Calcium dynamics in astrocyte processes during neurovascular coupling

Nature Neuroscience

Volumn 18, Issue 2, 2015, Pages 210-218

  Otsu, Yo ^a,b   Couchman, Kiri ^a,b   Lyons, Declan G ^a,b   Collot, Mayeul ^c,d   Agarwal, Amit ^e   Mallet, Jean Maurice ^c,d   Pfrieger, Frank W ^f   Bergles, Dwight E ^e   Charpak, Serge ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c CNRS   (France)

^d Centre National de la Recherche Scientifique   (France)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CONNEXIN 30; GLUTAMATE TRANSPORTER; GRM5 PROTEIN, MOUSE; METABOTROPIC RECEPTOR 5;

ADULT; ANIMAL CELL; ARTICLE; ASTROCYTE; AUDITORY STIMULATION; CONTROLLED STUDY; GRANULE CELL; MACROGLIA; MOUSE; NEUROLOGICAL AND SENSORIAL PROCEDURES; NEUROVASCULAR COUPLING; NONHUMAN; OLFACTORY BULB; OLFACTORY NERVE; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPATIOTEMPORAL ANALYSIS; SUBVENTRICULAR ZONE; ANIMAL; BRAIN CIRCULATION; CALCIUM SIGNALING; CYTOLOGY; METABOLISM; OLFACTORY RECEPTOR; PHYSIOLOGY; SYNAPSE; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; CALCIUM SIGNALING; CEREBROVASCULAR CIRCULATION; MICE; MICE, TRANSGENIC; OLFACTORY BULB; OLFACTORY RECEPTOR NEURONS; RECEPTOR, METABOTROPIC GLUTAMATE 5; SYNAPSES;

EID: 84923184526     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3906     Document Type: Article

References (50)

1. Iadecola, C. & Nedergaard, M. Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369-1376 (2007).
2. Attwell, D., Buchan, A. & Charpak, S. Glial and neuronal control of brain blood flow. Nature 468, 232-243 (2010).
3. Dunn, K.M. & Nelson, M.T. Neurovascular signaling in the brain and the pathological consequences of hypertension. Am. J. Physiol. Heart Circ. Physiol. 306, H1-H14 (2014).
4. Peppiatt, C.M., Howarth, C., Mobbs, P. & Attwell, D. Bidirectional control of CNS capillary diameter by pericytes. Nature 443, 700-704 (2006).
5. Bell, R.D. et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68, 409-427 (2010).
6. Hall, C.N. et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature 508, 55-60 (2014).
7. Masamoto, K. & Kanno, I. Anesthesia and the quantitative evaluation of neurovascular coupling. J. Cereb. Blood Flow Metab. 32, 1233-1247 (2012).
8. Wang, X. et al. Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nat. Neurosci. 9, 816-823 (2006).
9. Schummers, J., Yu, H. & Sur, M. Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320, 1638-1643 (2008).
10. Schulz, K. et al. Simultaneous BOLD fMRI and fiber-optic calcium recording in rat neocortex. Nat. Methods 9, 597-602 (2012).
11. Nizar, K. et al. In Vivo stimulus-induced vasodilation occurs without IP3 receptor activation and may precede astrocytic calcium increase. J. Neurosci. 33, 8411-8422 (2013).
12. Mulligan, S.J. & MacVicar, B.A. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431, 195-199 (2004).
13. Panatier, A. et al. Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146, 785-798 (2011).
14. Di Castro, M.A. et al. Local Ca2+ detection and modulation of synaptic release by astrocytes. Nat. Neurosci. 14, 1276-1284 (2011).
15. Shigetomi, E. & Kracun, S. A genetically targeted optical sensor to monitor calcium signals in astrocyte processes. Nat. Neurosci. 13, 759-766 (2010).
16. Shigetomi, E. et al. Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. J. Gen. Physiol. 141, 633-647 (2013).
17. Volterra, A., Liaudet, N. & Savtchouk, I. Astrocyte Ca2+ signalling: an unexpected complexity. Nat. Rev. Neurosci. 15, 327-335 (2014).
18. Haustein, M.D. et al. Conditions and constraints for astrocyte calcium signaling in the hippocampal mossy fiber pathway. Neuron 82, 413-429 (2014).
19. Rusakov, D.A.a, Bard, L., Stewart, M.G. & Henneberger, C. Diversity of astroglial functions alludes to subcellular specialisation. Trends Neurosci. 37, 228-242 (2014).
20. Paukert, M. et al. Norepinephrine controls astroglial responsiveness to local circuit activity. Neuron 82, 1263-1270 (2014).
21. Calcinaghi, N. et al. Metabotropic glutamate receptor mGluR5 is not involved in the early hemodynamic response. J. Cereb. Blood Flow Metab. 31, e1-e10 (2011).
22. Sun, W. et al. Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science (80). 339, 197-200 (2013).
23. Jego, P., Pacheco-Torres, J., Araque, A. & Canals, S. Functional MRI in mice lacking IP3-dependent calcium signaling in astrocytes. J. Cereb. Blood Flow Metab. 34, 1599-1603 (2014).
24. Fiacco, T.A. et al. Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron 54, 611-626 (2007).
25. Gurden, H., Uchida, N. & Mainen, Z.F. Sensory-evoked intrinsic optical signals in the olfactory bulb are coupled to glutamate release and uptake. Neuron 52, 335-345 (2006).
26. Petzold, G.C., Albeanu, D.F., Sato, T.F. & Murthy, V.N. Coupling of neural activity to blood flow in olfactory glomeruli is mediated by astrocytic pathways. Neuron 58, 897-910 (2008).
27. Chaigneau, E. et al. The relationship between blood flow and neuronal activity in the rodent olfactory bulb. J. Neurosci. 27, 6452-6460 (2007).
28. Shepherd, G.M., Chen, W.R. & Greer, C.A. in The Synaptic Organization of the Brain (ed. Shepherd, G.M.) 165-216 (Oxford University Press, 2004).
29. Dong, H.-W., Hayar, A. & Ennis, M. Activation of group I metabotropic glutamate receptors on main olfactory bulb granule cells and periglomerular cells enhances synaptic inhibition of mitral cells. J. Neurosci. 27, 5654-5663 (2007).
30. Jian, K., Cifelli, P., Pignatelli, A., Frigato, E. & Belluzzi, O. Metabotropic glutamate receptors 1 and 5 differentially regulate bulbar dopaminergic cell function. Brain Res. 1354, 47-63 (2010).
31. Kosaka, T. & Kosaka, K. "Interneurons" in the olfactory bulb revisited. Neurosci. Res. 69, 93-99 (2011).
32. Kunzelmann, P. et al. Late onset and increasing expression of the gap junction protein connexin30 in adult murine brain and long-term cultured astrocytes. Glia 25, 111-119 (1999).
33. Yang, Y. et al. Molecular comparison of GLT1+ and ALDH1L1+ astrocytes in vivo in astroglial reporter mice. Glia 59, 200-207 (2011).
34. Jabaudon, D. et al. Inhibition of uptake unmasks rapid extracellular turnover of glutamate of nonvesicular origin. Proc. Natl. Acad. Sci. USA 96, 8733-8738 (1999).
35. Van Den Pol, A.N. Presynaptic metabotropic glutamate receptors in adult and developing neurons: autoexcitation in the olfactory bulb. J. Comp. Neurol. 359, 253-271 (1995).
36. Slezak, M. et al. Transgenic mice for conditional gene manipulation in astroglial cells. Glia 55, 1565-1576 (2007).
37. Bonfanti, L. & Peretto, P. Radial glial origin of the adult neural stem cells in the subventricular zone. Prog. Neurobiol. 83, 24-36 (2007).
38. Oheim, M. et al. New red-fluorescent calcium indicators for optogenetics, photoactivation and multi-color imaging. Biochim. Biophys. Acta 1843, 2284-2306 (2014).
39. Roux, L., Benchenane, K., Rothstein, J.D., Bonvento, G. & Giaume, C. Plasticity of astroglial networks in olfactory glomeruli. Proc. Natl. Acad. Sci. USA 108, 18442-18446 (2011).
40. Lecoq, J., Tiret, P. & Charpak, S. Peripheral adaptation codes for high odor concentration in glomeruli. J. Neurosci. 29, 3067-3072 (2009).
41. Reeves, A.M.B., Shigetomi, E. & Khakh, B.S. Bulk loading of calcium indicator dyes to study astrocyte physiology: key limitations and improvements using morphological maps. J. Neurosci. 31, 9353-9358 (2011).
42. Winship, I.R., Plaa, N. & Murphy, T.H. Rapid astrocyte calcium signals correlate with neuronal activity and onset of the hemodynamic response in vivo. J. Neurosci. 27, 6268-6272 (2007).
43. Lind, B.L., Brazhe, R., Jessen, S.B., Tan, F.C.C. & Lauritzen, M.J. Rapid stimulus-evoked astrocyte Ca2+ elevations and hemodynamic responses in mouse somatosensory cortex in vivo. Proc. Natl. Acad. Sci. USA 110, E4678-E4687 (2013).
44. Winpenny, E. et al. Sequential generation of olfactory bulb glutamatergic neurons by Neurog2-expressing precursor cells. Neural Dev. 6, 12 (2011).
45. Nissant, A. & Pallotto, M. Integration and maturation of newborn neurons in the adult olfactory bulb-from synapses to function. Eur. J. Neurosci. 33, 1069-1077 (2011).
46. Hartfuss, E., Galli, R., Heins, N. & Götz, M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229, 15-30 (2001).
47. Takata, N. et al. Cerebral blood flow modulation by basal forebrain or whisker stimulation can occur independently of large cytosolic Ca2+ signaling in astrocytes. PLoS ONE 8, e66525 (2013).
48. Bonder, D.E. & McCarthy, K.D. Astrocytic Gq-GPCR-linked IP3R-dependent Ca2+ signaling does not mediate neurovascular coupling in mouse visual cortex in vivo. J. Neurosci. 34, 13139-13150 (2014).
49. Kleinfeld, D., Mitra, P.P., Helmchen, F. & 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, 15741-15746 (1998).
50. Jukovskaya, N., Tiret, P., Lecoq, J. & Charpak, S. What does local functional hyperemia tell about local neuronal activation? J. Neurosci. 31, 1579-1582 (2011).