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Frontiers in Neuroenergetics ·

Volume 2 - 2010 | https://doi.org/10.3389/fnene.2010.00016

Vascular Tone and Neurovascular Coupling: Considerations Toward an Improved In Vitro Model

  • Jessica A. Filosa1*corresponding author
  1. 1 Department of Physiology, Medical College of Georgia Augusta, GA, USA
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Abstract

Neurovascular research has made significant strides toward understanding how the brain neurovascular unit accomplishes rapid and spatial increases in blood flow following neuronal activation. Among the experimental models used, the in vitro brain slice preparation provides unique information revealing the potential signals and cellular mechanisms involved in functional hyperemia. The most crucial limitation of this model, however, is the lack of intraluminal pressure and flow in the vessels being studied. Moreover, differences in basal vascular tone have led to varied interpretations regarding the polarity of vascular responses following neuron-to-glial stimulation. Given the complexity of astrocyte-induced neurovascular responses, we propose the use of a modified in vitro brain slice preparation, where intraluminal arteriolar pressure and flow are retained. Throughout this review, we discuss the advantages and disadvantages to be considered when using brain slices for neurovascular studies. Potential ways to overcome the current limitations are proposed.

Keywords

References

  1. Aguado F., Espinosa-Parrilla J. F., Carmona M. A., Soriano E. (2002). Neuronal activity regulates correlated network properties of spontaneous calcium transients in astrocytes in situ. J. Neurosci. 22, 9430 – 9444.
  2. Alonso-Galicia M., Drummond H. A., Reddy K. K., Falck J. R., Roman R. J. (1997). Inhibition of 20-HETE production contributes to the vascular responses to nitric oxide. Hypertension 29, 320 – 325.
  3. Anderson C. M., Bergher J. P., Swanson R. A. (2004). ATP-induced ATP release from astrocytes. J. Neurochem. 88, 246 – 256. doi:10.1111/j.1471-4159.2004.02204.x
  4. Andresen J., Shafi N. I., Bryan R. M. Jr. (2006). Endothelial influences on cerebrovascular tone. J. Appl. Physiol. 100, 318 – 327. doi:10.1152/japplphysiol.00937.2005
  5. Bal-Price A., Moneer Z., Brown G. C. (2002). Nitric oxide induces rapid, calcium-dependent release of vesicular glutamate and ATP from cultured rat astrocytes. Glia 40, 312 – 323.
  6. Blanco V. M., Stern J. E., Filosa J. A. (2008). Tone-dependent vascular responses to astrocyte-derived signals. Am. J. Physiol. Heart Circ. Physiol. 294, H2855 – 2863. doi:10.1152/ajpheart.91451.2007
  7. Brahma B., Forman R. E., Stewart E. E., Nicholson C., Rice M. E. (2000). Ascorbate inhibits edema in brain slices. J. Neurochem. 74, 1263 – 1270. doi:10.1046/j.1471-4159.2000.741263.x
  8. Brayden J. E., Earley S., Nelson M. T., Reading S. (2008). Transient receptor potential (TRP) channels, vascular tone and autoregulation of cerebral blood flow. Clin. Exp. Pharmacol. Physiol. 35, 1116 – 1120. doi:10.1111/j.1440-1681.2007.04855.x
  9. Brown L. A., Key B. J., Lovick T. A. (2000). Fluorescent imaging of nitric oxide production in neuronal varicosities associated with intraparenchymal arterioles in rat hippocampal slices. Neurosci. Lett. 294, 9 – 12. doi:10.1016/S0304-3940(00)01521-4
  10. Carmignoto G., Gomez-Gonzalo M. (2009). The contribution of astrocyte signaling to neurovascular coupling. Brain Res Rev.
  11. Casellas D., Moore L. C. (2003). The juxtamedullary nephron preparation. Methods Mol. Med. 86, 413 – 427.
  12. Casellas D., Navar L. G. (1984). In vitro perfusion of juxtamedullary nephrons in rats. Am. J. Physiol. 246, F349 – F358.
  13. Cauli B., Tong X. K., Rancillac A., Serluca N., Lambolez B., Rossier J., Hamel E. (2004). Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J. Neurosci. 24, 8940 – 8949. doi:10.1523/JNEUROSCI.3065-04.2004
  14. Chan B. S., Endo S., Kanai N., Schuster V. L. (2002). Identification of lactate as a driving force for prostanoid transport by prostaglandin transporter PGT. Am. J. Physiol. Renal Physiol. 282, F1097 – F1102.
  15. Chisari M., Salomone S., Laureanti F., Copani A., Sortino M. A. (2004). Modulation of cerebral vascular tone by activated glia: involvement of nitric oxide. J. Neurochem. 91, 1171 – 1179. doi:10.1111/j.1471-4159.2004.02782.x
  16. Cipolla M. J., Li R., Vitullo L. (2004). Perivascular innervation of penetrating brain parenchymal arterioles. J. Cardiovasc. Pharmacol. 44, 1 – 8. doi:10.1097/00005344-200407000-00001
  17. Cipolla M. J., Smith J., Kohlmeyer M. M., Godfrey J. A. (2009). SKCa and IKCa channels, myogenic tone, and vasodilator responses in middle cerebral arteries and parenchymal arterioles: effect of ischemia and reperfusion. Stroke 40, 1451 – 1457. doi:10.1161/STROKEAHA.108.535435
  18. Collingridge G. L. (1995). The brain slice preparation: a tribute to the pioneer Henry McIlwain. J. Neurosci. Methods 59, 5 – 9. doi:10.1016/0165-0270(94)00187-L
  19. Cornell-Bell A. H., Finkbeiner S. M., Cooper M. S., Smith S. J. (1990). Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470 – 473. doi:10.1126/science.1967852
  20. D'Agostino D. P., Putnam R. W., Dean J. B. (2007). Superoxide (*O2−) production in CA1 neurons of rat hippocampal slices exposed to graded levels of oxygen. J. Neurophysiol. 98, 1030 – 1041. doi:10.1152/jn.01003.2006
  21. Dacey R. G. Jr., Duling B. R. (1982). A study of rat intracerebral arterioles: methods, morphology, and reactivity. Am. J. Physiol. 243, H598 – H606.
  22. Dacey R. G. Jr., Duling B. R. (1984). Effect of norepinephrine on penetrating arterioles of rat cerebral cortex. Am. J. Physiol. 246, H380 – H385.
  23. de Labra C., Rivadulla C., Espinosa N., Dasilva M., Cao R., Cudeiro J. (2009). Different sources of nitric oxide mediate neurovascular coupling in the lateral geniculate nucleus of the cat. Front. Syst. Neurosci. 3, 9. doi:10.3389/neuro.06.009.2009
  24. del Zoppo G. J. (2010). The neurovascular unit in the setting of stroke. J. Intern. Med. 267, 156 – 171. doi:10.1111/j.1365-2796.2009.02199.x
  25. Devor A., Tian P., Nishimura N., Teng I. C., Hillman E. M., Narayanan S. N., Ulbert I., Boas D. A., Kleinfeld D., Dale A. M. (2007). Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal. J. Neurosci. 27, 4452 – 4459. doi:10.1523/JNEUROSCI.0134-07.2007
  26. Drake C. T., Iadecola C. (2007). The role of neuronal signaling in controlling cerebral blood flow. Brain Lang. 102, 141 – 152. doi:10.1016/j.bandl.2006.08.002
  27. Dunn K. M., Nelson M. T. (2010). Potassium channels and neurovascular coupling. Circ. J. 74, 608 – 616. doi:10.1253/circj.CJ-10-0174
  28. Edvinsson L. M., MacKenzie E. T. (2002). General and Comparative Anatomy of the Cerebral Circulation, 2nd Edn. New York: Lippincott Williams and Wilkins.
  29. Feletou M. (2009). Calcium-activated potassium channels and endothelial dysfunction: therapeutic options? Br. J. Pharmacol. 156, 545 – 562. doi:10.1111/j.1476-5381.2009.00052.x
  30. Feletou M., Tang E. H., Vanhoutte P. M. (2008). Nitric oxide the gatekeeper of endothelial vasomotor control. Front. Biosci. 13, 4198 – 4217. doi:10.2741/3000
  31. Feletou M., Vanhoutte P. M. (2009). EDHF: an update. Clin. Sci. 117, 139 – 155. doi:10.1042/CS20090096
  32. Fellin T., Carmignoto G. (2004). Neurone-to-astrocyte signalling in the brain represents a distinct multifunctional unit. J. Physiol. (Lond.) 559, 3 – 15. doi:10.1113/jphysiol.2004.063214
  33. Fergus A., Jin Y., Thai Q. A., Kassell N. F., Lee K. S. (1995). Vasodilatory actions of calcitonin gene-related peptide and nitric oxide in parenchymal microvessels of the rat hippocampus. Brain Res. 694, 78 – 84. doi:10.1016/0006-8993(95)00768-L
  34. Fergus A., Jin Y., Thai Q. A., Kassell N. F., Lee K. S. (1996). Tonic protein kinase C-mediated vasoconstriction is unmasked when nitric oxide synthase is inhibited in cerebral microvessels. Neuroscience 74, 927 – 934. doi:10.1016/0306-4522(96)00158-3
  35. Ferraro G., Sardo P. (2004). Nitric oxide and brain hyperexcitability. In Vivo 18, 357 – 366.
  36. Figueroa X. F., Duling B. R. (2009). Gap junctions in the control of vascular function. Antioxid. Redox Signal. 11, 251 – 266. doi:10.1089/ars.2008.2117
  37. Filosa J. A., Bonev A. D., Nelson M. T. (2004). Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling. Circ. Res. 95, e73 – e81. doi:10.1161/01.RES.0000148636.60732.2e
  38. Filosa J. A., Bonev A. D., Straub S. V., Meredith A. L., Wilkerson M. K., Aldrich R. W., Nelson M. T. (2006). Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat. Neurosci. 9, 1397 – 1403. doi:10.1038/nn1779
  39. Flamion B., Bungay P. M., Gibson C. C., Spring K. R. (1991). Flow rate measurements in isolated perfused kidney tubules by fluorescence photobleaching recovery. Biophys. J. 60, 1229 – 1242. doi:10.1016/S0006-3495(91)82157-9
  40. Gebremedhin D., Narayanan J., Harder D. R. (2005). Role of astrocytic KCa channel openings in the glutamate receptor mediated release of EETs from rat brain astrocytes. FASEB J. 19, A1257.
  41. Gebremedhin D., Yamaura K., Zhang C., Bylund J., Koehler R. C., Harder D. R. (2003). Metabotropic glutamate receptor activation enhances the activities of two types of Ca 2+ -activated K + channels in rat hippocampal astrocytes. J. Neurosci. 23, 1678 – 1687.
  42. Giaume C., Koulakoff A., Roux L., Holcman D., Rouach N. (2010). Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat. Rev. Neurosci. 11, 87 – 99. doi:10.1038/nrn2757
  43. Girouard H., Bonev A. D., Hannah R. M., Meredith A., Aldrich R. W., Nelson M. T. (2010). Astrocytic endfoot Ca 2+ and BK channels determine both arteriolar dilation and constriction. Proc. Natl. Acad. Sci. U.S.A. 107, 3811 – 3816. doi:10.1073/pnas.0914722107
  44. Goadsby P. J., Edvinson L. (2002). Neurovascular Control of the Cerebral Circulation, 2nd Edn. New York: Lippincott Williams and Wilkins.
  45. Gordon G. R., Choi H. B., Rungta R. L., Ellis-Davies G. C., MacVicar B. A. (2008). Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456, 745 – 749. doi:10.1038/nature07525
  46. Gulbenkian S., Uddman R., Edvinsson L. (2001). Neuronal messengers in the human cerebral circulation. Peptides 22, 995 – 1007. doi:10.1016/S0196-9781(01)00408-9
  47. Hájos N., Mody I. (2009). Establishing a physiological environment for visualized in vitro brain slice recordings by increasing oxygen supply and modifying aCSF content. J. Neurosci. Methods 183, 107 – 113. doi:10.1016/j.jneumeth.2009.06.005
  48. Hamel E. (2004). Cholinergic modulation of the cortical microvascular bed. Prog. Brain Res. 145, 171 – 178. doi:10.1016/S0079-6123(03)45012-7
  49. Hamel E. (2006). Perivascular nerves and the regulation of cerebrovascular tone. J. Appl. Physiol. 100, 1059 – 1064. doi:10.1152/japplphysiol.00954.2005
  50. Harder D. R., Zhang C., Gebremedhin D. (2002). Astrocytes function in matching blood flow to metabolic activity. News Physiol. Sci. 17, 27 – 31.
  51. Iadecola C. (1998). Neurogenic control of the cerebral microcirculation: is dopamine minding the store? Nat. Neurosci. 1, 263 – 265. doi:10.1038/1074
  52. Iadecola C., Nedergaard M. (2007). Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369 – 1376. doi:10.1038/nn2003
  53. Inoue R., Morita H., Ito Y. (2004). Newly emerging Ca 2+ entry channel molecules that regulate the vascular tone. Expert Opin. Ther. Targets 8, 321 – 334. doi:10.1517/14728222.8.4.321
  54. Kacem K., Lacombe P., Seylaz J., Bonvento G. (1998). Structural organization of the perivascular astrocyte endfeet and their relationship with the endothelial glucose transporter: a confocal microscopy study. Glia 23, 1 – 10.
  55. Kitaura H., Uozumi N., Tohmi M., Yamazaki M., Sakimura K., Kudoh M., Shimizu T., Shibuki K. (2007). Roles of nitric oxide as a vasodilator in neurovascular coupling of mouse somatosensory cortex. Neurosci. Res. 59, 160 – 171. doi:10.1016/j.neures.2007.06.1469
  56. Knot H. J., Nelson M. T. (1998). Regulation of arterial diameter and wall [Ca 2+ ] in cerebral arteries of rat by membrane potential and intravascular pressure. J. Physiol. (Lond.) 508 (Pt 1), 199 – 209.
  57. Koehler R. C., Roman R. J., Harder D. R. (2009). Astrocytes and the regulation of cerebral blood flow. Trends Neurosci. 32, 160 – 169. doi:10.1016/j.tins.2008.11.005
  58. Kojima H., Hirata M., Kudo Y., Kikuchi K., Nagano T. (2001). Visualization of oxygen-concentration-dependent production of nitric oxide in rat hippocampal slices during aglycemia. J. Neurochem. 76, 1404 – 1410. doi:10.1046/j.1471-4159.2001.00161.x
  59. Kozlov A. S., Angulo M. C., Audinat E., Charpak S. (2006). Target cell-specific modulation of neuronal activity by astrocytes. Proc. Natl. Acad. Sci. U.S.A. 103, 10058 – 10063. doi:10.1073/pnas.0603741103
  60. Krimer L. S., Muly E. C. 3rd,, Williams, G. V, Goldman-Rakic P. S. (1998). Dopaminergic regulation of cerebral cortical microcirculation. Nat. Neurosci. 1, 286 – 289. doi:10.1038/1099
  61. Ledo A., Barbosa R., Cadenas E., Laranjinha J. (2010). Dynamic and interacting profiles of *NO and O2 in rat hippocampal slices. Free Radic. Biol. Med. 48, 1044 – 1050. doi:10.1016/j.freeradbiomed.2010.01.024
  62. Ledo A., Barbosa R. M., Gerhardt G. A., Cadenas E., Laranjinha J. (2005). Concentration dynamics of nitric oxide in rat hippocampal subregions evoked by stimulation of the NMDA glutamate receptor. Proc. Natl. Acad. Sci. U.S.A. 102, 17483 – 17488. doi:10.1073/pnas.0503624102
  63. Leybaert L., Cabooter L., Braet K. (2004). Calcium signal communication between glial and vascular brain cells. Acta Neurol. Belg. 104, 51 – 56.
  64. Li N., Sul J. Y., Haydon P. G. (2003). A calcium-induced calcium influx factor, nitric oxide, modulates the refilling of calcium stores in astrocytes. J. Neurosci. 23, 10302 – 10310.
  65. Lindauer U., Leithner C., Kaasch H., Rohrer B., Foddis M., Fuchtemeier M., Offenhauser N., Steinbrink J., Royl G., Kohl-Bareis M., Dirnagl U. (2010). Neurovascular coupling in rat brain operates independent of hemoglobin deoxygenation. J. Cereb. Blood Flow Metab. 30, 757 – 768. doi:10.1038/jcbfm.2009.259
  66. Lindauer U., Megow D., Matsuda H., Dirnagl U. (1999). Nitric oxide: a modulator, but not a mediator, of neurovascular coupling in rat somatosensory cortex. Am. J. Physiol. 277, H799 – H811.
  67. Lovick T. A., Brown L. A., Key B. J. (1999). Neurovascular relationships in hippocampal slices: physiological and anatomical studies of mechanisms underlying flow-metabolism coupling in intraparenchymal microvessels. Neuroscience 92, 47 – 60. doi:10.1016/S0306-4522(98)00737-4
  68. Lovick T. A., Brown L. A., Key B. J. (2005). Neuronal activity-related coupling in cortical arterioles: involvement of astrocyte-derived factors. Exp. Physiol. 90, 131 – 140. doi:10.1113/expphysiol.2004.028811
  69. Ma X., Qiu S., Luo J., Ma Y., Ngai C. Y., Shen B., Wong C. O., Huang Y., Yao X. (2010) Functional role of vanilloid transient receptor potential 4-canonical transient receptor potential 1 complex in flow-induced Ca 2+ influx. Arterioscler. Thromb. Vasc. Biol. 30, 851 – 858. doi:10.1161/ATVBAHA.109.196584
  70. Metea M. R., Newman E. A. (2006). Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J. Neurosci. 26, 2862 – 2870. doi:10.1523/JNEUROSCI.4048-05.2006
  71. Moore C. I., Cao R. (2008). The hemo-neural hypothesis: on the role of blood flow in information processing. J. Neurophysiol. 99, 2035 – 2047. doi:10.1152/jn.01366.2006
  72. Mulligan S. J., MacVicar B. A. (2004). Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431, 195 – 199. doi:10.1038/nature02827
  73. Nelson M. T., Cheng H., Rubart M., Santana L. F., Bonev A. D., Knot H. J., Lederer W. J. (1995). Relaxation of arterial smooth muscle by calcium sparks. Science 270, 633 – 637. doi:10.1126/science.270.5236.633
  74. Ngai A. C., Winn H. R. (1995). Modulation of cerebral arteriolar diameter by intraluminal flow and pressure. Circ. Res. 77, 832 – 840.
  75. Paton J. F., Waki H., Abdala A. P., Dickinson J., Kasparov S. (2007). Vascular-brain signaling in hypertension: role of angiotensin II and nitric oxide. Curr. Hypertens. Rep. 9, 242 – 247. doi:10.1007/s11906-007-0043-1
  76. Peppiatt C., Attwell D. (2004). Neurobiology: feeding the brain. Nature 431, 137 – 138. doi:10.1038/431137a
  77. Rancillac A., Rossier J., Guille M., Tong X. K., Geoffroy H., Amatore C., Arbault S., Hamel E., Cauli B. (2006). Glutamatergic control of microvascular tone by distinct GABA neurons in the cerebellum. J. Neurosci. 26, 6997 – 7006. doi:10.1523/JNEUROSCI.5515-05.2006
  78. Reid K. H., Edmonds H. L. Jr., Schurr A., Tseng M. T., West C. A. (1988). Pitfalls in the use of brain slices. Prog. Neurobiol. 31, 1 – 18. doi:10.1016/0301-0082(88)90020-2
  79. Rossier J. (2009). Wiring and plumbing in the brain. Front. Hum. Neurosci. 3, 2. doi:10.3389/neuro.09.002.2009
  80. Silver I. A., Erecinska M. (1994). Extracellular glucose concentration in mammalian brain: continuous monitoring of changes during increased neuronal activity and upon limitation in oxygen supply in normo-, hypo-, and hyperglycemic animals. J. Neurosci. 14, 5068 – 5076.
  81. Simard M., Arcuino G., Takano T., Liu Q. S., Nedergaard M. (2003). Signaling at the gliovascular interface. J. Neurosci. 23, 9254 – 9262.
  82. Takano T., Tian G. F., Peng W., Lou N., Libionka W., Han X., Nedergaard M. (2006). Astrocyte-mediated control of cerebral blood flow. Nat. Neurosci. 9, 260 – 267. doi:10.1038/nn1623
  83. Theis M., Sohl G., Eiberger J., Willecke K. (2005). Emerging complexities in identity and function of glial connexins. Trends Neurosci. 28, 188 – 195. doi:10.1016/j.tins.2005.02.006
  84. Tong X. K., Hamel E. (2000). Basal forebrain nitric oxide synthase (NOS)-containing neurons project to microvessels and NOS neurons in the rat neocortex: cellular basis for cortical blood flow regulation. Eur. J. Neurosci. 12, 2769 – 2780. doi:10.1046/j.1460-9568.2000.00158.x
  85. Udosen I. T., Jiang H., Hercule H. C., Oyekan A. O. (2003). Nitric oxide-epoxygenase interactions and arachidonate-induced dilation of rat renal microvessels. Am. J. Physiol. Heart Circ. Physiol. 285, H2054 – H2063.
  86. Vaucher E., Hamel E. (1995). Cholinergic basal forebrain neurons project to cortical microvessels in the rat: electron microscopic study with anterogradely transported Phaseolus vulgaris leucoagglutinin and choline acetyltransferase immunocytochemistry. J. Neurosci. 15, 7427 – 7441.
  87. Vaucher E., Linville D., Hamel E. (1997). Cholinergic basal forebrain projections to nitric oxide synthase-containing neurons in the rat cerebral cortex. Neuroscience 79, 827 – 836. doi:10.1016/S0306-4522(97)00033-X
  88. Wiencken A. E., Casagrande V. A. (1999). Endothelial nitric oxide synthetase (eNOS) in astrocytes: another source of nitric oxide in neocortex. Glia 26, 280 – 290.
  89. Wrzosek A. (2009). Endothelium as target for large-conductance calcium-activated potassium channel openers. Acta Biochim. Pol. 56, 393 – 404.
  90. Xu H. L., Koenig H. M., Ye S., Feinstein D. L., Pelligrino D. A. (2004). Influence of the glia limitans on pial arteriolar relaxation in the rat. Am. J. Physiol. Heart Circ. Physiol. 287, H331 – H339. doi:10.1152/ajpheart.00831.2003
  91. Xu H. L., Mao L., Ye S., Paisansathan C., Vetri F., Pelligrino D. A. (2008). Astrocytes are a key conduit for upstream signaling of vasodilation during cerebral cortical neuronal activation in vivo. Am. J. Physiol. Heart Circ. Physiol. 294, H622 – H632. doi:10.1152/ajpheart.00530.2007
  92. Yang G., Chen G., Ebner T. J., Iadecola C. (1999). Nitric oxide is the predominant mediator of cerebellar hyperemia during somatosensory activation in rats. Am. J. Physiol. 277, R1760 – R1770.
  93. Yang G., Huard J. M., Beitz A. J., Ross M. E., Iadecola C. (2000). Stellate neurons mediate functional hyperemia in the cerebellar molecular layer. J. Neurosci. 20, 6968 – 6973.
  94. Zhang D. X., Mendoza S. A., Bubolz A. H., Mizuno A., Ge Z. D., Li R., Warltier D. C., Suzuki M., Gutterman D. D. (2009). Transient receptor potential vanilloid type 4-deficient mice exhibit impaired endothelium-dependent relaxation induced by acetylcholine in vitro and in vivo. Hypertension 53, 532 – 538. doi:10.1161/HYPERTENSIONAHA.108.127100
  95. Zonta M., Sebelin A., Gobbo S., Fellin T., Pozzan T., Carmignoto G. (2003a). Glutamate-mediated cytosolic calcium oscillations regulate a pulsatile prostaglandin release from cultured rat astrocytes. J. Physiol. (Lond.) 553, 407 – 414. doi:10.1113/jphysiol.2003.046706
  96. Zonta M., Angulo M. C., Gobbo S., Rosengarten B., Hossmann K. A., Pozzan T., Carmignoto G. (2003b). Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat. Neurosci. 6, 43 – 50. doi:10.1038/nn980

Citation

Filosa, J. A. (2010). Vascular Tone and Neurovascular Coupling: Considerations Toward an Improved In Vitro Model. Frontiers in Neuroenergetics, Volume 2. https://doi.org/
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Copyright © 2010 Filosa.

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*Correspondence: Jessica A. Filosa

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