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Synaptic plasticity and Ca2+ signalling in astrocytes

Published online by Cambridge University Press:  13 October 2010

Christian Henneberger  and
Dmitri A. Rusakov
Christian Henneberger*
Affiliation:
UCL Institute of Neurology, University College London, Queen Square, London, UK
Dmitri A. Rusakov*
Affiliation:
UCL Institute of Neurology, University College London, Queen Square, London, UK
*
Correspondence should be addressed to: Dmitri Rusakov and Christian Henneberger, UCL Institute of Neurology, University College London, Queen Square, London WC1N 2BG, UK emails: d.rusakov@ion.ucl.ac.uk and c.henneberger@ion.ucl.ac.uk
Correspondence should be addressed to: Dmitri Rusakov and Christian Henneberger, UCL Institute of Neurology, University College London, Queen Square, London WC1N 2BG, UK emails: d.rusakov@ion.ucl.ac.uk and c.henneberger@ion.ucl.ac.uk
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Abstract

There is a growing body of evidence suggesting a functional relationship between Ca2+ signals generated in astroglia and the functioning of nearby excitatory synapses. Interference with endogenous Ca2+ homeostasis inside individual astrocytes has been shown to affect synaptic transmission and its use-dependent changes. However, establishing the causal link between source-specific, physiologically relevant intracellular Ca2+ signals, the astrocytic release machinery and the consequent effects on synaptic transmission has proved difficult. Improved methods of Ca2+ monitoring in situ will be essential for resolving the ambiguity in understanding the underlying Ca2+ signalling cascades.

Keywords

Astrocyteplasticitygliasynapse
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Issue 3 , August 2010 , pp. 141 - 146
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Agulhon, C., Petravicz, J., McMullen, A.B., Sweger, E.J., Minton, S.K., Taves, S.R. et al. (2008) What is the role of astrocyte calcium in neurophysiology? Neuron 59, 932–946.CrossRefGoogle ScholarPubMed
Agulhon, C., Fiacco, T.A. and McCarthy, K.D. (2010) Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca2+ signaling. Science 327, 1250–1254.CrossRefGoogle Scholar
Andersson, M. and Hanse, E. (2010) Astrocytes impose postburst depression of release probability at hippocampal glutamate synapses. Journal of Neuroscience 30, 5776–5780.CrossRefGoogle ScholarPubMed
Baker, P.F., Knight, D.E. and Umbach, J.A. (1985) Calcium clamp of the intracellular environment. Cell Calcium 6, 5–14.CrossRefGoogle ScholarPubMed
Bashir, Z.I., Tam, B. and Collingridge, G.L. (1990) Activation of the glycine site in the NMDA receptor is necessary for the induction of LTP. Neuroscience Letters 108, 261–266.CrossRefGoogle ScholarPubMed
Bashir, Z.I., Bortolotto, Z.A., Davies, C.H., Berretta, N., Irving, A.J., Seal, A.J. et al. (1993) Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 363, 347–350.CrossRefGoogle ScholarPubMed
Belan, P.V., Kostyuk, P.G., Snitsarev, V.A. and Tepikin, A.V. (1993) Calcium clamp in single nerve cells. Cell Calcium 14, 419–425.CrossRefGoogle ScholarPubMed
Bliss, T. and Collingridge, G. (1993) A synaptic model of memory – long-term potentiation in the hippocampus. Nature 361, 31–39.CrossRefGoogle ScholarPubMed
Bliss, T. and Lomo, T. (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. Journal of Physiology 232, 331–356.CrossRefGoogle ScholarPubMed
Bolshakov, V.Y. and Siegelbaum, S.A. (1995) Regulation of hippocampal transmitter release during development and long-term potentiation. Science 269, 1730–1734.CrossRefGoogle ScholarPubMed
Buchanan, K.A. and Mellor, J.R. (2007) The development of synaptic plasticity induction rules and the requirement for postsynaptic spikes in rat hippocampal CA1 pyramidal neurones. Journal of Physiology 585, 429–445.CrossRefGoogle ScholarPubMed
Bucurenciu, I., Kulik, A., Schwaller, B., Frotscher, M. and Jonas, P. (2008) Nanodomain coupling between Ca2+ channels and Ca2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 57, 536–545.CrossRefGoogle Scholar
Cai, Z., Schools, G.P. and Kimelberg, H.K. (2000) Metabotropic glutamate receptors in acutely isolated hippocampal astrocytes: developmental changes of mGluR5 mRNA and functional expression. Glia 29, 70–80.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Diamond, J.S., Bergles, D.E. and Jahr, C.E. (1998) Glutamate release monitored with astrocyte transporter currents during LTP. Neuron 21, 425–433.CrossRefGoogle ScholarPubMed
Ding, J.B., Takasaki, K.T. and Sabatini, B.L. (2009) Supraresolution imaging in brain slices using stimulated-emission depletion two-photon laser scanning microscopy. Neuron 63, 429–437.CrossRefGoogle ScholarPubMed
Dudek, S.M. and Bear, M.F. (1993) Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. Journal of Neuroscience 13, 2910–2918.CrossRefGoogle ScholarPubMed
Fellin, T., Halassa, M.M., Terunuma, M., Succol, F., Takano, H., Frank, M. et al. (2009) Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo. Proceedings of the National Academy of Sciences of the U.S.A. 106, 15037–15042.CrossRefGoogle ScholarPubMed
Fiacco, T.A. and McCarthy, K.D. (2004) Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons. Journal of Neuroscience 24, 722–732.CrossRefGoogle ScholarPubMed
Fiacco, T.A., Agulhon, C., Taves, S.R., Petravicz, J., Casper, K.B., Dong, X. et al. (2007) Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron 54, 611–626.CrossRefGoogle Scholar
Fiacco, T.A., Agulhon, C. and McCarthy, K.D. (2009) Sorting out astrocyte physiology from pharmacology. Annual Review of Pharmacology and Toxicology 49, 151–174.CrossRefGoogle ScholarPubMed
Foskett, J.K., White, C., Cheung, K.H. and Mak, D.O. (2007) Inositol trisphosphate receptor Ca2+ release channels. Physiological Reviews 87, 593–658.CrossRefGoogle ScholarPubMed
Ge, W.P. and Duan, S.M. (2007) Persistent enhancement of neuron-glia signaling mediated by increased extracellular K+ accompanying long-term synaptic potentiation. Journal of Neurophysiology 97, 2564–2569.CrossRefGoogle ScholarPubMed
Gersbach, M., Boiko, D.L., Niclass, C., Petersen, C.C. and Charbon, E. (2009) Fast-fluorescence dynamics in nonratiometric calcium indicators. Optics Letters 34, 362–364.CrossRefGoogle ScholarPubMed
Gomez-Gonzalo, M., Losi, G., Chiavegato, A., Zonta, M., Cammarota, M., Brondi, M. et al. (2010) An excitatory loop with astrocytes contributes to drive neurons to seizure threshold. PLoS Biology 8, e1000352.CrossRefGoogle ScholarPubMed
Gourine, A.V., Kasymov, V., Marina, N., Tang, F., Figueiredo, M.F., Lane, S. et al. (2010) Astrocytes control breathing through pH-dependent release of ATP. Science 329, 571–575.CrossRefGoogle ScholarPubMed
Halassa, M.M., Florian, C., Fellin, T., Munoz, J.R., Lee, S.Y., Abel, T. et al. (2009) Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61, 213–219.CrossRefGoogle ScholarPubMed
Hamilton, N.B. and Attwell, D. (2010) Do astrocytes really exocytose neurotransmitters? Nature Reviews. Neuroscience 11, 227–238.CrossRefGoogle ScholarPubMed
Haydon, P.G. (2001) GLIA: listening and talking to the synapse. Nature Reviews. Neuroscience 2, 185–193.CrossRefGoogle Scholar
Haydon, P.G. and Carmignoto, G. (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiological Reviews 86, 1009–1031.CrossRefGoogle ScholarPubMed
Hell, S.W. (2007) Far-field optical nanoscopy. Science 316, 1153–1158.CrossRefGoogle ScholarPubMed
Henneberger, C., Papouin, T., Oliet, S.H. and Rusakov, D.A. (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463, 232–236.CrossRefGoogle ScholarPubMed
Johnson, J.W. and Ascher, P. (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529–531.CrossRefGoogle ScholarPubMed
Jourdain, P., Bergersen, L.H., Bhaukaurally, K., Bezzi, P., Santello, M., Domercq, M. et al. (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nature Neuroscience 10, 331–339.CrossRefGoogle ScholarPubMed
Koester, H.J. and Sakmann, B. (2000) Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. Journal of Physiology 529, 625–646.CrossRefGoogle ScholarPubMed
Lu, Y.M., Jia, Z.P., Janus, C., Henderson, J.T., Gerlai, R., Wojtowicz, J.M. et al. (1997) Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. Journal of Neuroscience 17, 5196–5205.CrossRefGoogle ScholarPubMed
Luscher, C., Malenka, R.C. and Nicoll, R.A. (1998) Monitoring glutamate release during LTP with glial transporter currents. Neuron 21, 435–441.CrossRefGoogle ScholarPubMed
Manahan-Vaughan, D. (1997) Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats. Journal of Neuroscience 17, 3303–3311.CrossRefGoogle ScholarPubMed
Marchaland, J., Cali, C., Voglmaier, S.M., Li, H., Regazzi, R., Edwards, R.H. et al. (2008) Fast subplasma membrane Ca2+ transients control exo-endocytosis of synaptic-like microvesicles in astrocytes. Journal of Neuroscience 28, 9122–9132.CrossRefGoogle ScholarPubMed
Mothet, J.P., Pollegioni, L., Ouanounou, G., Martineau, M., Fossier, P. and Baux, G. (2005) Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proceedings of the National Academy of Sciences of the U.S.A. 102, 5606–5611.CrossRefGoogle ScholarPubMed
Nagerl, U.V., Willig, K.I., Hein, B., Hell, S.W. and Bonhoeffer, T. (2008) Live-cell imaging of dendritic spines by STED microscopy. Proceedings of the National Academy of Sciences of the U.S.A. 105, 18982–18987.CrossRefGoogle ScholarPubMed
Navarrete, M. and Araque, A. (2008) Endocannabinoids mediate neuron-astrocyte communication. Neuron 57, 883–893.CrossRefGoogle ScholarPubMed
Oertner, T.G., Sabatini, B.L., Nimchinsky, E.A. and Svoboda, K. (2002) Facilitation at single synapses probed with optical quantal analysis. Nature Neuroscience 5, 657–664.CrossRefGoogle ScholarPubMed
Panatier, A., Theodosis, D.T., Mothet, J.P., Touquet, B., Pollegioni, L., Poulain, D.A. et al. (2006) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125, 775–784.CrossRefGoogle ScholarPubMed
Pasti, L., Volterra, A., Pozzan, T. and Carmignoto, G. (1997) Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. Journal of Neuroscience 17, 7817–7830.CrossRefGoogle ScholarPubMed
Perea, G. and Araque, A. (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317, 1083–1086.CrossRefGoogle ScholarPubMed
Perea, G. and Araque, A. (2010) GLIA modulates synaptic transmission. Brain Research Review 63, 93–102.CrossRefGoogle ScholarPubMed
Platel, J.C., Dave, K.A., Gordon, V., Lacar, B., Rubio, M.E. and Bordey, A. (2010) NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron 65, 859–872.CrossRefGoogle ScholarPubMed
Porter, J.T. and McCarthy, K.D. (1996) Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. Journal of Neuroscience 16, 5073–5081.CrossRefGoogle ScholarPubMed
Porter, J.T. and McCarthy, K.D. (1997) Astrocytic neurotransmitter receptors in situ and in vivo. Progress in Neurobiology 51, 439–455.CrossRefGoogle ScholarPubMed
Rollenhagen, A., Satzler, K., Rodriguez, E.P., Jonas, P., Frotscher, M. and Lubke, J.H. (2007) Structural determinants of transmission at large hippocampal mossy fiber synapses. Journal of Neuroscience 27, 10434–10444.CrossRefGoogle ScholarPubMed
Ruas, M., Rietdorf, K., Arredouani, A., Davis, L.C., Lloyd-Evans, E., Koegel, H. et al. (2010) Purified TPC isoforms form NAADP receptors with distinct roles for Ca2+ signaling and endolysosomal trafficking. Current Biology 20, 703–709.CrossRefGoogle ScholarPubMed
Scott, R. and Rusakov, D.A. (2006) Main determinants of presynaptic Ca2+ dynamics at individual mossy fiber-CA3 pyramidal cell synapses. Journal of Neuroscience 26, 7071–7081.CrossRefGoogle ScholarPubMed
Scott, R., Ruiz, A., Henneberger, C., Kullmann, D.M. and Rusakov, D.A. (2008) Analog modulation of mossy fiber transmission is uncoupled from changes in presynaptic Ca2+. Journal of Neuroscience 28, 7765–7773.CrossRefGoogle ScholarPubMed
Selig, D.K., Lee, H.K., Bear, M.F. and Malenka, R.C. (1995) Reexamination of the effects of MCPG on hippocampal LTP, LTD, and depotentiation. Journal of Neurophysiology 74, 1075–1082.CrossRefGoogle ScholarPubMed
Shigetomi, E., Kracun, S., Sofroniew, M.V. and Khakh, B.S. (2010) A genetically targeted optical sensor to monitor calcium signals in astrocyte processes. Nature Neuroscience 13, 759–766.CrossRefGoogle ScholarPubMed
Todd, K.J., Darabid, H. and Robitaille, R. (2010) Perisynaptic glia discriminate patterns of motor nerve activity and influence plasticity at the neuromuscular junction. Journal of Neuroscience 30, 11870–11882.CrossRefGoogle ScholarPubMed
Ventura, R. and Harris, K.M. (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. Journal of Neuroscience 19, 6897–6906.CrossRefGoogle ScholarPubMed
Verkhratsky, A. and Kettenmann, H. (1996) Calcium signalling in glial cells. Trends in Neuroscience 19, 346–352.CrossRefGoogle ScholarPubMed
Verkhratsky, A., Orkand, R.K. and Kettenmann, H. (1998) Glial calcium: homeostasis and signaling function. Physiological Reviews 78, 99–141.CrossRefGoogle ScholarPubMed
Volterra, A. and Meldolesi, J. (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nature Reviews. Neuroscience 6, 626–640.CrossRefGoogle ScholarPubMed
Wilms, C.D., Schmidt, H. and Eilers, J. (2006) Quantitative two-photon Ca2+ imaging via fluorescence lifetime analysis. Cell Calcium 40, 73–79.CrossRefGoogle ScholarPubMed
Wilt, B.A., Burns, L.D., Wei Ho, E.T., Ghosh, K.K., Mukamel, E.A. and Schnitzer, M.J. (2009) Advances in light microscopy for neuroscience. Annual Review of Neuroscience 32, 435–506.CrossRefGoogle ScholarPubMed
Witcher, M.R., Kirov, S.A. and Harris, K.M. (2007) Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus. Glia 55, 13–23.CrossRefGoogle ScholarPubMed
Yang, Y., Ge, W., Chen, Y., Zhang, Z., Shen, W., Wu, C. et al. (2003) Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proceedings of the National Academy of Sciences of the U.S.A. 100, 15194–15199.CrossRefGoogle ScholarPubMed