Coupling of Neural Activity to Blood Flow in Olfactory Glomeruli Is Mediated by Astrocytic Pathways

Neuron

Volumn 58, Issue 6, 2008, Pages 897-910

  Petzold, Gabor C ^a   Albeanu, Dinu F ^a   Sato, Tomokazu F ^a   Murthy, Venkatesh N ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

MOLNEURO; SYSNEURO

Indexed keywords

GLUTAMATE RECEPTOR 5; GLUTAMATE TRANSPORTER; PROSTAGLANDIN SYNTHASE;

ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN BLOOD FLOW; CELL ACTIVITY; CONTROLLED STUDY; ELECTRIC ACTIVITY; ELECTROENCEPHALOGRAM; ENZYME ACTIVATION; ERYTHROCYTE; FLUORESCENCE; GLOMERULUS CAPILLARY; HYPEREMIA; MOUSE; MULTIPHOTON MICROSCOPY; NERVE CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; OLFACTORY BULB; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; SMELLING; SYNAPTIC TRANSMISSION;

ANIMALS; ASTROCYTES; CEREBROVASCULAR CIRCULATION; MICE; OLFACTORY BULB; OLFACTORY RECEPTOR NEURONS; RECEPTORS, ODORANT; SIGNAL TRANSDUCTION;

EID: 45249086342     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2008.04.029     Document Type: Article

References (51)

1. Albeanu D.F., Soucy E., Sato T.F., Meister M., and Murthy V.N. LED arrays as cost effective and efficient light sources for widefield microscopy. PLoS One. 3 (2008) e2146 10.1371/journal.pone.0002146
2. Aroniadou-Anderjaska V., Ennis M., and Shipley M.T. Glomerular synaptic responses to olfactory nerve input in rat olfactory bulb slices. Neuroscience 79 (1997) 425-434
3. Attwell D., and Laughlin S.B. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 21 (2001) 1133-1145
4. Bernardinelli Y., Magistretti P.J., and Chatton J.Y. Astrocytes generate Na+-mediated metabolic waves. Proc. Natl. Acad. Sci. USA 101 (2004) 14937-14942
5. Bozza T., McGann J.P., Mombaerts P., and Wachowiak M. In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 42 (2004) 9-21
6. Brenneis C., Maier T.J., Schmidt R., Hofacker A., Zulauf L., Jakobsson P.J., Scholich K., and Geisslinger G. Inhibition of prostaglandin E2 synthesis by SC-560 is independent of cyclooxygenase 1 inhibition. FASEB J. 20 (2006) 1352-1360
7. Brickley S.G., Farrant M., Swanson G.T., and Cull-Candy S.G. CNQX increases GABA-mediated synaptic transmission in the cerebellum by an AMPA/kainate receptor-independent mechanism. Neuropharmacology 41 (2001) 730-736
8. Chaigneau E., Oheim M., Audinat E., and Charpak S. Two-photon imaging of capillary blood flow in olfactory bulb glomeruli. Proc. Natl. Acad. Sci. USA 100 (2003) 13081-13086
9. Chaigneau E., Tiret P., Lecoq J., Ducros M., Knopfel T., and Charpak S. The relationship between blood flow and neuronal activity in the rodent olfactory bulb. J. Neurosci. 27 (2007) 6452-6460
10. Dawson L.A., Djali S., Gonzales C., Vinegra M.A., and Zaleska M.M. Characterization of transient focal ischemia-induced increases in extracellular glutamate and aspartate in spontaneously hypertensive rats. Brain Res. Bull. 53 (2000) 767-776
11. De Saint Jan D., and Westbrook G.L. Detecting activity in olfactory bulb glomeruli with astrocyte recording. J. Neurosci. 25 (2005) 2917-2924
12. Dirnagl U., Villringer A., and Einhaupl K.M. In-vivo confocal scanning laser microscopy of the cerebral microcirculation. J. Microsc. 165 (1992) 147-157
13. Ennis M., Zhu M., Heinbockel T., and Hayar A. Olfactory nerve-evoked, metabotropic glutamate receptor-mediated synaptic responses in rat olfactory bulb mitral cells. J. Neurophysiol. 95 (2006) 2233-2241
14. Filosa J.A., Bonev A.D., and Nelson M.T. Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling. Circ. Res. 95 (2004) e73-e81
15. Gsell W., Burke M., Wiedermann D., Bonvento G., Silva A.C., Dauphin F., Buhrle C., Hoehn M., and Schwindt W. Differential effects of NMDA and AMPA glutamate receptors on functional magnetic resonance imaging signals and evoked neuronal activity during forepaw stimulation of the rat. J. Neurosci. 26 (2006) 8409-8416
16. Gurden H., Uchida N., and Mainen Z.F. Sensory-evoked intrinsic optical signals in the olfactory bulb are coupled to glutamate release and uptake. Neuron 52 (2006) 335-345
17. Hirase H., Qian L., Bartho P., and Buzsaki G. Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol. 2 (2004) E96 10.1371/journal.pbio.0020096
18. Iadecola C., and Nedergaard M. Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10 (2007) 1369-1376
19. Kida I., Xu F., Shulman R.G., and Hyder F. Mapping at glomerular resolution: fMRI of rat olfactory bulb. Magn. Reson. Med. 48 (2002) 570-576
20. Kleinfeld D., Mitra P.P., Helmchen F., and 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 (1998) 15741-15746
21. Lancet D., Greer C.A., Kauer J.S., and Shepherd G.M. Mapping of odor-related neuronal activity in the olfactory bulb by high-resolution 2-deoxyglucose autoradiography. Proc. Natl. Acad. Sci. USA 79 (1982) 670-674
22. Lauritzen M. Reading vascular changes in brain imaging: is dendritic calcium the key?. Nat. Rev. Neurosci. 6 (2005) 77-85
23. Logothetis N.K., and Wandell B.A. Interpreting the BOLD signal. Annu. Rev. Physiol. 66 (2004) 735-769
24. Marcaggi P., and Attwell D. Role of glial amino acid transporters in synaptic transmission and brain energetics. Glia 47 (2004) 217-225
25. McGann J.P., Pirez N., Gainey M.A., Muratore C., Elias A.S., and Wachowiak M. Odorant representations are modulated by intra- but not interglomerular presynaptic inhibition of olfactory sensory neurons. Neuron 48 (2005) 1039-1053
26. Meister M., and Bonhoeffer T. Tuning and topography in an odor map on the rat olfactory bulb. J. Neurosci. 21 (2001) 1351-1360
27. Miesenböck G., De Angelis D.A., and Rothman J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394 (1998) 192-195
28. Mombaerts P., Wang F., Dulac C., Chao S.K., Nemes A., Mendelsohn M., Edmondson J., and Axel R. Visualizing an olfactory sensory map. Cell 87 (1996) 675-686
29. Mukamel R., Gelbard H., Arieli A., Hasson U., Fried I., and Malach R. Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science 309 (2005) 951-954
30. Mulligan S.J., and MacVicar B.A. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431 (2004) 195-199
31. Nawroth J.C., Greer C.A., Chen W.R., Laughlin S.B., and Shepherd G.M. An energy budget for the olfactory glomerulus. J. Neurosci. 27 (2007) 9790-9800
32. Niwa K., Araki E., Morham S.G., Ross M.E., and Iadecola C. Cyclooxygenase-2 contributes to functional hyperemia in whisker-barrel cortex. J. Neurosci. 20 (2000) 763-770
33. Niwa K., Haensel C., Ross M.E., and Iadecola C. Cyclooxygenase-1 participates in selected vasodilator responses of the cerebral circulation. Circ. Res. 88 (2001) 600-608
34. Offenhauser N., Thomsen K., Caesar K., and Lauritzen M. Activity-induced tissue oxygenation changes in rat cerebellar cortex: interplay of postsynaptic activation and blood flow. J. Physiol. 565 (2005) 279-294
35. Raichle M.E., and Mintun M.A. Brain work and brain imaging. Annu. Rev. Neurosci. 29 (2006) 449-476
36. Rees G., Friston K., and Koch C. A direct quantitative relationship between the functional properties of human and macaque V5. Nat. Neurosci. 3 (2000) 716-723
37. Schaffer C.B., Friedman B., Nishimura N., Schroeder L.F., Tsai P.S., Ebner F.F., Lyden P.D., and Kleinfeld D. Two-Photon Imaging of Cortical Surface Microvessels Reveals a Robust Redistribution in Blood Flow after Vascular Occlusion. PLoS Biol. 4 (2006) e22 10.1371/journal.pbio.0040022
38. Simard M., Arcuino G., Takano T., Liu Q.S., and Nedergaard M. Signaling at the gliovascular interface. J. Neurosci. 23 (2003) 9254-9262
39. Stosiek C., Garaschuk O., Holthoff K., and Konnerth A. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. USA 100 (2003) 7319-7324
40. Takano T., Tian G.F., Peng W., Lou N., Libionka W., Han X., and Nedergaard M. Astrocyte-mediated control of cerebral blood flow. Nat. Neurosci. 9 (2006) 260-267
41. Tsai P.S., Nishimura N., Yoder E.J., White A., Dolnick E., and Kleinfeld D. Principles, design and construction of a two photon scanning microscope for in vitro and in vivo studies. In: Frostig R. (Ed). Methods for In Vivo Optical Imaging (2002), CRC Press, Boca Raton, FL 113-171
42. Utsumi M., Ohno K., Onchi H., Sato K., and Tohyama M. Differential expression patterns of three glutamate transporters (GLAST, GLT1 and EAAC1) in the rat main olfactory bulb. Brain Res. Mol. Brain Res. 92 (2001) 1-11
43. van den Pol A.N. Presynaptic metabotropic glutamate receptors in adult and developing neurons: autoexcitation in the olfactory bulb. J. Comp. Neurol. 359 (1995) 253-271
44. Vlassenko A.G., Rundle M.M., Raichle M.E., and Mintun M.A. Regulation of blood flow in activated human brain by cytosolic NADH/NAD+ ratio. Proc. Natl. Acad. Sci. USA 103 (2006) 1964-1969
45. Voutsinos-Porche B., Bonvento G., Tanaka K., Steiner P., Welker E., Chatton J.Y., Magistretti P.J., and Pellerin L. Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex. Neuron 37 (2003) 275-286
46. Wachowiak M., McGann J.P., Heyward P.M., Shao Z., Puche A.C., and Shipley M.T. Inhibition of olfactory receptor neuron input to olfactory bulb glomeruli mediated by suppression of presynaptic calcium influx. J. Neurophysiol. 94 (2005) 2700-2712
47. Wang X., Lou N., Xu Q., Tian G.F., Peng W.G., Han X., Kang J., Takano T., and Nedergaard M. Astrocytic Ca(2+) signaling evoked by sensory stimulation in vivo. Nat. Neurosci. 9 (2006) 816-823
48. Westerink B.H., and De Vries J.B. A method to evaluate the diffusion rate of drugs from a microdialysis probe through brain tissue. J. Neurosci. Methods 109 (2001) 53-58
49. Yang G., and Iadecola C. Glutamate microinjections in cerebellar cortex reproduce cerebrovascular effects of parallel fiber stimulation. Am. J. Physiol. 271 (1996) R1568-R1575
50. Zonta M., Angulo M.C., Gobbo S., Rosengarten B., Hossmann K.A., Pozzan T., and Carmignoto G. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat. Neurosci. 6 (2003) 43-50
51. Zonta M., Sebelin A., Gobbo S., Fellin T., Pozzan T., and Carmignoto G. Glutamate-mediated cytosolic calcium oscillations regulate a pulsatile prostaglandin release from cultured rat astrocytes. J. Physiol. 553 (2003) 407-414