A Neuron–Glial Perspective for Computational Neuroscience

  • Maurizio De PittàEmail author
  • Hugues Berry
Part of the Springer Series in Computational Neuroscience book series (NEUROSCI)


There is growing excitement around glial cells, as compelling evidence point to new, previously unimaginable roles for these cells in information processing of the brain, with the potential to affect behavior and higher cognitive functions. Among their many possible functions, glial cells could be involved in practically every aspect of the brain physiology in health and disease. As a result, many investigators in the field welcome the notion of a neuron–glial paradigm of brain function, as opposed to Ramon y Cajal’s more classical neuronal doctrine which identifies neurons as the prominent, if not the only, cells capable of a signaling role in the brain. The demonstration of a brain-wide neuron–glial paradigm however remains elusive and so does the notion of what neuron–glial interactions could be functionally relevant for the brain computational tasks. In this perspective, we present a selection of arguments inspired by available experimental and modeling studies with the aim to computational neuroscience that no longer is a mere prerogative of neuronal signaling but rather it is the outcome of complex interaction between neurons and glial cells.


Neuron–glia paradigm Calcium coding Neuron–glial systems Oligodendrocytes Microglia 





\(\upalpha \)-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (receptor)


Astrocyte-to-neuron lactate shuttle


Action potential


Aquaporin channel type 4


Cyclic adenosine monophosphate


Calcium-induced calcium release


Central nervous system


Extracellular space


\(\upgamma \)-Aminobutyric acid


Glutamate–glutamine cycle


G protein–coupled receptor


Inositol 1,4,5-trisphosphate


Inwardly rectifying \({\mathrm{K}^+}\) channel


Long-term depression


Long-term potentiation


Monocarboxylate transporter




\({\mathrm{Na}^+}\)-\({\mathrm{HCO}_3^-}\) cotransporter


\({\mathrm{Na}^+}\)/\({\mathrm{K}^+}\)-ATPase pump


N-Methyl-d-aspartate (receptor)


Slow inward (outward) current


Supraoptic nucleus


Steady-state synaptic release

TNF\(\upalpha \)

Tumor necrosis factor alpha


Primary visual cortex



MDP acknowledges the support of Pôle emploi Rhône-Alpes and of the Junior Leader Postdoctoral Fellowship Program by “la Caixa” Banking Foundation (LCF/BQ/LI18/11630006). Completion of this chapter was also possible thank to the support of the Basque Government by the BERC 2018–2021 program and by the Spanish Ministry of Science, Innovation and Universities: BCAM Severo Ochoa accreditation SEV-2017-0718.


  1. Abbott LF, DePasquale B, Memmesheimer R-M (2016) Building functional networks of spiking model neurons. Nat Neurosci 19(3):350PubMedPubMedCentralCrossRefGoogle Scholar
  2. 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 59:932–946PubMedPubMedCentralCrossRefGoogle Scholar
  3. Alberdi E, Sánchez-Gómez MV, Marino A, Matute C (2002) Ca\(^{2+}\) influx through AMPA or kainate receptors alone is sufficient to initiate excitotoxicity in cultured oligodendrocytes. Neurobiol Dis 9(2):234–243PubMedCrossRefGoogle Scholar
  4. Allaman I, Belanger M, Magistretti PJ (2011) Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 34(2):76–87PubMedCrossRefGoogle Scholar
  5. Allen NJ (2013) Role of glia in developmental synapse formation. Curr Opin Neurobiol 23(6):1027–1033CrossRefGoogle Scholar
  6. Alvarellos-González A, Pazos A, Porto-Pazos AB (2012) Computational models of neuron-astrocyte interactions lead to improved efficacy in the performance of neural networks. Comput Math Methods Med 2012:476324PubMedPubMedCentralCrossRefGoogle Scholar
  7. Amzica F, Massimini M, Manfridi A (2002) Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo. J Neurosci 22(3):1042–1053PubMedCrossRefGoogle Scholar
  8. Angulo MC, Le Meur K, Kozlov AS, Charpak S, Audinat E (2008) GABA, a forgotten gliotransmitter. Prog Neurobiol 86(3):297–303PubMedCrossRefGoogle Scholar
  9. Aoyama K, Watabe M, Nakaki T (2008) Regulation of neuronal glutathione synthesis. J Pharmacol Sci 108(3):227–238PubMedCrossRefGoogle Scholar
  10. Arancibia-Carcamo IL, Ford MC, Cossell L, Ishida K, Tohyama K, Attwell D (2017) Node of Ranvier length as a potential regulator of myelinated axon conduction speed. eLife 6:e23329Google Scholar
  11. Araque A, Carmignoto G, Haydon PG, Oliet SHR, Robitaille R, Volterra A (2014) Gliotransmitters travel in time and space. Neuron 81(4):728–739PubMedPubMedCentralCrossRefGoogle Scholar
  12. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 23(5):208–215CrossRefGoogle Scholar
  13. Attwell D, Buchan AM, Charpak S, Lauritzen M, MacVicar BA, Newman EA (2010) Glial and neuronal control of brain blood flow. Nature 468(7321):232–243PubMedPubMedCentralCrossRefGoogle Scholar
  14. Barbour B (2001) An evaluation of synapse independence. J Neurosci 21(20):7969–7984PubMedPubMedCentralCrossRefGoogle Scholar
  15. Barres B (2008) The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60(3):430–440PubMedCrossRefPubMedCentralGoogle Scholar
  16. Bear MF, Malenka RC (1994) Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4(3):389–399PubMedCrossRefPubMedCentralGoogle Scholar
  17. Beck JM, Ma WJ, Kiani R, Hanks T, Churchland AK, Roitman J, Shadlen MN, Latham PE, Pouget A (2008) Probabilistic population codes for Bayesian decision making. Neuron 60(6):1142–1152PubMedPubMedCentralCrossRefGoogle Scholar
  18. Becquet D, Girardet C, Guillaumond F, François-Bellan A-M, Bosler O (2008) Ultrastructural plasticity in the rat suprachiasmatic nucleus. Possible involvement in clock entrainment. Glia 56(3):294–305PubMedCrossRefPubMedCentralGoogle Scholar
  19. Bélanger M, Allaman I, Magistretti PJ (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab 14(6):724–738PubMedCrossRefGoogle Scholar
  20. Bellesi M, de Vivo L, Tononi G, Cirelli C (2015) Effects of sleep and wake on astrocytes: clues from molecular and ultrastructural studies. BMC Biol 13(1):66PubMedPubMedCentralCrossRefGoogle Scholar
  21. Bellesi M, Pfister-Genskow M, Maret S, Keles S, Tononi G, Cirelli C (2013) Effects of sleep and wake on oligodendrocytes and their precursors. J Neurosci 33(36):14288–14300PubMedPubMedCentralCrossRefGoogle Scholar
  22. Benz B, Grima G, Do KQ (2004) Glutamate-induced homocysteic acid release from astrocytes: possible implication in glia-neuron signaling. Neuroscience 124(2):377–386PubMedCrossRefGoogle Scholar
  23. Bernardinelli Y, Muller D, Nikonenko I (2014a) Astrocyte-synapse structural plasticity. Neural Plast 2014:23215CrossRefGoogle Scholar
  24. Bernardinelli Y, Randall J, Janett E, Nikonenko I, König S, Jones EV, Flores CE, Murai KK, Bochet CG, Holtmaat A, Muller D (2014b) Activity-dependent structural plasticity of perisynaptic astrocytic domains promotes excitatory synapse stability. Curr Biol 24(15):1679–1688PubMedCrossRefGoogle Scholar
  25. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11–21CrossRefGoogle Scholar
  26. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A (2001) CXCR4-activated astrocyte glutamate release via TNF\(\alpha \): amplification by microglia triggers neurotoxicity. Nat Neurosci 4(7):702–710PubMedCrossRefGoogle Scholar
  27. Bezzi P, Volterra A (2001) A neuron-glia signalling network in the active brain. Curr Opin Neurobiol 11:387–394PubMedCrossRefGoogle Scholar
  28. Bialek W, Rieke F (1992) Reliability and information transmission in spiking neurons. Trends Neurosci 15(11):428–434PubMedCrossRefGoogle Scholar
  29. Biber K, Laurie DJ, Berthele A, Sommer B, Tölle TR, Gebicke-Härter P-J, Van Calker D, Boddeke HWGM (1999) Expression and signaling of group I metabotropic glutamate receptors in astrocytes and microglia. J Neurochem 72(4):1671–1680PubMedCrossRefGoogle Scholar
  30. Bienenstock E, Cooper L, Munro P (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2(1):32–48PubMedCrossRefGoogle Scholar
  31. Bindocci E, Savtchouk I, Liaudet N, Becker D, Carriero G, Volterra A (2017) Three-dimensional Ca\(^{2+}\) imaging advances understanding of astrocyte biology. Science 356:6339CrossRefGoogle Scholar
  32. Bjorness TE, Dale N, Mettlach G, Sonneborn A, Sahin B, Fienberg AA, Yanagisawa M, Bibb JA, Greene RW (2016) An adenosine-mediated glial-neuronal circuit for homeostatic sleep. J Neurosci 36(13):3709–3721PubMedPubMedCentralCrossRefGoogle Scholar
  33. Bowser DN, Khakh BS (2007) Vesicular ATP is the predominant cause of intercellular calcium waves in astrocytes. J Gen Physiol 129(6):485–491PubMedPubMedCentralCrossRefGoogle Scholar
  34. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocyte in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22(1):183–192CrossRefPubMedPubMedCentralGoogle Scholar
  35. Butt AM (2006) Neurotransmitter-mediated calcium signalling in oligodendrocyte physiology and pathology. Glia 54(7):666–675PubMedCrossRefGoogle Scholar
  36. Butt AM, Pugh M, Hubbard P, James G (2004) Functions of optic nerve glia: axoglial signalling in physiology and pathology. Eye 18(11):1110PubMedCrossRefGoogle Scholar
  37. Buzsáki G (2010) Neural syntax: cell assemblies, synapsembles, and readers. Neuron 68(3):362–385PubMedPubMedCentralCrossRefGoogle Scholar
  38. Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304(5679):1926–1929PubMedCrossRefGoogle Scholar
  39. Carr CE, Konishi M (1990) A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10(10):3227–3246PubMedCrossRefGoogle Scholar
  40. Castro MA, Beltrán FA, Brauchi S, Concha II (2009) A metabolic switch in brain: glucose and lactate metabolism modulation by ascorbic acid. J Neurochem 110(2):423–440PubMedCrossRefGoogle Scholar
  41. Chao TI, Rickmann M, Wolff JR (2002) The synapse-astrocyte boundary: an anatomical basis for an integrative role of glia in synaptic transmission. In: Volterra A, Magistretti PJ, Haydon PG (eds) The tripartite synapse: glia in synaptic transmission (Chap. 1). Oxford University Press, New York, pp 3–23Google Scholar
  42. Chen N, Sugihara H, Sharma J, Perea G, Petravicz J, Le C, Sur M (2012) Nucleus basalis enabled stimulus specific plasticity in the visual cortex is mediated by astrocytes. Proc Natl Acad Sci USA 109(41):E2832–E2841CrossRefPubMedPubMedCentralGoogle Scholar
  43. Chever O, Djukic B, McCarthy KD, Amzica F (2010) Implication of Kir4.1 channel in excess potassium clearance: an in vivo study on anesthetized glial-conditional Kir4.1 knock-out mice. J Neurosci 30(47):15769–15777PubMedCrossRefGoogle Scholar
  44. Churchill L, Rector DM, Yasuda K, Fix C, Rojas MJ, Yasuda T, Krueger JM (2008) Tumor necrosis factor \(\alpha \): activity dependent expression and promotion of cortical column sleep in rats. Neuroscience 156(1):71–80PubMedPubMedCentralCrossRefGoogle Scholar
  45. Cirelli C, Gutierrez CM, Tononi G (2004) Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41(1):35–43PubMedCrossRefGoogle Scholar
  46. Clarke LE, Barres BA (2013) Emerging roles of astrocytes in neural circuit development. Nat Rev Neurosci 14(5):311–321PubMedPubMedCentralCrossRefGoogle Scholar
  47. Clements JD (1996) Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci 19(5):163–171CrossRefGoogle Scholar
  48. Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, Matteoli M, Verderio C (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278(2):1354–1362PubMedPubMedCentralCrossRefGoogle Scholar
  49. Colombo JA, Reisin HD (2004) Interlaminar astroglia of the cerebral cortex: a marker of the primate brain. Brain Res 1006(1):126–131PubMedCrossRefGoogle Scholar
  50. Condamine S, Lavoie R, Verdier D, Kolta A (2018) Functional rhythmogenic domains defined by astrocytic networks in the trigeminal main sensory nucleus. Glia 66(2):311–326PubMedCrossRefGoogle Scholar
  51. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247(4941):470–473PubMedPubMedCentralCrossRefGoogle Scholar
  52. Cui Y, Yang Y, Ni Z, Dong Y, Cai G, Foncelle A, Ma S, Sang K, Tang S, Li Y, Berry H, Shengzi W, Hailan H (2018) Astroglial Kir4.1 in the lateral habenula drives neuronal bursts in depression. Nature 554(7692):323PubMedCrossRefGoogle Scholar
  53. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105PubMedCrossRefGoogle Scholar
  54. Dani JW, Chernjavsky A, Smith SJ (1992) Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8:429–440CrossRefPubMedPubMedCentralGoogle Scholar
  55. De Pittà M, Brunel N (2016) Modulation of synaptic plasticity by glutamatergic gliotransmission: a modeling study. Neural Plast p 7607924Google Scholar
  56. De Pittà M, Brunel N, Volterra A (2015) Astrocytes: orchestrating synaptic plasticity? NeuroscienceGoogle Scholar
  57. De Pittà M, Goldberg M, Volman V, Berry H, Ben-Jacob E (2009) Glutamate-dependent intracellular calcium and IP\(_{3}\) oscillating and pulsating dynamics in astrocytes. J Biol Phys 35:383–411PubMedPubMedCentralCrossRefGoogle Scholar
  58. De Pittà M, Volman V, Berry H, Ben-Jacob E (2011) A tale of two stories: astrocyte regulation of synaptic depression and facilitation. PLoS Comput Biol 7(12):e1002293PubMedPubMedCentralCrossRefGoogle Scholar
  59. De Pittà M, Volman V, Levine H, Pioggia G, De Rossi D, Ben-Jacob E (2008) Coexistence of amplitude and frequency modulations in intracellular calcium dynamics. Phys Rev E 77(3):030903(R)CrossRefGoogle Scholar
  60. Deco G, Jirsa VK, McIntosh AR (2011) Emerging concepts for the dynamical organization of resting-state activity in the brain. Nat Rev Neurosci 12(1):43PubMedCrossRefGoogle Scholar
  61. Deitmer JW, Rose CR (1996) pH regulation and proton signalling by glial cells. Prog Neurobiol 48(2):73–103PubMedCrossRefGoogle Scholar
  62. Del Negro CA, Funk GD, Feldman JL (2018) Breathing matters. Nat Rev Neurosci 19(6):351–367PubMedCrossRefGoogle Scholar
  63. Devaraju P, Sun M-Y, Myers TL, Lauderdale K, Fiacco TA (2013) Astrocytic group I mGluR-dependent potentiation of astrocytic glutamate and potassium uptake. J Neurophysiol 109(9):2404–2414PubMedCrossRefGoogle Scholar
  64. Di Castro M, Chuquet J, Liaudet N, Bhaukaurally K, Santello M, Bouvier D, Tiret P, Volterra A (2011) Local Ca\(^{2+}\) detection and modulation of synaptic release by astrocytes. Nat Neurosci 14:1276–1284CrossRefGoogle Scholar
  65. Diamond MC, Scheibel AB, Murphy GM Jr, Harvey T (1985) On the brain of a scientist: Albert Einstein. Exp Neurol 88(1):198–204PubMedCrossRefGoogle Scholar
  66. Dienel GA (2012) Fueling and imaging brain activation. ASN Neuro 4(AN20120021):5Google Scholar
  67. Dimou L, Simon C, Kirchhoff F, Takebayashi H, Götz M (2008) Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci 28(41):10434–10442PubMedCrossRefGoogle Scholar
  68. Dittman JS, Kreitzer AC, Regehr WG (2000) Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20(4):1374–1385PubMedCrossRefGoogle Scholar
  69. Djukic B, Casper KB, Philpot BD, Chin L-S, McCarthy KD (2007) Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J Neurosci 27(42):11354–11365PubMedPubMedCentralCrossRefGoogle Scholar
  70. Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI (1997) Differential activation of transcription factors induced by Ca\(^{2+}\) response amplitude and duration. Nature 386(24):855–858PubMedCrossRefGoogle Scholar
  71. 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 281:30684–30696PubMedPubMedCentralCrossRefGoogle Scholar
  72. Dringen R (2000) Metabolism and functions of glutathione in brain. Prog Neurobiol 62(6):649–671PubMedCrossRefGoogle Scholar
  73. Eroglu C, Barres BA (2010) Regulation of synaptic connectivity by glia. Nature 468(7321):223–231PubMedPubMedCentralCrossRefGoogle Scholar
  74. Fiacco TA, McCarthy KD (2018) Multiple lines of evidence indicate that gliotransmission does not occur under physiological conditions. J Neurosci 38(1):3–13PubMedPubMedCentralCrossRefGoogle Scholar
  75. Fields RD (2008) White matter in learning, cognition and psychiatric disorders. Trends Neurosci 31(7):361–370PubMedPubMedCentralCrossRefGoogle Scholar
  76. Fields RD (2009a) The other brain: From dementia to schizophrenia, how new discoveries about the brain are revolutionizing medicine and science (1st ed). Simon and SchusterGoogle Scholar
  77. Fields RD (2009b) Regulation of myelination by functional activity. In: Kettenmann H, Ransom BR (eds) Neuroglia (3rd ed) (Chap. 45). Oxford University Press, Oxford, pp 573–586Google Scholar
  78. Fields RD, Woo DH, Basser PJ (2015) Glial regulation of the neuronal connectome through local and long-distant communication. Neuron 86(2):374–386PubMedPubMedCentralCrossRefGoogle Scholar
  79. Florence CM, Baillie LD, Mulligan SJ (2012) Dynamic volume changes in astrocytes are an intrinsic phenomenon mediated by bicarbonate ion flux. PLoS One 7(11):e51124PubMedPubMedCentralCrossRefGoogle Scholar
  80. Florian C, Vecsey CG, Halassa MM, Haydon PG, Abel T (2011) Astrocyte-derived adenosine and A1 receptor activity contribute to sleep loss-induced deficits in hippocampal synaptic plasticity and memory in mice. J Neurosci 31(19):6956–6962PubMedPubMedCentralCrossRefGoogle Scholar
  81. Ford MC, Alexandrova O, Cossell L, Stange-Marten A, Sinclair J, Kopp-Scheinpflug C, Pecka M, Attwell D, Grothe B (2015) Tuning of Ranvier node and internode properties in myelinated axons to adjust action potential timing. Nat Commun 6:8073Google Scholar
  82. Fortune ES, Rose GJ (2001) Short-term synaptic plasticity as a temporal filter. Trends Neurosci 24(7):381–385PubMedCrossRefGoogle Scholar
  83. Fourcaud-Trocmé N, Hansel D, van Vreeswijk C, Brunel N (2003) How spike generation mechanisms determine the neuronal response to fluctuating inputs. J Neurosci 23(37):11628–11640PubMedCrossRefGoogle Scholar
  84. Froemke RC, Dan Y (2002) Spike-timing-dependent synaptic modification induced by natural spike trains. Nature 416(6879):433–438PubMedCrossRefGoogle Scholar
  85. Froemke RC, Debanne D, Bi G (2010) Temporal modulation of spike-timing-dependent plasticity. Frontiers Synaptic Neurosci 2(19):1–16Google Scholar
  86. Froemke RC, Tsay IA, Raad M, Long JD, Dan Y (2006) Contribution of individual spikes in burst-induced long-term synaptic modification. J Neurophysiol 95(3):1620–1629PubMedCrossRefGoogle Scholar
  87. Frühbeis C, Fröhlich D, Kuo WP, Amphornrat J, Thilemann S, Saab AS, Kirchhoff F, Möbius W, Goebbels S, Nave K (2013) Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol 11(7):e1001604PubMedPubMedCentralCrossRefGoogle Scholar
  88. Ganmor E, Segev R, Schneidman E (2015) A thesaurus for a neural population code. eLife 4:e06134Google Scholar
  89. Garnier A, Vidal A, Benali H (2016) A theoretical study on the role of astrocytic activity in neuronal hyperexcitability by a novel neuron-glia mass model. J Math Neurosci 6(1):10PubMedPubMedCentralCrossRefGoogle Scholar
  90. Gerstner W, Kistler WM (2002) Mathematical formulations of Hebbian learning. Biol Cybern 87(5–6):404–415PubMedCrossRefGoogle Scholar
  91. Gilman AG (1987) G proteins: transducers of receptor-generated signals. Annu Rev Biochem 56(1):615–649PubMedCrossRefGoogle Scholar
  92. Gordon GRJ, Mulligan SJ, MacVicar BA (2007) Astrocyte control of the cerebrovasculature. Glia 55(12):1214–1221PubMedCrossRefGoogle Scholar
  93. Götz M (2013) Neuroglia, chapter Radial glial cells. Oxford University Press, Oxford, pp 50–61CrossRefGoogle Scholar
  94. Graupner M, Brunel N (2010) Mechanisms of induction and maintenance of spike-timing dependent plasticity in biophysical synapse models. Frontiers Comput Neurosci 4(136):1–19Google Scholar
  95. Grosche J, Kettenmann H, Reichenbach A (2002) Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons. J Neurosci Res 68:128–149CrossRefGoogle Scholar
  96. Grosche J, Matyash V, Möller T, Verkhratsky A, Reichenbach A, Kettenmann H (1999) Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nature 2(2):139–143PubMedCrossRefGoogle Scholar
  97. Habbas S, Santello M, Becker D, Stubbe H, Zappia G, Liaudet N, Klaus FR, Kollias G, Fontana A, Pryce CR, Suter T, Volterra A (2015) Neuroinflammatory TNF\(\alpha \) impairs memory via astrocyte signaling. Cell 163(7):1730–1741CrossRefGoogle Scholar
  98. Haber M, Zhou L, Murai KK (2006) Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci 26(35):8881–8891PubMedCrossRefGoogle Scholar
  99. Halassa M, Haydon P (2010) Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu Rev Physiol 72:335–355PubMedPubMedCentralCrossRefGoogle Scholar
  100. Halassa MM, Florian C, Fellin T, Munoz JR, Lee SY, Abel T, Haydon PG, Frank MG (2009) Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61(2):213–219PubMedPubMedCentralCrossRefGoogle Scholar
  101. Hamilton N, Vayro S, Kirchhoff F, Verkhratsky A, Robbins J, Gorecki DC, Butt AM (2008) Mechanisms of ATP- and glutamate-mediated calcium signaling in white matter astrocytes. Glia 56(7):734–749PubMedCrossRefGoogle Scholar
  102. Han X, Chen M, Wang F, Windrem M, Wang S, Shanz S, Xu Q, Oberheim NA, Bekar L, Betstadt S, Silva AJ, Takano T, Goldman SA, Nedergaard M (2013) Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 12(3):342–353PubMedPubMedCentralCrossRefGoogle Scholar
  103. Hartline DK (2011) The evolutionary origins of glia. Glia 59(9):1215–1236PubMedCrossRefGoogle Scholar
  104. Haydon PG (2001) Glia: listening and talking to the synapse. Nat Rev Neurosci 2:185–193PubMedPubMedCentralCrossRefGoogle Scholar
  105. Haydon PG, Carmignoto G (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86:1009–1031CrossRefGoogle Scholar
  106. Heller JP, Rusakov DA (2015) Morphological plasticity of astroglia: understanding synaptic microenvironment. Glia 63(12):2133–2151PubMedPubMedCentralCrossRefGoogle Scholar
  107. Henneberger C, Papouin T, Oliet SHR, Rusakov DA (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463:232–237PubMedPubMedCentralCrossRefGoogle Scholar
  108. Hertz L (1965) Possible role of neuroglia: a potassium-mediated neuronal-neuroglial-neuronal impulse transmission system. Nature 206(4989):1091PubMedCrossRefGoogle Scholar
  109. Hertz L (2013) The glutamate-glutamine (GABA) cycle: importance of late postnatal development and potential reciprocal interactions between biosynthesis and degradation. Frontiers Endocrinol 4:59CrossRefGoogle Scholar
  110. Hirase H, Qian L, Barthó P, Buzsáki G (2004) Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol 2(4):0494–0496CrossRefGoogle Scholar
  111. Hoffmann A, Kann O, Ohlemeyer C, Hanisch U-K, Kettenmann H (2003) Elevation of basal intracellular calcium as a central element in the activation of brain macrophages (microglia): suppression of receptor-evoked calcium signaling and control of release function. J Neurosci 23(11):4410–4419PubMedCrossRefGoogle Scholar
  112. 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 Nat Acad Sci 106(9):3496–3501PubMedCrossRefGoogle Scholar
  113. Hughes EG, Orthmann-Murphy JL, Langseth AJ, Bergles DE (2018) Myelin remodeling through experience-dependent oligodendrogenesis in the adult somatosensory cortex. Nat Neurosci 21:696–706PubMedPubMedCentralCrossRefGoogle Scholar
  114. Iadecola C, Nedergaard M (2007) Glial regulation of the cerebral microvasculature. Nat Neurosci 10(11):1369–1376PubMedCrossRefGoogle Scholar
  115. Imura Y, Morizawa Y, Komatsu R, Shibata K, Shinozaki Y, Kasai H, Moriishi K, Moriyama Y, Koizumi S (2013) Microglia release ATP by exocytosis. Glia 61(8):1320–1330PubMedCrossRefGoogle Scholar
  116. Ismailov I, Kalikulov D, Inoue T, Friedlander MJ (2004) The kinetic profile of intracellular calcium predicts long-term potentiation and long-term depression. J Neurosci 24(44):9847–9861PubMedCrossRefGoogle Scholar
  117. Izhikevich EM (2006) Polychronization: computation with spikes. Neural Comput 18(2):245–282PubMedCrossRefGoogle Scholar
  118. Jackson FR (2011) Glial cell modulation of circadian rhythms. Glia 59(9):1341–1350PubMedCrossRefGoogle Scholar
  119. Jadhav AP, Roesch K, Cepko CL (2009) Development and neurogenic potential of Müller glial cells in the vertebrate retina. Prog Retinal Eye Res 28(4):249–262CrossRefGoogle Scholar
  120. Jaffe LF (1993) Classes and mechanisms of calcium waves. Cell Calcium 14(10):736–745CrossRefGoogle Scholar
  121. Jeftinija SD, Jeftinija KV, Stefanovic G, Liu F (1996) Neuroligand-evoked calcium-dependent release of excitatory amino acids from cultured astrocytes. J Neurochem 66:676–684PubMedCrossRefGoogle Scholar
  122. Jiang P, Xing F, Guo B, Yang J, Li Z, Wei W, Hu F, Lee I, Zhang X, Pan L, Xu J (2017) Nucleotide transmitters ATP and ADP mediate intercellular calcium wave communication via P2Y\(_{12/13}\) receptors among BV-2 microglia. PloS One 12(8):e0183114PubMedPubMedCentralCrossRefGoogle Scholar
  123. Jiménez-González C, Pirttimaki T, Cope DW, Parri HR (2011) Non-neuronal, slow GABA signalling in the ventrobasal thalamus targets \(\delta \)-subunit-containing GABA\(_\text{A}\) receptors. Eur J Neurosci 33(8):1471–1482Google Scholar
  124. Johnston D, Wu SM-S (1995) Foundations of cellular neurophysiology. MIT Press, Cambridge, MAGoogle Scholar
  125. Kadala A, Verdier D, Morquette P, Kolta A (2015) Ion homeostasis in rhythmogenesis: the interplay between neurons and astroglia. Physiology 30(5):371–388PubMedCrossRefGoogle Scholar
  126. Kaneko M, Stellwagen D, Malenka RC, Stryker MP (2008) Tumor necrosis factor-alpha mediates one component of competitive, experience-dependent plasticity in developing visual cortex. Neuron 58:673–680PubMedPubMedCentralCrossRefGoogle Scholar
  127. Káradóttir R, Attwell D (2007) Neurotransmitter receptors in the life and death of oligodendrocytes. Neuroscience 145(4):1426–1438PubMedPubMedCentralCrossRefGoogle Scholar
  128. Kaschube M, Schnabel M, Löwel S, Coppola DM, White LE, Wolf F (2010) Universality in the evolution of orientation columns in the visual cortex. Science 330(6007):1113–1116PubMedPubMedCentralCrossRefGoogle Scholar
  129. Kasthuri N, Hayworth K, Berger DR, Schalek RL, Conchello JA, Knowles-Barley S, Lee D, Vázquez-Reina A, Kaynig V, Jones TR, Roberts M, Lyskowski JM, Tapia JC, Seung HS, Roncal WG, Vogelstein JT, Burns R, Sussman DL, Priebe CE, Pfister H, Lichtman JW (2015) Saturated reconstruction of a volume of neocortex. Cell 162(3):648–661PubMedPubMedCentralCrossRefGoogle Scholar
  130. Katagiri H, Tanaka K, Manabe T (2001) Requirement of appropriate glutamate concentrations in the synaptic cleft for hippocampal LTP induction. Eur J Neurosci 14(3):547–553PubMedCrossRefGoogle Scholar
  131. Kettenmann H, Hanisch U-K, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91(2):461–553CrossRefGoogle Scholar
  132. Kettenmann H, Kirchhoff F, Verkhratsky A (2013) Microglia: new roles for the synaptic stripper. Neuron 77(1):10–18CrossRefGoogle Scholar
  133. Kettenmann H, Ransom BR (2013) Neuroglia, 3rd edn. Oxford University Press, OxfordCrossRefGoogle Scholar
  134. Khakh BS, Sofroniew MV (2015) Diversity of astrocyte functions and phenotypes in neural circuits. Nat Neurosci 18(7):942PubMedPubMedCentralCrossRefGoogle Scholar
  135. Kimura F, Itami C (2009) Myelination and isochronicity in neural networks. Frontiers Neuroanat 3:12CrossRefGoogle Scholar
  136. Kinney JP, Spacek J, Bartol TM, Bajaj CL, Harris KM, Sejnowski TJ (2013) Extracellular sheets and tunnels modulate glutamate diffusion in hippocampal neuropil. J Comp Neurol 521(2):448–464PubMedPubMedCentralCrossRefGoogle Scholar
  137. Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129(4):1043–1054CrossRefGoogle Scholar
  138. Kozlov AS, Angulo MC, Audinat E, Charpak S (2006) Target cell-specific modulation of neuronal activity by astrocytes. Proc Natl Acad Sci USA 103(26):10058–10063PubMedCrossRefGoogle Scholar
  139. Krämer-Albers E-M, Bretz N, Tenzer S, Winterstein C, Möbius W, Berger H, Nave K-A, Schild H, Trotter J (2007) Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: trophic support for axons? Proteomics-Clin Appl 1(11):1446–1461PubMedCrossRefGoogle Scholar
  140. Krzan M, Stenovec N, Kreft M, Pangrsic T, Grilc S, Haydon PG, Zorec R (2003) Calcium-dependent exocytosis of atrial natriuretic peptide from astrocytes. J Neurosci 23:1580–1583PubMedCrossRefGoogle Scholar
  141. Kuga N, Sasaki T, Takahara Y, Matsuki N, Ikegaya Y (2011) Large-scale calcium waves traveling through astrocytic networks in vivo. J Neurosci 31(7):2607–2614PubMedPubMedCentralCrossRefGoogle Scholar
  142. Kummer U, Olsen LF, Green AK, Bomberg-Bauer E, Baier G (2000) Switching from simple to complex oscillations in calcium signaling. Biophys J 79:1188–1199PubMedPubMedCentralCrossRefGoogle Scholar
  143. Lang EJ, Rosenbluth J (2003) Role of myelination in the development of a uniform olivocerebellar conduction time. J Neurophysiol 89(4):2259–2270PubMedCrossRefGoogle Scholar
  144. Larsen BR, Assentoft M, Cotrina ML, Hua SZ, Nedergaard M, Kaila K, Voipio J, MacAulay N (2014) Contributions of the Na\(^+\)/K\(^+\)-ATPase, NKCC1, and Kir4.1 to hippocampal K\(^+\) clearance and volume responses. Glia 62(4):608–622PubMedPubMedCentralCrossRefGoogle Scholar
  145. Laughlin SB, Sejnowski TJ (2003) Communication in neuronal networks. Science 301(5641):1870–1874PubMedPubMedCentralCrossRefGoogle Scholar
  146. Lawson LJ, Perry VH, Dri P, Gordon S (1990) Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39(1):151–170PubMedCrossRefGoogle Scholar
  147. Le Meur K, Mendizabal-Zubiaga J, Grandes P, Audinat E (2012) GABA release by hippocampal astrocytes. Front Comp Neurosci p 6Google Scholar
  148. Lee HS, Ghetti A, Pinto-Duarte A, Wang X, Dziewczapolski G, Galimi F, Huitron-Resendiz S, Piña-Crespo JC, Roberts AJ, Verma IM, Sejnowski TJ, Heinemann SF (2014) Astrocytes contribute to gamma oscillations and recognition memory. Proc Nat Acad Sci USA pp E3343–E3352CrossRefGoogle Scholar
  149. Lehre KP, Rusakov DA (2002) Asymmetry of glia near central synapses favors presynaptically directed glutamate escape. Biophys J 83(1):125–134PubMedPubMedCentralCrossRefGoogle Scholar
  150. Levy LM, Warr O, Attwell D (1998) Stoichiometry of the glial glutamate transporter GLT-1 expressed inducibly in a chinese hamster ovary cell line selected for low endogenous Na\(^+\)-dependent glutamate uptake. J Neurosci 18(23):9620–9628PubMedCrossRefGoogle Scholar
  151. Lewitus GM, Konefal SC, Greenhalgh AD, Pribiag H, Augereau K, Stellwagen D (2016) Microglial TNF-\(\alpha \) suppresses cocaine-induced plasticity and behavioral sensitization. Neuron 90(3):483–491PubMedPubMedCentralCrossRefGoogle Scholar
  152. Lewitus GM, Pribiag H, Duseja R, St-Hilaire M, Stellwagen D (2014) An adaptive role of TNF\(\alpha \) in the regulation of striatal synapses. J Neurosci 34(18):6146–6155PubMedCrossRefGoogle Scholar
  153. Leybaert L, Sanderson MJ (2012) Intercellular Ca\(^{2+}\) waves: mechanisms and function. Physiol Rev 92(3):1359–1392PubMedPubMedCentralCrossRefGoogle Scholar
  154. Lind BL, Brazhe AR, Jessen SB, Tan FCC, Lauritzen MJ (2013) Rapid stimulus-evoked astrocyte Ca\(^{2+}\) elevations and hemodynamic responses in mouse somatosensory cortex in vivo. Proc Nat Acad Sci 110(48):E4678–E4687PubMedCrossRefGoogle Scholar
  155. Lippman JJ, Lordkipanidze T, Buell ME, Yoon SO, Dunaevsky A (2008) Morphogenesis and regulation of Bergmann glial processes during Purkinje cell dendritic spine ensheathment and synaptogenesis. Glia 56(13):1463–1477PubMedPubMedCentralCrossRefGoogle Scholar
  156. Lippman JJ, Lordkipanidze T, Cobb N, Dunaevsky A (2010) Bergmann glial ensheathment of dendritic spines regulates synapse number without affecting spine motility. Neuron Glia Biol 6(3):193–200CrossRefGoogle Scholar
  157. Liu GJ, Kalous A, Werry EL, Bennett MR (2006) Purine release from spinal cord microglia after elevation of calcium by glutamate. Mol Pharmacol 70(3):851–859PubMedCrossRefGoogle Scholar
  158. López-Hidalgo M, Hoover WB, Schummers J (2016) Spatial organization of astrocytes in ferret visual cortex. J Comp Neurol 524(17):3561–3576PubMedPubMedCentralCrossRefGoogle Scholar
  159. López-Hidalgo M, Schummers J (2014) Cortical maps: a role for astrocytes? Curr Opin Neurobiol 24:176–189PubMedCrossRefGoogle Scholar
  160. Lushnikova I, Skibo G, Muller D, Nikonenko I (2009) Synaptic potentiation induces increased glial coverage of excitatory synapses in CA1 hippocampus. Hippocampus 19(8):753–762PubMedCrossRefPubMedCentralGoogle Scholar
  161. Mackenzie B, Erickson JD (2004) Sodium-coupled neutral amino acid (System N/A) transporters of the SLC38 gene family. Pflügers Archiv - Eur J Physiol 447(5):784–795CrossRefGoogle Scholar
  162. Magistretti PJ, Allaman I (2015) A cellular perspective on brain energy metabolism and functional imaging. Neuron 86(4):883–901PubMedCrossRefPubMedCentralGoogle Scholar
  163. Marchaland J, Calì C, Voglmaier SM, Li H, Regazzi R, Edwards RH, Bezzi P (2008) Fast subplasma membrane Ca\(^{2+}\) transients control exo-endocytosis of synaptic-like microvesicles in astrocytes. J Neurosci 28(37):9122–9132PubMedPubMedCentralCrossRefGoogle Scholar
  164. Marchant JS, Parker I (2001) Role of elementary Ca\(^{2+}\) puffs in generating repetitive Ca\(^{2+}\) oscillations. EMBO J 20(1–2):65–76PubMedPubMedCentralCrossRefGoogle Scholar
  165. Markram H, Lübke J, Frotscher M, Roth A, Sakmann B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500(2):409–440PubMedPubMedCentralCrossRefGoogle Scholar
  166. Martín R, Bajo-Grañeras R, Moratalla R, Perea G, Araque A (2015) Circuit-specific signaling in astrocyte-neuron networks in basal ganglia pathways. Science 349(6249):730–734CrossRefGoogle Scholar
  167. Mashimo M, Okubo Y, Yamazawa T, Yamasaki M, Watanabe M, Murayama T, Iino M (2010) Inositol 1,4,5-trisphosphate signaling maintains the activity of glutamate uptake in Bergmann glia. Eur J Neurosci 32(10):1668–1677PubMedCrossRefGoogle Scholar
  168. McAlpine D, Grothe B (2003) Sound localization and delay lines-do mammals fit the model? Trends Neurosci 26(7):347–350PubMedCrossRefGoogle Scholar
  169. Medvedev N, Popov V, Henneberger C, Kraev I, Rusakov DA, Stewart MG (2014) Glia selectively approach synapses on thin dendritic spines. Phil Trans R Soc B 369(1654):20140047PubMedCrossRefGoogle Scholar
  170. Men W, Falk D, Sun T, Chen W, Li J, Yin D, Zang L, Fan M (2014) The corpus callosum of Albert Einsteins brain: another clue to his high intelligence? Brain 137(4):e268–e268PubMedCrossRefGoogle Scholar
  171. Mergenthaler P, Lindauer U, Dienel GA, Meisel A (2013) Sugar for the brain: the role of glucose in physiological and pathological brain function. Trends Neurosci 36(10):587–597PubMedPubMedCentralCrossRefGoogle Scholar
  172. Mesejo P, Ibánez O, Fernández-Blanco E, Cedrón F, Pazos A, Porto-Pazos AB (2015) Artificial neuron-glia networks learning approach based on cooperative coevolution. Int J Neural Syst 25(04):1550012PubMedCrossRefGoogle Scholar
  173. Min R, Nevian T (2012) Astrocyte signaling controls spike timing-dependent depression at neocortical synapses. Nat Neurosci 15(5):746–753CrossRefGoogle Scholar
  174. Molofsky AV, Kelley KW, Tsai H-H, Redmond SA, Chang SM, Madireddy L, Chan JR, Baranzini SE, Ullian EM, Rowitch DH (2014) Astrocyte-encoded positional cues maintain sensorimotor circuit integrity. Nature 509(7499):189PubMedPubMedCentralCrossRefGoogle Scholar
  175. Morquette P, Verdier D, Kadala A, Féthière J, Philippe AG, Robitaille R, Kolta A (2015) An astrocyte-dependent mechanism for neuronal rhythmogenesis. Nat Neurosci 18(6):844PubMedCrossRefGoogle Scholar
  176. Mothet J-P, Parent AT, Wolosker H, Brady RO, Linden DJ, Ferris CD, Rogawski MA, Snyder SH (2000) D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc Nat Acad Sci 97(9):4926–4931PubMedCrossRefGoogle Scholar
  177. Mulligan S, MacVicar B (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431(7005):195–199PubMedCrossRefGoogle Scholar
  178. Nagelhus EA, Mathiisen TM, Ottersen OP (2004) Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience 129(4):905–913PubMedCrossRefGoogle Scholar
  179. Nave K-A (2010) Myelination and support of axonal integrity by glia. Nature 468(7321):244CrossRefGoogle Scholar
  180. Nedergaard M (1994) Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 263(5154):1768PubMedCrossRefGoogle Scholar
  181. Nedergaard M, Ransom BR, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26(10):523–530PubMedPubMedCentralCrossRefGoogle Scholar
  182. Nevian T, Sakmann B (2006) Spine Ca\(^{2+}\) signaling in spike-timing-dependent plasticity. J Neurosci 26(43):11001–11013PubMedCrossRefGoogle Scholar
  183. Newman E (2005) Calcium increases in retinal glial cells evoked by light-induced neuronal activity. J Neurosci 25(23):5502–5510PubMedPubMedCentralCrossRefGoogle Scholar
  184. Newman EA (2001) Propagation of intercellular calcium waves in retinal astrocytes and Müller cells. J Neurosci 21:2215–2223PubMedPubMedCentralCrossRefGoogle Scholar
  185. Newman EA, Zahs KR (1997) Calcium waves in retinal glial cells. Science 275:844–847PubMedPubMedCentralCrossRefGoogle Scholar
  186. Newman LA, Korol DL, Gold PE (2011) Lactate produced by glycogenolysis in astrocytes regulates memory processing. PloS One 6(12):e28427PubMedPubMedCentralCrossRefGoogle Scholar
  187. Nicoll RA, Schmitz D (2005) Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6(11):863PubMedCrossRefGoogle Scholar
  188. Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308(5726):1314–1318PubMedCrossRefGoogle Scholar
  189. Nimmerjahn A, Kirchhoff F, Kerr JND, Helmchen F (2004) Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 1:31–37PubMedPubMedCentralCrossRefGoogle Scholar
  190. Nir Y, Staba RJ, Andrillon T, Vyazovskiy VV, Cirelli C, Fried I, Tononi G (2011) Regional slow waves and spindles in human sleep. Neuron 70(1):153–169PubMedPubMedCentralCrossRefGoogle Scholar
  191. Oberheim NA, Takano T, Han X, He W, Lin JHC, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann JG, Ransom BR, Goldman SA, Nedergaard M (2009) Uniquely hominid features of adult human astrocytes. J Neurosci 29(10):3276–3287PubMedPubMedCentralCrossRefGoogle Scholar
  192. Oliet SHR, Mothet J (2009) Regulation of \(N\)-methyl-D-aspartate receptors by astrocytic D-serine. Neuroscience 158(1):275–283PubMedPubMedCentralCrossRefGoogle Scholar
  193. Oliet SHR, Piet R, Poulain DA (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292:923–926PubMedCrossRefGoogle Scholar
  194. Oliveira JF, Sardinha VM, Guerra-Gomes S, Araque A, Sousa N (2015) Do stars govern our actions? Astrocyte involvement in rodent behavior. Trends Neurosci 38(9):535–549PubMedCrossRefGoogle Scholar
  195. Omrani A, Melone M, Bellesi M, Safiulina V, Aida T, Tanaka K, Cherubini E, Conti F (2009) Up-regulation of GLT-1 severely impairs LTD at mossy fibre-CA3 synapses. J Physiol 587(19):4575–4588PubMedPubMedCentralCrossRefGoogle Scholar
  196. O’Neill LAJ, Kaltschmidt C (1997) NF-\(\kappa \)B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 20(6):252–258PubMedCrossRefGoogle Scholar
  197. Orkand RK, Nicholls JG, Kuffler SW (1966) Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol 29(4):788–806PubMedCrossRefGoogle Scholar
  198. Østby I, Øyehaug L, Einevoll GT, Nagelhus EA, Plahte E, Zeuthen T, Lloyd CM, Ottersen OP, Omholt SW (2009) Astrocytic mechanisms explaining neural-activity-induced shrinkage of extraneuronal space. PLoS Comput Biol 5(1):e1000272PubMedPubMedCentralCrossRefGoogle Scholar
  199. Øyehaug L, Østby I, Lloyd CM, Omholt SW, Einevoll GT (2012) Dependence of spontaneous neuronal firing and depolarisation block on astroglial membrane transport mechanisms. J Comput Neurosci 32(1):147–165PubMedCrossRefGoogle Scholar
  200. Palygin O, Lalo U, Verkhratsky A, Pankratov Y (2010) Ionotropic NMDA and P2X\(_{1/5}\) receptors mediate synaptically induced Ca\(^{2+}\) signalling in cortical astrocytes. Cell Calcium 48(4):225–231PubMedCrossRefGoogle Scholar
  201. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA, Oliet SH (2006) Glia-derived d-serine controls nmda receptor activity and synaptic memory. Cell 125:775–784PubMedCrossRefGoogle Scholar
  202. Papouin T, Ladépêche L, Ruel J, Sacchi S, Labasque M, Hanini M, Groc L, Pollegioni L, Mothet J, Oliet S (2012) Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell 150(3):633–646PubMedCrossRefGoogle Scholar
  203. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369:744–747PubMedPubMedCentralCrossRefGoogle Scholar
  204. Parpura V, Haydon PG (2000) Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc Natl Acad Sci USA 97(15):8629–8634PubMedPubMedCentralCrossRefGoogle Scholar
  205. Parys B, Côté A, Gallo V, De Koninck P, Sík A (2010) Intercellular calcium signaling between astrocytes and oligodendrocytes via gap junctions in culture. Neuroscience 167(4):1032–1043PubMedCrossRefGoogle Scholar
  206. Pascual O, Ben Achour S, Rostaing P, Triller A, Bessis A (2011) Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Nat Acad Sci pp 1–9Google Scholar
  207. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310:113–116PubMedPubMedCentralCrossRefGoogle Scholar
  208. Pasti L, Volterra A, Pozzan T, Carmignoto G (1997) Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J Neurosci 17(20):7817–7830PubMedPubMedCentralCrossRefGoogle Scholar
  209. Pasti L, Zonta M, Pozzan T, Vicini S, Carmignoto G (2001) Cytosolic calcium oscillations in astrocytes may regulate exocytotic release of glutamate. J Neurosci 21(2):477–484PubMedCrossRefGoogle Scholar
  210. Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Nat Acad Sci 91(22):10625–10629PubMedCrossRefPubMedCentralGoogle Scholar
  211. Pellerin L, Magistretti PJ (2012) Sweet sixteen for ANLS. J Cereb Blood Flow Metab 32(7):1152–1166PubMedCrossRefPubMedCentralGoogle Scholar
  212. Pelvig DP, Pakkenberg H, Stark AK, Pakkenberg B (2008) Neocortical glial cell numbers in human brains. Neurobiol Aging 29(11):1754–1762PubMedCrossRefPubMedCentralGoogle Scholar
  213. 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 34(38):12738–12744PubMedCrossRefPubMedCentralGoogle Scholar
  214. Perkel DH, Bullock TH (1968) Neural coding: a report based on an NRP work session. Neurosci Res Program Bull 6:219–349Google Scholar
  215. Petit J-M, Magistretti PJ (2016) Regulation of neuron-astrocyte metabolic coupling across the sleep-wake cycle. Neuroscience 323:135–156PubMedCrossRefPubMedCentralGoogle Scholar
  216. Philips RT, Sur M, Chakravarthy VS (2017) The influence of astrocytes on the width of orientation hypercolumns in visual cortex: A computational perspective. PLoS Comput Biol 13(10):e1005785PubMedPubMedCentralCrossRefGoogle Scholar
  217. Piet R, Vargová L, Syková E, Poulain D, Oliet S (2004) Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk. Proc Natl Acad Sci USA 101(7):2151–2155PubMedCrossRefGoogle Scholar
  218. Pocock JM, Kettenmann H (2007) Neurotransmitter receptors on microglia. Trends Neurosci 30(10):527–535PubMedCrossRefPubMedCentralGoogle Scholar
  219. Porter JT, McCarthy KD (1996) Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J Neurosci 16(16):5073–5081PubMedCrossRefPubMedCentralGoogle Scholar
  220. Porter JT, McCarthy KD (1997) Astrocytic neurotransmitter receptors in situ and in vivo. Prog Neurobiol 51(4):439–455PubMedCrossRefGoogle Scholar
  221. Porto-Pazos AB, Veiguela N, Mesejo P, Navarrete M, Alvarellos A, Ibáñez O, Pazos A, Araque A (2011) Artificial astrocytes improve neural network performance. PloS One 6(4):e19109PubMedPubMedCentralCrossRefGoogle Scholar
  222. Poskanzer KE, Yuste R (2016) Astrocytes regulate cortical state switching in vivo. Proc Nat Acad Sci 113(19):E2675–E2684PubMedCrossRefGoogle Scholar
  223. Pribiag H, Stellwagen D (2013) TNF-\(\upalpha \) downregulates inhibitory neurotransmission through protein phosphatase 1-dependent trafficking of GABA\(_{\rm A}\) receptors. J Neurosci 33(40):15879–15893Google Scholar
  224. Price DL, Ludwig JW, Mi H, Schwarz TL, Ellisman MH (2002) Distribution of rSlo Ca\(^{2+}\)-activated K\(^+\) channels in rat astrocyte perivascular endfeet. Brain Res 956(2):183–193PubMedCrossRefGoogle Scholar
  225. Ransom CB, Ransom BR, Sontheimer H (2000) Activity-dependent extracellular K\(^+\) accumulation in rat optic nerve: the role of glial and axonal Na\(^+\) pumps. J Physiol 522(3):427–442PubMedPubMedCentralCrossRefGoogle Scholar
  226. Reichenbach A, Derouiche A, Kirchhoff F (2010) Morphology and dynamics of perisynaptic glia. Brain Res Rev 63(1):11–25PubMedCrossRefGoogle Scholar
  227. Rigotti M, Barak O, Warden MR, Wang X-J, Daw ND, Miller EK, Fusi S (2013) The importance of mixed selectivity in complex cognitive tasks. Nature 497(7451):585PubMedPubMedCentralCrossRefGoogle Scholar
  228. Rose CR, Chatton J-Y (2016) Astrocyte sodium signaling and neuro-metabolic coupling in the brain. Neuroscience 323:121–134PubMedCrossRefGoogle Scholar
  229. Rothman DL, Behar KL, Hyder F, Shulman RG (2003) In vivo NMR studies of the glutamate neurotransmitter flux and neuroenergetics: implications for brain function. Annu Rev Physiol 65(1):401–427PubMedCrossRefGoogle Scholar
  230. Roxin A, Brunel N, Hansel D (2005) Role of delays in shaping spatiotemporal dynamics of neuronal activity in large networks. Phys Rev Lett 94(23):238103PubMedCrossRefGoogle Scholar
  231. Roxin A, Montbrió E (2011) How effective delays shape oscillatory dynamics in neuronal networks. Phys D 240(3):323–345CrossRefGoogle Scholar
  232. Rusakov DA (2001) The role of perisynaptic glial sheaths in glutamate spillover and extracellular Ca\(^{2+}\) depletion. Biophys J 81(4):1947–1959PubMedPubMedCentralCrossRefGoogle Scholar
  233. Rusakov DA (2015) Disentangling calcium-driven astrocyte physiology. Nat Rev Neurosci 16:226–233PubMedPubMedCentralCrossRefGoogle Scholar
  234. Sahlender DA, Savtchouk I, Volterra A (2014) What do we know about gliotransmitter release from astrocytes? Phil Tran R Soc B 369:20130592CrossRefGoogle Scholar
  235. Santello M, Bezzi P, Volterra A (2011) TNF\(\upalpha \) controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69:988–1001Google Scholar
  236. Santello M, Volterra A (2012) TNF\(\upalpha \) in synaptic function: switching gears. Trends Neurosci 35(10):638–647Google Scholar
  237. Savin C, Triesch J, Meyer-Hermann M (2009) Epileptogenesis due to glia-mediated synaptic scaling. J R Soc Interface 6(37):655–668PubMedPubMedCentralCrossRefGoogle Scholar
  238. Savtchenko LP, Rusakov DA (2014) Regulation of rhythm genesis by volume-limited, astroglia-like signals in neural networks. Phil Trans Royal Soc B: Biol Sci 369(1654):20130614CrossRefGoogle Scholar
  239. Savtchouk I, Volterra A (2018) Gliotransmission: beyond black-and-white. J Neurosci 38(1):14–25CrossRefGoogle Scholar
  240. Scemes E, Giaume C (2006) Astrocyte calcium waves: What they are and what they do. Glia 54:716–725PubMedPubMedCentralCrossRefGoogle Scholar
  241. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74(4):691–705PubMedPubMedCentralCrossRefGoogle Scholar
  242. Schipke CG, Boucsein C, Ohlemeyer C, Kirchhoff F, Kettenmann H (2002) Astrocyte Ca\(^{2+}\) waves trigger responses in microglial cells in brain slices. FASEB J 16(2):255–257CrossRefPubMedPubMedCentralGoogle Scholar
  243. Schmitt L, Sims R, Dale N, Haydon P (2012) Wakefulness affects synaptic and network activity by increasing extracellular astrocyte-derived adenosine. J Neurosci 32(13):4417–4425PubMedPubMedCentralCrossRefGoogle Scholar
  244. Schummers J, Yu H, Sur M (2008) Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Sci STKE 320(5883):1638Google Scholar
  245. Schuster S, Marhl M, Höfer T (2002) Modelling of simple and complex calcium oscillations from single-cell responses to intercellular signalling. Eur J Biochem 269:1333–1355PubMedPubMedCentralCrossRefGoogle Scholar
  246. Seidl AH, Rubel EW, Harris DM (2010) Mechanisms for adjusting interaural time differences to achieve binaural coincidence detection. J Neurosci 30(1):70–80PubMedPubMedCentralCrossRefGoogle Scholar
  247. Sherwood MW, Arizono M, Hisatsune C, Bannai H, Ebisui E, Sherwood JL, Panatier A, Oliet SHR, Mikoshiba K (2017) Astrocytic IP\(_{3}\)Rs: Contribution to Ca\(^{2+}\) signalling and hippocampal ltp. Glia 65(3):502–513PubMedCrossRefGoogle Scholar
  248. 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 33(24):10143–10153PubMedPubMedCentralCrossRefGoogle Scholar
  249. Shigetomi E, Tong X, Kwan K, Corey D, Khakh B (2012) TRPA1 channels regulate astrocyte resting calcium levels and inhibitory synapse efficacy via GAT-3. Nat Neurosci 15(1):70–80CrossRefGoogle Scholar
  250. Sild M, Ruthazer ES (2011) Radial glia: progenitor, pathway, and partner. Neuroscientist 17(3):288–302PubMedCrossRefGoogle Scholar
  251. Simard M, Nedergaard M (2004) The neurobiology of glia in the context of water and ion homeostasis. Neuroscience 129(4):877–896PubMedCrossRefPubMedCentralGoogle Scholar
  252. Simpson IA, Carruthers A, Vannucci SJ (2007) Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J Cereb Blood Flow Metab 27(11):1766–1791PubMedPubMedCentralCrossRefGoogle Scholar
  253. Skupin A, Kettenmann H, Winkler U, Wartenberg M, Sauer H, Tovey SC, Taylor CW, Falcke M (2008) How does intracellular Ca\(^{2+}\) oscillate: by chance or by clock? Biophys J 94:2404–2411PubMedPubMedCentralCrossRefGoogle Scholar
  254. Somjen GG (2002) Ion regulation in the brain: implications for pathophysiology. Neuroscientist 8(3):254–267PubMedCrossRefGoogle Scholar
  255. Somjen GG, Kager H, Wadman WJ (2008) Computer simulations of neuron-glia interactions mediated by ion flux. J Comput Neurosci 25(2):349–365PubMedCrossRefPubMedCentralGoogle Scholar
  256. Srinivasan R, Huang BS, Venugopal S, Johnston AD, Chai H, Zeng H, Golshani P, Khakh BS (2015) Ca\(^{2+}\) signaling in astrocytes from Ip3r2\(^{-/-}\) mice in brain sslice and during startle responses in vivo. Nat Neurosci 18:708–717PubMedPubMedCentralCrossRefGoogle Scholar
  257. Stassart R, Goebbels S, Nave K-A (2013) Factors controlling myelin formation. In: Kettenmann H, Ransom BR (eds) Neuroglia (3rd ed) (Chap. 44). Oxford University Press, Oxford, pp 555–572Google Scholar
  258. Stehberg J, Moraga-Amaro R, Salazar C, Becerra A, Echeverría C, Orellana JA, Bultynck G, Ponsaerts R, Leybaert L, Simon F, Simon F, Sáez JC, Retamal MA (2012) Release of gliotransmitters through astroglial connexin 43 hemichannels is necessary for fear memory consolidation in the basolateral amygdala. FASEB J 26(9):3649–3657PubMedCrossRefGoogle Scholar
  259. Steinhaüser C, Berger T, Frotscher M, Kettenmann H (1992) Heterogeneity in the membrane current pattern of identified glial cells in the hippocampal slice. Eur J Neurosci 4(6):472–484PubMedCrossRefGoogle Scholar
  260. Steinmetz CC, Turrigiano GG (2010) Tumor necrosis factor-\(\upalpha \) signaling maintains the ability of cortical synapses to express synaptic scaling. J Neurosci 30(44):14685–14690Google Scholar
  261. Stellwagen D, Beattie EC, Seo JY, Malenka RC (2005) Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-\(\upalpha \). J Neurosci 25(12):3219–3228Google Scholar
  262. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK, Huberman AD, Stafford B, Sher A, Litke AM, Lambris JD, Smith SJ, John SWM, Barres BA (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131(6):1164–1178PubMedCrossRefGoogle Scholar
  263. Stevens J-LR, Law JS, Antolík J, Bednar JA (2013) Mechanisms for stable, robust, and adaptive development of orientation maps in the primary visual cortex. J Neurosci 33(40):15747–15766PubMedCrossRefGoogle Scholar
  264. Stout CE, Costantin JL, Naus CCG, Charles AC (2002) Intercellular calcium signaling in astocytes via ATP release through connexin hemichannels. J Biol Chem 277(12):10482–10488PubMedCrossRefGoogle Scholar
  265. Suadicani SO, Brosnan CF, Scemes E (2006) P2X\(_7\) receptors mediate ATP release and amplification of astrocytic intercellular Ca\(^{2+}\) signaling. J Neurosci 26(5):1378–1385PubMedPubMedCentralCrossRefGoogle Scholar
  266. Sugihara I, Lang EJ, Llinás R (1993) Uniform olivocerebellar conduction time underlies purkinje cell complex spike synchronicity in the rat cerebellum. J Physiol 470(1):243–271PubMedPubMedCentralCrossRefGoogle Scholar
  267. Suzuki A, Stern SA, Bozdagi O, Huntely G, Wlaker RH, Magistretti PJ, Alberini CM (2011) Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144:810–823PubMedPubMedCentralCrossRefGoogle Scholar
  268. Takeda M, Nelson DJ, Soliven B (1995) Calcium signaling in cultured rat oligodendrocytes. Glia 14(3):225–236PubMedCrossRefGoogle Scholar
  269. Tani H, Dulla CG, Farzampour Z, Taylor-Weiner A, Huguenard JR, Reimer RJ (2014) A local glutamate-glutamine cycle sustains synaptic excitatory transmitter release. Neuron 81(4):888–900PubMedPubMedCentralCrossRefGoogle Scholar
  270. Tasaki I, Chang JJ (1958) Electric response of glia cells in cat brain. Science 128(3333):1209–1210PubMedCrossRefGoogle Scholar
  271. Thurley K, Falcke M (2011) Derivation of Ca\(^{2+}\) signals from puff properties reveals that pathway function is robust against cell variability but sensitive for control. Proc Nat Acad Sci USA 108(1):427–432PubMedCrossRefGoogle Scholar
  272. Thurley K, Skupin A, Thul R, Falcke M (2012) Fundamental properties of Ca\(^{2+}\) signals. Biochim Biophys Acta 1820:1185–1194PubMedCrossRefGoogle Scholar
  273. Thurley K, Tovey SC, Moenke G, Prince VL, Meena A, Thomas AP, Skupin A, Taylor CW, Falcke M (2014) Reliable encoding of stimulus intensities within random sequences of intracellular Ca\(^{2+}\) spikes. Sci Signaling 7(331):ra59CrossRefGoogle Scholar
  274. Tomassy GS, Berger DR, Chen H, Kasthuri N, Hayworth KJ, Vercelli A, Seung HS, Lichtman JW, Arlotta P (2014) Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex. Science 344(6181):319–324PubMedPubMedCentralCrossRefGoogle Scholar
  275. Tremblay M-È, Lowery RL, Majewska AK (2010) Microglial interactions with synapses are modulated by visual experience. PLoS Biol 8(11):e1000527PubMedPubMedCentralCrossRefGoogle Scholar
  276. Tsodyks M (2005) Activity-dependent transmission in neocortical synapses. In: Chow C, Gutkin B, Hansel D, Meunier C, Dalibard J (eds) Methods and models in neurophysics (Chap. 7). Elsevier, Amsterdam, pp 245–265Google Scholar
  277. Tsvetkov E, Shin R-M, Bolshakov VY (2004) Glutamate uptake determines pathway specificity of long-term potentiation in the neural circuitry of fear conditioning. Neuron 41(1):139–151PubMedCrossRefGoogle Scholar
  278. Ullah G, Cressman JR Jr, Barreto E, Schiff SJ (2009) The influence of sodium and potassium dynamics on excitability, seizures, and the stability of persistent states: II. Network and glial dynamics. J Comput Neurosci 26(2):171–183PubMedCrossRefPubMedCentralGoogle Scholar
  279. Ullén F (2009) Is activity regulation of late myelination a plastic mechanism in the human nervous system? Neuron Glia Biol 5(1–2):29–34PubMedCrossRefGoogle Scholar
  280. Vaishnavi SN, Vlassenko AG, Rundle MM, Snyder AZ, Mintun MA, Raichle ME (2010) Regional aerobic glycolysis in the human brain. Proc Nat Acad Sci 107(41):17757–17762PubMedCrossRefPubMedCentralGoogle Scholar
  281. Valtcheva S, Venance L (2016) Astrocytes gate Hebbian synaptic plasticity in the striatum. Nat Commun 7:13845PubMedPubMedCentralCrossRefGoogle Scholar
  282. Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19(16):6897–6906PubMedCrossRefGoogle Scholar
  283. Verbich D, Prenosil GA, Chang PK-Y, Murai KK, McKinney RA (2012) Glial glutamate transport modulates dendritic spine head protrusions in the hippocampus. Glia 60(7):1067–1077PubMedCrossRefPubMedCentralGoogle Scholar
  284. Verderio C, Matteoli M (2001) ATP mediates calcium signaling between astrocytes and microglial cells: modulation by IFN-\(\gamma \). J Immunol 166(10):6383–6391PubMedCrossRefPubMedCentralGoogle Scholar
  285. Verkhratsky A, Kettenmann H (1996) Calcium signaling in glial cells. Trends Neurosci 19:346–352PubMedCrossRefGoogle Scholar
  286. Verkhratsky A, Nedergaard M (2016) The homeostatic astroglia emerges from evolutionary specialization of neural cells. Phil Trans R Soc B 371(1700):20150428PubMedCrossRefGoogle Scholar
  287. Violin JD, DiPilato LM, Yildirim N, Elston TC, Zhang J, Lefkowitz RJ (2008) \(\upbeta \)2-adrenergic receptor signaling and desensitization elucidated by quantitative modeling of real time cAMP dynamics. J Biol Chem 283(5):2949–2961Google Scholar
  288. Volman V, Bazhenov M, Sejnowski TJ (2013) Divide and conquer: functional segregation of synaptic inputs by astrocytic microdomains could alleviate paroxysmal activity following brain trauma. PLoS Comput Biol 9(1):e1002856PubMedPubMedCentralCrossRefGoogle Scholar
  289. Volterra A, Liaudet N, Savtchouk I (2014) Astrocyte Ca\(^{2+}\) signalling: an unexpected complexity. Nat Rev Neurosci 15:327–334PubMedPubMedCentralCrossRefGoogle Scholar
  290. Vyazovskiy VV, Olcese U, Hanlon EC, Nir Y, Cirelli C, Tononi G (2011) Local sleep in awake rats. Nature 472(7344):443PubMedPubMedCentralCrossRefGoogle Scholar
  291. Waehneldt TV, Matthieu J-M, Jeserich G (1986) Appearance of myelin proteins during vertebrate evolution. Neurochem Int 9(4):463–474PubMedCrossRefGoogle Scholar
  292. Wake H, Moorhouse AJ, Jinno S, Kohsaka S, Nabekura J (2009) Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J Neurosci 29(13):3974–3980PubMedCrossRefGoogle Scholar
  293. Wake H, Moorhouse AJ, Miyamoto A, Nabekura J (2013) Microglia: actively surveying and shaping neuronal circuit structure and function. Trends Neurosci 36(4):209–217PubMedCrossRefGoogle Scholar
  294. Walz W (2000) Role of astrocytes in the clearance of excess extracellular potassium. Neurochem Int 36(4–5):291–300PubMedCrossRefGoogle Scholar
  295. Wang X, Lou N, Xu Q, Tian G-F, Peng WG, Han X, Kang J, Takano T, Nedergaard M (2006) Astrocytic Ca\(^{2+}\) signaling evoked by sensory stimulation in vivo. Nat Neurosci 9(6):816–823PubMedCrossRefPubMedCentralGoogle Scholar
  296. Witcher M, Kirov S, Harris K (2007) Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus. Glia 55(1):13–23PubMedCrossRefGoogle Scholar
  297. Wu X, Pan L, Liu Y, Jiang P, Lee I, Drevensek-Olenik I, Zhang X, Xu J (2013) Cell-cell communication induces random spikes of spontaneous calcium oscillations in multi-BV-2 microglial cells. Biochem Biophys Res Commun 431(4):664–669PubMedCrossRefGoogle Scholar
  298. Yang L, Qi Y, Yang Y (2015) Astrocytes control food intake by inhibiting AGRP neuron activity via adenosine a1 receptors. Cell Rep 11(5):798–807PubMedCrossRefGoogle Scholar
  299. Ying W (2008) NAD\(^+\)/NADH and NADP\(^+\)/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid Redox Signal 10(2):179–206PubMedCrossRefGoogle Scholar
  300. Young KM, Psachoulia K, Tripathi RB, Dunn S, Cossell L, Attwell D, Tohyama K, Richardson WD (2013) Oligodendrocyte dynamics in the healthy adult CNS: evidence for myelin remodeling. Neuron 77(5):873–885PubMedPubMedCentralCrossRefGoogle Scholar
  301. Zalc B, Colman DR (2000) Origins of vertebrate success. Science 288(5464):271–271PubMedCrossRefGoogle Scholar
  302. Zalc B, Goujet D, Colman D (2008) The origin of the myelination program in vertebrates. Curr Biol 18(12):R511–R512PubMedCrossRefGoogle Scholar
  303. Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR, O’Keeffe S, Phatnani HP, Guarnieri P, Caneda C, Ruderisch N, Deng S, Liddelow SA, Zhang C, Daneman R, Maniatis T, Barres BA, Wu JQ (2014) An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci 34(36):11929–11947PubMedPubMedCentralCrossRefGoogle Scholar
  304. 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 6:43–40CrossRefGoogle Scholar
  305. Zorec R, Araque A, Carmignoto G, Haydon P, Verkhratsky A, Parpura V (2012) Astroglial excitability and gliotransmission: An appraisal of Ca\(^{2+}\) as a signaling route. ASN Neuro 4(2):e00080PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Group of Mathematical, Computational and Experimental NeuroscienceBasque Center for Applied MathematicsBilbao, BiscaySpain
  2. 2.EPI BEAGLE, INRIA Rhône-AlpesVilleurbanneFrance

Personalised recommendations