Advertisement

Gliotransmitter Exocytosis and Its Consequences on Synaptic Transmission

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

Abstract

Calcium-dependent exocytosis of glutamate and purines from astrocytes is the mechanism of gliotransmission that has best been characterized up-to-date, but its putative functional consequences remain elusive. Here we review and expand a mathematical modeling framework originally introduced by De Pittà et al. (2011) to study how gliotransmission could affect synaptic coding and mechanisms of short-term plasticity. Consideration of analytical solutions for rate-based, mean field dynamics of gliotransmission-mediated synaptic neurotransmitter release provides a testable rationale to record functional modulations of synaptic transmission by gliotransmitters in experiments. At the same time, we present theoretical arguments that reveal how functional gliotransmission is a complex phenomenon that depends on the nature of structural and functional coupling between astrocytic and synaptic elements.

Keywords

Gliotransmitter release Short-term synaptic plasticity Synaptic coding Tripartite synapse Mean field dynamics 

Notes

Acknowledgements

Research work presented here is supported by the Junior Leader Postdoctoral Fellowship Program from “la Caixa” Banking Foundation (grant LCF/BQ/LI18/11630006) and was also previously sponsored by the European Commission through an International Outgoing Marie Skłodowska-Curie Fellowship (Project 331486 “Neuron-Astro-Nets”). MDP also wishes to acknowledge the support of the Basque Government by the BERC 2018–2021 program, as well as the support by the Spanish Ministry of Science, Innovation and Universities through the BCAM Severo Ochoa accreditation SEV-2017-0718.

References

  1. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H (2009) Purinergic signalling in the nervous system: an overview. Trends Neurosci. 32:19–29PubMedCrossRefGoogle Scholar
  2. Amit DJ, Tsodyks MV (1991) Quantitative study of attractor neural network retrieving at low spike rates: I. Substrate-spikes, rates and neuronal gain. Network 2:259–273CrossRefGoogle Scholar
  3. Anderson MC, Swanson RA (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1–14PubMedCrossRefGoogle Scholar
  4. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1998a) Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur. J. Neurosci. 10:2129–2142PubMedCrossRefGoogle Scholar
  5. Araque A, Sanzgiri RP, Parpura V, Haydon PG (1998b) Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J. Neurosci. 18(17):6822–6829PubMedCrossRefGoogle Scholar
  6. 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
  7. 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
  8. Bains JS, Oliet SHR (2007) Glia: they make your memories stick!. Trends Neurosci. 30(8):417–424PubMedCrossRefGoogle Scholar
  9. Baldwin SA, Yao SYM, Hyde RJ, Ng AML, Foppolo S, Barnes K, Ritzel MWL, Cass CE, Young JD (2005) Functional characterization of novel human and mouse equilibrative nucleoside transporters (hENT3 and mENT3) located in intracellular membranes. J Biol Chem 280(16):15880–15887PubMedCrossRefGoogle Scholar
  10. Barnes K, Dobrzynski H, Foppolo S, Beal PR, Ismat F, Scullion ER, Sun L, Tellez J, Ritzel MWL, Claycomb WC, Cass CE, Yound JD, Billeter-Clark R, Boyett MR, Baldwin SA (2006) Distribution and functional characterization of equilibrative nucleoside transporter-4, a novel cardiac adenosine transporter activated at acidic pH. Circ Res 99(5):510–519PubMedCrossRefPubMedCentralGoogle Scholar
  11. Bergersen LH, Gundersen V (2009) Morphological evidence for vesicular glutamate release from astrocytes. Neuroscience 158:260–265PubMedCrossRefGoogle Scholar
  12. Bergersen L, Morland C, Ormel L, Rinholm JE, Larsson M, Wold JFH, Røe AT, Stranna A, Santello M, Bouvier D, Ottersen OP, Volterra A, Gundersen V (2012) Immunogold detection of L-glutamate and D-serine in small synaptic-like microvesicles in adult hippocampal astrocytes. Cereb Cortex 22(7):1690–1697PubMedCrossRefPubMedCentralGoogle Scholar
  13. Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhäuser C, Pilati E, Volterra A (2004) Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 7(6):613–620PubMedCrossRefGoogle Scholar
  14. Bollmann JH, Sakmann B, Gerard J, Borst G (2000) Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289:953–957PubMedGoogle Scholar
  15. 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 33:1483–1492PubMedCrossRefGoogle Scholar
  16. Bowser DN, Khakh BS (2007) Two forms of single-vesicle astrocyte exocytosis imaged with total internal reflection fluorescence microscopy. Proc Natl Acad Sci U S A 104(10):4212–4217PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chen X, Wang L, Zhou Y, Zheng L-H, Zhou Z (2005) “Kiss-and-run” glutamate secretion in cultured and freshly isolated rat hippocampal astrocytes. J Neurosci 25(40):9236–9243PubMedCrossRefGoogle Scholar
  18. Clements JD (1996) Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci 19(5):163–171PubMedCrossRefGoogle Scholar
  19. 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):1354–1362PubMedCrossRefPubMedCentralGoogle Scholar
  20. Covelo A, Araque A (2018) Neuronal activity determines distinct gliotransmitter release from a single astrocyte. eLife 7:e32237PubMedPubMedCentralCrossRefGoogle Scholar
  21. Crippa D, Schenk U, Francolini M, Rosa P, Verderio C, Zonta M, Pozzan T, Matteoli M, Carmignoto G (2006) Synaptobrevin2-expressing vesicles in rat astrocytes: insights into molecular characterization, dynamics and exocytosis. J Physiol 570(3):567–582PubMedCrossRefGoogle Scholar
  22. Cunhaa R, Ribeiro J (2000) ATP as a presynaptic modulator. Life Sci 68:119–137CrossRefGoogle Scholar
  23. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105PubMedCrossRefGoogle Scholar
  24. Danbolt NC, Lehre KP, Dehnes Y, Ullensvang K (2002) Transporters for synaptic transmitter on the glial cell plasma membrane. In: Volterra A, Magistretti PJ, Haydon PG (eds) The tripartite synapse: Glia in synaptic transmission, Chapter 1. Oxford University Press, New York, pp 47–61Google Scholar
  25. De Pittà M, Brunel N (2016) Modulation of synaptic plasticity by glutamatergic gliotransmission: a modeling study. Neural Plast 7607924Google Scholar
  26. 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
  27. De Pittà M, Volman V, Berry H, Parpura V, Liaudet N, Volterra A, Ben-Jacob E (2013) Computational quest for understanding the role of astrocyte signaling in synaptic transmission and plasticity. Front Comput Neurosci 6:98Google Scholar
  28. De Pittà M, Brunel N, Volterra A (2015) Astrocytes: orchestrating synaptic plasticity? NeuroscienceGoogle Scholar
  29. Debanne D, Guerineau NC, Giihwiler BH, Thompson SM (1996) Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J Physiol 491(1):163–176PubMedPubMedCentralCrossRefGoogle Scholar
  30. Destexhe A, Mainen ZF, Sejnowski TJ (1994) Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J Comput Neurosci 1:195–230PubMedCrossRefGoogle Scholar
  31. Diamond JS (2005) Deriving the glutamate clearance time course from transporter currents in CA1 hippocampal astrocytes: transmitter uptake gets faster during development. J Neurosci 25(11):2906–2916PubMedCrossRefGoogle Scholar
  32. 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 281:30684–30696PubMedPubMedCentralGoogle Scholar
  33. Fiacco TA, McCarthy KD (2004) Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons. J Neurosci 24(3):722–732PubMedCrossRefPubMedCentralGoogle Scholar
  34. 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
  35. Fuhrmann G, Segev I, Markram H, Tsodyks M (2002) Coding of temporal information by activity-dependent synapses. J Neurophysiol 87:140–148PubMedCrossRefGoogle Scholar
  36. Griffiths M, Yao YMS, Abidi F, Phillips EVS, Cass EC, Young DJ, Baldwin AS (1997) Molecular cloning and characterization of a nitrobenzylthioinosine-insensitive (ei) equilibrative nucleoside transporter from human placenta. Biochem J 328(3):739–743PubMedPubMedCentralCrossRefGoogle Scholar
  37. 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):1730–1741PubMedCrossRefGoogle Scholar
  38. Halassa M, Haydon P (2010) Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu Rev Physiol 72:335–355PubMedPubMedCentralCrossRefGoogle Scholar
  39. Haydon PG, Carmignoto G (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86:1009–1031PubMedCrossRefGoogle Scholar
  40. Jaiswal J, Fix M, Takano T, Nedergaard M, Simon S (2007) Resolving vesicle fusion from lysis to monitor calcium-triggered lysosomal exocytosis in astrocytes. Proc Natl Acad Sci U S A 104(35):14151–14156PubMedPubMedCentralCrossRefGoogle Scholar
  41. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, Domercq M, Matute C, Tonello F, Gundersen V, Volterra A (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nat Neurosci 10(3):331–339PubMedPubMedCentralCrossRefGoogle Scholar
  42. King AE, Ackley MA, Cass CE, Young JD, Baldwin SA (2006) Nucleoside transporters: from scavengers to novel therapeutic targets. Trends Pharmacol Sci 27(8):416–425PubMedCrossRefGoogle Scholar
  43. Kreft M, Stenovec M, Rupnik M, Grilc S, Kržan M, Potokar M, Pangršič T, Haydon PG, Zorec R (2004) Properties of Ca\(^{2+}\)-dependent exocytosis in cultured astrocytes. Glia 46(4):437–445PubMedPubMedCentralCrossRefGoogle Scholar
  44. Lehre KP, Danbolt NC (1998) The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J Neurosci 18(21):8751–8757PubMedCrossRefGoogle Scholar
  45. Liu Q, Xu Q, Arcuino G, Kang J, Nedergaard M (2004a) Astrocyte-mediated activation of neuronal kainate receptors. Proc Natl Acad Sci U S A 101(9):3172–3177PubMedPubMedCentralCrossRefGoogle Scholar
  46. Liu Q-S, Xu Q, Kang J, Nedergaard M (2004b) Astrocyte activation of presynaptic metabotropic glutamate receptors modulates hippocampal inhibitory synaptic transmission. Neuron Glia Biol 1:307–316PubMedPubMedCentralCrossRefGoogle Scholar
  47. Losi G, Mariotti L, Carmignoto G (2014) GABAergic interneuron to astrocyte signalling: a neglected form of cell communication in the brain. Philos Trans R Soc B Biol Sci 369(1654):20130609CrossRefGoogle Scholar
  48. Malarkey E, Parpura V (2011) Temporal characteristics of vesicular fusion in astrocytes: examination of synaptobrevin 2-laden vesicles at single vesicle resolution. J Physiol 589(17):4271–4300PubMedPubMedCentralCrossRefGoogle Scholar
  49. 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
  50. Milshtejn G (1975) Approximate integration of stochastic differential equations. Theory Probab Appl 19(3):557–562CrossRefGoogle Scholar
  51. Montana V, Ni Y, Sunjara V, Hua X, Parpura V (2004) Vesicular glutamate transporter-dependent glutamate release from astrocytes. J Neurosci 24(11):2633–2642PubMedCrossRefPubMedCentralGoogle Scholar
  52. Montana V, Malarkey EB, Verderio C, Matteoli M, Parpura V (2006) Vesicular transmitter release from astrocytes. Glia 54:700–715PubMedCrossRefPubMedCentralGoogle Scholar
  53. Mothet J-P, 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
  54. Navarrete M, Araque A (2010) Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron 68(1):113–126PubMedCrossRefGoogle Scholar
  55. Newman EA (2003) Glial cell inhibition of neurons by release of ATP. J Neurosci 23(5):1659–1666PubMedPubMedCentralCrossRefGoogle Scholar
  56. Panatier A, Vallée J, Haber M, Murai K, Lacaille J, Robitaille R (2011) Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146:785–798CrossRefGoogle Scholar
  57. Pangršič T, Potokar M, Stenovec M, Kreft M, Fabbretti E, Nistri A, Pryazhnikov E, Khiroug L, Giniatullin R, Zorec R (2007) Exocytotic release of ATP from cultured astrocytes. J Biol Chem 282(39):28749–28758PubMedPubMedCentralCrossRefGoogle Scholar
  58. Papouin T, Oliet SHR (2014) Organization, control and function of extrasynaptic NMDA receptors. Philos Trans R Soc B Biol Sci 369(1654):20130601CrossRefGoogle Scholar
  59. 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
  60. Parpura V, Fang Y, Basarsky T, Jahn R, Haydon PG (1995) Expression of synaptobrevin II, cellubrevin and syntaxin but not SNAP-25 in cultured astrocytes. FEBS Lett 377:489–492CrossRefPubMedPubMedCentralGoogle Scholar
  61. 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 310:113–116CrossRefPubMedPubMedCentralGoogle Scholar
  62. 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
  63. Perea G, Araque A (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317:1083–1086CrossRefPubMedPubMedCentralGoogle Scholar
  64. 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
  65. Pinheiro PS, Mulle C (2008) Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat Rev Neurosci 9:423–436PubMedCrossRefGoogle Scholar
  66. Pryazhnikov E, Khiroug L (2008) Sub-micromolar increase in [Ca\(^{2+}\)]\(_{i}\) triggers delayed exocytosis of ATP in cultured astrocytes. Glia 56(1):38–49PubMedCrossRefGoogle Scholar
  67. Rebola N, Rodrigues R, Lopes L, Richardson P, Oliveira C, Cunha R (2005) Adenosine A\(_{1}\) and A\(_{2\rm A}\) receptors are co-expressed in pyramidal neurons and co-localized in glutamatergic nerve terminals of the rat hippocampus. Neuroscience 133(1):79–83PubMedPubMedCentralCrossRefGoogle Scholar
  68. Rusakov DA (2001) The role of perisynaptic glial sheaths in glutamate spillover and extracellular Ca\(^{2+}\) depletion. Biophys J 81(4):1947–1959PubMedPubMedCentralCrossRefGoogle Scholar
  69. Santello M, Volterra A (2009) Synaptic modulation by astrocytes via Ca\(^{2+}\)-dependent glutamate release. Neuroscience 158(1):253–259PubMedCrossRefPubMedCentralGoogle Scholar
  70. Santello M, Volterra A (2012) TNF\(\upalpha \) in synaptic function: switching gears. Trends Neurosci 35(10):638–647Google Scholar
  71. Santello M, Bezzi P, Volterra A (2011) TNF\(\upalpha \) controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69:988–1001Google Scholar
  72. Savtchouk I, Volterra A (2018) Gliotransmission: beyond black-and-white. J Neurosci 38(1):14–25PubMedCrossRefGoogle Scholar
  73. Sawada K, Echigo N, Juge N, Miyaji T, Otsuka M, Omote H, Yamamoto A, Moriyama Y (2008) Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci U S A 105(15):5683–5686PubMedPubMedCentralCrossRefGoogle Scholar
  74. Schneggenburger R, Neher E (2000) Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406:889–893PubMedCrossRefGoogle Scholar
  75. Schubert V, Bouvier D, Volterra A (2011) SNARE protein expression in synaptic terminals and astrocytes in the adult hippocampus: A comparative analysis. Glia 59(10):1472–1488PubMedCrossRefGoogle Scholar
  76. Serrano A, Haddjeri N, Lacaille J, Robitaille R (2006) GABAergic network activation of glial cells underlies heterosynaptic depression. J Neurosci 26(20):5370–5382PubMedCrossRefPubMedCentralGoogle Scholar
  77. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor P, Neki A, Abe T, Nakanishi S, Mizuno N (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17(19):7503–7522PubMedCrossRefGoogle Scholar
  78. Skupin A, Falcke M (2010) Statistical analysis of calcium oscillations. Eur Phys J Spec Top 187:231–240CrossRefGoogle Scholar
  79. Softky W, Koch C (1993) The highly irregular firing pattern of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13:334–350PubMedPubMedCentralCrossRefGoogle Scholar
  80. Stenovec M, Kreft M, Grilc S, Pokotar M, Kreft ME, Pangršič T, Zorec R (2007) Ca\(^{2+}\)-dependent mobility of vesicles capturing anti-VGLUT1 antibodies. Exp Cell Res 313:3809–3818PubMedCrossRefPubMedCentralGoogle Scholar
  81. Südhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509–547PubMedCrossRefGoogle Scholar
  82. Tang F, Lane S, Korsak A, Paton JFR, Gourine AV, Kasparov S, Teschemacher AG (2014) Lactate-mediated glia-neuronal signalling in the mammalian brain. Nat Commun 5:3284PubMedPubMedCentralCrossRefGoogle Scholar
  83. Todd KJ, Darabid H, Robitaille R (2010) Perisynaptic glia discriminate patterns of motor nerve activity and influence plasticity at the neuromuscular junction. J Neurosci 30(35):11870–11882PubMedCrossRefGoogle Scholar
  84. 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, pp 245–265Google Scholar
  85. Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci U S A 94:719–723PubMedPubMedCentralCrossRefGoogle Scholar
  86. Tsodyks M, Pawelzik K, Markram H (1998) Neural networks with dynamic synapses. Neural Comput 10:821–835PubMedCrossRefGoogle Scholar
  87. Tzingounis AV, Wadiche JI (2007) Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 8:935–947PubMedCrossRefGoogle Scholar
  88. Zhang J-M, Wang H-K, Ye C-Q, Ge W, Chen Y, Jiang Z-L, Wu C-P, Poo M-M, Duan S (2003) ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40:971–982PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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
  90. Zhang Z, Chen G, Zhou W, Song A, Xu T, Luo Q, Wang W, Gu X, Duan S (2007) Regulated ATP release from astrocytes through lysosome exocytosis. Nat Cell Biol 9(8):945–953PubMedCrossRefPubMedCentralGoogle Scholar
  91. 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
  92. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355–405PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Basque Center of Applied MathematicsBilbaoSpain

Personalised recommendations