Glia selectively approach synapses on thin dendritic spines

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1654, 2014, Pages

  Medvedev, Nikolai ^a   Popov, Victor ^a,b   Henneberger, Christian ^c,d   Kraev, Igor ^a   Rusakov, Dmitri A ^c   Stewart, Michael G ^a  

^a OPEN UNIVERSITY   (United Kingdom)

^b INSTITUTE OF CELL BIOPHYSICS   (Russian Federation)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF BONN   (Germany)

Author keywords

Glia protection; Synapses; Thin spines

Indexed keywords

DIFFUSION; ENZYME ACTIVITY; FRAGMENTATION; THREE-DIMENSIONAL MODELING;

ANIMAL; BIOLOGICAL MODEL; DENDRITIC SPINE; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; GLIA; IMAGE PROCESSING; MALE; NEUROPIL; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; RAT; SYNAPSE; WISTAR RAT;

ANIMALS; DENDRITIC SPINES; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MODELS, NEUROLOGICAL; NEUROGLIA; NEUROPIL; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; SYNAPSES;

EID: 84907202362     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0047     Document Type: Article

References (41)

1. Bergles DE, Jahr CE. 1998 Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J. Neurosci. 18, 7709-7716.
2. Lehre KP, Danbolt NC. 1998 The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J. Neurosci. 18, 8751-8757.
3. Danbolt NC. 2001 Glutamate uptake. Progr. Neurobiol. 65, 1-105. (doi:10.1016/S0301-0082(00)00067-8)
4. Diamond JS. 2001 Neuronal glutamate transporters limit activation of NMDA receptors by neurotransmitter spillover on CA1 pyramidal cells. J. Neurosci. 21, 8328-8338.
5. Herman MA, Jahr CE. 2007 Extracellular glutamate concentration in hippocampal slice. J. Neurosci. 27, 9736-9741. (doi:10.1523/JNEUROSCI.3009-07.2007)
6. Lehre KP, Rusakov DA. 2002 Asymmetry of glia near central synapses favors presynaptically directed glutamate escape. Biophys. J. 83, 125-134. (doi:10.1016/S0006-3495(02)75154-0)
7. Arnth-Jensen N, Jabaudon D, Scanziani M. 2002 Cooperation between independent hippocampal synapses is controlled by glutamate uptake. Nat. Neurosci. 5, 325-331. (doi:10.1038/nn825)
8. Lozovaya NA, Grebenyuk SE, Tsintsadze T, Feng B, Monaghan DT, Krishtal OA. 2004 Extrasynaptic NR2B and NR2D subunits of NMDA receptors shape ‘superslow’ afterburst EPSC in rat hippocampus. J. Physiol. 558, 451-463. (doi:10.1113/jphysiol. 2004.063792)
9. Scimemi A, Fine A, Kullmann DM, Rusakov DA. 2004 NR2B-containing receptors mediate cross talk among hippocampal synapses. J. Neurosci. 24, 4767-4777. (doi:10.1523/JNEUROSCI.0364-04.2004)
10. Ventura R, Harris KM. 1999 Three-dimensional relationships between hippocampal synapses and astrocytes. J. Neurosci. 19, 6897-6906.
11. Witcher MR, Kirov SA, Harris KM. 2007 Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus. Glia 55, 13-23. (doi:10. 1002/glia.20415)
12. Oliet SH., Piet R, Poulain DA. 2001 Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292, 923-926. (doi:10.1126/science.1059162)
13. Piet R, Vargova L, Sykova E, Poulain DA, Oliet SH. 2004 Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk. Proc. Natl Acad. Sci. USA 101, 2151-2155. (doi:10. 1073/pnas.0308408100)
14. Harris KM, Jensen FE, Tsao B. 1992 Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J. Neurosci. 12, 2685-2705.
15. Kirov SA, Sorra KE, Harris KM. 1999 Slices have more synapses than perfusion-fixed hippocampus from both young and mature rats. J. Neurosci. 19, 2876-2886.
16. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H. 2001 Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4, 1086-1092. (doi:10.1038/nn736)
17. 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, 86-95. (doi:10. 1002/cne.10950)
18. Medvedev NI, Rodriguez-Arellano JJ, Popov VI, Davies HA, Tigaret CM, Schoepfer R, Stewart MG. 2008 The glutamate receptor 2 subunit controls post-synaptic density complexity and spine shape in the dentate gyrus. Eur. J. Neurosci. 27, 315-325. (doi:10.1111/j.1460-9568.2007.06005.x)
19. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H. 2004 Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761-766. (doi:10.1038/nature02617)
20. Xie Z, Huganir RL, Penzes P. 2005 Activity-dependent dendritic spine structural plasticity is regulated by small GTPase Rap1 and its target AF-6. Neuron 48, 605-618. (doi:10.1016/j.neuron.2005.09.027)
21. Bourne J, Harris KM. 2007 Do thin spines learn tobe mushroom spines that remember? Curr. Opin. Neurobiol. 17, 381-386. (doi:10.1016/j.conb.2007. 04.009)
22. Emptage NJ, Reid CA, Fine A, Bliss TV. 2003 Optical quantal analysis reveals a presynaptic component of LTP at hippocampal Schaffer-associational synapses. Neuron 38, 797-804. (doi:10.1016/S0896-6273(03)00325-8)
23. Scott R, Rusakov DA. 2006 Main determinants of presynaptic Ca2þ dynamics at individual mossy fiber-CA3 pyramidal cell synapses. J. Neurosci. 26, 7071-7081. (doi:10.1523/JNEUROSCI.0946-06.2006)
24. Isokawa M, McKhann II GM. 2005 Electrophysiological and morphological characterization of dentate astrocytes in the hippocampus. J. Neurobiol. 65, 125-134. (doi:10. 1002/neu.20186)
25. Popov VI, Davies HA, Rogachevsky VV, Patrushev IV, Errington ML, Gabbott PL, Bliss TV, Stewart MG. 2004 Remodelling of synaptic morphology but unchanged synaptic density during late phase long-term potentiation (LTP): a serial section electron micrograph study in the dentate gyrus in the anaesthetised rat. Neuroscience 128, 251-262. (doi:10.1016/j.neuroscience.2004.06.029)
26. Fiala JC, Harris KM. 2001 Cylindrical diameters method for calibrating section thickness in serial electron microscopy. J. Microsc. 202, 468-472. (doi:10.1046/j.1365-2818.2001.00926.x)
27. Popov V, Stewart MG. 2009 Complexity of contacts between synaptic boutons and dendritic spines in adult mammalian hippocampus: three-dimensional reconstructions from serial ultrathin sections in vivo. Synapse 63, 369-377. (doi:10.1002/syn.20613)
28. Stewart MG, Popov V, Kraev IV, Medvedev N, Davies HA. 2014 Structure and complexity of the synapse and dendritic spine, ch. 1. In The synapse: structure and function (eds V Pickel, M Segal), pp 1-20. Amsterdam, The Netherlands: Academic Press.
29. Volterra A, Meldolesi J. 2005 Astrocytes, from brain glue to communication elements: the revolution continues. Nat. Rev. Neurosci. 6, 626-640. (doi:10. 1038/nrn1722)
30. Ogata K, Kosaka T. 2002 Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience 113, 221-233. (doi:10.1016/S0306-64522(02)00041-6)
31. Bushong EA, Martone ME, Jones YZ, Ellisman MH. 2002 Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J. Neurosci. 22, 183-192.
32. Bernardinelli Y, Muller D, Nikonenko I. 2014 Astrocyte-synapse structural plasticity. Neural Plast. 2014, 1-13. (doi:10.1155/2014/232105)
33. Geinisman Y, de Toledo-Morrell L, Morrell F, Persina IS, Rossi M. 1992 Structural synaptic plasticity associated with the induction of long-term potentiation is preserved in the dentate gyrus of aged rats. Hippocampus 2, 445-456. (doi:10.1002/hipo.450020412)
34. Rusakov DA, Harrison E, Stewart MG. 1998 Synapses in hippocampus occupy only 1-2% of cell membranes and are spaced less than half-micron apart: a quantitative ultrastructural analysis with discussion of physiological implications. Neuropharmacology 37, 513-521. (doi:10.1016/ S0028-3908(98)00023-9)
35. Rusakov DA, Kullmann DM. 1998 Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J. Neurosci. 18, 3158-3170.
36. Liao DZ, Hessler NA, Malinow R. 1995 Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400-404. (doi:10.1038/375400a0)
37. Isaac JTR, Nicoll RA, Malenka RC. 1995 Evidence for silent synapses: implications for the expression of LTP. Neuron 15, 427-434. (doi:10.1016/0896-6273(95)90046-2)
38. Segal M. 2010 Dendritic spines, synaptic plasticity and neuronal survival: activity shapes dendritic spines to enhance neuronal viability. Eur. J. Neurosci. 31, 2178-2184. (doi:10.1111/j. 1460-9568.2010.07270.x)
39. Bergles DE, Diamond JS, Jahr CE. 1999 Clearance of glutamate inside the synapse and beyond. Curr. Opin. Neurobiol. 9, 293-298. (doi:10.1016/S0959-4388(99)80043-9)
40. Jourdain P., et al. 2007 Glutamate exocytosis from astrocytes controls synaptic strength. Nat. Neurosci. 10, 331-339. (doi:10.1038/nn1849)
41. Perea G, Araque A. 2007 Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317, 1083-1086. (doi:10.1126/science.1144640)