Neurovascular coupling in hippocampus is mediated via diffusion by neuronal-derived nitric oxide

Free Radical Biology and Medicine

Volumn 73, Issue , 2014, Pages 421-429

  Lourenço, Cátia F ^a   Santos, Ricardo M ^a   Barbosa, Rui M ^a   Cadenas, Enrique ^b   Radi, Rafael ^c   Laranjinha, João ^a  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

Author keywords

Brain; Free radicals; Functional hyperemia; Hippocampus; Neurons; Neurovascular coupling; Nitric oxide

Indexed keywords

GUANYLATE CYCLASE; NITRIC OXIDE; CELL RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEURONAL NITRIC OXIDE SYNTHASE; OXYGEN; SCAVENGER; SOLUBLE GUANYLYL CYCLASE;

ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BLOOD VESSEL REACTIVITY; BRAIN BLOOD FLOW; CONTROLLED STUDY; DIFFUSION; ENDOTHELIUM CELL; HIPPOCAMPUS; IN VIVO STUDY; MALE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; VASCULARIZATION; ANIMAL; ELECTROENCEPHALOGRAM; ENZYME ACTIVATION; METABOLISM; PHYSIOLOGY; SURGERY; WISTAR RAT;

ANIMALS; ASTROCYTES; BRAIN WAVES; ENZYME ACTIVATION; FREE RADICAL SCAVENGERS; GLUTAMIC ACID; GUANYLATE CYCLASE; HIPPOCAMPUS; MALE; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; OXYGEN; RATS; RATS, WISTAR; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84903846214     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.05.021     Document Type: Article

References (52)

1. C. Iadecola Neurovascular regulation in the normal brain and in Alzheimer's disease Nat. Rev. Neurosci. 5 2004 347 360 (Pubitemid 38568496)
2. D. Attwell, A.M. Buchan, S. Charpak, M. Lauritzen, B.A. Macvicar, and E.A. Newman Glial and neuronal control of brain blood flow Nature 468 2010 232 243
3. W. Sun, E. McConnell, J.F. Pare, Q. Xu, M. Chen, W. Peng, D. Lovatt, X. Han, Y. Smith, and M. Nedergaard Glutamate-dependent neuroglial calcium signaling differs between young and adult brain Science 339 2013 197 200
4. G.C. Petzold, and V.N. Murthy Role of astrocytes in neurovascular coupling Neuron 71 2011 782 797
5. M. Zonta, M.C. Angulo, S. Gobbo, B. Rosengarten, K.A. Hossmann, T. Pozzan, and G. Carmignoto Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation Nat. Neurosci. 6 2003 43 50 (Pubitemid 36026331)
6. G. Carmignoto, and M. Gomez-Gonzalo The contribution of astrocyte signalling to neurovascular coupling Brain Res. Rev. 63 2010 138 148
7. D.R. Harder, N.J. Alkayed, A.R. Lange, D. Gebremedhin, and R.J. Roman Functional hyperemia in the brain: hypothesis for astrocyte-derived vasodilator metabolites Stroke 29 1998 229 234 (Pubitemid 28046968)
8. F.M. Faraci nNOS-containing perivascular nerves: stranger by the minute Circ. Res. 91 2002 7 8 (Pubitemid 34778935)
9. C. Iadecola Regulation of the cerebral microcirculation during neural activity: is nitric oxide the missing link? Trends Neurosci. 16 1993 206 214 (Pubitemid 23139183)
10. W. Meng, J.R. Tobin, and D.W. Busija Glutamate-induced cerebral vasodilation is mediated by nitric oxide through N-methyl-D-aspartate receptors Stroke 26 1995 857 862 (discussion 863)
11. F.J. Northington, J.R. Tobin, R.C. Koehler, and R.J. Traystman in vivo production of nitric oxide correlates with NMDA-induced cerebral hyperemia in newborn sheep Am. J. Physiol. 269 1995 H215 H221
12. D.A. Pelligrino, R.L. Gay 3rd, V.L. Baughman, and Q. Wang NO synthase inhibition modulates NMDA-induced changes in cerebral blood flow and EEG activity Am. J. Physiol. 271 1996 H990 H995
13. J. Garthwaite, and C.L. Boulton Nitric oxide signaling in the central nervous system Annu. Rev. Physiol. 57 1995 683 706
14. H.S. Sun, T.A. Doucette, Y. Liu, Y. Fang, L. Teves, M. Aarts, C.L. Ryan, P.B. Bernard, A. Lau, J.P. Forder, M.W. Salter, Y.T. Wang, R.A. Tasker, and M. Tymianski Effectiveness of PSD95 inhibitors in permanent and transient focal ischemia in the rat Stroke 39 2008 2544 2553
15. P. Pacher, J.S. Beckman, and L. Liaudet Nitric oxide and peroxynitrite in health and disease Physiol. Rev. 87 2007 315 424 (Pubitemid 46217686)
16. N. Akgoren, M. Fabricius, and M. Lauritzen Importance of nitric oxide for local increases of blood flow in rat cerebellar cortex during electrical stimulation Proc. Natl. Acad. Sci. USA 91 1994 5903 5907 (Pubitemid 24188250)
17. F.M. Faraci, and K.R. Breese Nitric oxide mediates vasodilatation in response to activation of N-methyl-D-aspartate receptors in brain Circ. Res. 72 1993 476 480 (Pubitemid 23024535)
18. K. Adachi, S. Takahashi, P. Melzer, K.L. Campos, T. Nelson, C. Kennedy, and L. Sokoloff Increases in local cerebral blood flow associated with somatosensory activation are not mediated by NO Am. J. Physiol. 267 1994 H2155 H2162
19. J.H. Greenberg, N.W. Sohn, and P.J. Hand Nitric oxide and the cerebral-blood-flow response to somatosensory activation following deafferentation Exp. Brain Res. 129 1999 541 550
20. Q. Wang, T. Kjaer, M.B. Jorgensen, O.B. Paulson, N.A. Lassen, N.H. Diemer, and H.C. Lou Nitric oxide does not act as a mediator coupling cerebral blood flow to neural activity following somatosensory stimuli in rats Neurol. Res. 15 1993 33 36 (Pubitemid 23065383)
21. U. Lindauer, D. Megow, H. Matsuda, and U. Dirnagl Nitric oxide: a modulator, but not a mediator, of neurovascular coupling in rat somatosensory cortex Am. J. Physiol. 277 1999 H799 H811
22. D.G. Buerk, B.M. Ances, J.H. Greenberg, and J.A. Detre Temporal dynamics of brain tissue nitric oxide during functional forepaw stimulation in rats NeuroImage 18 2003 1 9 (Pubitemid 36062743)
23. C.F. Lourenço, R. Santos, R.M. Barbosa, G. Gerhardt, E. Cadenas, and J. Laranjinha in vivo modulation of nitric oxide concentration dynamics upon glutamatergic neuronal activation in the hippocampus Hippocampus 21 2011 622 630
24. R.M. Santos, C.F. Lourenco, A.P. Piedade, R. Andrews, F. Pomerleau, P. Huettl, G.A. Gerhardt, J. Laranjinha, and R.M. Barbosa A comparative study of carbon fiber-based microelectrodes for the measurement of nitric oxide in brain tissue Biosens. Bioelectron. 24 2008 704 709
25. R.M. Barbosa, A.J. Lopes Jesus, R.M. Santos, C.L. Pereira, C.F. Marques, B.S. Rocha, N.R. Ferreira, A. Ledo, and J. Laranjinha Preparation, standardization and measurement of nitric oxide solutions Global J. Anal. Chem 2 2011 272 284
26. J.R. Steinert, C. Kopp-Scheinpflug, C. Baker, R.A. Challiss, R. Mistry, M.D. Haustein, S.J. Griffin, H. Tong, B.P. Graham, and I.D. Forsythe Nitric oxide is a volume transmitter regulating postsynaptic excitability at a glutamatergic synapse Neuron 60 2008 642 656
27. R.M. Santos, C.F. Lourenco, F. Pomerleau, P. Huettl, G.A. Gerhardt, J. Laranjinha, and R.M. Barbosa Brain nitric oxide inactivation is governed by the vasculature Antioxid. Redox Signaling 14 2011 1011 1021
28. B. Li, and R.D. Freeman High-resolution neurometabolic coupling in the lateral geniculate nucleus J. Neurosci. 27 2007 10223 10229 (Pubitemid 47450465)
29. M. Feelisch, P. Kotsonis, J. Siebe, B. Clement, and H.H. Schmidt The soluble guanylyl cyclase inhibitor 1H-[1,2,4]oxadiazolo[4,3,-a]quinoxalin-1-one is a nonselective heme protein inhibitor of nitric oxide synthase and other cytochrome P-450 enzymes involved in nitric oxide donor bioactivation Mol. Pharmacol. 56 1999 243 253 (Pubitemid 29347599)
30. F. Fonnum, A. Johnsen, and B. Hassel Use of fluorocitrate and fluoroacetate in the study of brain metabolism Glia 21 1997 106 113 (Pubitemid 27389646)
31. J.J. Iliff, R. D'Ambrosio, A.C. Ngai, and H.R. Winn Adenosine receptors mediate glutamate-evoked arteriolar dilation in the rat cerebral cortex Am. J. Physiol. Heart Circ. Physiol. 284 2003 H1631 H1637
32. H.L. Xu, and D.A. Pelligrino ATP release and hydrolysis contribute to rat pial arteriolar dilatation elicited by neuronal activation Exp. Physiol. 92 2007 647 651 (Pubitemid 47024942)
33. B.B. Fredholm Adenosine receptors as drug targets Exp. Cell Res. 316 2010 1284 1288
34. S. Gotti, M. Sica, C. Viglietti-Panzica, and G. Panzica Distribution of nitric oxide synthase immunoreactivity in the mouse brain Microsc. Res. Tech. 68 2005 13 35 (Pubitemid 41464006)
35. G. Yang, and C. Iadecola Glutamate microinjections in cerebellar cortex reproduce cerebrovascular effects of parallel fiber stimulation Am. J. Physiol. 271 1996 R1568 R1575
36. C.I. Moore, and R. Cao The hemo-neural hypothesis: on the role of blood flow in information processing J. Neurophysiol. 99 2008 2035 2047
37. A. Ledo, R.M. Barbosa, G.A. Gerhardt, E. Cadenas, and J. Laranjinha Concentration dynamics of nitric oxide in rat hippocampal subregions evoked by stimulation of the NMDA glutamate receptor Proc. Natl. Acad. Sci. USA 102 2005 17483 17488 (Pubitemid 41740892)
38. T.A. Lovick, L.A. Brown, and B.J. Key Neurovascular relationships in hippocampal slices: physiological and anatomical studies of mechanisms underlying flow-metabolism coupling in intraparenchymal microvessels Neuroscience 92 1999 47 60 (Pubitemid 29249017)
39. A.I. Oleinick, C. Amatore, M. Guille, S. Arbault, O.V. Klymenko, and I. Svir Modelling release of nitric oxide in a slice of rat's brain: describing stimulated functional hyperemia with diffusion-reaction equations Math. Med. Biol. 23 2006 27 44
40. J.J. Iliff, R. Wang, D.C. Zeldin, and N.J. Alkayed Epoxyeicosanoids as mediators of neurogenic vasodilation in cerebral vessels Am. J. Physiol. Heart Circ. Physiol. 296 2009 H1352 H1363
41. S.J. Mulligan, and B.A. MacVicar Calcium transients in astrocyte endfeet cause cerebrovascular constrictions Nature 431 2004 195 199 (Pubitemid 39243473)
42. U. Lalo, Y. Pankratov, F. Kirchhoff, R.A. North, and A. Verkhratsky NMDA receptors mediate neuron-to-glia signaling in mouse cortical astrocytes J. Neurosci. 26 2006 2673 2683 (Pubitemid 43357850)
43. M. Oka, M. Wada, A. Yamamoto, Y. Itoh, and T. Fujita Functional expression of constitutive nitric oxide synthases regulated by voltage-gated Na+ and Ca2+ channels in cultured human astrocytes Glia 46 2004 53 62 (Pubitemid 38461723)
44. I.M. Devonshire, N.G. Papadakis, M. Port, J. Berwick, A.J. Kennerley, J.E. Mayhew, and P.G. Overton Neurovascular coupling is brain region-dependent NeuroImage 59 2012 1997 2006
45. A. Devor, A.K. Dunn, M.L. Andermann, I. Ulbert, D.A. Boas, and A.M. Dale Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex Neuron 39 2003 353 359 (Pubitemid 36897555)
46. A. Norup Nielsen, and M. Lauritzen Coupling and uncoupling of activity-dependent increases of neuronal activity and blood flow in rat somatosensory cortex J. Physiol. 533 2001 773 785 (Pubitemid 32600532)
47. C. Mathiesen, K. Caesar, N. Akgoren, and M. Lauritzen Modification of activity-dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex J. Physiol. 512 1998 555 566 (Pubitemid 28486899)
48. N. Offenhauser, K. Thomsen, K. Caesar, and M. Lauritzen Activity-induced tissue oxygenation changes in rat cerebellar cortex: interplay of postsynaptic activation and blood flow J. Physiol. 565 2005 279 294 (Pubitemid 40723709)
49. B.E. Kalisch, B.P. Connop, K. Jhamandas, R.J. Beninger, and R.J. Boegman Differential action of 7-nitro indazole on rat brain nitric oxide synthase Neurosci. Lett. 219 1996 75 78 (Pubitemid 26396318)
50. M.A. Franceschini, H. Radhakrishnan, K. Thakur, W. Wu, S. Ruvinskaya, S. Carp, and D.A. Boas The effect of different anesthetics on neurovascular coupling NeuroImage 51 2010 1367 1377
51. A. Rancillac, J. Rossier, M. Guille, X.K. Tong, H. Geoffroy, C. Amatore, S. Arbault, E. Hamel, and B. Cauli Glutamatergic control of microvascular tone by distinct GABA neurons in the cerebellum J. Neurosci. 26 2006 6997 7006 (Pubitemid 44309867)
52. G. Paxinos, and C. Watson The Rat Brain in Sterotaxic Coordinates 2007 Academic Press San Diego