Synaptic information processing by astrocytes

Glial cells were classically considered as supportive cells that do not contribute to information processing in the nervous system. However, considerable amount of evidence obtained by several groups during the last few years has demonstrated the existence of a bidirectional communication between astrocytes and neurons, which prompted a re-examination of the role of glial cells in the physiology of the nervous system. This review will discuss recent advances in the neuron-to-astrocyte communication, focusing on the recently reported properties of the synaptically evoked astrocyte Ca2+ signal that indicate that astrocytes show integrative properties for synaptic information processing. Indeed, we have recently shown that hippocampal astrocytes discriminate between the activity of different synapses, and respond selectively to different axon pathways. Furthermore, the astrocyte Ca2+ signal is modulated by the simultaneous activity of different synaptic inputs. This Ca2+ signal modulation depends on cellular intrinsic properties of the astrocytes, is bidirectionally regulated by the level of synaptic activity, and controls the spatial extension of the intracellular Ca2+ signal. Consequently, we propose that astrocytes can be considered as cellular elements involved in information processing by the nervous system.

[1]  Shih-Chun Lin,et al.  Synaptic signaling between neurons and glia , 2004, Glia.

[2]  Dwight E Bergles,et al.  Clearance of glutamate inside the synapse and beyond , 1999, Current Opinion in Neurobiology.

[3]  Alfonso Araque,et al.  Glial calcium signaling and neuron-glia communication. , 2005, Cell calcium.

[4]  S. Goldman,et al.  New roles for astrocytes: Redefining the functional architecture of the brain , 2003, Trends in Neurosciences.

[5]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[6]  E. Newman Glial modulation of synaptic transmission in the retina , 2004, Glia.

[7]  K. Ballanyi,et al.  Neuron–Glia Signaling via α1 Adrenoceptor-Mediated Ca2+ Release in Bergmann Glial Cells In Situ , 1999, The Journal of Neuroscience.

[8]  A. Fatatis,et al.  Vasoactive intestinal peptide increases intracellular calcium in astroglia: synergism with alpha-adrenergic receptors. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Richard Robitaille,et al.  Glial modulation of synaptic transmission at the neuromuscular junction , 2004, Glia.

[10]  K. McCarthy,et al.  Hippocampal Astrocytes Exhibit Ca2+ ‐Elevating Muscarinic Cholinergic and Histaminergic Receptors In Situ , 2000, Journal of neurochemistry.

[11]  B. MacVicar,et al.  Calcium transients in astrocyte endfeet cause cerebrovascular constrictions , 2004, Nature.

[12]  Pierre J. Magistretti,et al.  The tripartite synapse: glia in synaptic transmission , 2002 .

[13]  Jai-Yoon Sul,et al.  Astrocytic connectivity in the hippocampus. , 2004, Neuron glia biology.

[14]  M. C. Angulo,et al.  Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation , 2003, Nature Neuroscience.

[15]  C. Zorumski,et al.  Basal levels of adenosine modulate mGluR5 on rat hippocampal astrocytes , 2001, Glia.

[16]  Maiken Nedergaard,et al.  Astrocyte-mediated activation of neuronal kainate receptors. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Todd A Fiacco,et al.  Intracellular Astrocyte Calcium Waves In Situ Increase the Frequency of Spontaneous AMPA Receptor Currents in CA1 Pyramidal Neurons , 2004, The Journal of Neuroscience.

[18]  S. W. Kuffler,et al.  Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. , 1966, Journal of neurophysiology.

[19]  A. Charles,et al.  Intercellular signaling in glial cells: Calcium waves and oscillations in response to mechanical stimulation and glutamate , 1991, Neuron.

[20]  Tomas C. Bellamy,et al.  Short‐term plasticity of Bergmann glial cell extrasynaptic currents during parallel fiber stimulation in rat cerebellum , 2005, Glia.

[21]  B. Barres,et al.  Signaling between glia and neurons: focus on synaptic plasticity , 2005, Current Opinion in Neurobiology.

[22]  P. Haydon,et al.  Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Araque,et al.  SNARE Protein-Dependent Glutamate Release from Astrocytes , 2000, The Journal of Neuroscience.

[24]  S. Koizumi,et al.  Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Mu-ming Poo,et al.  ATP Released by Astrocytes Mediates Glutamatergic Activity-Dependent Heterosynaptic Suppression , 2003, Neuron.

[26]  K. McCarthy,et al.  Mature hippocampal astrocytes exhibit functional metabotropic and ionotropic glutamate receptors in situ , 1999, Glia.

[27]  K. McCarthy,et al.  ASTROCYTIC NEUROTRANSMITTER RECEPTORS IN SITU AND IN VIVO , 1997, Progress in Neurobiology.

[28]  S. R. Cajal Textura del Sistema Nervioso del Hombre y de los Vertebrados, 1899–1904 , 2019 .

[29]  M. C. Angulo,et al.  Glutamate Released from Glial Cells Synchronizes Neuronal Activity in the Hippocampus , 2004, The Journal of Neuroscience.

[30]  G. Perea,et al.  Properties of Synaptically Evoked Astrocyte Calcium Signal Reveal Synaptic Information Processing by Astrocytes , 2005, The Journal of Neuroscience.

[31]  Loredano Pollegioni,et al.  Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Clemens Boucsein,et al.  Astrocyte Ca2+ waves trigger responses in microglial cells in brain slices , 2002, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[33]  Cathryn L. Kubera,et al.  Astrocytic Purinergic Signaling Coordinates Synaptic Networks , 2005, Science.

[34]  R. Vertes Hippocampal theta rhythm: A tag for short‐term memory , 2005, Hippocampus.

[35]  A. Reichenbach,et al.  Microdomains for neuron–glia interaction: parallel fiber signaling to Bergmann glial cells , 1999, Nature Neuroscience.

[36]  R. Llinás,et al.  Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. , 1980, The Journal of physiology.

[37]  T. Takano,et al.  Intercellular calcium signaling mediated by point-source burst release of ATP , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[38]  S. Goldman,et al.  Astrocyte-mediated potentiation of inhibitory synaptic transmission , 1998, Nature Neuroscience.

[39]  K. Zahs,et al.  Modulation of Neuronal Activity by Glial Cells in the Retina , 1998, The Journal of Neuroscience.

[40]  T. Pozzan,et al.  Intracellular Calcium Oscillations in Astrocytes: A Highly Plastic, Bidirectional Form of Communication between Neurons and Astrocytes In Situ , 1997, The Journal of Neuroscience.

[41]  S. Oliet,et al.  Glia-Derived d-Serine Controls NMDA Receptor Activity and Synaptic Memory , 2006, Cell.

[42]  Wade Morishita,et al.  Control of Synaptic Strength by Glial TNFα , 2002, Science.

[43]  Stephen J. Smith,et al.  Neuronal activity triggers calcium waves in hippocampal astrocyte networks , 1992, Neuron.

[44]  Giorgio Carmignoto,et al.  Reciprocal communication systems between astrocytes and neurones , 2000, Progress in Neurobiology.

[45]  Vitaly Filippov,et al.  Nitric Oxide Signals Parallel Fiber Activity to Bergmann Glial Cells in the Mouse Cerebellar Slice , 2001, Molecular and Cellular Neuroscience.

[46]  A. Araque,et al.  Tripartite synapses: glia, the unacknowledged partner , 1999, Trends in Neurosciences.

[47]  V. Gundersen,et al.  Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate , 2004, Nature Neuroscience.

[48]  H. Sontheimer Voltage‐dependent ion channels in glial cells , 1994, Glia.

[49]  A. Araque,et al.  Glutamate‐dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons , 1998, The European journal of neuroscience.

[50]  Tullio Pozzan,et al.  Prostaglandins stimulate calcium-dependent glutamate release in astrocytes , 1998, Nature.

[51]  H. Kettenmann,et al.  Different Mechanisms Promote Astrocyte Ca2+ Waves and Spreading Depression in the Mouse Neocortex , 2003, The Journal of Neuroscience.

[52]  J. Rinzel,et al.  The role of dendrites in auditory coincidence detection , 1998, Nature.

[53]  S. Oloff,et al.  Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity. , 2002, Journal of neurophysiology.

[54]  A. Araque,et al.  Calcium Elevation in Astrocytes Causes an NMDA Receptor-Dependent Increase in the Frequency of Miniature Synaptic Currents in Cultured Hippocampal Neurons , 1998, The Journal of Neuroscience.

[55]  P. Haydon Glia: listening and talking to the synapse , 2001, Nature Reviews Neuroscience.

[56]  M. Bennett,et al.  New roles for astrocytes: Gap junction hemichannels have something to communicate , 2003, Trends in Neurosciences.

[57]  Mark Ellisman,et al.  Protoplasmic Astrocytes in CA1 Stratum Radiatum Occupy Separate Anatomical Domains , 2002, The Journal of Neuroscience.

[58]  K. McCarthy,et al.  Hippocampal Astrocytes In Situ Respond to Glutamate Released from Synaptic Terminals , 1996, The Journal of Neuroscience.

[59]  Alfonso Araque,et al.  Glial modulation of synaptic transmission in culture , 2004, Glia.

[60]  Eric A Newman,et al.  Glial Cells Dilate and Constrict Blood Vessels: A Mechanism of Neurovascular Coupling , 2006, The Journal of Neuroscience.

[61]  R. Robitaille,et al.  Glial cells as active partners in synaptic functions. , 2001, Progress in brain research.

[62]  Christian Steinhäuser,et al.  Glial modulation of synaptic transmission in the hippocampus , 2004, Glia.

[63]  J. Lacaille,et al.  Differential mechanisms of Ca2+ responses in glial cells evoked by exogenous and endogenous glutamate in rat hippocampus , 2001, Hippocampus.

[64]  A. Verkhratsky,et al.  Glial calcium: homeostasis and signaling function. , 1998, Physiological reviews.

[65]  J. Lacaille,et al.  GABAergic Network Activation of Glial Cells Underlies Hippocampal Heterosynaptic Depression , 2006, The Journal of Neuroscience.

[66]  Eduardo Soriano,et al.  Neuronal Activity Regulates Correlated Network Properties of Spontaneous Calcium Transients in Astrocytes In Situ , 2002, The Journal of Neuroscience.

[67]  S. Duan,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S7 References Long-term Potentiation of Neuron-glia Synapses Mediated by Ca 2+ -permeable Ampa Receptors , 2022 .

[68]  Eduardo D. Martín,et al.  Synaptically Released Acetylcholine Evokes Ca2+Elevations in Astrocytes in Hippocampal Slices , 2002, The Journal of Neuroscience.

[69]  H. Parri,et al.  Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation , 2001, Nature Neuroscience.

[70]  S. Finkbeiner,et al.  Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. , 1990, Science.

[71]  Robert F. Miller,et al.  D‐Serine as a glial modulator of nerve cells , 2004, Glia.

[72]  A. Araque,et al.  Dynamic signaling between astrocytes and neurons. , 2001, Annual review of physiology.