Brain metabolism dictates the polarity of astrocyte control over arterioles (original) (raw)

References

  1. Mukamel, R. et al. Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science 309, 951–954 (2005)
    Article ADS CAS Google Scholar
  2. Zonta, M. et al. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nature Neurosci. 6, 43–50 (2003)
    Article CAS Google Scholar
  3. Schummers, J., Yu, H. & Sur, M. Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320, 1638–1643 (2008)
    Article ADS CAS Google Scholar
  4. Simard, M., Arcuino, G., Takano, T., Liu, Q. S. & Nedergaard, M. Signaling at the gliovascular interface. J. Neurosci. 23, 9254–9262 (2003)
    Article CAS Google Scholar
  5. Mulligan, S. J. & MacVicar, B. A. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431, 195–199 (2004)
    Article ADS CAS Google Scholar
  6. Metea, M. R. & Newman, E. A. Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J. Neurosci. 26, 2862–2870 (2006)
    Article CAS Google Scholar
  7. Chuquet, J., Hollender, L. & Nimchinsky, E. A. High-resolution in vivo imaging of the neurovascular unit during spreading depression. J. Neurosci. 27, 4036–4044 (2007)
    Article CAS Google Scholar
  8. Filosa, J. A., Bonev, A. D. & Nelson, M. T. Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling. Circ. Res. 95, e73–e81 (2004)
    Article CAS Google Scholar
  9. Takano, T. et al. Astrocyte-mediated control of cerebral blood flow. Nature Neurosci. 9, 260–267 (2006)
    Article CAS Google Scholar
  10. Filosa, J. A. et al. Local potassium signaling couples neuronal activity to vasodilation in the brain. Nature Neurosci. 9, 1397–1403 (2006)
    Article CAS Google Scholar
  11. Mintun, M. A., Vlassenko, A. G., Rundle, M. M. & Raichle, M. E. Increased lactate/pyruvate ratio augments blood flow in physiologically activated human brain. Proc. Natl Acad. Sci. USA 101, 659–664 (2004)
    Article ADS CAS Google Scholar
  12. Ido, Y., Chang, K. & Williamson, J. R. NADH augments blood flow in physiologically activated retina and visual cortex. Proc. Natl Acad. Sci. USA 101, 653–658 (2004)
    Article ADS CAS Google Scholar
  13. Vlassenko, A. G., Rundle, M. M., Raichle, M. E. & Mintun, M. A. Regulation of blood flow in activated human brain by cytosolic NADH/NAD+ ratio. Proc. Natl Acad. Sci. USA 103, 1964–1969 (2006)
    Article ADS CAS Google Scholar
  14. Kasischke, K. A., Vishwasrao, H. D., Fisher, P. J., Zipfel, W. R. & Webb, W. W. Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305, 99–103 (2004)
    Article ADS CAS Google Scholar
  15. Vanzetta, I. & Grinvald, A. Increased cortical oxidative metabolism due to sensory stimulation: implications for functional brain imaging. Science 286, 1555–1558 (1999)
    Article CAS Google Scholar
  16. Ances, B. M., Buerk, D. G., Greenberg, J. H. & Detre, J. A. Temporal dynamics of the partial pressure of brain tissue oxygen during functional forepaw stimulation in rats. Neurosci. Lett. 306, 106–110 (2001)
    Article CAS Google Scholar
  17. Offenhauser, N., Thomsen, K., Caesar, K. & Lauritzen, M. Activity-induced tissue oxygenation changes in rat cerebellar cortex: interplay of postsynaptic activation and blood flow. J. Physiol. 565, 279–294 (2005)
    Article CAS Google Scholar
  18. Malonek, D. et al. Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc. Natl Acad. Sci. USA 94, 14826–14831 (1997)
    Article ADS CAS Google Scholar
  19. Devor, A. et al. Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity. Proc. Natl Acad. Sci. USA 102, 3822–3827 (2005)
    Article ADS CAS Google Scholar
  20. Fox, P. T. & Raichle, M. E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl Acad. Sci. USA 83, 1140–1144 (1986)
    Article ADS CAS Google Scholar
  21. Fox, P. T., Raichle, M. E., Mintun, M. A. & Dence, C. Nonoxidative glucose consumption during focal physiologic neural activity. Science 241, 462–464 (1988)
    Article ADS CAS Google Scholar
  22. Hu, Y. & Wilson, G. S. A temporary local energy pool coupled to neuronal activity: fluctuations of extracellular lactate levels in rat brain monitored with rapid-response enzyme-based sensor. J. Neurochem. 69, 1484–1490 (1997)
    Article CAS Google Scholar
  23. Pellerin, L. & Magistretti, P. J. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl Acad. Sci. USA 91, 10625–10629 (1994)
    Article ADS CAS Google Scholar
  24. Hein, T. W., Xu, W. & Kuo, L. Dilation of retinal arterioles in response to lactate: role of nitric oxide, guanylyl cyclase, and ATP-sensitive potassium channels. Invest. Ophthalmol. Vis. Sci. 47, 693–699 (2006)
    Article Google Scholar
  25. Yamanishi, S., Katsumura, K., Kobayashi, T. & Puro, D. G. Extracellular lactate as a dynamic vasoactive signal in the rat retinal microvasculature. Am. J. Physiol. Heart Circ. Physiol. 290, H925–H934 (2006)
    Article CAS Google Scholar
  26. Devor, A. et al. Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal. J. Neurosci. 27, 4452–4459 (2007)
    Article CAS Google Scholar
  27. Ellis-Davies, G. C. Caged compounds: photorelease technology for control of cellular chemistry and physiology. Nature Methods 4, 619–628 (2007)
    Article CAS Google Scholar
  28. Chan, B. S., Endo, S., Kanai, N. & Schuster, V. L. Identification of lactate as a driving force for prostanoid transport by prostaglandin transporter PGT. Am. J. Physiol. Renal Physiol. 282, F1097–F1102 (2002)
    Article CAS Google Scholar
  29. Wender, R. et al. Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J. Neurosci. 20, 6804–6810 (2000)
    Article CAS Google Scholar
  30. Chance, B., Cohen, P., Jobsis, F. & Schoener, B. Intracellular oxidation-reduction states in vivo. Science 137, 499–508 (1962)
    Article ADS CAS Google Scholar
  31. Nimmerjahn, A., Kirchhoff, F., Kerr, J. N. & Helmchen, F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nature Methods 1, 31–37 (2004)
    Article CAS Google Scholar
  32. Frenguelli, B. G., Llaudet, E. & Dale, N. High-resolution real-time recording with microelectrode biosensors reveals novel aspects of adenosine release during hypoxia in rat hippocampal slices. J. Neurochem. 86, 1506–1515 (2003)
    Article CAS Google Scholar
  33. Brust, T. B., Cayabyab, F. S., Zhou, N. & MacVicar, B. A. p38 mitogen-activated protein kinase contributes to adenosine A1 receptor-mediated synaptic depression in area CA1 of the rat hippocampus. J. Neurosci. 26, 12427–12438 (2006)
    Article CAS Google Scholar
  34. Murphy, K. et al. Adenosine-A2a receptor down-regulates cerebral smooth muscle L-type Ca2+ channel activity via protein tyrosine phosphatase, not cAMP-dependent protein kinase. Mol. Pharmacol. 64, 640–649 (2003)
    Article CAS Google Scholar
  35. Chi, Y., Khersonsky, S. M., Chang, Y. T. & Schuster, V. L. Identification of a new class of prostaglandin transporter inhibitors and characterization of their biological effects on prostaglandin E2 transport. J. Pharmacol. Exp. Ther. 316, 1346–1350 (2006)
    Article CAS Google Scholar
  36. Chan, B. S., Satriano, J. A., Pucci, M. & Schuster, V. L. Mechanism of prostaglandin E2 transport across the plasma membrane of HeLa cells and Xenopus oocytes expressing the prostaglandin transporter ‘PGT’. J. Biol. Chem. 273, 6689–6697 (1998)
    Article CAS Google Scholar
  37. Fox, P. T. & Raichle, M. E. Stimulus rate dependence of regional cerebral blood flow in human striate cortex, demonstrated by positron emission tomography. J. Neurophysiol. 51, 1109–1120 (1984)
    Article CAS Google Scholar
  38. Kleinfeld, D., Mitra, P. P., Helmchen, F. & Denk, W. Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc. Natl Acad. Sci. USA 95, 15741–15746 (1998)
    Article ADS CAS Google Scholar
  39. Chaigneau, E. et al. The relationship between blood flow and neuronal activity in the rodent olfactory bulb. J. Neurosci. 27, 6452–6460 (2007)
    Article CAS Google Scholar
  40. Cauli, B. et al. Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J. Neurosci. 24, 8940–8949 (2004)
    Article CAS Google Scholar
  41. Peppiatt, C. M., Howarth, C., Mobbs, P. & Attwell, D. Bidirectional control of CNS capillary diameter by pericytes. Nature 443, 700–704 (2006)
    Article ADS CAS Google Scholar
  42. D’Agostino, D. P., Putnam, R. W. & Dean, J. B. Superoxide (·O2-) production in CA1 neurons of rat hippocampal slices exposed to graded levels of oxygen. J. Neurophysiol. 98, 1030–1041 (2007)
    Article Google Scholar
  43. Xu, C., Zipfel, W., Shear, J. B., Williams, R. M. & Webb, W. W. Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy. Proc. Natl Acad. Sci. USA 93, 10763–10768 (1996)
    Article ADS CAS Google Scholar
  44. Denk, W. Two-photon scanning photochemical microscopy: mapping ligand-gated ion channel distributions. Proc. Natl Acad. Sci. USA 91, 6629–6633 (1994)
    Article ADS CAS Google Scholar
  45. Klaidman, L. K., Leung, A. C. & Adams, J. D. High-performance liquid chromatography analysis of oxidized and reduced pyridine dinucleotides in specific brain regions. Anal. Biochem. 228, 312–317 (1995)
    Article CAS Google Scholar
  46. Vishwasrao, H. D., Heikal, A. A., Kasischke, K. A. & Webb, W. W. Conformational dependence of intracellular NADH on metabolic state revealed by associated fluorescence anisotropy. J. Biol. Chem. 280, 25119–25126 (2005)
    Article CAS Google Scholar
  47. Sorg, O. & Magistretti, P. J. Characterization of the glycogenolysis elicited by vasoactive intestinal peptide, noradrenaline and adenosine in primary cultures of mouse cerebral cortical astrocytes. Brain Res. 563, 227–233 (1991)
    Article CAS Google Scholar
  48. Brown, A. M. & Ransom, B. R. Astrocyte glycogen and brain energy metabolism. Glia 55, 1263–1271 (2007)
    Article Google Scholar
  49. Ryu, J. K. et al. Microglial activation and cell death induced by the mitochondrial toxin 3-nitropropionic acid: in vitro and in vivo studies. Neurobiol. Dis. 12, 121–132 (2003)
    Article CAS Google Scholar

Download references