Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T23:14:46.309Z Has data issue: false hasContentIssue false
  • English
  • Français

Astrocytes process synaptic information

Published online by Cambridge University Press:  27 February 2009

Alfonso Araque
Alfonso Araque*
Affiliation:
Instituto Cajal, Consejo Superior de Investigaciones Científicas, Madrid 28002, Spain
*
Correspondence should be addressed to: Alfonso Araque, Instituto Cajal, Doctor Arce 37, Madrid 28002, Spain phone: +34-91-5854710 fax: +34-91-585 4754 email: araque@cajal.csic.es
Get access Rights & Permissions [Opens in a new window]

Abstract

Astrocytes were classically considered as simple supportive cells for neurons without a significant role in information processing by the nervous system. However, considerable amounts of evidence obtained by several groups during the past years demonstrated the existence of a bidirectional communication between astrocytes and neurons, which prompted a re-examination of the role of astrocytes in the physiology of the nervous system. While neurons base their excitability on electrical signals generated across the membrane, astrocytes base their cellular excitability on variations of the Ca2+ concentration in the cytosol. This article discusses our current knowledge of the properties of the synaptically evoked astrocyte Ca2+ signal, which reveals that astrocytes display integrative properties for synaptic information processing. Astrocytes respond selectively to different axon pathways, discriminate between the activity of different synapses and their Ca2+ signal is non-linearly modulated by the simultaneous activity of different synaptic inputs. Furthermore, this Ca2+ signal modulation depends on astrocyte cellular intrinsic properties and is bidirectionally regulated by the level of synaptic activity. Finally, astrocyte Ca2+ elevations can trigger the release of gliotransmitters, which modulate neuronal activity as well as synaptic transmission and plasticity, hence granting the bidirectional communication with neurons. Consequently, astrocytes can be considered as cellular elements involved in information processing by the nervous system.

Keywords

Neuron–astrocyte communicationCa2+ signalinformation processingastrocyte intrinsic propertiessynaptic transmission
Type
Essay
Information
Neuron Glia Biology , Volume 4 , Issue 1 , February 2008 , pp. 3 - 10
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Agmon-Snir, H., Carr, C.E. and Rinzel, J. (1998) The role of dendrites in auditory coincidence detection. Nature 393, 268–272.CrossRefGoogle ScholarPubMed
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 Scholar
Allen, N.J. and Barres, B.A. (2005) Signaling between glia and neurons: focus on synaptic plasticity. Current Opinion in Neurobiology 15, 542–548.CrossRefGoogle ScholarPubMed
Araque, A., Li, N., Doyle, R.T. and Haydon, P.G. (2000) SNARE protein-dependent glutamate release from astrocytes. Journal of Neuroscience 20, 666–673.CrossRefGoogle Scholar
Araque, A., Martin, E.D., Perea, G., Arellano, J.I. and Buño, W. (2002) Synaptically-released acetylcholine evokes Ca2+ elevations in astrocytes in hippocampal slices. Journal of Neuroscience 22, 2443–2450.CrossRefGoogle Scholar
Araque, A., Parpura, V., Sanzgiri, R.P. and Haydon, P.G. (1998a) Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. European Journal of Neuroscience 10, 2129–2142.CrossRefGoogle Scholar
Araque, A., Parpura, V., Sanzgiri, R.P. and Haydon, P.G. (1999) Tripartite synapses: glia, the unacknowledged partner. Trends in Neurosciences 22, 208–215.CrossRefGoogle Scholar
Araque, A. and Perea, G. (2004) Glial modulation of synaptic transmission in culture. Glia 47, 241–248.CrossRefGoogle Scholar
Araque, A., Sanzgiri, R.P., Parpura, V. and Haydon, P.G. (1998b) Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. Journal of Neuroscience 18, 6822–6829.CrossRefGoogle Scholar
Arcuino, G., Lin, J.H., Takano, T., Liu, C., Jiang, L., Gao, Q. et al. (2002) Intercellular calcium signaling mediated by point-source burst release of ATP. Proceedings of the National Academy of Sciences of the U.S.A. 99, 9840–9845.CrossRefGoogle Scholar
Beattie, E.C., Stellwagen, D., Morishita, W., Bresnahan, J.C., Ha, B.K., Von Zastrow, M. et al. (2002) Control of synaptic strength by glial TNFα. Science 295, 2282–2285.Google Scholar
Bekar, L.K., He, W. and Nedergaard, M. (2008) Locus coeruleus α-adrenergic-mediated activation of cortical astrocytes in vivo. Cerebral Cortex 18, 2789–2795.Google Scholar
Bezzi, P., Carmignoto, G., Pasti, L., Vesce, S., Rossi, D., Rizzini, B. et al. (1998) Prostaglandins stimulate Ca2+-dependent glutamate release in astrocytes. Nature 391, 281–285.CrossRefGoogle Scholar
Bezzi, P., Gundersen, V., Galbete, J.L., Seifert, G., Steinhauser, C., Pilati, E. et al. (2004) Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nature Neuroscience 7, 613–620.CrossRefGoogle Scholar
Catsicas, M. and Mobbs, P. (2001) GABAb receptors regulate chick retinal calcium waves. Journal of Neuroscience 21, 897–910.CrossRefGoogle Scholar
Charles, A.C., Merrill, J.E., Dirksen, E.R. and Sanderson, M.J. (1991) Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron 6, 983–992.CrossRefGoogle Scholar
Colomar, A. and Robitaille, R. (2004) Glial modulation of synaptic transmission at the neuromuscular junction. Glia 47, 284–289.CrossRefGoogle Scholar
Cormier, R.J., Mennerick, S., Melbostad, H. and Zorumski, C.F. (2001) Basal levels of adenosine modulate mGluR5 on rat hippocampal astrocytes. Glia 33, 24–35.Google Scholar
Cornell-Bell, A.H., Finkbeiner, S.M., Cooper, M.S. and Smith, S.J. (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470–473.CrossRefGoogle Scholar
Dombeck, D.A., Khabbaz, A.N., Collman, F., Adelman, T.L. and Tank, D.W. (2007) Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56, 43–57.CrossRefGoogle Scholar
Fatatis, A., Holtzclaw, L.A., Avidor, R., Brenneman, D.E. and Russell, J.T. (1994) Vasoactive intestinal peptide increases intracellular calcium in astroglia: synergism with alpha-adrenergic receptors. Proceedings of the National Academy of Sciences of the U.S.A. 91, 2036–2040.CrossRefGoogle Scholar
Fellin, T. and Carmignoto, G. (2004) Neurone-to-astrocyte signalling in the brain represents a distinct multifunctional unit. Journal of Physiology 559, 3–15.CrossRefGoogle Scholar
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 Scholar
Göbel, W., Kampa, B.M. and Helmchen, F. (2007) Imaging cellular network dynamics in three dimensions using fast 3D laser scanning. Nature Methods 4, 73–79.Google Scholar
Gordon, G.R., Mulligan, S.J. and MacVicar, B.A. (2007) Astrocyte control of the cerebrovasculature. Glia 55, 1214–1221.CrossRefGoogle Scholar
Grosche, J., Matyash, V., Moller, T., Verkhratsky, A., Reichenbach, A. and Kettenmann, H. (1999) Microdomains for neuron–glia interaction: parallel fiber signaling to Bergmann glial cells. Nature Neuroscience 2, 139–143.CrossRefGoogle Scholar
Haydon, P.G. and Araque, A. (2002) Astrocytes as modulators of synaptic transmission. In Volterra, A., Magistretti, P.J. & Haydon, P.G. (eds) The Tripartite Synapse: Glia in Synaptic Transmission. Oxford University Press, New York, pp. 185–198.Google Scholar
Hille, B. (2001) Ion Channels of Excitable Membranes. Sinauer Associates, Sunderland.Google Scholar
Hirase, H., Qian, L., Barthó, P. and Buzsáki, G. (2004) Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biology 2, E96.CrossRefGoogle Scholar
Huang, Y.H. and Bergles, D.E. (2004) Glutamate transporters bring competition to the synapse. Current Opinion in Neurobiology 14, 346–352.Google Scholar
Iadecola, C. and Nedergaard, M. (2007) Glial regulation of the cerebral microvasculature. Nature Neuroscience 10, 1369–1376.CrossRefGoogle Scholar
Kang, J., Jiang, L., Goldman, S.A. and Nedergaard, M. (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nature Neuroscience 1, 683–692.CrossRefGoogle ScholarPubMed
Kettenmann, H. and Ransom, B.R. (2004) Neuroglia. Oxford University Press, New York.CrossRefGoogle Scholar
Koizumi, S., Fujishita, K., Tsuda, M., Shigemoto-Mogami, Y. and Inoue, K. (2003) Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures. Proceedings of the National Academy of Sciences of the U.S.A. 100, 11023–11028.CrossRefGoogle Scholar
Kulik, A., Haentzsch, A., Luckermann, M., Reichelt, W. and Ballanyi, K. (1999) Neuron-glia signaling via a1 adrenoceptor-mediated Ca2+ release in Bergmann glial cells in situ. Journal of Neuroscience 19, 8401–8408.CrossRefGoogle Scholar
Llinas, R. and Sugimori, M. (1980) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. Journal of Physiology 305, 197–213.CrossRefGoogle Scholar
Malarkey, E.B. and Parpura, V. Mechanisms of glutamate release from astrocytes. Neurochemistry International 52, 142–154.Google Scholar
Matyash, V., Filippov, V., Mohrhagen, V. and Kettenmann, H. (2001) Nitric oxide signals parallel fiber activity to Bergmann glial cells in the mouse cerebellar slice. Molecular and Cellular Neurosciences 18, 664–670.CrossRefGoogle Scholar
Navarrete, M. and Araque, A. (2008) Endocannabinoids mediate neuron–astrocyte communication. Neuron 57, 883–893.CrossRefGoogle Scholar
Nett, W.J., Oloff, S.H. and McCarthy, K.D. (2002) Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity. Journal of Neurophysiology 87, 528–537.CrossRefGoogle Scholar
Newman, E.A. (2004) Glial modulation of synaptic trasnmission in the retina. Glia 47, 268–274.Google Scholar
Nimmerjahn, A., Kirchhoff, F., Kerr, J.N. and Helmchen, F. (2004) Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nature Methods 1, 31–37.CrossRefGoogle Scholar
Orkand, R.K., Nicholls, J.G. and Kuffler, S.W. (1966) Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibian. Journal of Neurophysiology 29, 788–806.CrossRefGoogle Scholar
Parri, R., Gould, T.M. and Crunelli, V. (2001) Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Nature Neuroscience 4, 803–812.CrossRefGoogle Scholar
Parri, R., Gould, T.M. and Crunelli, V. (2004) A heterogeneity of responses to synaptic stimulation in astrocytes in thalamic astrocytes. Society for Neuroscience Abstracts 30, 976.4.Google Scholar
Pascual, O., Casper, K.B., Kubera, C., Zhang, J., Revilla-Sanchez, R., Sul, J.Y. et al. (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310, 113–116.Google Scholar
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 Scholar
Perea, G. and Araque, A. (2005a) Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. Journal of Neuroscience 25, 2192–2203.CrossRefGoogle Scholar
Perea, G. and Araque, A. (2005b) Glial calcium signalling and neuron-glia communication. Cell Calcium 38, 375–382.CrossRefGoogle Scholar
Perea, G. and Araque, A. (2006) Synaptic information processing by astrocytes. Journal of Physiology (Paris) 99, 92–97.CrossRefGoogle Scholar
Perea, G. and Araque, A. (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317, 1083–1086.CrossRefGoogle Scholar
Peters, O., Schipke, C.G., Hashimoto, Y. and Kettenmann, H. (2003) Different mechanisms promote astrocyte Ca2+ waves and spreading depression in the mouse neocortex. Journal of Neuroscience 23, 9888–9896.CrossRefGoogle Scholar
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 Scholar
Porter, J.T. and McCarthy, K.D. (1997) Astrocytic neurotransmitter receptors in situ and in vivo. Progress in Neurobiology 51, 439–455.CrossRefGoogle Scholar
Ramón y Cajal, S. (1897) Algo sobre la significación fisiológica de la neuroglia. Revista Trimestral Micrográfica 1, 1–86.Google Scholar
Ramón y Cajal, S. (1899) Textura del sistema nervioso del hombre y de los vertrebrados. Tomo I, N, Moya, Madrid.Google Scholar
Schipke, C.G., Haas, B. and Kettenmann, H. (2008) Astrocytes discriminate and selectively respond to the activity of a subpopulation of neurons within the barrel cortex. Cerebral Cortex 18, 2450–2459.Google Scholar
Schousboe, A. (2003) Role of astrocytes in the maintenance and modulation of glutamatergic and GABAergic neurotransmission. Neurochemical Research 28, 347–352.Google Scholar
Schummers, J., Yu, H. and Sur, M. (2008) Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320, 1638–1643.CrossRefGoogle Scholar
Seifert, G., Schilling, K. and Steinhäuser, C. (2006) Astrocyte dysfunction in neurological disorders: a molecular perspective. Nature Reviews Neuroscience 7, 194–206.CrossRefGoogle Scholar
Seifert, G. and Steinhäuser, C. (2001) Ionotropic glutamate receptors in astrocytes. Progress in Brain Research 132, 287–299.Google Scholar
Serrano, A., Haddjeri, N., Lacaille, J.C. and Robitaille, R. (2006) GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. Journal of Neuroscience 26, 5370–5382.Google Scholar
Sontheimer, H. (1994) Voltage-dependent ion channels in glial cells. Glia 11, 156–172.CrossRefGoogle Scholar
Sul, J.Y., Orosz, G., Givens, R.S. and Haydon, P.G. (2004) Astrocytic connectivity in the hippocampus. Neuron Glia Biology 1, 3–11.CrossRefGoogle Scholar
Takata, N. and Hirase, H. (2008) Cortical layer 1 and layer 2/3 astrocytes exhibit distinct calcium dynamics in vivo. PLoS ONE 3, e2525; doi:10.1371/journal.pone.0002525.CrossRefGoogle Scholar
Verkhratsky, A. and Steinhäuser, C. (2000) Ion channels in glial cells. Brain Research Brain Research Reviews 32, 380–412.CrossRefGoogle Scholar
Volterra, A. and Bezzi, P. (2002) Release of transmitters from glial cells. In Volterra, A., Magistretti, P.J. & Haydon, P.G. (eds) The Tripartite Synapse: Glia in Synaptic Transmission. Oxford University Press, New York, pp. 164–184.Google Scholar
Volterra, A. and Meldolesi, J. (2005) Quantal release of transmitter: not only for neurons but from astrocytes as well? In Kettenman, H. & Ransom, B. (eds) Neuroglia. Oxford University Press, New York, pp. 190–201.Google Scholar
Volterra, A. and Steinhauser, C. (2004) Glial modulation of synaptic transmission in the hippocampus. Glia 47, 249–257.CrossRefGoogle ScholarPubMed
Wallraff, A., Köhling, R., Heinemann, U., Theis, M., Willecke, K. and Steinhäuser, C. (2006) The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. Journal of Neuroscience 26, 5438–5447.CrossRefGoogle Scholar
Wang, X., Lou, N., Xu, Q., Tian, G.F., Peng, W.G., Han, X. et al. (2006) Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nature Neuroscience 9, 816–823.CrossRefGoogle Scholar
Zhang, J., Wang, H., Ye, C., Ge, W., Chen, Y., Jiang, Z. et al. (2003) ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40, 971–982.CrossRefGoogle Scholar
Zonta, M., Angulo, M.C., Gobbo, S., Rosengarten, B., Hossmann, K.A., Pozzan, T. et al. (2003) Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nature Neuroscience 6, 43–50.CrossRefGoogle Scholar