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Gliotransmission at Tripartite Synapses

  • Candela González-Arias
  • Gertrudis PereaEmail author
Chapter
Part of the Springer Series in Computational Neuroscience book series (NEUROSCI)

Abstract

Signal exchange between astrocytes and neurons at tripartite synapses has emerged as a crucial element of neural circuits in the brain. The position of astrocyte processes facing synapses provides the proper structural and functional conditions for neuron-astrocyte communication giving rise to the concept of “tripartite synapse”. These synapses envisage an active role for astrocytes in their function whereby: (i) astrocytes sense neurotransmission by neurotransmitter transporter and receptors; (ii) synaptic activity stimulates astrocytic intracellular Ca2+ levels; (iii) astrocytes release neuroactive substances, gliotransmitters, that in turn regulate neuronal excitability and synaptic transmission. The ability of astrocytes to release different gliotransmitters and modulate synaptic activity deepens our knowledge of the brain physiology. In addition to the traditional homeostatic roles in the extracellular ion balance, neurotransmitter uptake from the extracellular space, and metabolic energy supply to neurons, astrocytes play active roles in synaptic transmission and plasticity, being involved in the coding information and cognitive processes by brain networks.

Keywords

Astrocytes Gliotransmission Tripartite synapse Synaptic plasticity Information coding 

Notes

Acknowledgements

The authors would like to thank Dr. Washington Buño for his helpful comments on the manuscript. This work was supported by grants from Ministerio de Economia y Competitividad, Spain, MINECO: Consolider, CSD2010-00045; Ramón y Cajal Program, RYC-2012-12014; and BFU2013-47265R.

References

  1. Agulhon C, Fiacco TA, McCarthy KD (2010) Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca2+ signaling. Science 327(5970):1250–1254PubMedCrossRefGoogle Scholar
  2. Agulhon C, Boyt KM, Xie AX, Friocourt F, Roth BL, McCarthy KD (2013) Modulation of the autonomic nervous system and behaviour by acute glial cell Gq protein-coupled receptor activation in vivo. J Physiol 591(22):5599–5609PubMedPubMedCentralCrossRefGoogle Scholar
  3. Allen NJ (2013) Role of glia in developmental synapse formation. Curr Opin Neurobiol 23(6):1027–1033PubMedCrossRefGoogle Scholar
  4. Angulo MC, Kozlov AS, Charpak S, Audinat E (2004) Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J Neurosci: Official J Soc Neurosci 24(31):6920–6927CrossRefGoogle Scholar
  5. Araque A, Sanzgiri RP, Parpura V, Haydon PG (1998) Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J Neurosci: Official J Soc Neurosci 18(17):6822–6829CrossRefGoogle Scholar
  6. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22(5):208–215PubMedPubMedCentralCrossRefGoogle Scholar
  7. Araque A, Li N, Doyle RT, Haydon PG (2000) SNARE protein-dependent glutamate release from astrocytes. J Neurosci: Official J Soc Neurosci 20(2):666–673CrossRefGoogle Scholar
  8. Araque A, Carmignoto G, Haydon PG, Oliet SH, Robitaille R, Volterra A (2014) Gliotransmitters travel in time and space. Neuron 81(4):728–739PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bazargani N, Attwell D (2016) Astrocyte calcium signaling: the third wave. Nat Neurosci 19(2):182–189PubMedPubMedCentralCrossRefGoogle Scholar
  10. Beppu K, Sasaki T, Tanaka KF, Yamanaka A, Fukazawa Y, Shigemoto R et al (2014) Optogenetic countering of glial acidosis suppresses glial glutamate release and ischemic brain damage. Neuron 81(2):314–320PubMedCrossRefGoogle Scholar
  11. Bernardinelli Y, Randall J, Janett E, Nikonenko I, Konig S, Jones EV et al (2014) Activity-dependent structural plasticity of perisynaptic astrocytic domains promotes excitatory synapse stability. Current Biol: CB 24(15):1679–1688PubMedCrossRefGoogle Scholar
  12. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL et al (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391(6664):281–285PubMedCrossRefGoogle Scholar
  13. Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhauser C, Pilati E et al (2004) Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 7(6):613–620PubMedCrossRefGoogle Scholar
  14. Bonansco C, Couve A, Perea G, Ferradas CA, Roncagliolo M, Fuenzalida M (2011) Glutamate released spontaneously from astrocytes sets the threshold for synaptic plasticity. Eur J Neurosci 33(8):1483–1492PubMedCrossRefGoogle Scholar
  15. Bowser DN (2007) Khakh BS (2007) Vesicular ATP is the predominant cause of intercellular calcium waves in astrocytes. J Gener Physiol 129(6):485–491CrossRefGoogle Scholar
  16. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci: Official J Soc Neurosci 22(1):183–192CrossRefGoogle Scholar
  17. Cao X, Li LP, Wang Q, Wu Q, Hu HH, Zhang M et al (2013) Astrocyte-derived ATP modulates depressive-like behaviors. Nat Med 19(6):773–777PubMedCrossRefGoogle Scholar
  18. Chen N, Sugihara H, Sharma J, Perea G, Petravicz J, Le C et al (2012) Nucleus basalis-enabled stimulus-specific plasticity in the visual cortex is mediated by astrocytes. Proc Natl Acad Sci U S A 109(41):E2832–E2841PubMedPubMedCentralCrossRefGoogle Scholar
  19. Citri A, Malenka RC (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacol Official Publ Am Coll Neuropsychopharmacol 33(1):18–41CrossRefGoogle Scholar
  20. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247(4941):470–473CrossRefPubMedPubMedCentralGoogle Scholar
  21. D’Ascenzo M, Fellin T, Terunuma M, Revilla-Sanchez R, Meaney DF, Auberson YP et al (2007) mGluR5 stimulates gliotransmission in the nucleus accumbens. Proc Natl Acad U S A 104(6):1995–2000CrossRefGoogle Scholar
  22. Di Castro MA, Chuquet J, Liaudet N, Bhaukaurally K, Santello M, Bouvier D et al (2011) Local Ca2+ detection and modulation of synaptic release by astrocytes. Nature Neurosci 14(10):1276–1284PubMedCrossRefGoogle Scholar
  23. Ding S, Fellin T, Zhu Y, Lee SY, Auberson YP, Meaney DF et al (2007) Enhanced astrocytic Ca2+ signals contribute to neuronal excitotoxicity after status epilepticus. J Neurosci: Official J Soc Neurosci 27(40):10674–10684PubMedCrossRefGoogle Scholar
  24. Ding F, O’Donnell J, Thrane AS, Zeppenfeld D, Kang H, Xie L et al (2013) alpha1-Adrenergic receptors mediate coordinated Ca2+ signaling of cortical astrocytes in awake, behaving mice. Cell Calcium 54(6):387–394PubMedCrossRefPubMedCentralGoogle Scholar
  25. 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(1):43–57PubMedPubMedCentralCrossRefGoogle Scholar
  26. Domercq M, Brambilla L, Pilati E, Marchaland J, Volterra A, Bezzi P (2006) P2Y1 receptor-evoked glutamate exocytosis from astrocytes: control by tumor necrosis factor-alpha and prostaglandins. J Biol Chem 281(41):30684–30696PubMedPubMedCentralCrossRefGoogle Scholar
  27. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, Carmignoto G (2004) Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43(5):729–743PubMedCrossRefGoogle Scholar
  28. Fellin T, Halassa MM, Terunuma M, Succol F, Takano H, Frank M et al (2009) Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo. Proc Natl Acad Sci U S A 106(35):15037–15042PubMedPubMedCentralCrossRefGoogle Scholar
  29. Fiacco TA, Agulhon C, Taves SR, Petravicz J, Casper KB, Dong X et al (2007) Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron 54(4):611–626PubMedCrossRefGoogle Scholar
  30. Figueiredo M, Lane S, Stout RF Jr, Liu B, Parpura V, Teschemacher AG et al (2014) Comparative analysis of optogenetic actuators in cultured astrocytes. Cell Calcium 56(3):208–214PubMedPubMedCentralCrossRefGoogle Scholar
  31. Fujita T, Chen MJ, Li B, Smith NA, Peng W, Sun W et al (2014) Neuronal transgene expression in dominant-negative SNARE mice. J Neurosci: Official J Soc Neurosci 34(50):16594–16604CrossRefGoogle Scholar
  32. Gee JM, Smith NA, Fernandez FR, Economo MN, Brunert D, Rothermel M et al (2014) Imaging activity in neurons and glia with a Polr2a-based and cre-dependent GCaMP5G-IRES-tdTomato reporter mouse. Neuron 83(5):1058–1072PubMedPubMedCentralCrossRefGoogle Scholar
  33. Gomez-Gonzalo M, Navarrete M, Perea G, Covelo A, Martin-Fernandez M, Shigemoto R et al (2014) Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission. Cereb CortexGoogle Scholar
  34. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S et al (2010) Astrocytes control breathing through pH-dependent release of ATP. Science 329(5991):571–575PubMedPubMedCentralCrossRefGoogle Scholar
  35. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K (2009) Optical deconstruction of parkinsonian neural circuitry. Science 324(5925):354–359PubMedCrossRefGoogle Scholar
  36. Habbas S, Santello M, Becker D, Stubbe H, Zappia G, Liaudet N et al (2015) Neuroinflammatory TNF alpha impairs memory via astrocyte signaling. Cell 163(7):1730–1741PubMedCrossRefGoogle Scholar
  37. Haber M, Zhou L, Murai KK (2006) Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci: Official J Soc Neurosci 26(35):8881–8891PubMedCrossRefGoogle Scholar
  38. Halassa MM, Fellin T, Takano H, Dong JH, Haydon PG (2007) Synaptic islands defined by the territory of a single astrocyte. J Neurosci: Official J Soc Neurosci 27(24):6473–6477CrossRefGoogle Scholar
  39. Halassa MM, Florian C, Fellin T, Munoz JR, Lee SY, Abel T et al (2009) Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61(2):213–219PubMedPubMedCentralCrossRefGoogle Scholar
  40. Hamilton NB, Attwell D (2010) Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci 11(4):227–238PubMedPubMedCentralCrossRefGoogle Scholar
  41. Henneberger C, Papouin T, Oliet SH, Rusakov DA (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463(7278):232–236PubMedPubMedCentralCrossRefGoogle Scholar
  42. Jahn HM, Scheller A, Kirchhoff F (2015) Genetic control of astrocyte function in neural circuits. Front Cell Neurosci 9:310PubMedPubMedCentralCrossRefGoogle Scholar
  43. Jo S, Yarishkin O, Hwang YJ, Chun YE, Park M, Woo DH et al (2014) GABA from reactive astrocytes impairs memory in mouse models of Alzheimer’s disease. Nat Med 20(8):886–896PubMedCrossRefGoogle Scholar
  44. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, Domercq M et al (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nat Neurosci 10(3):331–339PubMedPubMedCentralCrossRefGoogle Scholar
  45. Kim TK, Eberwine JH (2010) Mammalian cell transfection: the present and the future. Anal Bioanal Chem 397(8):3173–3178PubMedPubMedCentralCrossRefGoogle Scholar
  46. Le Bail M, Martineau M, Sacchi S, Yatsenko N, Radzishevsky I, Conrod S et al (2015) Identity of the NMDA receptor coagonist is synapse specific and developmentally regulated in the hippocampus. Proc Natl Acad Sci U S A 112(2):E204–E213PubMedCrossRefGoogle Scholar
  47. Lee S, Yoon BE, Berglund K, Oh SJ, Park H, Shin HS et al (2010) Channel-mediated tonic GABA release from glia. Science 330(6005):790–806PubMedCrossRefGoogle Scholar
  48. Lee HS, Ghetti A, Pinto-Duarte A, Wang X, Dziewczapolski G, Galimi F et al (2014) Astrocytes contribute to gamma oscillations and recognition memory. Proc Natl Acad Sci U S A 111(32):E3343–E3352PubMedPubMedCentralCrossRefGoogle Scholar
  49. Lima A, Sardinha VM, Oliveira AF, Reis M, Mota C, Silva MA et al (2014) Astrocyte pathology in the prefrontal cortex impairs the cognitive function of rats. Mol Psychiatry 19(7):834–841PubMedCrossRefGoogle Scholar
  50. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M et al (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304(5673):1021–1024PubMedCrossRefGoogle Scholar
  51. Mariotti L, Losi G, Sessolo M, Marcon I, Carmignoto G (2016) The inhibitory neurotransmitter GABA evokes long-lasting Ca2+ oscillations in cortical astrocytes. Glia 64(3):363–373PubMedCrossRefGoogle Scholar
  52. Masamoto K, Unekawa M, Watanabe T, Toriumi H, Takuwa H, Kawaguchi H et al (2015) Unveiling astrocytic control of cerebral blood flow with optogenetics. Sci Rep 5:11455PubMedPubMedCentralCrossRefGoogle Scholar
  53. Matos M, Shen HY, Augusto E, Wang Y, Wei CJ, Wang YT et al (2015) Deletion of adenosine A2A receptors from astrocytes disrupts glutamate homeostasis leading to psychomotor and cognitive impairment: relevance to schizophrenia. Biol Psychiat 78(11):763–774PubMedCrossRefGoogle Scholar
  54. Min R, Nevian T (2012) Astrocyte signaling controls spike timing-dependent depression at neocortical synapses. Nat Neurosci 15(5):746–753PubMedCrossRefGoogle Scholar
  55. Mothet JP, Pollegioni L, Ouanounou G, Martineau M, Fossier P, Baux G (2005) Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proc Natl Acad Sci U S A 102(15):5606–5611PubMedPubMedCentralCrossRefGoogle Scholar
  56. Mothet JP, Le Bail M, Billard JM (2015) Time and space profiling of NMDA receptor co-agonist functions. J Neurochem 135(2):210–225PubMedCrossRefGoogle Scholar
  57. Navarrete M, Araque A (2008) Endocannabinoids mediate neuron-astrocyte communication. Neuron 57(6):883–893PubMedCrossRefGoogle Scholar
  58. Navarrete M, Araque A (2010) Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron 68(1):113–126PubMedCrossRefGoogle Scholar
  59. Navarrete M, Perea G, Fernandez de Sevilla D, Gomez-Gonzalo M, Nunez A, Martin ED et al (2012) Astrocytes mediate in vivo cholinergic-induced synaptic plasticity. PLoS Biol 10(2):e1001259PubMedPubMedCentralCrossRefGoogle Scholar
  60. Nimmerjahn A, Mukamel EA, Schnitzer MJ (2009) Motor behavior activates Bergmann glial networks. Neuron 62(3):400–412PubMedPubMedCentralCrossRefGoogle Scholar
  61. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA et al (2006) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125(4):775–784PubMedCrossRefGoogle Scholar
  62. Panatier A, Vallee J, Haber M, Murai KK, Lacaille JC, Robitaille R (2011) Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146(5):785–798CrossRefGoogle Scholar
  63. Pankratov Y, Lalo U (2015) Role for astroglial alpha1-adrenoreceptors in gliotransmission and control of synaptic plasticity in the neocortex. Front Cell Neurosci 9:230PubMedPubMedCentralCrossRefGoogle Scholar
  64. Papouin T, Ladepeche L, Ruel J, Sacchi S, Labasque M, Hanini M et al (2012) Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell 150(3):633–646PubMedCrossRefGoogle Scholar
  65. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY et al (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310(5745):113–116PubMedPubMedCentralCrossRefGoogle Scholar
  66. Paukert M, Agarwal A, Cha J, Doze VA, Kang JU, Bergles DE (2014) Norepinephrine controls astroglial responsiveness to local circuit activity. Neuron 82(6):1263–70PubMedPubMedCentralCrossRefGoogle Scholar
  67. Perea G, Araque A (2005) Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci 25(9):2192–2203PubMedCrossRefGoogle Scholar
  68. Perea G, Araque A (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317(5841):1083–1086CrossRefPubMedPubMedCentralGoogle Scholar
  69. Perea G, Navarrete M, Araque A (2009) Tripartite synapses: astrocytes process and control synaptic information. Trends in Neurosci 32(8):421–431CrossRefGoogle Scholar
  70. Perea G, Sur M, Araque A (2014a) Neuron-glia networks: integral gear of brain function. Front Cell Neurosci 8:378PubMedPubMedCentralCrossRefGoogle Scholar
  71. Perea G, Yang A, Boyden ES, Sur M (2014b) Optogenetic astrocyte activation modulates response selectivity of visual cortex neurons in vivo. Nat Commun 5:3262PubMedPubMedCentralCrossRefGoogle Scholar
  72. Perez-Alvarez A, Navarrete M, Covelo A, Martin ED, Araque A (2014) Structural and functional plasticity of astrocyte processes and dendritic spine interactions. J Neurosci: Official J Soc Neurosci 34(38):12738–12744PubMedCrossRefGoogle Scholar
  73. Perry E, Walker M, Grace J, Perry R (1999) Acetylcholine in mind: a neurotransmitter correlate of consciousness? Trends Neurosci 22(6):273–280PubMedCrossRefGoogle Scholar
  74. Pirttimaki TM, Codadu NK, Awni A, Pratik P, Nagel DA, Hill EJ et al (2013) alpha7 Nicotinic receptor-mediated astrocytic gliotransmitter release: Abeta effects in a preclinical Alzheimer’s mouse model. PloS One 8(11):e81828PubMedPubMedCentralCrossRefGoogle Scholar
  75. Saab AS, Neumeyer A, Jahn HM, Cupido A, Simek AA, Boele HJ et al (2012) Bergmann glial AMPA receptors are required for fine motor coordination. Science 337(6095):749–753PubMedCrossRefGoogle Scholar
  76. Santello M, Bezzi P, Volterra A (2011) TNF alpha controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69(5):988–1001PubMedCrossRefGoogle Scholar
  77. Santello M, Cali C, Bezzi P (2012) Gliotransmission and the tripartite synapse. Adv Exp Med Biol 970:307–331PubMedCrossRefGoogle Scholar
  78. Sasaki T, Kuga N, Namiki S, Matsuki N, Ikegaya Y (2011) Locally synchronized astrocytes. Cerebral cortex. 21(8):1889–1900PubMedCrossRefGoogle Scholar
  79. Sasaki T, Beppu K, Tanaka KF, Fukazawa Y, Shigemoto R, Matsui K (2012) Application of an optogenetic byway for perturbing neuronal activity via glial photostimulation. Proc Natl Acad Sci U S A 109(50):20720–20725PubMedPubMedCentralCrossRefGoogle Scholar
  80. Scofield MD, Boger HA, Smith RJ, Li H, Haydon PG, Kalivas PW (2015) Gq-DREADD selectively initiates glial glutamate release and inhibits Cue-induced cocaine seeking. Biol Psychiatry 78(7):441–451PubMedCrossRefGoogle Scholar
  81. Serrano A, Haddjeri N, Lacaille JC, Robitaille R (2006) GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J Neurosci 26(20):5370–5382PubMedCrossRefPubMedCentralGoogle Scholar
  82. Shigetomi E, Bowser DN, Sofroniew MV, Khakh BS (2008) Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons. J Neurosci 28(26):6659–6663PubMedPubMedCentralCrossRefGoogle Scholar
  83. Shigetomi E, Jackson-Weaver O, Huckstepp RT, O’Dell TJ, Khakh BS (2013) TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release. J Neurosci: Official J Soc Neurosci 33(24):10143–10153CrossRefGoogle Scholar
  84. Sloan SA, Barres BA (2014) Looks can be deceiving: reconsidering the evidence for gliotransmission. Neuron 84(6):1112–1115PubMedPubMedCentralCrossRefGoogle Scholar
  85. Takata N, Mishima T, Hisatsune C, Nagai T, Ebisui E, Mikoshiba K et al (2011) Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo. J Neurosci: Official J Soc Neurosci 31(49):18155–18165PubMedCrossRefGoogle Scholar
  86. Talantova M, Sanz-Blasco S, Zhang X, Xia P, Akhtar MW, Okamoto S et al (2013) Abeta induces astrocytic glutamate release, extrasynaptic NMDA receptor activation, and synaptic loss. Proc Natl Acad Sci U S A 110(27):E2518–E2527Google Scholar
  87. Tang F, Lane S, Korsak A, Paton JF, Gourine AV, Kasparov S et al (2014) Lactate-mediated glia-neuronal signalling in the mammalian brain. Nat Commun 5:3284PubMedPubMedCentralCrossRefGoogle Scholar
  88. Volterra A, Bezzi P (2002) Release of transmitters from glial cells. In: Volterra A, Magistretti PJ, Haydon PG (eds) The tripartite synapse: glia in synaptic transmission. Oxford University Press, pp 164–184Google Scholar
  89. Volterra A, Liaudet N, Savtchouk I (2014) Astrocyte Ca2+ signalling: an unexpected complexity. Nat Rev Neurosci 15(5):327–335CrossRefPubMedPubMedCentralGoogle Scholar
  90. Wang X, Lou N, Xu Q, Tian GF, Peng WG, Han X et al (2006) Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nat Neurosci 9(6):816–823PubMedCrossRefGoogle Scholar
  91. Xie AX, Petravicz J, McCarthy KD (2015) Molecular approaches for manipulating astrocytic signaling in vivo. Front Cell Neurosci 9:144PubMedPubMedCentralCrossRefGoogle Scholar
  92. Yang J, Yu H, Zhou D, Zhu K, Lou H, Duan S et al (2015) Na+–Ca2+ exchanger mediates ChR2-induced [Ca2+]i elevation in astrocytes. Cell Calcium 58(3):307–316PubMedCrossRefGoogle Scholar
  93. Yoo SS, Hu PT, Gujar N, Jolesz FA, Walker MP (2007) A deficit in the ability to form new human memories without sleep. Nat Neurosci 10(3):385–392PubMedCrossRefGoogle Scholar
  94. Yoon BE, Lee CJ (2014) GABA as a rising gliotransmitter. Front Neural Circ 8:141Google Scholar
  95. Zhang Q, Fukuda M, Van Bockstaele E, Pascual O, Haydon PG (2004) Synaptotagmin IV regulates glial glutamate release. Proc Natl Acad Sci U S A 101(25):9441–9446PubMedPubMedCentralCrossRefGoogle Scholar
  96. Zhang F, Gradinaru V, Adamantidis AR, Durand R, Airan RD, de Lecea L et al (2010) Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat Protoc 5(3):439–456PubMedPubMedCentralCrossRefGoogle Scholar
  97. Zorec R, Araque A, Carmignoto G, Haydon PG, Verkhratsky A, Parpura V (2012) Astroglial excitability and gliotransmission: an appraisal of Ca2+ as a signalling route. ASN Neuro 4(2)CrossRefGoogle Scholar
  98. Zorec R, Verkhratsky A, Rodriguez JJ, Parpura V (2015) Astrocytic vesicles and gliotransmitters: slowness of vesicular release and synaptobrevin2-laden vesicle nanoarchitecture. NeuroscienceGoogle Scholar

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Authors and Affiliations

  1. 1.Functional and Systems NeurobiologyCajal Institute (CSIC)MadridSpain

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