Activity-dependent increases in local oxygen consumption correlate with postsynaptic currents in the mouse cerebellum in vivo

Journal of Neuroscience

Volumn 31, Issue 50, 2011, Pages 18327-18337

  Mathiesen, Claus ^a   Caesar, Kirsten ^a   Thomsen, Kirsten ^a   Hoogland, Tycho M ^b   Witgen, Brent M ^a   Brazhe, Alexey ^c   Lauritzen, Martin ^a,d  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

^d GLOSTRUP UNIVERSITY HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

(MICRO OXO) BIS (TRANSFORMATOTETRAMINE RUTHENIUM); 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; CALCIUM ION; GREEN FLUORESCENT PROTEIN; MUSCIMOL; OMEGA AGATOXIN IVA; RUTHENIUM; UNCLASSIFIED DRUG;

ACTION POTENTIAL; AEROBIC METABOLISM; ANIMAL EXPERIMENT; ARTICLE; BRAIN BLOOD FLOW; BRAIN MITOCHONDRION; CEREBELLUM; CEREBELLUM CORTEX; CEREBRAL METABOLIC RATE OF OXYGEN; CLIMBING FIBER; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; EVOKED RESPONSE; IMAGE ANALYSIS; ION CURRENT; MALE; MICROSCOPY; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; OXYGEN TISSUE LEVEL; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PURKINJE CELL; SYNAPTIC POTENTIAL; TRANSGENIC MOUSE;

ANIMALS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CEREBELLUM; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; MICE; OMEGA-AGATOXIN IVA; OXYGEN CONSUMPTION; PURKINJE CELLS; SYNAPSES;

EID: 83455199143     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4526-11.2011     Document Type: Article

References (46)

1. 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
2. Caesar K, Thomsen K, Lauritzen M (2003) Dissociation of spikes, synaptic activity, and activity-dependent increments in rat cerebellar blood flow by tonic synaptic inhibition. Proc Natl Acad Sci U S A 100:16000-16005
3. Caesar K, Hashemi P, Douhou A, Bonvento G, Boutelle MG, Walls AB, Lauritzen M (2008a) Glutamate receptor-dependent increments in lactate, glucose and oxygen metabolism evoked in rat cerebellum in vivo. J Physiol 586:1337-1349
4. Caesar K, Offenhauser N, LauritzenM (2008b) Gamma-aminobutyric acid modulates local brain oxygen consumption and blood flow in rat cerebellar cortex. J Cereb Blood Flow Metab 28:906-915
5. Callaway JC, Lasser-Ross N, Ross WN (1995) IPSPs strongly inhibit climbing fiber-activated [Ca 2]i increases in the dendrites of cerebellar Purkinje neurons. J Neurosci 15:2777-2787
6. Chen G, Hanson CL, Ebner TJ (1996) Functional parasagittal compartments in the rat cerebellar cortex: an in vivo optical imaging study using neutral red. J Neurophysiol 76:4169-4174
7. Clarke DD, Sokoloff L (1994) Circulation and energy metabolism of the brain. In: Basic neurochemistry: molecular, cellular, and medical (Siegel GJ, Agranoff BW, Albers RW, Molinoff PB, eds), pp 645-680 New York: Raven.
8. de Graaf RA, Mason GF, Patel AB, Rothman DL, Behar KL (2004) Regional glucose metabolism and glutamatergic neurotransmission in rat brain in vivo. Proc Natl Acad Sci U S A 101:12700-12705
9. Doroshenko PA, Woppmann A, Miljanich G, Augustine GJ (1997) Pharmacologically distinct presynaptic calcium channels in cerebellar excitatory and inhibitory synapses. Neuropharmacology 36:865-872
10. Erecinska M, Silver IA (1989) ATP and brain function. J Cereb Blood Flow Metab 9:2-19
11. Fabricius M, Lauritzen M, (1996) Laser-Doppler evaluation of rat brain microcirculation: comparison with the [14C]-iodoantipyrine method suggests discordance during cerebral blood flow increases. J Cereb Blood Flow Metab 16:156-161
12. Fabricius M, Akgoren N, Dirnagl U, Lauritzen M, (1997) Laminar analysis of cerebral blood flow in cortex of rats by laser-Doppler flowmetry: a pilot study. J Cereb Blood Flow Metab 17:1326-1336
13. Frey U, Egert U, Heer F, Hafizovic S, Hierlemann A (2009) Microelectronic system for high-resolution mapping of extracellular electric fields applied to brain slices. Biosens Bioelectron 24:2191-2198
14. Gellerich FN, Gizatullina Z, Trumbeckaite S, Nguyen HP, Pallas T, Arandarcikaite O, Vielhaber S, Seppet E, Striggow F (2010) The regulation of OXPHOS by extramitochondrial calcium. Biochim Biophys Acta 1797:1018-1027
15. Gjedde A (2005) Blood-brain transfer and metabolism of oxygen. In: Bloodbrain barriers: from ontogeny to artificial interfaces, (Dermietzel R, Spray DC, Nedergaard M, eds), pp 523-550 Hoboken: John Wiley and Sons.
16. Gunter TE, Sheu SS (2009) Characteristics and possible functions of mitochondrial Ca(2) transport mechanisms. Biochim Biophys Acta 1787:1291-1308
17. Gunter TE, Yule DI, Gunter KK, Eliseev RA, Salter JD (2004) Calcium and mitochondria. FEBS Lett 567:96-102
18. Hanson CL, Chen G, Ebner TJ (2000) Role of climbing fibers in determining the spatial patterns of activation in the cerebellar cortex to peripheral stimulation: an optical imaging study. Neuroscience 96:317-331
19. Hayakawa Y, Nemoto T, Iino M, Kasai H (2005) Rapid Ca-2(-)dependent increase in oxygen consumption by mitochondria in single mammalian central neurons. Cell Calcium 37:359-370
20. Kann O, Kovacs R (2007) Mitochondria and neuronal activity. AmJ Physiol Cell Physiol 292:C641-C657.
21. Kasischke KA (2008) A new pathway for lactate production in the CNS. J Physiol 586:1207-1208
22. Krogsgaard-Larsen P, Johnston GA (1978) Structure-activity studies on the inhibition of GABA binding to rat brain membranes by muscimol and related compounds. J Neurochem 30:1377-1382
23. Lauritzen M (2005) Opinion: reading vascular changes in brain imaging: is dendritic calcium the key? Nat Rev Neurosci 6:77-85
24. Lecoq J, Tiret P, Najac M, Shepherd GM, Greer CA, Charpak S (2009) Odorevoked oxygen consumption by action potential and synaptic transmission in the olfactory bulb. J Neurosci 29:1424-1433
25. Leithner C, Royl G, Offenhauser N, Fuchtemeier M, Kohl-Bareis M, Villringer A, Dirnagl U, Lindauer U (2010) Pharmacological uncoupling of activation induced increases in CBF and CMRO2. J Cereb Blood Flow Metab 30:311-322
26. Lin AL, Fox PT, Hardies J, Duong TQ, Gao JH (2010) Nonlinear coupling between cerebral blood flow, oxygen consumption, and ATP production in human visual cortex. Proc Natl Acad Sci U S A 107:8446-8451
27. Llinas RR (1981) Electrophysiology of cerebellar networks. In: Handbook of physiology, section I, the nervous system, Vol II, motor control, Part 2, American Physiological Society (Brooks VB, ed), pp 831-877 Baltimore, MD: Williams and Wilkins.
28. Mathiesen C, Caesar K, Akgoren N, Lauritzen M (1998) Modification of activity-dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex. Journal of Physiology 512:555-566
29. 2+uptake into mitochondria in vitro and in situ in single cardiac myocytes. J Biol Chem 273:10223-10231
30. McDonough SI, Boland LM, Mintz IM, Bean BP (2002) Interactions among toxins that inhibit N-type and P-type calcium channels. J Gen Physiol 119:313-328
31. Nakagawa H, Matsumoto N (1998) ON and OFF channels of the frog optic tectum revealed by current source density analysis. J Neurophysiol 80:1886-1899
32. Nicholson C, Freeman JA (1975) Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. J Neurophysiol 38:356-368
33. Offenhauser N, Thomsen K, Caesar K, Lauritzen M (2005) Activity-induced tissue oxygenation changes in rat cerebellar cortex: interplay of postsynaptic activation and blood flow. J Physiol 565:279-294
34. 2+signals to neuronal mitochondria. J Biol Chem 281:1039-1047
35. Pivovarova NB, Hongpaisan J, Andrews SB, Friel DD (1999) Depolarizationinduced mitochondrial Ca accumulation in sympathetic neurons: spatial and temporal characteristics. J Neurosci 19:6372-6384
36. Raichle ME, Mintun MA (2006) Brain work and brain imaging. Annu Rev Neurosci 29:449-476
37. Reinert KC, Gao W, Chen G, Wang X, Peng YP, Ebner TJ (2011) Cellular and metabolic origins of flavoprotein autofluorescence in the cerebellar cortex in vivo. Cerebellum 10:585-599
38. Rizzuto R, Pozzan T (2006) Microdomains of intracellular Ca2: molecular determinants and functional consequences. Physiol Rev 86:369-408
39. Satrústegui J, Pardo B, del Arco A (2007) Mitochondrial transporters as novel targets for intracellular calcium signaling. Physiol Rev 87:29-67
40. Schreurs BG, Sanchez-Andres JV, Alkon DL (1992) GABA-induced responses in Purkinje cell dendrites of the rabbit cerebellar slice. Brain Res 597:99-107
41. Stam AH, de Vries B, Janssens AC, Vanmolkot KR, Aulchenko YS, Henneman P, Oostra BA, Frants RR, van den Maagdenberg AM, Ferrari MD, van Duijn CM, Terwindt GM (2010) Shared genetic factors in migraine and depression Evidence from a genetic isolate Evidence from a genetic isolate. Neurology 74:288-294
42. Thomsen K, Piilgaard H, Gjedde A, Bonvento G, Lauritzen M (2009) Principal cell spiking, postsynaptic excitation, and oxygen consumption in the rat cerebellar cortex. J Neurophysiol 102:1503-1512
43. Viswanathan A, Freeman RD (2007) Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity. Nat Neurosci 10:1308-1312
44. Womack MD, Hoang C, Khodakhah K (2009) Large conductance calciumactivated potassium channels affect both spontaneous firing and intracellular calcium concentration in cerebellar Purkinje neurons. Neuroscience 162:989-1000
45. Ying WL, Emerson J, Clarke MJ, Sanadi DR (1991) Inhibition of mitochondrial calcium ion transport by an oxo-bridged dinuclear ruthenium ammine complex. Biochemistry 30:4949-4952
46. Zhu XH, Zhang Y, Tian RX, Lei H, Zhang N, Zhang X, Merkle H, Ugurbil K, Chen W (2002) Development of O-17 NMR approach for fast imaging of cerebral metabolic rate of oxygen in rat brain at high field. Proc Natl Acad Sci U S A 99:13194-13199.