, Y., Alioua, A., Sailer, C. A., Stefani, E., & Toro, L. (2009) · Glia · doi:10.1002/glia.20847 · Cited by 20 · see citing works
Altered NO Function Contributes to Impairment of uPA and tPA Cerebrovasodilation after Brain Injury
Armstead, W. M., Cines, D. B., & Higazi, A. A. (2004) · Journal of Neurotrauma · doi:10.1089/neu.2004.21.1204 · Cited by 18 · see citing works
Effects of prostaglandins E1 and E2 on cultured smooth muscle cells and strips of rat aorta
Serebryakov, V. N., Zakharenko, S. S., Snetkov, V. A., & Takeda, K. (1994) · Prostaglandins · doi:10.1016/0090-6980(94)90053-1 · Cited by 17 · see citing works

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The blood-brain barrier
Daneman, R., & Prat, A. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020412 · Cited by 3,437 · see citing works
Neuroinflammation and microglial activation in Alzheimer disease: where do we go from here?
Leng, F., & Edison, P. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-020-00435-y · Cited by 3,179 · see citing works
Pericytes: Developmental, Physiological, and Pathological Perspectives, Problems, and Promises
Armulik, A., Genové, G., & Betsholtz, C. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.07.001 · Cited by 2,653 · see citing works
The Neurovascular Unit Coming of Age: A Journey through Neurovascular Coupling in Health and Disease
Iadecola, C. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.030 · Cited by 2,480 · see citing works
Brain energy metabolism: focus on Astrocyte-neuron metabolic cooperation
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Purification and Characterization of Progenitor and Mature Human Astrocytes Reveals Transcriptional and Functional Differences with Mouse
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Capillary pericytes regulate cerebral blood flow in health and disease
Hall, C. N., Reynell, C., Gesslein, B., Hamilton, N. B., Mishra, A., Sutherland, B. A., O’Farrell, F. M., Buchan, A. M., Lauritzen, M., & Attwell, D. (2014) · Nature · doi:10.1038/nature13165 · Cited by 1,870 · see citing works
Self-citation
Synaptic Energy Use and Supply
Harris, J. J., Jolivet, R., & Attwell, D. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.019 · Cited by 1,747 · see citing works
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Physiology of Astroglia
Verkhratsky, A., & Nedergaard, M. (2018) · Physiological Reviews · doi:10.1152/physrev.00042.2016 · Cited by 1,678 · see citing works
Establishment and Dysfunction of the Blood-Brain Barrier
Zhao, Z., Nelson, A. R., Betsholtz, C., & Zlokovic, B. V. (2015) · Cell · doi:10.1016/j.cell.2015.10.067 · Cited by 1,670 · see citing works
Sugar for the brain: the role of glucose in physiological and pathological brain function
Mergenthaler, P., Lindauer, U., Dienel, G. A., & Meisel, A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.07.001 · Cited by 1,612 · see citing works
Reactive Gliosis and the Multicellular Response to CNS Damage and Disease
Burda, J. E., & Sofroniew, M. V. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.034 · Cited by 1,431 · see citing works
Transfer of mitochondria from astrocytes to neurons after stroke
Hayakawa, K., Esposito, E., Wang, X., Terasaki, Y., Liu, Y., Xing, C., Ji, X., & Lo, E. H. (2016) · Nature · doi:10.1038/nature18928 · Cited by 1,423 · see citing works
Gliotransmitters Travel in Time and Space
Araque, A., Carmignoto, G., Haydon, P. G., Oliet, S. H. R., Robitaille, R., & Volterra, A. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.007 · Cited by 1,308 · see citing works
A Cellular Perspective on Brain Energy Metabolism and Functional Imaging
Magistretti, P. J., & Allaman, I. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.035 · Cited by 1,285 · see citing works
Cerebral blood flow regulation and neurovascular dysfunction in Alzheimer disease
Kisler, K., Nelson, A. R., Montagne, A., & Zlokovic, B. V. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.48 · Cited by 1,243 · see citing works
Diversity of astrocyte functions and phenotypes in neural circuits
Khakh, B. S., & Sofroniew, M. V. (2015) · Nature Neuroscience · doi:10.1038/nn.4043 · Cited by 1,239 · see citing works
The progress in understanding and treatment of diabetic retinopathy
Stitt, A. W., Curtis, T. M., Chen, M., Medina, R. J., McKay, G. J., Jenkins, A. J., Gardiner, T. A., Lyons, T. J., Hammes, H., Simó, R., et al. (2015) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2015.08.001 · Cited by 1,178 · see citing works
Pericytes of the neurovascular unit: key functions and signaling pathways
Sweeney, M. D., Ayyadurai, S., & Zlokovic, B. V. (2016) · Nature Neuroscience · doi:10.1038/nn.4288 · Cited by 1,125 · see citing works
Innate immunity in the central nervous system
Ransohoff, R. M., & Brown, M. A. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58644 · Cited by 1,034 · see citing works
Astrocyte calcium signaling: the third wave
Bazargani, N., & Attwell, D. (2016) · Nature Neuroscience · doi:10.1038/nn.4201 · Cited by 949 · see citing works
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Integrative regulation of human brain blood flow
Willie, C. K., Tzeng, Y., Fisher, J. A., & Ainslie, P. N. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2013.268953 · Cited by 879 · see citing works
The many faces of insulin-like peptide signalling in the brain
Fernandez, A. M., & Torres-Alemán, I. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3209 · Cited by 872 · see citing works
A neurocentric perspective on glioma invasion
Cuddapah, V. A., Robel, S., Watkins, S., & Sontheimer, H. W. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3765 · Cited by 826 · see citing works
Multi-sensory Gamma Stimulation Ameliorates Alzheimer’s-Associated Pathology and Improves Cognition
Martorell, A. J., Paulson, A. L., Suk, H.-J., Abdurrob, F., Drummond, G. T., Guan, W., Young, J. Z., Kim, D. N.-W., Kritskiy, O., Barker, S. J., et al. (2019) · Cell · doi:10.1016/j.cell.2019.02.014 · Cited by 798 · see citing works
The blood–brain barrier in health and disease
Daneman, R. (2012) · Annals of Neurology · doi:10.1002/ana.23648 · Cited by 756 · see citing works
Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease
Kur, J., Newman, E. A., & Chan‐Ling, T. (2012) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2012.04.004 · Cited by 685 · see citing works
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Astrocytes and disease: a neurodevelopmental perspective
Molofsky, A. V., Krenick, R., Ullian, E., Tsai, H.-H., Deneen, B., Richardson, W. D., Barres, B. A., & Rowitch, D. H. (2012) · Genes & Development · doi:10.1101/gad.188326.112 · Cited by 682 · see citing works
Ongoing Cortical Activity at Rest: Criticality, Multistability, and Ghost Attractors
Deco, G., & Jirsa, V. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2523-11.2012 · Cited by 680 · see citing works
The dual role of astrocyte activation and reactive gliosis
Pekny, M., Wilhelmsson, U., & Pekna, M. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2013.12.071 · Cited by 666 · see citing works
The blood-brain barrier: an engineering perspective
Wong, A. D., Ye, M., Levy, A. F., Rothstein, J. D., Bergles, D. E., & Searson, P. C. (2013) · Frontiers in Neuroengineering · doi:10.3389/fneng.2013.00007 · Cited by 662 · see citing works
Revisiting the neurovascular unit
Schaeffer, S. M., & Iadecola, C. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00904-7 · Cited by 654 · see citing works
What is a pericyte?
Attwell, D., Mishra, A., Hall, C. N., O’Farrell, F. M., & Dalkara, T. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x15610340 · Cited by 648 · see citing works
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Glial responses to implanted electrodes in the brain
Salatino, J. W., Ludwig, K. A., Kozai, T. D. Y., & Purcell, E. K. (2017) · Nature Biomedical Engineering · doi:10.1038/s41551-017-0154-1 · Cited by 642 · see citing works
Activity-Regulated Transcription: Bridging the Gap between Neural Activity and Behavior
Yap, E.-L., & Greenberg, M. E. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.013 · Cited by 626 · see citing works
Brain Tissue Responses to Neural Implants Impact Signal Sensitivity and Intervention Strategies
Kozai, T. D. Y., Jaquins-Gerstl, A. S., Vazquez, A. L., Michael, A. C., & Cui, X. T. (2015) · ACS Chemical Neuroscience · doi:10.1021/cn500256e · Cited by 622 · see citing works
Coupling Mechanism and Significance of the BOLD Signal: A Status Report
Hillman, E. M. C. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071013-014111 · Cited by 615 · see citing works
Astroglial Kir4.1 in the lateral habenula drives neuronal bursts in depression
Cui, Y., Yang, Y., Ni, Z., Dong, Y., Cai, G., Foncelle, A., Ma, S., Sang, K., Tang, S., Li, Y., et al. (2018) · Nature · doi:10.1038/nature25752 · Cited by 597 · see citing works
Astrocytes, therapeutic targets for neuroprotection and neurorestoration in ischemic stroke
Liu, Z., & Chopp, M. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.09.008 · Cited by 596 · see citing works
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Authors: Attwell, D., Buchan, A. M., Charpak, S., Lauritzen, M., MacVicar, B. A., & Newman, E. A.
Affiliations: University College London (GB)
John Radcliffe Hospital (GB)
Centre National de la Recherche Scientifique (FR)
University of Copenhagen (DK)
University of British Columbia (CA)
University of Minnesota (US)
ORCID: Attwell, David
Buchan, Alastair M.
Charpak, Serge
Lauritzen, Martin
MacVicar, Brian A.
Newman, Eric A.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2010-11-10
Volume: 468
Issue: 7321
Pages: 232-243
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature09613
PMC: PMC3206737
OpenAlex: W2163234334
Cited by: 2,511
References: 135
Citations by year: 2026: 144 · 2025: 163 · 2024: 163 · 2023: 147 · 2022: 176 · 2021: 197 · 2020: 180 · 2019: 177 · 2018: 177 · 2017: 172 · 2016: 156 · 2015: 174 · 2014: 146 · 2013: 147 · 2012: 120
FWCI: 9.04
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
UCL Discovery (University College London) (submittedVersion)
Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
Funders: Wellcome Trust
Canadian Institutes of Health Research
National Eye Institute (R01EY004077, P30EY011374)
Topics: Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: cerebral autoregulation, astrocytes, neurons, neurotransmitter signalling, oxygen sensing, capillary blood flow, arterioles, neurovascular coupling, functional neuroimaging, neurological disorders
MeSH terms: Alzheimer Disease, Brain, Brain Ischemia, Cerebrovascular Circulation, Humans, Neuroglia, Neurons, Nitric Oxide, Oxygen, Signal Transduction, Neurotransmitter Agents

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