Astrocytic calcium signaling: Mechanism and implications for functional brain imaging

Methods in Molecular Biology

Volumn 489, Issue , 2009, Pages 93-109

  Wang, Xiaohai ^a   Takano, Takahiro ^a   Nedergaard, Maiken ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

2 photon imaging; Functional brain imaging; Photolysis

Indexed keywords

EID: 84934438166     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-59745-543-5_5     Document Type: Review

References (75)

1. Cornell-Bell, A.H., et al., Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science, 1990. 247(4941): pp. 470-3.
2. Nedergaard, M., Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science, 1994. 263(5154): pp. 1768-71.
3. Parpura, V., et al., Glutamate-mediated astrocyte-neuron signalling. Nature, 1994. 369(6483): pp. 744-7.
4. Kang, J., et al., Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci, 1998. 1(8): pp. 683-92.
5. Porter, J.T. and K.D. McCarthy, Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J Neurosci, 1996. 16(16): pp. 5073-81.
6. Pasti, L., et al., Intracellular calcium oscillations in astrocytes: A highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J Neurosci, 1997. 17(20): pp. 7817-30.
7. Pascual, O., et al., Astrocytic purinergic signaling coordinates synaptic networks. Science, 2005. 310(5745): pp. 113-6.
8. Newman, E.A. and K.R. Zahs, Modulation of neuronal activity by glial cells in the retina. J Neurosci, 1998. 18(11): pp. 4022-8.
9. Wang, X., et al., Astrocytic Ca(2+) signaling evoked by sensory stimulation in vivo. Nat Neurosci, 2006. 9(6): pp. 816-23.
10. Zonta, M., et al., Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci, 2003. 6(1): pp. 43-50.
11. Araque, A., et al., Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J Neurosci, 1998. 18(17): pp. 6822-9.
12. Rzigalinski, B.A., et al., Intracellular free calcium dynamics in stretch-injured astrocytes. J Neurochem, 1998. 70(6): pp. 2377-85.
13. Fellin, T., et al., Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron, 2004. 43(5): pp. 729-43.
14. Newman, E.A., Calcium increases in retinal glial cells evoked by light-induced neuronal activity. J Neurosci, 2005. 25(23): pp. 5502-10.
15. Haydon, P.G. and G. Carmignoto, Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev, 2006. 86(3): pp. 1009-31.
16. Fox, P.T. and M.E. Raichle, Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc Natl Acad Sci U S A, 1986. 83(4): pp. 1140-4.
17. Mulligan, S.J. and B.A. MacVicar, Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature, 2004. 431(7005): pp. 195-9.
18. Metea, M.R. and E.A. Newman, Glial cells dilate and constrict blood vessels: A mechanism of neurovascular coupling. J Neurosci, 2006. 26(11): pp. 2862-70.
19. Filosa, J.A., et al., Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat Neurosci, 2006. 9(11): pp. 1397-403.
20. Peppiatt, C.M., et al., Bidirectional control of CNS capillary diameter by pericytes. Nature, 2006. 443(7112): pp. 700-4.
21. Mathiesen, C., K. Caesar, and M. Lauritzen, Temporal coupling between neuronal activity and blood flow in rat cerebellar cortex as indicated by field potential analysis. J Physiol, 2000. 523 Pt 1: pp. 235-46.
22. Ngai, A.C., et al., Frequency-dependent changes in cerebral blood flow and evoked potentials during somatosensory stimulation in the rat. Brain Res, 1999. 837(1-2): pp. 221-8.
23. Charles, A.C., Glia-neuron intercellular calcium signaling. Dev Neurosci, 1994. 16(3-4): pp. 196-206.
24. Porter, J.T. and K.D. McCarthy, Astrocytic neurotransmitter receptors in situ and in vivo. Prog Neurobiol, 1997. 51(4): pp. 439-55.
25. Duffy, S. and B.A. MacVicar, Adrenergic calcium signaling in astrocyte networks within the hippocampal slice. J Neurosci, 1995. 15(8): pp. 5535-50.
26. Perea, G. and A. Araque, Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci, 2005. 25(9): pp. 2192-203.
27. Verkhratsky, A., R.K. Orkand, and H. Kettenmann, Glial calcium: Homeostasis and signaling function. Physiol Rev, 1998. 78(1): pp. 99-141.
28. Volterra, A. and J. Meldolesi, Astrocytes, from brain glue to communication elements: The revolution continues. Nat Rev Neurosci, 2005. 6(8): pp. 626-40.
29. Bergles, D.E. and C.E. Jahr, Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron, 1997. 19(6): pp. 1297-308.
30. Porter, J.T. and K.D. McCarthy, - Astrocytic neurotransmitter receptors in situ and in vivo. 1997. 51: p. 455.
31. Matsui, K. and C.E. Jahr, Ectopic release of synaptic vesicles. Neuron, 2003. 40(6): pp. 1173-83.
32. Zoli, M., et al., The emergence of the volume transmission concept. Brain Res Brain Res Rev, 1998. 26(2-3): pp. 136-47.
33. Cotrina, M.L., J.H. Lin, and M. Nedergaard, Cytoskeletal assembly and ATP release regulate astrocytic calcium signaling. J Neurosci, 1998. 18(21): pp. 8794-804.
34. Schell, M.J., M.E. Molliver, and S.H. Snyder, D-serine, an endogenous synaptic modulator: Localization to astrocytes and glutamate-stimulated release. Proc Natl Acad Sci U S A, 1995. 92(9): pp. 3948-52.
35. Beattie, E.C., et al., Control of synaptic strength by glial TNFalpha. Science, 2002. 295(5563): pp. 2282-5.
36. Simard, M., et al., Signaling at the gliovascular interface. J Neurosci, 2003. 23(27): pp. 9254-62.
37. Price, D.L., et al., Distribution of rSlo Ca2+-activated K+ channels in rat astrocyte perivascular endfeet. Brain Res, 2002. 956(2): pp. 183-93.
38. Filosa, J.A., A.D. Bonev, and M.T. Nelson, Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling. Circ Res, 2004. 95(10): pp. e73-81.
39. Denk, W., J.H. Strickler, and W.W. Webb, Two-photon laser scanning fluorescence microscopy. Science, 1990. 248(4951): pp. 73-6.
40. Stosiek, C., et al., In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci U S A, 2003. 100(12): pp. 7319-24.
41. Hirase, H., et al., Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol, 2004. 2(4): pp. E96.
42. Svoboda, K. and R. Yasuda, Principles of two-photon excitation microscopy and its applications to neuroscience. Neuron, 2006. 50(6): pp. 823-39.
43. Svoboda, K., et al., Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex in vivo. Nat Neurosci, 1999. 2(1): pp. 65-73.
44. Nimmerjahn, A., et al., Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods, 2004. 1(1): pp. 31-7.
45. Friedberg, M.H., S.M. Lee, and F.F. Ebner, Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. J Neurophysiol, 1999. 81(5): pp. 2243-52.
46. Kerr, J.N., D. Greenberg, and F. Helmchen, Imaging input and output of neocortical networks in vivo. Proc Natl Acad Sci U S A, 2005. 102(39): pp. 14063-8.
47. Kang, J., et al., Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci, 1998. 1(8): pp. 683-92.
48. Sosnik, R., S. Haidarliu, and E. Ahissar, Temporal frequency of whisker movement. I. Representations in brain stem and thalamus. J Neurophysiol, 2001. 86(1): pp. 339-53.
49. Pinto, D.J., J.C. Brumberg, and D.J. Simons, Circuit dynamics and coding strategies in rodent somatosensory cortex. J Neurophysiol, 2000. 83(3): pp. 1158-66.
50. Petersen, C.C., A. Grinvald, and B. Sakmann, Spatiotemporal dynamics of sensory responses in layer 2/3 of rat barrel cortex measured in vivo by voltage-sensitive dye imaging combined with whole-cell voltage recordings and neuron reconstructions. J Neurosci, 2003. 23(4): pp. 1298-309.
51. Takano, T., et al., Astrocyte-mediated control of cerebral blood flow. Nat Neurosci, 2006. 9(2): pp. 260-7.
52. Logothetis, N.K. and B.A. Wandell, Interpreting the BOLD signal. Annu Rev Physiol, 2004. 66: pp. 735-69.
53. Mathiesen, C., et al., Modification of activity-dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex. J Physiol, 1998. 512 (Pt 2): pp. 555-66.
54. Peppiatt, C. and D. Attwell, Neurobiology: Feeding the brain. Nature, 2004. 431(7005): pp. 137-8.
55. Lauritzen, M., Reading vascular changes in brain imaging: Is dendritic calcium the key? Nat Rev Neurosci, 2005. 6(1): pp. 77-85.
56. Bergles, D.E., J.S. Diamond, and C.E. Jahr, Clearance of glutamate inside the synapse and beyond. Curr Opin Neurobiol, 1999. 9(3): pp. 293-8.
57. Pellerin, L. and P.J. Magistretti, Food for thought: Challenging the dogmas. J Cereb Blood Flow Metab, 2003. 23(11): pp. 1282-6.
58. Pellerin, L. and P.J. Magistretti, Glutamate uptake into astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A, 1994. 91(22): pp. 10625-9.
59. Dienel, G.A. and N.F. Cruz, Nutrition during brain activation: Does cell-to-cell lactate shuttling contribute significantly to sweet and sour food for thought? Neurochem Int, 2004. 45(2-3): pp. 321-51.
60. Pysh, Y. and T. Khan, Variation in mitochondrial structure and content of neurons and neuroglia in rat brain: An electron microscopic study. Brain Research, 1972. 36(1): pp. 1-18.
61. Peters, A., L.P. Sandford, and H.D. Webster, Fine structure of the Nervous System: Neurons and Their Supporting Cells. 3rd edition ed. 1991: Oxford University Press, Oxford.
62. Hertz, L., L. Peng, and G. Dienel, Energy metabolism in astrocytes: High rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. Journal of Cerebral Blood Flow & Metabolism, 2007. 27: pp. 219-249.
63. van den Pol, A.N., C. Romano, and P. Ghosh, Metabotropic glutamate receptor mGluR5 subcellular distribution and developmental expression in hypothalamus. J Comp Neurol, 1995. 362(1): pp. 134-50.
64. Munoz, A., X.B. Liu, and E.G. Jones, Development of metabotropic glutamate receptors from trigeminal nuclei to barrel cortex in postnatal mouse. J Comp Neurol, 1999. 409(4): pp. 549-66.
65. Brookes, P.S., et al., Calcium, ATP, and ROS: A mitochondrial love-hate triangle. Am J Physiol Cell Physiol, 2004. 287(4): pp. C817-33.
66. Attwell, D. and S. Laughlin, An Energy Budget for Signaling in the Grey Matter of the Brain. Journal of Cerebral Blood Flow and Metabolism, 2001. 21: pp. 1133-1145.
67. Lebon, V., et al., Astroglial Contribution to Brain Energy Metabolism in Humans Revealed by 13C Nuclear Magnetic Resonance Spectroscopy: Elucidation of the Dominant Pathway for Neurotransmitter Glutamate Repletion and Measurement of Astrocytic Oxidative Metabolism. J Neurosci, 2002. 22(5): pp. 1523-1531.
68. Oz, G., et al., Neuroglial Metabolism in the Awake Rat Brain: CO2 Fixation Increases with Brain Activity. The Journal of Neuroscience, 2004. 22(50): pp. 11273-11279.
69. Kahlert, S. and G. Reiser, Requirement of Glycolytic and Mitochondrial Energy Supply for Loading of Ca2+ Stores and InsP3-Mediated Ca2+ Signaling in Rat Hippocampus Astrocytes. J Neurosci Res, 2000. 61: pp. 409-420.
70. Feustel, P.J., Y. Jin, and H.K. Kimelberg, Volume-regulated anion channels are the predominant contributors to release of excitatory amino acids in the ischemic cortical penumbra. 2004. 35: p. 1168.
71. Arcuino, G., et al., Intercellular calcium signaling mediated by point-source burst release of ATP. Proc Natl Acad Sci U S A, 2002. 99(15): pp. 9840-5.
72. Zhang, J.M., et al., ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron, 2003. 40(5): pp. 971-82.
73. Davalos, D., et al., ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci, 2005. 8(6): pp. 752-8.
74. Brennan, A.M., J.A. Connor, and C.W. Shuttleworth, NAD(P)H fluorescent transients after synaptic activity in brain slices: Predominant role of mitochondrial function. J Cereb Blood Flow Metab, 2006. 26(11): pp. 1389-406.
75. Takano, T., et al., Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci, 2007. 10(6): pp. 754-62.