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Neuron—Glial Communication at Synapses: Insights From Vertebrates and Invertebrates
Keith K. Murai
Centre for Research in Neuroscience, Department of Neurology and Neurosurgery, McGill University the Research Institute of the McGill University Health Centre, Montreal, Quebec, Canada, keith.murai{at}mcgill.ca
Donald J. Van Meyel
Centre for Research in Neuroscience, Department of Neurology and Neurosurgery, McGill University the Research Institute of the McGill University Health Centre, Montreal, Quebec, Canada, don.vanmeyel{at}mcgill.ca
Glial cells are instrumental for many aspects of nervous-system function. Interestingly, complex neuron—glial interactions at synapses are commonly found in both invertebrates and vertebrates. Although these interactions are known to be important for synaptic physiology, the cellular processes and molecular mechanisms involved have not been fully uncovered. Identifying the common and unique features of neuron—glial interactions between invertebrates and vertebrates may provide valuable insights into the relationship of neuron—glial cross-talk to nervous-system function. This review highlights selected studies that have revealed structural and functional insights into neuron—glial interactions at synapses in invertebrate and vertebrate model systems. NEUROSCIENTIST 13(6): 657—666, 2007. DOI: 10.1177/1073858407304393
Key Words: Neuroglia Neuromodulation Nervous system Drosophila Astrocyte Plasticity
References
- Altenhein B., Becker A., Busold C., Beckmann B., Hoheisel JD, Technau GM 2006. Expression profiling of glial genes during Drosophila embryogenesis. Dev Biol 296(2):545-60.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Augustin H., Grosjean Y., Chen K., Sheng Q., Featherstone DE 2007. Nonvesicular release of glutamate by glial xCT transporters suppresses glutamate receptor clustering in vivo. J Neurosci 27(1):111-23.[Abstract/Free Full Text]
- Bailey MS, Shipley MT 1993. Astrocyte subtypes in the rat olfactory bulb: morphological heterogeneity and differential laminar distribution. J Comp Neurol 328(4):501-26.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Beattie EC, Stellwagen D., Morishita W., Bresnahan JC, Ha BK, Von Zastrow M, and others. 2002. Control of synaptic strength by glial TNFalpha. Science 295(5563):2282-5.[Abstract/Free Full Text]
- Bellamy TC 2006. Interactions between Purkinje neurones and Bergmann glia. Cerebellum 5(2):116-26.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Borycz J., Vohra M., Tokarczyk G., Meinertzhagen IA 2000. The determination of histamine in the Drosophila head. J Neurosci Methods 101(2):141-8.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Bringmann A., Pannicke T., Grosche J., Francke M., Wiedemann P., Skatchkov SN, and others. 2006. Muller cells in the healthy and diseased retina. Prog Retinal Eye Res 25(4):397-424.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Bushong EA, Martone ME, Ellisman MH 2004. Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int J Dev Neurosci 22(2):73-86.[Web of Science][Medline]
[Order article via Infotrieve]
- Bushong EA, Martone ME, Jones YZ, Ellisman MH 2002. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22(1):183-92.[Abstract/Free Full Text]
- Cantera R., Trujillo-Cenoz O. 1996. Glial cells in insect ganglia. Microsc Res Tech 35(3):285-93.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A., and others. 2005. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120(3):421-33.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Coles JA 1989. Functions of glial cells in the retina of the honeybee drone. GLIA 2(1):1-9.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ 1990. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247(4941):470-3.[Abstract/Free Full Text]
- Distler C., Dreher Z., Stone J. 1991. Contact spacing among astrocytes in the central nervous system: an hypothesis of their structural role. GLIA 4(5):484-94.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Egger B., Leemans R., Loop T., Kammermeier L., Fan Y., Radimerski T., and others. 2002. Gliogenesis in Drosophila: genome-wide analysis of downstream genes of glial cells missing in the embryonic nervous system. Development 129(14):3295-309.[Web of Science][Medline]
[Order article via Infotrieve]
- Fabian-Fine R., Verstreken P., Hiesinger PR, Horne JA, Kostyleva R., Zhou Y., and others. 2003. Endophilin promotes a late step in endocytosis at glial invaginations in Drosophila photoreceptor terminals. J Neurosci 23(33):10732-44.[Abstract/Free Full Text]
- Featherstone DE, Rushton E., Broadie K. 2002. Developmental regulation of glutamate receptor field size by nonvesicular glutamate release. Nat Neurosci 5(2):141-6.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Featherstone DE, Rushton E., Rohrbough J., Liebl F., Karr J., Sheng Q., and others. 2005. An essential Drosophila glutamate receptor subunit that functions in both central neuropil and neuromuscular junction. J Neurosci 25(12):3199-208.[Abstract/Free Full Text]
- 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):722-32.[Abstract/Free Full Text]
- Fiacco TA, McCarthy KD 2006. Astrocyte calcium elevations: properties, propagation, and effects on brain signaling. GLIA 54(7):676-90.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Freeman MR, Delrow J., Kim J., Johnson E., Doe CQ 2003. Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function. Neuron 38(4):567-80.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Frohlich A., Meinertzhagen IA 1982. Synaptogenesis in the first optic neuropile of the fly's visual system. J Neurocytol 11(1):159-80.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Ganeshina O., Berry RW, Petralia RS, Nicholson DA, Geinisman Y. 2004. Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J Comp Neurol 468(1):86-95.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Goriely AR, Secomb TW, Tolbert LP 2002. Effect of the glial envelope on extracellular K(+) diffusion in olfactory glomeruli. J Neurophysiol 87(4):1712-22.[Abstract/Free Full Text]
- Grosche J., Matyash V., Moller T., Verkhratsky A., Reichenbach A., Kettenmann H. 1999. Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci 2(2):139-43.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Haber M., Murai KK 2006. Reshaping neuron—glial communication at hippocampal synapses. Neuron Glia Biol 2:59-66.[CrossRef][Web of Science]
- Haber M., Zhou L., Murai KK 2006. Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci 26(35):8881-91.[Abstract/Free Full Text]
- Harris KM, Sultan P. 1995. Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses. Neuropharmacology 34(11):1387-95.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Hatton GI 1997. Function-related plasticity in hypothalamus. Annu Rev Neurosci 20:375-97.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Hawrylak N., Chang FL, Greenough WT 1993. Astrocytic and synaptic response to kindling in hippocampal subfield CA1. II. Synaptogenesis and astrocytic process increases to in vivo kindling. Brain Res 603(2):309-16.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Hirase H., Qian L., Bartho P., Buzsaki G. 2004. Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biology 2(4):E96.[CrossRef][Medline]
[Order article via Infotrieve]
- Hirrlinger J., Hulsmann S., Kirchhoff F. 2004. Astroglial processes show spontaneous motility at active synaptic terminals in situ. Eur J Neurosci 20(8):2235-9.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Horridge GA 1965. Arthropoda: general anatomy. In: Bullock TH, Horridge GA, editors. Structure and function in the nervous systems of invertebrates. San Francisco (CA) and London: W. H. Freeman and Company. p 801-964.
- Hoyle G. 1986. Glial cells of an insect ganglion. J Comp Neurol 246(1):85-103.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Huang YH, Bergles DE 2004. Glutamate transporters bring competition to the synapse. Curr Opin Neurobiol 14(3):346-52.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Ishii Y., Nakamura S., Osumi N. 2000. Demarcation of early mammalian cortical development by differential expression of fringe genes. Brain Res Dev Brain Res 119(2):307-20.[CrossRef][Medline]
[Order article via Infotrieve]
- Ito K., Urban J., Technau GM 1995. Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux's Arch Dev Biol 204:284-307.
- Jones BW 2005. Transcriptional control of glial cell development in Drosophila. Dev Biol 278(2):265-73.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Jones TA, Greenough WT 1996. Ultrastructural evidence for increased contact between astrocytes and synapses in rats reared in a complex environment. Neurobiol Learn Mem 65(1):48-56.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Jourdain P., Bergersen LH, Bhaukaurally K., Bezzi P., Santello M., Domercq M., and others. 2007. Glutamate exocytosis from astrocytes controls synaptic strength. Nat Neurosci 10(3):331-9.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Kirov SA, Sorra KE, Harris KM 1999. Slices have more synapses than perfusion-fixed hippocampus from both young and mature rats. J Neurosci 19(8):2876-86.[Abstract/Free Full Text]
- Kretzschmar D., Pflugfelder GO 2002. Glia in development, function, and neurodegeneration of the adult insect brain. Brain Res Bull 57(1):121-31.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Kulik A., Haentzsch A., Luckermann M., Reichelt W., Ballanyi K. 1999. Neuron-glia signaling via alpha(1) adrenoceptor-mediated Ca(2+) release in Bergmann glial cells in situ. J Neurosci 19(19):8401-8.[Abstract/Free Full Text]
- Kullmann DM, Asztely F. 1998. Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends Neurosci 21(1):8-14.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Laming PR, Kimelberg H., Robinson S., Salm A., Hawrylak N., Muller C., and others. 2000. Neuronal-glial interactions and behaviour. Neurosci Biobehav Rev 24(3):295-340.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J., Danbolt NC 1995. Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J Neurosci 15(3 Pt 1):1835-53.[Abstract]
- Lehre KP, Rusakov DA 2002. Asymmetry of glia near central synapses favors presynaptically directed glutamate escape. Biophys J 83(1):125-34.[Web of Science][Medline]
[Order article via Infotrieve]
- Lohr C., Deitmer JW 1999. Dendritic calcium transients in the leech giant glial cell in situ. GLIA 26(2):109-18.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Lohr C., Deitmer JW 2006. Calcium signaling in invertebrate glial cells. GLIA 54(7):642-9.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Lohr C., Heil JE, Deitmer JW 2005. Blockage of voltage-gated calcium signaling impairs migration of glial cells in vivo. GLIA 50(3):198-211.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Mahr A., Aberle H. 2006. The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Express Patt 6(3):299-309.[CrossRef]
- Matthias K., Kirchhoff F., Seifert G., Huttmann K., Matyash M., Kettenmann H., and others. 2003. Segregated expression of AMPAtype glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 23(5):1750-8.[Abstract/Free Full Text]
- Matyash V., Filippov V., Mohrhagen K., Kettenmann H. 2001. Nitric oxide signals parallel fiber activity to Bergmann glial cells in the mouse cerebellar slice. Mol Cell Neurosci 18(6):664-70.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Montana V., Malarkey EB, Verderio C., Matteoli M., Parpura V. 2006. Vesicular transmitter release from astrocytes. GLIA 54(7):700-15.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Murai KK, Nguyen LN, Irie F., Yamaguchi Y., Pasquale EB 2003. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat Neurosci 6(2):153-60.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Nedergaard M., Ransom B., Goldman SA 2003. New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26(10):523-30.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Nishida H., Okabe S. 2007. Direct astrocytic contacts regulate local maturation of dendritic spines. J Neurosci 27(2):331-40.[Abstract/Free Full Text]
- Ogata K., Kosaka T. 2002. Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience 113(1):221-33.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Oliet SH, Mothet JP 2006. Molecular determinants of D-serine-mediated gliotransmission: from release to function. GLIA 54(7):726-37.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Oliet SH, Piet R. 2004. Anatomical remodelling of the supraoptic nucleus: changes in synaptic and extrasynaptic transmission. J Neuroendocrinol 16(4):303-7.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Panatier A., Theodosis DT, Mothet JP, Touquet B., Pollegioni L., Poulain DA, and others. 2006. Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125(4):775-84.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Parri HR, Gould TM, Crunelli V. 2001. Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Nat Neurosci 4(8):803-12.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Pascual O., Casper KB, Kubera C., Zhang J., Revilla-Sanchez R., Sul JY, and others. 2005. Astrocytic purinergic signaling coordinates synaptic networks. Science 310(5745):113-6.[Abstract/Free Full Text]
- Pasik P., Pasik T., trans. 1999. Texture of the nervous system of man and the vertebrates [an annotated and edited translation of the original Spanish text by Ramon y Cajal S, with the additions of the French version]. Moya N, ed. New York: Springer.
- Porter JT, McCarthy KD 1996. Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J Neurosci 16(16):5073-81.[Abstract/Free Full Text]
- Radojcic T., Pentreath VW 1979. Invertebrate glia. Prog Neurobiol 12(2):115-79.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Reichenbach A., Schneider H., Leibnitz L., Reichelt W., Schaaf P., Schumann R. 1989. The structure of rabbit retinal Muller (glial) cells is adapted to the surrounding retinal layers. Anat Embryol 180(1):71-9.[CrossRef][Medline]
[Order article via Infotrieve]
- Richardt A., Rybak J., Stortkuhl KF, Meinertzhagen IA, Hovemann BT 2002. Ebony protein in the Drosophila nervous system: optic neuropile expression in glial cells. J Comp Neurol 452(1):93-102.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Rival T., Soustelle L., Cattaert D., Strambi C., Iche M., Birman S. 2006. Physiological requirement for the glutamate transporter dEAAT1 at the adult Drosophila neuromuscular junction. J Neurobiol 66:1061-74.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Rival T., Soustelle L., Strambi C., Besson MT, Iché M., Birman S. 2004. Decreasing glutamate buffering capacity triggers oxidative stress and neuropil degeneration in the Drosophila brain. Curr Biol 14:599-605.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Robinson SR, Dreher Z. 1990. Muller cells in adult rabbit retinae: morphology, distribution and implications for function and development. Journal of Comparative Neurology 292(2):178-92.
- Rothstein JD, Dykes-Hoberg M., Pardo CA, Bristol LA, Jin L., Kuncl RW, and others. 1996. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16(3):675-86.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Saint Marie RL, Carlson SD 1983. The fine structure of neuroglia in the lamina ganglionaris of the housefly, Musca domestica L. J Neurocytol 12(2):213-41.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Scemes E., Giaume C. 2006. Astrocyte calcium waves: what they are and what they do. GLIA 54(7):716-25.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Serrano A., Haddjeri N., Lacaille J., Robitaille R. 2006. GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J Neurosci 26(20):5370-82.[Abstract/Free Full Text]
- Slezak M., Pfrieger FW 2003. New roles for astrocytes: regulation of CNS synaptogenesis. Trends Neurosci 26(10):531-5.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Somjen GG 1988. Nervenkitt: notes on the history of the concept of neuroglia. GLIA 1(1):2-9.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Soustelle L., Besson MT, Rival T., Birman S. 2002. Terminal glial differentiation involves regulated expression of the excitatory amino acid transporters in the Drosophila embryonic CNS. Dev Biol 248:294-306.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Stacey SM, Thomas GB, Labbé A., van Meyel DJ. 2007. Longitudinal glia in the fly CNS: pushing the envelope on glial diversity and neuron-glial interactions. Neuron Glia Biol in press.
- Stark WS, Carlson SD 1986. Ultrastructure of capitate projections in the optic neuropil of Diptera. Cell Tissue Res 246(3):481-6.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Steinhauser C., Jabs R., Kettenmann H. 1994. Properties of GABA and glutamate responses in identified glial cells of the mouse hippocampal slice. Hippocampus 4(1):19-35.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Stellwagen D., Malenka RC 2006. Synaptic scaling mediated by glial TNF-alpha. Nature 440(7087):1054-9.[CrossRef][Medline]
[Order article via Infotrieve]
- Sykova E. 2004. Extrasynaptic volume transmission and diffusion parameters of the extracellular space. Neuroscience 129(4):861-76.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Tanaka K., Watase K., Manabe T., Yamada K., Watanabe M., Takahashi K., and others. 1997. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276(5319): 1699-702.[Abstract/Free Full Text]
- Thomas GB, van Meyel DJ. 2007. The glycosyltransferase fringe promotes delta-notch signaling between neurons and glia, and is required for subtype-specific glial gene expression. Development 134(3):591-600.[Abstract/Free Full Text]
- Tolbert LP, Oland LA, Tucker ES, Gibson NJ, Higgins MR, Lipscomb BW 2004. Bidirectional influences between neurons and glial cells in the developing olfactory system. Prog Neurobiol 73(2):73-105.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- True JR, Yeh SD, Hovemann BT, Kemme T., Meinertzhagen IA, Edwards TN, and others. 2005. Drosophila tan encodes a novel hydrolase required in pigmentation and vision. PLoS Genetics 1(5):e63.
- Tsacopoulos M., Veuthey AL 1993. The nutritive function of glia in a crystal-like nervous tissue: the retina of the honeybee drone. Dev Neurosci 15(3-5):336-42.[Web of Science][Medline]
[Order article via Infotrieve]
- Valverde F., Santacana M., Heredia M. 1992. Formation of an olfactory glomerulus: morphological aspects of development and organization. Neuroscience 49(2):255-75.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Ventura R., Harris KM 1999. Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19(16):6897-906.[Abstract/Free Full Text]
- Volterra A., Meldolesi J. 2005. Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6(8):626-40.[Medline]
[Order article via Infotrieve]
- Wagner S., Heseding C., Szlachta K., True JR, Prinz H., Hovemann BT 2007. Drosophila photoreceptors express cysteine peptidase tan. J Comp Neurol 500(4):601-11.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Walz W. 2000a. Controversy surrounding the existence of discrete functional classes of astrocytes in adult gray matter. GLIA 31(2):95-103.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Walz W. 2000b. Role of astrocytes in the clearance of excess extracellular potassium. Neurochem Int 36(4-5):291-300.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Wang X., Lou N., Xu Q., Tian GF, Peng WG, Han X., and others. 2006. Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nat Neurosci 9(6):816-23.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Wenzel J., Lammert G., Meyer U., Krug M. 1991. 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 Res 560(1-2):122-31.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Witcher MR, Kirov SA, Harris KM 2007. Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus. GLIA 55(1):13-23.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Xu-Friedman MA, Harris KM, Regehr WG 2001. Three-dimensional comparison of ultrastructural characteristics at depressing and facilitating synapses onto cerebellar Purkinje cells. J Neurosci 21(17):6666-72.[Abstract/Free Full Text]
- Yang Y., Ge W., Chen Y., Zhang Z., Shen W., Wu C., and others. 2003. Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proc Natl Acad Sci U S A 100(25): 15194-9.[Abstract/Free Full Text]
- Yuan LL, Ganetzky B. 1999. A glial-neuronal signaling pathway revealed by mutations in a neurexin-related protein. Science 283(5406):1343-5.[Abstract/Free Full Text]
This version was published on December
1, 2007
The Neuroscientist, Vol. 13, No. 6,
657-666 (2007)
DOI: 10.1177/1073858407304393

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