In vivo stimulus-induced vasodilation occurs without IP3 receptor activation and may precede astrocytic calcium increase

Journal of Neuroscience

Volumn 33, Issue 19, 2013, Pages 8411-8422

  Nizar, Krystal ^a   Uhlirova, Hana ^b   Tian, Peifang ^c,f   Saisan, Payam A ^c   Cheng, Qun ^c   Reznichenko, Lidia ^c   Weldy, Kimberly L ^c   Steed, Tyler C ^a   Sridhar, Vishnu B ^d   MacDonald, Christopher L ^d   Cui, Jianxia ^d   Gratiy, Sergey L ^b   Sakadžić, Sava ^g   Boas, David A ^g   Beka, Thomas I ^c,h   Einevoll, Gaute T ^h   Chen, Ju ^e   Masliah, Eliezer ^c   Dale, Anders M ^b,c   Silva, Gabriel A ^a,d   Devor, Anna ^b,c,g   more..

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f JOHN CARROLL UNIVERSITY   (United States)

^g HARVARD MEDICAL SCHOOL   (United States)

^h NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; INOSITOL 1, 4, 5 TRISPHOSPHATE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BLOOD FLOW VELOCITY; CALCIUM MOBILIZATION; CEREBROSPINAL FLUID; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; FUNCTIONAL NEUROIMAGING; HYPEREMIA; IN VIVO STUDY; MOUSE; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; REGRESSION ANALYSIS; VASODILATATION;

EID: 84877269867     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3285-12.2013     Document Type: Article

References (72)

1. Agulhon C, Petravicz J, McMullen AB, Sweger EJ, Minton SK, Taves SR, Casper KB, Fiacco TA, McCarthy KD (2008) What is the role of astrocyte calcium in neurophysiology? Neuron 59:932-946. CrossRef Medline
2. Allaman I, Bélanger M, Magistretti PJ (2011) Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 34:76-87. CrossRef Medline
3. Anderson LA, Christianson GB, Linden JF (2009) Mouse auditory cortex differs from visual and somatosensory cortices in the laminar distribution of cytochrome oxidase and acetylcholinesterase. Brain Res 1252:130-142. CrossRef Medline
4. Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA (2010) Glial and neuronal control of brain blood flow. Nature 468:232-243. CrossRef Medline
5. Bergles DE, Jahr CE (1997) Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19:1297-1308. CrossRef Medline
6. Boas DA, Jones SR, Devor A, Huppert TJ, Dale AM (2008) A vascular anatomical network model of the spatio-temporal response to brain activation. Neuroimage 40:1116-1129. CrossRef Medline
7. Buzsáki G (2004) Large-scale recording of neuronal ensembles. Nat Neurosci 7:446-451. CrossRef Medline
8. Calcinaghi N, Jolivet R, Wyss MT, Ametamey SM, Gasparini F, Buck A, Weber B (2011) Metabotropic glutamate receptor mGluR5 is not involved in the early hemodynamic response. J Cereb Blood Flow Metab 31:e1-10. CrossRef Medline
9. Cauli B, Hamel E (2010) Revisiting the role of neurons in neurovascular coupling. Front Neuroenergetics 2:9. Medline
10. Devor A, Dunn AK, Andermann ML, Ulbert I, Boas DA, Dale AM (2003) Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex. Neuron 39:353-359. CrossRef Medline
11. Devor A, Ulbert I, Dunn AK, Narayanan SN, Jones SR, Andermann ML, Boas DA, Dale AM (2005) Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity. Proc Natl Acad Sci U S A 102: 3822-3827. CrossRef Medline
12. Devor A, Tian P, Nishimura N, Teng IC, Hillman EM, Narayanan SN, Ulbert I, Boas DA, Kleinfeld D, Dale AM (2007) Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal. J Neurosci 27:4452-4459. CrossRef Medline
13. Devor A, Hillman EM, Tian P, Waeber C, Teng IC, Ruvinskaya L, Shalinsky MH, Zhu H, Haslinger RH, Narayanan SN, Ulbert I, Dunn AK, Lo EH, Rosen BR, Dale AM, Kleinfeld D, Boas DA (2008) Stimulus-induced changes in blood flow and 2-deoxyglucose uptake dissociate in ipsilateral somatosensory cortex. J Neurosci 28:14347-14357. CrossRef Medline
14. 2+ detection and modulation of synaptic release by astrocytes. Nat Neurosci 14:1276-1284. CrossRef Medline
15. Dombeck DA, Khabbaz AN, Collman F, Adelman TL, Tank DW (2007) Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56:43-57. CrossRef Medline
16. Drew PJ, Shih AY, Kleinfeld D (2011) Fluctuating and sensory-induced vasodynamics in rodent cortex extend arteriole capacity. Proc Natl Acad Sci U S A 108:8473-8478. CrossRef Medline
17. Einevoll GT, Franke F, Hagen E, Pouzat C, Harris KD (2012) Towards reliable spike-train recordings from thousands of neurons with multielectrodes. Curr Opin Neurobiol 22:11-17. CrossRef Medline
18. Fiacco TA, McCarthy KD (2006) Astrocyte calcium elevations: properties, propagation, and effects on brain signaling. Glia 54:676-690. CrossRef Medline
19. Garaschuk O, Milos RI, Konnerth A (2006) Targeted bulk-loading of fluorescent indicators for two-photon brain imaging in vivo. Nat Protoc 1:380-386. CrossRef Medline
20. Göbel W, Helmchen F (2007) In vivo calcium imaging of neural network function. Physiology 22:358-365. CrossRef Medline
21. Gordon GR, Choi HB, Rungta RL, Ellis-Davies GC, MacVicar BA (2008) Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456:745-749. CrossRef Medline
22. Halassa MM, Fellin T, Takano H, Dong JH, Haydon PG (2007) Synaptic islands defined by the territory of a single astrocyte. J Neurosci 27:6473-6477. CrossRef Medline
23. Halassa MM, Dal Maschio M, Beltramo R, Haydon PG, Benfenati F, Fellin T (2010) Integrated brain circuits: neuron-astrocyte interaction in sleeprelated rhythmogenesis. ScientificWorldJournal 10:1634-1645. CrossRef Medline
24. Hoogland TM, Kuhn B, Göbel W, Huang W, Nakai J, Helmchen F, Flint J, Wang SS (2009) Radially expanding transglial calcium waves in the intact cerebellum. Proc Natl Acad Sci U S A 106:3496-3501. CrossRef Medline
25. Huchzermeyer C, Albus K, Gabriel HJ, Otáhal J, Taubenberger N, Heinemann U, Kovács R, Kann O (2008) Gamma oscillations and spontaneous network activity in the hippocampus are highly sensitive to decreases in pO2 and concomitant changes in mitochondrial redox state. J Neurosci 28:1153-1162. CrossRef Medline
26. Iadecola C, Nedergaard M (2007) Glial regulation of the cerebral microvasculature. Nat Neurosci 10:1369-1376. CrossRef Medline
27. Jaffe DB, Brown TH (1994) Metabotropic glutamate receptor activation induces calcium waves within hippocampal dendrites. J Neurophysiol 72: 471-474. Medline
28. Ji N, Milkie DE, Betzig E (2010) Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues. Nat Methods 7:141-147. CrossRef Medline
29. Kleinfeld D, Mitra PP, Helmchen F, Denk W (1998) Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc Natl Acad SciU S A 95:15741-15746. CrossRef Medline
30. Koehler RC, Roman RJ, Harder DR (2009) Astrocytes and the regulation of cerebral blood flow. Trends Neurosci 32:160-169. CrossRef Medline
31. Lecrux C, Toussay X, Kocharyan A, Fernandes P, Neupane S, Lévesque M, Plaisier F, Shmuel A, Cauli B, Hamel E (2011) Pyramidal neurons are "neurogenic hubs" in the neurovascular coupling response to whisker stimulation. J Neurosci 31:9836-9847. CrossRef Medline
32. 2+ signaling is abolished in atrial myocytes of inositol-1,4,5-trisphosphate(IP3)-receptor type 2-deficient mice. Circ Res 96: 1274-1281. CrossRef Medline
33. Magistretti PJ, Pellerin L, Rothman DL, Shulman RG (1999) Energy on demand. Science 283:496-497. CrossRef Medline
34. Metea MR, Newman EA (2006) Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci 26:2862-2870. CrossRef Medline
35. Mulligan SJ, MacVicar BA (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431:195-199. CrossRef Medline
36. Navarrete M, Perea G, Fernandez de Sevilla D, Gómez-Gonzalo M, Nunez A, Martín ED, Araque A (2012) Astrocytes mediate in vivo cholinergicinduced synaptic plasticity. PLoS Biol 10:e1001259. CrossRef Medline
37. Nimmerjahn A (2009) Astrocytes going live: advances and challenges. J Physiol 587:1639-1647. CrossRef Medline
38. Nimmerjahn A, Kirchhoff F, Kerr JN, Helmchen F (2004) Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 1:31-37. CrossRef Medline
39. Nimmerjahn A, Mukamel EA, Schnitzer MJ (2009) Motor behavior activates Bergmann glial networks. Neuron 62:400-412. CrossRef Medline
40. Paulson OB, Hasselbalch SG, Rostrup E, Knudsen GM, Pelligrino D (2010) Cerebral blood flow response to functional activation. J Cereb Blood Flow Metab 30:2-14. CrossRef Medline
41. Pellerin L, Magistretti PJ (2012) Sweet sixteen for ANLS. J Cereb Blood Flow Metab 32:1152-1166. CrossRef Medline
42. Petravicz J, Fiacco TA, McCarthy KD (2008) Loss of IP3 receptordependent Ca2 increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. J Neurosci 28:4967-4973. CrossRef Medline
43. Pettersen KH, Einevoll GT (2008) Amplitude variability and extracellular low-pass filtering of neuronal spikes. Biophys J 94:784-802. CrossRef Medline
44. Petzold GC, Murthy VN (2011) Role of astrocytes in neurovascular coupling. Neuron 71:782-797. CrossRef Medline
45. Petzold GC, Albeanu DF, Sato TF, Murthy VN (2008) Coupling of neural activity to blood flow in olfactory glomeruli is mediated by astrocytic pathways. Neuron 58:897-910. CrossRef Medline
46. Poskanzer KE, Yuste R (2011) Astrocytic regulation of cortical UP states. Proc Natl Acad Sci U S A 108:18453-18458. CrossRef Medline
47. Reeves AM, Shigetomi E, Khakh BS (2011) Bulk loading of calcium indicator dyes to study astrocyte physiology: key limitations and improvements using morphological maps. J Neurosci 31:9353-9358. CrossRef Medline
48. Reznichenko L, Cheng Q, Nizar K, Gratiy SL, Saisan PA, Rockenstein EM, Tanya González T, Patrick C, Spencer B, Desplats P, Dale AM, Devor A, Masliah E (2012) In vivo alterations in calcium buffering capacity in transgenic mouse model of synucleinopathy. J Neurosci 32:9992-9998. CrossRef Medline
49. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C (2008) Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322:1551-1555. CrossRef Medline
50. Schulz K, Sydekum E, Krueppel R, Engelbrecht CJ, Schlegel F, Schröter A, Rudin M, Helmchen F (2012) Simultaneous BOLD fMRI and fiberoptic calcium recording in rat neocortex. Nat Methods 9:597-602. CrossRef Medline
51. Schummers J, Yu H, Sur M (2008) Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320:1638-1643. CrossRef Medline
52. Shen Z, Lu Z, Chhatbar PY, O'Herron P, Kara P (2012) An artery-specific fluorescent dye for studying neurovascular coupling. Nat Methods 9:273-276. CrossRef Medline
53. Shi Y, Liu X, Gebremedhin D, Falck JR, Harder DR, Koehler RC (2008) Interaction of mechanisms involving epoxyeicosatrienoic acids, adenosine receptors, and metabotropic glutamate receptors in neurovascular coupling in rat whisker barrel cortex. J Cereb Blood Flow Metab 28:111-125. CrossRef Medline
54. Shigetomi E, Kracun S, Khakh BS (2010a) Monitoring astrocyte calcium microdomains with improved membrane targeted GCaMP reporters. Neuron Glia Biol 6:183-191. CrossRef Medline
55. Shigetomi E, Kracun S, Sofroniew MV, Khakh BS (2010b) A genetically targeted optical sensor to monitor calcium signals in astrocyte processes. Nat Neurosci 13:759-766. CrossRef Medline
56. Shigetomi E, Tong X, Kwan KY, Corey DP, Khakh BS (2012) TRPA1 channels regulate astrocyte resting calcium and inhibitory synapse efficacy through GAT-3. Nat Neurosci 15:70-80. CrossRef Medline
57. Shin HK, Jones PB, Garcia-Alloza M, Borrelli L, Greenberg SM, Bacskai BJ, Frosch MP, Hyman BT, Moskowitz MA, Ayata C (2007) Age-dependent cerebrovascular dysfunction in a transgenic mouse model of cerebral amyloid angiopathy. Brain 130:2310-2319. CrossRef Medline
58. Simard M, Arcuino G, Takano T, Liu QS, Nedergaard M (2003) Signaling at the gliovascular interface. J Neurosci 23:9254-9262. Medline
59. Steriade M (2006) Grouping of brain rhythms in corticothalamic systems. Neuroscience 137:1087-1106. CrossRef Medline
60. Stosiek C, Garaschuk O, Holthoff K, Konnerth A (2003) In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci U S A 100: 7319-7324. CrossRef Medline
61. Sun W, McConnell E, Pare JF, Xu Q, Chen M, Peng W, Lovatt D, Han X, Smith Y, Nedergaard M (2013) Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 339:197-200. CrossRef Medline
62. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, Nedergaard M (2006) Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9:260-267. CrossRef Medline
63. Takata N, Mishima T, Hisatsune C, Nagai T, Ebisui E, Mikoshiba K, Hirase H (2011) Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo. J Neurosci 31:18155-18165. CrossRef Medline
64. Thrane AS, Rangroo Thrane V, Zeppenfeld D, Lou N, Xu Q, Nagelhus EA, Nedergaard M (2012) General anesthesia selectively disrupts astrocyte calcium signaling in the awake mouse cortex. Proc Natl Acad Sci U S A 109:18974-18979. CrossRef Medline
65. Tian P, Teng IC, May LD, Kurz R, Lu K, Scadeng M, Hillman EM, De Crespigny AJ, D'Arceuil HE, Mandeville JB, Marota JJ, Rosen BR, Liu TT, Boas DA, Buxton RB, Dale AM, Devor A (2010) Cortical depth-specific microvascular dilation underlies laminar differences in blood oxygenation level-dependent functional MRI signal. Proc Natl Acad Sci U S A 107:15246-15251. CrossRef Medline
66. Turner DA, Foster KA, Galeffi F, Somjen GG (2007) Differences in O2 availability resolve the apparent discrepancies in metabolic intrinsic optical signals in vivo and in vitro. Trends Neurosci 30:390-398. CrossRef Medline
67. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6:626-640. CrossRef Medline
68. Wang F, Smith NA, Xu Q, Fujita T, Baba A, Matsuda T, Takano T, Bekar L, Nedergaard M (2012) Astrocytes modulate neural network activity by Ca(2)(+)-dependent uptake of extracellular K(+). Sci Signal 5:ra26. CrossRef Medline
69. 2+) signaling evoked by sensory stimulation in vivo. Nat Neurosci 9:816-823. CrossRef Medline
70. Wang X, Takano H, Nedergaard M (2009) Astrocytic calcium signaling: mechanism and implications for functional brain imaging. In: Dynamic brain imaging: multi-modal methods and in vivo applications, vol. 489 (Hyder F, ed). New York: Humana.
71. Winship IR, Plaa N, Murphy TH (2007) Rapid astrocyte calcium signals correlate with neuronal activity and onset of the hemodynamic response in vivo. J Neurosci 27:6268-6272. CrossRef Medline
72. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, Carmignoto G (2003) Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6:43-50. CrossRef Medline