The function and efficacy of synaptic transmission are determined not only by the composition and activity of pre- and postsynaptic components but also by the environment in which a synapse is embedded. Glial cells constitute an important part of this environment and participate in several aspects of synaptic functions. Among the glial cell family, the roles played by astrocytes at the synaptic level are particularly important, ranging from the trophic support to the fine-tuning of transmission. Astrocytic structures are frequently observed in close association with glutamatergic synapses, providing a morphological entity for bidirectional interactions with synapses. Experimental evidence indicates that astrocytes sense neuronal activity by elevating their intracellular calcium in response to neurotransmitters and may communicate with neurons. The precise role of astrocytes in regulating synaptic properties, function, and plasticity remains however a subject of intense debate and many aspects of their interactions with neurons remain to be investigated. A particularly intriguing aspect is their ability to rapidly restructure their processes and modify their coverage of the synaptic elements. The present review summarizes some of these findings with a particular focus on the mechanisms driving this form of structural plasticity and its possible impact on synaptic structure and function. 1. Introduction Since the earliest studies on glial cells in the 19th century, Ramón y Cajal, Camillo Golgi, and their contemporary colleagues have described astrocytes as very particular cells in intimate contact with neurons and capillaries. Based on these observations, they made different hypotheses on their physiological function, ranging from passive space filling in the neuropil to active energy supply for neurons [1]. Almost 150 years later, the neurophysiological role of astrocytes is still a subject of intense debate, although increasing data suggest that they are active players in mechanisms of synaptic transmission and plasticity [2]. Numerous data demonstrate that thin astrocytic processes infiltrate brain tissue [3]. The most commonly used name for these thin processes is “peripheral astrocytic processes,” as it is often difficult to distinguish, with light microscopy, their exact position with regard to different neuropil elements. However, in this review we will mostly focus on the data, obtained with various techniques, concerning fine astrocytic processes that are in close association with synaptic contacts, and thus the term “perisynaptic astrocytic
References
[1]
H. Kettenmann and B. R. Ransom, Neuroglia, Oxford University Press, Oxford, UK, 2005.
[2]
A. Volterra and J. Meldolesi, “Astrocytes, from brain glue to communication elements: the revolution continues,” Nature Reviews Neuroscience, vol. 6, no. 8, pp. 626–640, 2005.
[3]
T. I. Chao, M. Rickman, and J. R. Wolff, “The synapse-astrocyte boundary: an anatomical basis for an integrative role of glia in synaptic transmission,” in Tripartite Synapse: Glia in Synaptic Transmission, A. Volterra, P. J. Magistretti, and P. G. Haydon, Eds., vol. 1, pp. 3–23, Oxford University Press, Oxford, UK.
[4]
M. Lavialle, G. Aumann, E. Anlauf, F. Pr？ls, M. Arpin, and A. Derouiche, “Structural plasticity of perisynaptic astrocyte processes involves ezrin and metabotropic glutamate receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 31, pp. 12915–12919, 2011.
[5]
N. C. Danbolt, “Glutamate uptake,” Progress in Neurobiology, vol. 65, no. 1, pp. 1–105, 2001.
[6]
D. M. Kullmann and F. Asztely, “Extrasynaptic glutamate spillover in the hippocampus: evidence and implications,” Trends in Neurosciences, vol. 21, no. 1, pp. 8–14, 1998.
[7]
V. Benfenati and S. Ferroni, “Water transport between CNS compartments: functional and molecular interactions between aquaporins and ion channels,” Neuroscience, vol. 168, no. 4, pp. 926–940, 2010.
[8]
I. Allaman, M. Bélanger, and P. J. Magistretti, “Astrocyte-neuron metabolic relationships: for better and for worse,” Trends in Neurosciences, vol. 34, no. 2, pp. 76–87, 2011.
[9]
A. Panatier, J. Vallée, M. Haber, K. K. Murai, J. C. Lacaille, and R. Robitaille, “Astrocytes are endogenous regulators of basal transmission at central synapses,” Cell, vol. 146, no. 5, pp. 785–798, 2011.
[10]
M. A. Di Castro, J. Chuquet, N. Liaudet et al., “Local Ca2+ detection and modulation of synaptic release by astrocytes,” Nature Neuroscience, vol. 14, no. 10, pp. 1276–1284, 2011.
[11]
G. Perea and A. Araque, “Glial calcium signaling and neuron-glia communication,” Cell Calcium, vol. 38, no. 3-4, pp. 375–382, 2005.
[12]
C. Agulhon, T. A. Fiacco, and K. D. McCarthy, “Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca2+ signaling,” Science, vol. 327, no. 5970, pp. 1250–1254, 2010.
[13]
A. Reichenbach, A. Derouiche, and F. Kirchhoff, “Morphology and dynamics of perisynaptic glia,” Brain Research Reviews, vol. 63, no. 1-2, pp. 11–25, 2010.
[14]
A. M. Benediktsson, S. J. Schachtele, S. H. Green, and M. E. Dailey, “Ballistic labeling and dynamic imaging of astrocytes in organotypic hippocampal slice cultures,” Journal of Neuroscience Methods, vol. 141, no. 1, pp. 41–53, 2005.
[15]
M. M. Halassa, T. Fellin, H. Takano, J. H. Dong, and P. G. Haydon, “Synaptic islands defined by the territory of a single astrocyte,” Journal of Neuroscience, vol. 27, no. 24, pp. 6473–6477, 2007.
[16]
E. Shigetomi, E. A. Bushong, M. D. Haustein et al., “Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses,” Journal of General Physiology, vol. 141, pp. 633–647, 2013.
[17]
E. A. Bushong, M. E. Martone, Y. Z. Jones, and M. H. Ellisman, “Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains,” Journal of Neuroscience, vol. 22, no. 1, pp. 183–192, 2002.
[18]
J. R. Wolff, “Quantitative aspects of astroglia,” in Proceedings of the 6th international Congress of Neuropathology, pp. 327–352, 1970.
[19]
J. Grosche, V. Matyash, T. M？ller, A. Verkhratsky, A. Reichenbach, and H. Kettenmann, “Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells,” Nature Neuroscience, vol. 2, no. 2, pp. 139–143, 1999.
[20]
K. Hama, T. Arii, E. Katayama, M. Marton, and M. H. Ellisman, “Tri-dimensional morphometric analysis of astrocytic processes with high voltage electron microscopy of thick Golgi preparations,” Journal of Neurocytology, vol. 33, no. 3, pp. 277–285, 2004.
[21]
A. Peters, S. L. Palay, and H. D. Webster, The Fine Structure of the Nervous System: Neurons and Their Supporting Cells, Oxford University Press, New York, NY, USA, 1991.
[22]
M. Gorath, T. Stahnke, T. Mronga, O. Goldbaum, and C. Richter-Landsberg, “Rapid morphological changes in astrocytes are accompanied by redistribution but not by quantitative changes of cytoskeletal proteins,” Glia, vol. 36, no. 1, pp. 102–115, 2001.
[23]
A. Derouiche and M. Frotscher, “Peripheral astrocyte processes: monitoring by selective immunostaining for the actin-binding ERM proteins,” Glia, vol. 36, no. 3, pp. 330–341, 2001.
[24]
D. Molotkov, S. Zobova, J. M. Arcas, and L. Khiroug, “Calcium-induced outgrowth of astrocytic peripheral processes requires actin binding by Profilin-1,” Cell Calcium, vol. 53, no. 5-6, pp. 338–348, 2013.
[25]
J. Spacek and K. M. Harris, “Three-dimensional organization of cell adhesion junctions at synapses and dendritic spines in area CA1 of the rat hippocampus,” Journal of Comparative Neurology, vol. 393, pp. 58–68, 1998.
[26]
J. Spacek, “Relationships between synaptic junctions, puncta adhaerentia and the spine apparatus at neocortical axo-spinous synapses. A serial section study,” Anatomy and Embryology, vol. 173, no. 1, pp. 129–135, 1985.
[27]
M. R. Witcher, S. A. Kirov, and K. M. Harris, “Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus,” Glia, vol. 55, no. 1, pp. 13–23, 2007.
[28]
I. Lushnikova, G. Skibo, D. Muller, and I. Nikonenko, “Synaptic potentiation induces increased glial coverage of excitatory synapses in CA1 hippocampus,” Hippocampus, vol. 19, no. 8, pp. 753–762, 2009.
[29]
R. Ventura and K. M. Harris, “Three-dimensional relationships between hippocampal synapses and astrocytes,” Journal of Neuroscience, vol. 19, no. 16, pp. 6897–6906, 1999.
[30]
A. Rollenhagen, K. S？tzler, E. P. Rodríguez, P. Jonas, M. Frotscher, and J. H. R. Lübke, “Structural determinants of transmission at large hippocampal mossy fiber synapses,” Journal of Neuroscience, vol. 27, no. 39, pp. 10434–10444, 2007.
[31]
M. A. Xu-Friedman and W. G. Regehr, “Ultrastructural contributions to desensitization at cerebellar mossy fiber to granule cell synapses,” Journal of Neuroscience, vol. 23, no. 6, pp. 2182–2192, 2003.
[32]
M. A. Xu-Friedman, K. M. Harris, and W. G. Regehr, “Three-dimensional comparison of ultrastructural characteristics at depressing and facilitating synapses onto cerebellar Purkinje cells,” Journal of Neuroscience, vol. 21, no. 17, pp. 6666–6672, 2001.
[33]
K. Chounlamountry and J. P. Kessler, “The ultrastructure of perisynaptic glia in the nucleus tractus solitarii of the adult rat: comparison between single synapses and multisynaptic arrangements,” Glia, vol. 59, no. 4, pp. 655–663, 2011.
[34]
M. Haber, L. Zhou, and K. K. Murai, “Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses,” Journal of Neuroscience, vol. 26, no. 35, pp. 8881–8891, 2006.
[35]
D. Verbich, G. A. Prenosil, P. K. Y. Chang, K. K. Murai, and R. A. Mckinney, “Glial glutamate transport modulates dendritic spine head protrusions in the hippocampus,” Glia, vol. 60, no. 7, pp. 1067–1077, 2012.
[36]
N. Ji, H. Shroff, H. Zhong, and E. Betzig, “Advances in the speed and resolution of light microscopy,” Current Opinion in Neurobiology, vol. 18, no. 6, pp. 605–616, 2008.
[37]
B. E. Nixdorf-Bergweiler, D. Albrecht, and U. Heinemann, “Developmental changes in the number, size, and orientation of GFAP-positive cells in the CA1 region of rat hippocampus,” Glia, vol. 12, no. 3, pp. 180–195, 1994.
[38]
K. Ogata and T. Kosaka, “Structural and quantitative analysis of astrocytes in the mouse hippocampus,” Neuroscience, vol. 113, no. 1, pp. 221–233, 2002.
[39]
S. L. Feig and L. B. Haberly, “Surface-associated astrocytes, not endfeet, form the glia limitans in posterior piriform cortex and have a spatially distributed, not a domain, organization,” Journal of Comparative Neurology, vol. 519, no. 10, pp. 1952–1969, 2011.
[40]
K. R. Lehre and D. A. Rusakov, “Asymmetry of glia near central synapses favors presynaptically directed glutamate escape,” Biophysical Journal, vol. 83, no. 1, pp. 125–134, 2002.
[41]
C. Genoud, C. Quairiaux, P. Steiner, H. Hirling, E. Welker, and G. W. Knott, “Plasticity of astrocytic coverage and glutamate transporter expression in adult mouse cortex,” PLoS Biology, vol. 4, no. 11, article e343, 2006.
[42]
J. Grosche, H. Kettenmann, and A. Reichenbach, “Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons,” Journal of Neuroscience Research, vol. 68, no. 2, pp. 138–149, 2002.
[43]
K. Yamada, M. Fukaya, T. Shibata et al., “Dynamic transformation of Bergmann glial fibers proceeds in correlation with dendritic outgrowth and synapse formation of cerebellar Purkinje cells,” Journal of Comparative Neurology, vol. 418, pp. 106–120, 2000.
[44]
D. T. Theodosis, D. A. Poulain, and J. D. Vincent, “Possible morphological bases for synchronisation of neuronal firing in the rat supraoptic nucleus during lactation,” Neuroscience, vol. 6, no. 5, pp. 919–929, 1981.
[45]
C. Montagnese, D. A. Poulain, J. D. Vincent, and D. T. Theodosis, “Synaptic and neuronal-glial plasticity in the adult oxytocinergic system in response to physiological stimuli,” Brain Research Bulletin, vol. 20, no. 6, pp. 681–692, 1988.
[46]
D. T. Theodosis, “Oxytocin-secreting neurons: a physiological model of morphological neuronal and glial plasticity in the adult hypothalamus,” Frontiers in Neuroendocrinology, vol. 23, no. 1, pp. 101–135, 2002.
[47]
D. T. Theodosis, A. Trailin, and D. A. Poulain, “Remodeling of astrocytes, a prerequisite for synapse turnover in the adult brain? Insights from the oxytocin system of the hypothalamus,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 290, no. 5, pp. R1175–R1182, 2006.
[48]
A. K. Salm, “Mechanisms of glial retraction in the hypothalamo-neurohypophysial system of the rat,” Experimental Physiology, vol. 85, 2000.
[49]
D. Becquet, C. Girardet, F. Guillaumond, A. M. Fran？ois-Bellan, and O. Bosler, “Ultrastructural plasticity in the rat suprachiasmatic nucleus. Possible involvement in clock entrainment,” Glia, vol. 56, no. 3, pp. 294–305, 2008.
[50]
A. H. Cornell-Bell, P. G. Thomas, and S. J. Smith, “The excitatory neurotransmitter glutamate causes filopodia formation in cultured hippocampal astrocytes,” Glia, vol. 3, no. 5, pp. 322–334, 1990.
[51]
J. Hirrlinger, S. Hülsmann, and F. Kirchhoff, “Astroglial processes show spontaneous motility at active synaptic terminals in situ,” European Journal of Neuroscience, vol. 20, no. 8, pp. 2235–2239, 2004.
[52]
M. W. Nestor, L. P. Mok, M. E. Tulapurkar, and S. M. Thompson, “Plasticity of neuron-glial interactions mediated by astrocytic EphARs,” Journal of Neuroscience, vol. 27, no. 47, pp. 12817–12828, 2007.
[53]
H. Nishida and S. Okabe, “Direct astrocytic contacts regulate local maturation of dendritic spines,” Journal of Neuroscience, vol. 27, no. 2, pp. 331–340, 2007.
[54]
J. J. Lippman Bell, T. Lordkipanidze, N. Cobb, and A. Dunaevsky, “Bergmann glial ensheathment of dendritic spines regulates synapse number without affecting spine motility,” Neuron Glia Biology, vol. 6, no. 3, pp. 193–200, 2010.
[55]
J. J. Lippman, T. Lordkipanidze, M. E. Buell, S. O. Yoon, and A. Dunaevsky, “Morphogenesis and regulation of Bergmann glial processes during Purkinje cell dendritic spine ensheathment and synaptogenesis,” Glia, vol. 56, no. 13, pp. 1463–1477, 2008.
[56]
T. A. Jones and W. T. Greenough, “Ultrastructural evidence for increased contact between astrocytes and synapses in rats reared in a complex environment,” Neurobiology of Learning and Memory, vol. 65, no. 1, pp. 48–56, 1996.
[57]
J. Wenzel, G. Lammert, U. Meyer, and M. Krug, “The influence of long-term potentiation on the spatial relationship between astrocyte processes and potentiated synapses in the dentate gyrus neuropil of rat brain,” Brain Research, vol. 560, no. 1-2, pp. 122–131, 1991.
[58]
N. Hawrylak, F. L. F. Chang, and W. T. Greenough, “Astrocytic and synaptic response to kindling in hippocampal subfield CA1. II: synaptogenesis and astrocytic process increases to in vivo kindling,” Brain Research, vol. 603, no. 2, pp. 309–316, 1993.
[59]
P. Caroni, F. Donato, and D. Muller, “Structural plasticity upon learning: regulation and functions,” Nature Reviews Neuroscience, vol. 13, pp. 478–490, 2012.
[60]
J. Kang, L. Jiang, S. A. Goldman, and M. Nedergaard, “Astrocyte-mediated potentiation of inhibitory synaptic transmission,” Nature Neuroscience, vol. 1, no. 8, pp. 683–692, 1998.
[61]
J. T. Neary, M. McCarthy, Y. Kang, and S. Zuniga, “Mitogenic signaling from P1 and P2 purinergic receptors to mitogen- activated protein kinase in human fetal astrocyte cultures,” Neuroscience Letters, vol. 242, no. 3, pp. 159–162, 1998.
[62]
M. Navarrete and A. Araque, “Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes,” Neuron, vol. 68, no. 1, pp. 113–126, 2010.
[63]
J. T. Porter and K. D. McCarthy, “Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals,” Journal of Neuroscience, vol. 16, no. 16, pp. 5073–5081, 1996.
[64]
J. Schummers, H. Yu, and M. Sur, “Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex,” Science, vol. 320, no. 5883, pp. 1638–1643, 2008.
[65]
X. Wang, N. Lou, Q. Xu et al., “Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo,” Nature Neuroscience, vol. 9, no. 6, pp. 816–823, 2006.
[66]
M. Iino, K. Goto, W. Kakegawa et al., “Glia-synapse interaction through Ca2+-permeable AMPA receptors in Bergmann glia,” Science, vol. 292, no. 5518, pp. 926–929, 2001.
[67]
G. Seifert, M. Weber, J. Schramm, and C. Steinh？user, “Changes in splice variant expression and subunit assembly of AMPA receptors during maturation of hippocampal astrocytes,” Molecular and Cellular Neuroscience, vol. 22, no. 2, pp. 248–258, 2003.
[68]
W. Sun, E. McConnell, J. F. Pare et al., “Glutamate-dependent neuroglial calcium signaling differs between young and adult brain,” Science, vol. 339, pp. 197–200, 2013.
[69]
S. J. Liu and I. Savtchouk, “Ca2+ permeable AMPA receptors switch allegiances: mechanisms and consequences,” Journal of Physiology, vol. 590, no. 1, pp. 13–20, 2012.
[70]
D. E. Bergles, R. Jabs, and C. Steinh？user, “Neuron-glia synapses in the brain,” Brain Research Reviews, vol. 63, no. 1-2, pp. 130–137, 2010.
[71]
M. L. Cotrina and M. Nedergaard, “Intacellular calcium control mechanism in glia,” in Neuroglia, H. Kettenmann and B. R. Ransom, Eds., vol. 2, pp. 229–239, Oxford University Press, Oxford, UK, 1st edition.
[72]
M. Tanaka, P. Y. Shih, H. Gomi et al., “Astrocytic Ca2+ signals are required for the functional integrity of tripartite synapses,” Molecular Brain, vol. 6, p. article 6, 2013.
[73]
A. A. Mongin and H. K. Kimelberg, “ATP regulates anion channel-mediated organic osmolyte release from cultured rat astrocytes via multiple Ca2+-sensitive mechanisms,” American Journal of Physiology—Cell Physiology, vol. 288, no. 1, pp. C204–C213, 2005.
[74]
M. è. Tremblay, M. Riad, S. Chierzi, K. K. Murai, E. B. Pasquale, and G. Doucet, “Developmental course of EphA4 cellular and subcellular localization in the postnatal rat hippocampus,” Journal of Comparative Neurology, vol. 512, no. 6, pp. 798–813, 2009.
[75]
K. K. Murai and E. B. Pasquale, “Eph receptors, ephrins, and synaptic function,” Neuroscientist, vol. 10, no. 4, pp. 304–314, 2004.
[76]
K. K. Murai, L. N. Nguyen, F. Irie, Y. Yu, and E. B. Pasquale, “Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling,” Nature Neuroscience, vol. 6, no. 2, pp. 153–160, 2003.
[77]
S. Y. Jung, J. Kim, O. B. Kwon et al., “Input-specific synaptic plasticity in the amygdala is regulated by neuroligin-1 via postsynaptic NMDA receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 10, pp. 4710–4715, 2010.
[78]
M. Gilbert, J. Smith, A. J. Roskams, and V. J. Auld, “Neuroligin 3 is a vertebrate gliotactin expressed in the olfactory ensheathing glia, a growth-promoting class of macroglia,” Glia, vol. 34, no. 3, pp. 151–164, 2001.
[79]
B. Chih, H. Engelman, and P. Scheiffele, “Control of excitatory and inhibitory synapse formation by neuroligins,” Science, vol. 307, no. 5713, pp. 1324–1328, 2005.
[80]
F. Cao, A. Yin, G. Wen et al., “Alteration of astrocytes and Wnt/beta-catenin signaling in the frontal cortex of autistic subjects,” Journal of Neuroinflammation, vol. 9, no. 1, article 223, 2012.
[81]
M. L. Bang and S. Owczarek, “A matter of balance: role of neurexin and neuroligin at the synapse,” Neurochemical Research, vol. 38, no. 6, pp. 1174–1189, 2013.
[82]
Y. H. Jiang and M. D. Ehlers, “Modeling autism by SHANK gene mutations in mice,” Neuron, vol. 78, pp. 8–27, 2013.
[83]
M. Grumet, S. Hoffman, C. M. Chuong, and G. M. Edelman, “Polypeptide components are binding functions of neuron-glia cell adhesion molecules,” Proceedings of the National Academy of Sciences of the United States of America, vol. 81, no. 24, pp. 7989–7993, 1984.
[84]
U. S. Sandau, Z. Alderman, G. Corfas, S. R. Ojeda, and J. Raber, “Astrocyte-specific disruption of SynCAM1 signaling results in ADHD-like behavioral manifestations,” PLoS ONE, vol. 7, no. 4, Article ID e36424, 2012.
[85]
D. T. Theodosis, R. Piet, D. A. Poulain, and S. H. R. Oliet, “Neuronal, glial and synaptic remodeling in the adult hypothalamus: functional consequences and role of cell surface and extracellular matrix adhesion molecules,” Neurochemistry International, vol. 45, no. 4, pp. 491–501, 2004.
[86]
G. W. Huntley, A. M. Elste, S. B. Patil, O. Bozdagi, D. L. Benson, and O. Steward, “Synaptic loss and retention of different classic cadherins with LTP-associated synaptic structural remodeling in vivo,” Hippocampus, vol. 22, no. 1, pp. 17–28, 2012.
[87]
P. Mendez, M. de Roo, L. Poglia, P. Klauser, and D. Muller, “N-cadherin mediates plasticity-induced long-term spine stabilization,” Journal of Cell Biology, vol. 189, no. 3, pp. 589–600, 2010.
[88]
S. Hirano and M. Takeichi, “Cadherins in brain morphogenesis and wiring,” Physiological Reviews, vol. 92, no. 2, pp. 597–634, 2012.
[89]
Y. Li, D. R. Serwanski, C. P. Miralles et al., “Synaptic and nonsynaptic localization of protocadherin-γc5 in the rat brain,” Journal of Comparative Neurology, vol. 518, no. 17, pp. 3439–3463, 2010.
[90]
S. H. R. Oliet, A. Panatier, R. Piet, J. P. Mothet, D. A. Poulain, and D. T. Theodosis, “Neuron-glia interactions in the rat supraoptic nucleus,” Progress in Brain Research, vol. 170, pp. 109–117, 2008.
[91]
G. I. Hatton, “Function-related plasticity in hypothalamus,” Annual Review of Neuroscience, vol. 20, pp. 375–397, 1997.
[92]
D. T. Theodosis and D. A. Poulain, “Activity-dependent neuronal-glial and synaptic plasticity in the adult mammalian hypothalamus,” Neuroscience, vol. 57, no. 3, pp. 501–535, 1993.
[93]
R. Piet, D. A. Poulain, and S. H. R. Oliet, “Contribution of astrocytes to synaptic transmission in the rat supraoptic nucleus,” Neurochemistry International, vol. 45, no. 2-3, pp. 251–257, 2004.
[94]
S. H. R. Oliet, R. Piet, and D. A. Poulain, “Control of glutamate clearance and synaptic efficacy by glial coverage of neurons,” Science, vol. 292, no. 5518, pp. 923–926, 2001.
[95]
A. Panatier, D. T. Theodosis, J. P. Mothet et al., “Glia-Derived d-Serine Controls NMDA Receptor Activity and Synaptic Memory,” Cell, vol. 125, no. 4, pp. 775–784, 2006.
[96]
L. M. Prolo, J. S. Takahashi, and E. D. Herzog, “Circadian rhythm generation and entrainment in astrocytes,” Journal of Neuroscience, vol. 25, no. 2, pp. 404–408, 2005.
[97]
D. A. Rusakov, “The role of perisynaptic glial sheaths in glutamate spillover and extracellular Ca2+ depletion,” Biophysical Journal, vol. 81, no. 4, pp. 1947–1959, 2001.
[98]
J. P. Kinney, J. Spacek, T. M. Bartol, C. L. Bajaj, K. M. Harris, and T. J. Sejnowski, “Extracellular sheets and tunnels modulate glutamate diffusion in hippocampal neuropil,” Journal of Comparative Neurology, vol. 521, pp. 448–464, 2013.
[99]
A. Derouiche and M. Frotscher, “Astroglial processes around identified glutamatergic synapses contain glutamine synthetase: evidence for transmitter degradation,” Brain Research, vol. 552, no. 2, pp. 346–350, 1991.
[100]
A. Derouiche and T. Rauen, “Coincidence of L-glutamate/L-aspartate transporter (GLAST) and glutamine synthetase (GS) immunoreactions in retinal glia: evidence for coupling of GLAST and GS in transmitter clearance,” Journal of Neuroscience Research, vol. 42, no. 1, pp. 131–143, 1995.
[101]
E. A. Nagelhus, T. M. Mathiisen, and O. P. Ottersen, “Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1,” Neuroscience, vol. 129, no. 4, pp. 905–913, 2004.
[102]
E. A. Newman, “Inward-rectifying potassium channels in retinal glial (Muller) cells,” Journal of Neuroscience, vol. 13, no. 8, pp. 3333–3345, 1993.
[103]
P. J. Magistretti, L. Pellerin, D. L. Rothman, and R. G. Shulman, “Energy on demand,” Science, vol. 283, no. 5401, pp. 496–497, 1999.
[104]
M. Martineau, T. Shi, J. Puyal et al., “Storage and uptake of D-serine into astrocytic synaptic-like vesicles specify gliotransmission,” Journal of Neuroscience, vol. 33, pp. 3413–3423, 2013.
[105]
P. Bezzi, V. Gundersen, J. L. Galbete et al., “Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate,” Nature Neuroscience, vol. 7, no. 6, pp. 613–620, 2004.
[106]
D. N. Bowser and B. S. Khakh, “Vesicular ATP is the predominant cause of intercellular calcium waves in astrocytes,” Journal of General Physiology, vol. 129, no. 6, pp. 485–491, 2007.
[107]
H. R. Parri, T. M. Gould, and V. Crunelli, “Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation,” Nature Neuroscience, vol. 4, no. 8, pp. 803–812, 2001.
[108]
T. A. Fiacco and K. D. McCarthy, “Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons,” Journal of Neuroscience, vol. 24, no. 3, pp. 722–732, 2004.
[109]
A. Serrano, N. Haddjeri, J. C. Lacaille, and R. Robitaille, “GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression,” Journal of Neuroscience, vol. 26, no. 20, pp. 5370–5382, 2006.
[110]
P. Jourdain, L. H. Bergersen, K. Bhaukaurally et al., “Glutamate exocytosis from astrocytes controls synaptic strength,” Nature Neuroscience, vol. 10, no. 3, pp. 331–339, 2007.
[111]
M. Navarrete, G. Perea, D. F. de Sevilla et al., “Astrocytes mediate in vivo cholinergic-induced synaptic plasticity,” PLoS Biology, vol. 10, no. 2, Article ID e1001259, 2012.
[112]
C. Henneberger, T. Papouin, S. H. R. Oliet, and D. A. Rusakov, “Long-term potentiation depends on release of d-serine from astrocytes,” Nature, vol. 463, no. 7278, pp. 232–236, 2010.
[113]
R. Min and T. Nevian, “Astrocyte signaling controls spike timing-dependent depression at neocortical synapses,” Nature Neuroscience, vol. 15, no. 5, pp. 746–753, 2012.
[114]
G. R. J. Gordon, K. J. Iremonger, S. Kantevari, G. C. R. Ellis-Davies, B. A. MacVicar, and J. S. Bains, “Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses,” Neuron, vol. 64, no. 3, pp. 391–403, 2009.
[115]
A. V. Gourine, V. Kasymov, N. Marina et al., “Astrocytes control breathing through pH-dependent release of ATP,” Science, vol. 329, no. 5991, pp. 571–575, 2010.
[116]
T. A. Fiacco, C. Agulhon, S. R. Taves et al., “Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity,” Neuron, vol. 54, no. 4, pp. 611–626, 2007.
[117]
J. Petravicz, T. A. Fiacco, and K. D. McCarthy, “Loss of IP3 receptor-dependent Ca2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity,” Journal of Neuroscience, vol. 28, no. 19, pp. 4967–4973, 2008.
[118]
P. Devaraju, M. Y. Sun, T. L. Myers, K. Lauderdale, and T. A. Fiacco, “Astrocytic group I mGluR dependent potentiation of astrocytic glutamate and potassium uptake,” Journal of Neurophysiology, vol. 109, no. 9, pp. 2404–2414, 2013.
[119]
O. H. Porras, I. Ruminot, A. Loaiza, and L. F. Barros, “Na+-Ca2+ cosignaling in the stimulation of the glucose transporter GLUT1 in cultured astrocytes,” Glia, vol. 56, no. 1, pp. 59–68, 2008.
[120]
Y. Bernardinelli, P. J. Magistretti, and J. Y. Chatton, “Astrocytes generate Na+-mediated metabolic waves,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 41, pp. 14937–14942, 2004.
[121]
A. Suzuki, S. A. Stern, O. Bozdagi et al., “Astrocyte-neuron lactate transport is required for long-term memory formation,” Cell, vol. 144, no. 5, pp. 810–823, 2011.
[122]
M. Simard and M. Nedergaard, “The neurobiology of glia in the context of water and ion homeostasis,” Neuroscience, vol. 129, no. 4, pp. 877–896, 2004.
[123]
M. de Roo, P. Klauser, and D. Muller, “LTP promotes a selective long-term stabilization and clustering of dendritic spines,” PLoS Biology, vol. 6, no. 9, article e219, 2008.
[124]
D. A. Richards, J. M. Mateos, S. Hugel et al., “Glutamate induces the rapid formation of spine head protrusions in hippocampal slice cultures,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 17, pp. 6166–6171, 2005.
[125]
M. Navarrete and A. Araque, “Basal synaptic transmission: astrocytes rule!,” Cell, vol. 146, no. 5, pp. 675–677, 2011.
[126]
Y. Zuo, A. Lin, P. Chang, and W. B. Gan, “Development of long-term dendritic spine stability in diverse regions of cerebral cortex,” Neuron, vol. 46, no. 2, pp. 181–189, 2005.
[127]
P. J. Harrison, “The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications,” Psychopharmacology, vol. 174, no. 1, pp. 151–162, 2004.
