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Astrocyte Sodium Signalling and Panglial Spread of Sodium Signals in Brain White Matter

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Abstract

In brain grey matter, excitatory synaptic transmission activates glutamate uptake into astrocytes, inducing sodium signals which propagate into neighboring astrocytes through gap junctions. These sodium signals have been suggested to serve an important role in neuro-metabolic coupling. So far, it is unknown if astrocytes in white matter—that is in brain regions devoid of synapses—are also able to undergo such intra- and intercellular sodium signalling. In the present study, we have addressed this question by performing quantitative sodium imaging in acute tissue slices of mouse corpus callosum. Focal application of glutamate induced sodium transients in SR101-positive astrocytes. These were largely unaltered in the presence of ionotropic glutamate receptors blockers, but strongly dampened upon pharmacological inhibition of glutamate uptake. Sodium signals induced in individual astrocytes readily spread into neighboring SR101-positive cells with peak amplitudes decaying monoexponentially with distance from the stimulated cell. In addition, spread of sodium was largely unaltered during pharmacological inhibition of purinergic and glutamate receptors, indicating gap junction-mediated, passive diffusion of sodium between astrocytes. Using cell-type-specific, transgenic reporter mice, we found that sodium signals also propagated, albeit less effectively, from astrocytes to neighboring oligodendrocytes and NG2 cells. Again, panglial spread was unaltered with purinergic and glutamate receptors blocked. Taken together, our results demonstrate that activation of sodium-dependent glutamate transporters induces sodium signals in white matter astrocytes, which spread within the astrocyte syncytium. In addition, we found a panglial passage of sodium signals from astrocytes to NG2 cells and oligodendrocytes, indicating functional coupling between these macroglial cells in white matter.

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Abbreviations

AMPA:

α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid

AP5:

D-(-)-2-Amino-5-phosphonopentanoic acid

ATP:

Adenosine triphosphate

CA1:

Cornu ammonis 1

Cx:

Connexin

DAPI:

4′,6-diamidino-2-phenylindole

EYFP:

Enhanced yellow fluorescent protein

GABA:

Gamma-aminobutyric acid

GFP:

Green fluorescent protein

GLAST:

Glutamate aspartate transporter

GLT1:

Glutamate transporter 1

hGFAP:

Human glial fibrillary acidic protein

Iba1:

Ionized calcium-binding adapter molecule 1

mGluR:

Metabotropic glutamate receptor

MPEP:

2-Methyl-6-(phenylethynyl)pyridine hydro-chloride

MRS2179:

2′-deoxy-N6-methyladenosine 3′,5′-bisphosphate tetrasodium salt

NBQX:

2,3-Dihydroxy-6-nitro-7-sulfamoyl-benzo(F) quinoxaline

NCX:

Sodium/calcium exchanger

NG2:

Neural/glial antigen 2

NMDA:

(R)-2-(Methylamino)succinic acid

PBS:

Phosphate buffered saline

PLP:

Proteolipid protein

PPADS:

Pyridoxalphosphate-6-azophenyl-2′,4′-disulfonic acid tetrasodium salt

ROI:

Region of interest

SBFI(-AM):

Sodium-binding benzofuran isophthalate(-acetoxymethyl ester)

SEM:

Standard error of the mean

SR101:

Sulforhodamine 101

TFB-TBOA:

(3 S)-3-[[3-[[4-(Trifluoromethyl)benzoyl]amino]phenyl]methoxy]-L-aspartic acid

TTX:

Tetrodotoxin

References

  1. Kirischuk S, Heja L, Kardos J, Billups B (2016) Astrocyte sodium signaling and the regulation of neurotransmission. Glia 64:1655–1666

    Article  PubMed  Google Scholar 

  2. Rose CR, Verkhratsky A (2016) Principles of sodium homeostasis and sodium signalling in astroglia. Glia 64:1611–1627

    Article  PubMed  Google Scholar 

  3. Chatton JY, Magistretti PJ, Barros LF (2016) Sodium signaling and astrocyte energy metabolism. Glia 64:1667–1676

    Article  PubMed  Google Scholar 

  4. Parpura V, Sekler I, Fern R (2016) Plasmalemmal and mitochondrial Na-Ca exchange in neuroglia. Glia 64:1646–1654

    Article  PubMed  Google Scholar 

  5. Kirischuk S, Parpura V, Verkhratsky A (2012) Sodium dynamics: another key to astroglial excitability? Trends Neurosci 35:497–506

    Article  CAS  PubMed  Google Scholar 

  6. Uwechue NM, Marx MC, Chevy Q, Billups B (2012) Activation of glutamate transport evokes rapid glutamine release from perisynaptic astrocytes. J Physiol 590:2317–2331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bak LK, Schousboe A, Waagepetersen HS (2006) The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J Neurochem 98:641–653

    Article  CAS  PubMed  Google Scholar 

  8. Unichenko P, Dvorzhak A, Kirischuk S (2013) Transporter-mediated replacement of extracellular glutamate for GABA in the developing murine neocortex. Eur J Neurosci 38:3580–3588

    Article  PubMed  Google Scholar 

  9. Rose CR, Ransom BR (1996) Mechanisms of H+ and Na+ changes induced by glutamate, kainate, and D-Aspartate in rat hippocampal astrocytes. J Neurosci 16:5393–5404

    CAS  PubMed  Google Scholar 

  10. Langer J, Rose CR (2009) Synaptically induced sodium signals in hippocampal astrocytes in situ. J Physiol 587:5859–5877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Karus C, Mondragao MA, Ziemens D, Rose CR (2015) Astrocytes restrict discharge duration and neuronal sodium loads during recurrent network activity. Glia 63:936–957

    Article  PubMed  Google Scholar 

  12. Kirischuk S, Kettenmann H, Verkhratsky A (2007) Membrane currents and cytoplasmic sodium transients generated by glutamate transport in Bergmann glial cells. Pflugers Arch 454:245–252

    Article  CAS  PubMed  Google Scholar 

  13. Bennay M, Langer J, Meier SD, Kafitz KW, Rose CR (2008) Sodium signals in cerebellar Purkinje neurons and Bergmann glial cells evoked by glutamatergic synaptic transmission. Glia 56:1138–1149

    Article  PubMed  Google Scholar 

  14. Chatton JY, Marquet P, Magistretti PJ (2000) A quantitative analysis of L-glutamate-regulated Na+ dynamics in mouse cortical astrocytes: implications for cellular bioenergetics. Eur J Neurosci 12:3843–3853

    Article  CAS  PubMed  Google Scholar 

  15. Unichenko P, Myakhar O, Kirischuk S (2012) Intracellular Na(+) concentration influences short-term plasticity of glutamate transporter-mediated currents in neocortical astrocytes. Glia 60:605–614

    Article  PubMed  Google Scholar 

  16. Chatton JY, Pellerin L, Magistretti PJ (2003) GABA uptake into astrocytes is not associated with significant metabolic cost: implications for brain imaging of inhibitory transmission. Proc Natl Acad Sci USA 100:12456–12461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Reyes RC, Verkhratsky A, Parpura V (2013) TRPC1-mediated Ca2+ and Na+ signalling in astroglia: differential filtering of extracellular cations. Cell Calcium 54:120–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Langer J, Gerkau NJ, Derouiche A, Kleinhans C, Moshrefi-Ravasdjani B, Fredrich M, Kafitz KW, Seifert G, Steinhäuser C, Rose CR (2017) Rapid sodium signaling couples glutamate uptake to breakdown of ATP in perivascular astrocyte endfeet. Glia 65:293–308

    Article  PubMed  Google Scholar 

  19. Rose CR, Ransom BR (1997) Gap junctions equalize intracellular Na+ concentration in astrocytes. Glia 20:299–307

    Article  CAS  PubMed  Google Scholar 

  20. Bernardinelli Y, Magistretti PJ, Chatton JY (2004) Astrocytes generate Na+-mediated metabolic waves. Proc Natl Acad Sci USA 101:14937–14942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Langer J, Stephan J, Theis M, Rose CR (2012) Gap junctions mediate intercellular spread of sodium between hippocampal astrocytes in situ. Glia 60:239–252

    Article  PubMed  Google Scholar 

  22. Augustin V, Bold C, Wadle SL, Langer J, Jabs R, Philippot C, Weingarten DJ, Rose CR, Steinhäuser C, Stephan J (2016) Functional anisotropic panglial networks in the lateral superior olive. Glia 64:1892–1911

    Article  PubMed  Google Scholar 

  23. Kukley M, Capetillo-Zarate E, Dietrich D (2007) Vesicular glutamate release from axons in white matter. Nat Neurosci 10:311–320

    Article  CAS  PubMed  Google Scholar 

  24. Ziskin JL, Nishiyama A, Rubio M, Fukaya M, Bergles DE (2007) Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10:321–330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Domercq M, Matute C (1999) Expression of glutamate transporters in the adult bovine corpus callosum. Brain Res Mol Brain Res 67:296–302

    Article  CAS  PubMed  Google Scholar 

  26. Goursaud S, Kozlova EN, Maloteaux JM, Hermans E (2009) Cultured astrocytes derived from corpus callosum or cortical grey matter show distinct glutamate handling properties. J Neurochem 108:1442–1452

    Article  CAS  PubMed  Google Scholar 

  27. Lundgaard I, Osorio MJ, Kress BT, Sanggaard S, Nedergaard M (2014) White matter astrocytes in health and disease. Neuroscience 276:161–173

    Article  CAS  PubMed  Google Scholar 

  28. Tress O, Maglione M, May D, Pivneva T, Richter N, Seyfarth J, Binder S, Zlomuzica A, Seifert G, Theis M, Dere E, Kettenmann H, Willecke K (2012) Panglial gap junctional communication is essential for maintenance of myelin in the CNS. J Neurosci 32:7499–7518

    Article  CAS  PubMed  Google Scholar 

  29. Maglione M, Tress O, Haas B, Karram K, Trotter J, Willecke K, Kettenmann H (2010) Oligodendrocytes in mouse corpus callosum are coupled via gap junction channels formed by connexin47 and connexin32. Glia 58:1104–1117

    Article  PubMed  Google Scholar 

  30. Griemsmann S, Hoft SP, Bedner P, Zhang J, von Staden E, Beinhauer A, Degen J, Dublin P, Cope DW, Richter N, Crunelli V, Jabs R, Willecke K, Theis M, Seifert G, Kettenmann H, Steinhäuser C (2015) Characterization of panglial gap junction networks in the thalamus, neocortex, and hippocampus reveals a unique population of glial cells. Cereb Cortex 25:3420–3433

    Article  PubMed  Google Scholar 

  31. Giaume C, Theis M (2010) Pharmacological and genetic approaches to study connexin-mediated channels in glial cells of the central nervous system. Brain Res Rev 63:160–176

    Article  CAS  PubMed  Google Scholar 

  32. Kafitz KW, Meier SD, Stephan J, Rose CR (2008) Developmental profile and properties of sulforhodamine 101-labeled glial cells in acute brain slices of rat hippocampus. J Neurosci Methods 169:84–92

    Article  CAS  PubMed  Google Scholar 

  33. Meier SD, Kovalchuk Y, Rose CR (2006) Properties of the new fluorescent Na+ indicator CoroNa Green: comparison with SBFI and confocal Na+ imaging. J Neurosci Methods 155:251–259

    Article  CAS  PubMed  Google Scholar 

  34. Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, Messing A (1997) Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol 187:36–42

    Article  CAS  PubMed  Google Scholar 

  35. Fuss B, Mallon B, Phan T, Ohlemeyer C, Kirchhoff F, Nishiyama A, Macklin WB (2000) Purification and analysis of in vivo-differentiated oligodendrocytes expressing the green fluorescent protein. Dev Biol 218:259–274

    Article  CAS  PubMed  Google Scholar 

  36. Karram K, Goebbels S, Schwab M, Jennissen K, Seifert G, Steinhäuser C, Nave KA, Trotter J (2008) NG2-expressing cells in the nervous system revealed by the NG2-EYFP-knockin mouse. Genesis 46:743–757

    Article  CAS  PubMed  Google Scholar 

  37. Moshrefi-Ravasdjani B, Dublin P, Seifert G, Jennissen K, Steinhäuser C, Kafitz KW, Rose CR (2016) Changes in the proliferative capacity of NG2 cell subpopulations during postnatal development of the mouse hippocampus. Brain Struct Funct. doi:10.1007/s00429-016-1249-2

    PubMed  Google Scholar 

  38. Sturrock RR (1976) Light microscopic identification of immature glial cells in semithin sections of the developing mouse corpus callosum. J Anat 122:521–537

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Bernstein M, Lyons SA, Moller T, Kettenmann H (1996) Receptor-mediated calcium signalling in glial cells from mouse corpus callosum slices. J Neurosci Res 46:152–163

    Article  CAS  PubMed  Google Scholar 

  40. Schipke CG, Boucsein C, Ohlemeyer C, Kirchhoff F, Kettenmann H (2002) Astrocyte Ca2+ waves trigger responses in microglial cells in brain slices. FASEB J 16:255–257

    CAS  PubMed  Google Scholar 

  41. Nimmerjahn A, Helmchen F (2012) In vivo labeling of cortical astrocytes with sulforhodamine 101 (SR101). Cold Spring Harbor Protoc 2012:326–334

    Google Scholar 

  42. Schnell C, Hagos Y, Hulsmann S (2012) Active sulforhodamine 101 uptake into hippocampal astrocytes. PLoS One 7:e49398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Scemes E, Giaume C (2006) Astrocyte calcium waves: what they are and what they do. Glia 54:716–725

    Article  PubMed  PubMed Central  Google Scholar 

  44. Haydon P (2001) Glia: listening talking to the synapse. Nat Neurosci Rev 2:185–193

    Article  CAS  Google Scholar 

  45. Butt AM, Fern RF, Matute C (2014) Neurotransmitter signaling in white matter. Glia 62:1762–1779

    Article  PubMed  Google Scholar 

  46. Fern RF, Matute C, Stys PK (2014) White matter injury: Ischemic and nonischemic. Glia 62:1780–1789

    Article  PubMed  Google Scholar 

  47. Serwanski DR, Jukkola P, Nishiyama A (2016) Heterogeneity of astrocyte and NG2 cell insertion at the node of ranvier. J Comp Neurol. doi:10.1002/cne.24083

    PubMed  Google Scholar 

  48. Butt AM, Duncan A, Hornby MF, Kirvell SL, Hunter A, Levine JM, Berry M (1999) Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia 26:84–91

    Article  CAS  PubMed  Google Scholar 

  49. Kriegler S, Chiu SY (1993) Calcium signaling of glial cells along mammalian axons. J Neurosci 13:4229–4245

    CAS  PubMed  Google Scholar 

  50. Hamilton N, Vayro S, Kirchhoff F, Verkhratsky A, Robbins J, Gorecki DC, Butt AM (2008) Mechanisms of ATP- and glutamate-mediated calcium signaling in white matter astrocytes. Glia 56:734–749

    Article  PubMed  Google Scholar 

  51. Berger T, Walz W, Schnitzer J, Kettenmann H (1992) GABA- and glutamate-activated currents in glial cells of the mouse corpus callosum slice. J Neurosci Res 31:21–27

    Article  CAS  PubMed  Google Scholar 

  52. Belachew S, Gallo V (2004) Synaptic and extrasynaptic neurotransmitter receptors in glial precursors’ quest for identity. Glia 48:185–196

    Article  PubMed  Google Scholar 

  53. Salter MG, Fern R (2005) NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438:1167–1171

    Article  CAS  PubMed  Google Scholar 

  54. Karadottir R, Cavelier P, Bergersen LH, Attwell D (2005) NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438:1162–1166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Hamilton N, Vayro S, Wigley R, Butt AM (2010) Axons and astrocytes release ATP and glutamate to evoke calcium signals in NG2-glia. Glia 58:66–79

    Article  PubMed  Google Scholar 

  56. Arranz AM, Hussein A, Alix JJ, Perez-Cerda F, Allcock N, Matute C, Fern R (2008) Functional glutamate transport in rodent optic nerve axons and glia. Glia 56:1353–1367

    Article  PubMed  Google Scholar 

  57. Martinez-Lozada Z, Waggener CT, Kim K, Zou S, Knapp PE, Hayashi Y, Ortega A, Fuss B (2014) Activation of sodium-dependent glutamate transporters regulates the morphological aspects of oligodendrocyte maturation via signaling through calcium/calmodulin-dependent kinase IIbeta’s actin-binding/-stabilizing domain. Glia 62:1543–1558

    Article  PubMed  PubMed Central  Google Scholar 

  58. Domercq M, Etxebarria E, Perez-Samartin A, Matute C (2005) Excitotoxic oligodendrocyte death and axonal damage induced by glutamate transporter inhibition. Glia 52:36–46

    Article  PubMed  Google Scholar 

  59. Regan MR, Huang YH, Kim YS, Dykes-Hoberg MI, Jin L, Watkins AM, Bergles DE, Rothstein JD (2007) Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J Neurosci 27:6607–6619

    Article  CAS  PubMed  Google Scholar 

  60. DeSilva TM, Kabakov AY, Goldhoff PE, Volpe JJ, Rosenberg PA (2009) Regulation of glutamate transport in developing rat oligodendrocytes. J Neurosci 29:7898–7908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Kukley M, Nishiyama A, Dietrich D (2010) The fate of synaptic input to NG2 glial cells: neurons specifically downregulate transmitter release onto differentiating oligodendroglial cells. J Neurosci 30:8320–8331

    Article  CAS  PubMed  Google Scholar 

  62. Ballanyi K, Kettenmann H (1990) Intracellular Na+ activity in cultured mouse oligodendrocytes. J Neurosci Res 26:455–460

    Article  CAS  PubMed  Google Scholar 

  63. Chen H, Kintner DB, Jones M, Matsuda T, Baba A, Kiedrowski L, Sun D (2007) AMPA-mediated excitotoxicity in oligodendrocytes: role for Na(+)-K(+)-Cl(-) co-transport and reversal of Na(+)/Ca(2+) exchanger. J Neurochem 102:1783–1795

    Article  CAS  PubMed  Google Scholar 

  64. Haberlandt C, Derouiche A, Wyczynski A, Haseleu J, Pohle J, Karram K, Trotter J, Seifert G, Frotscher M, Steinhäuser C, Jabs R (2011) Gray matter NG2 cells display multiple Ca2+-signaling pathways and highly motile processes. PLoS ONE 6:e17575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Hamilton N, Hubbard PS, Butt AM (2009) Effects of glutamate receptor activation on NG2-glia in the rat optic nerve. J Anat 214:208–218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Honsek SD, Walz C, Kafitz KW, Rose CR (2012) Astrocyte calcium signals at Schaffer collateral to CA1 pyramidal cell synapses correlate with the number of activated synapses but not with synaptic strength. Hippocampus 22:29–42

    Article  CAS  PubMed  Google Scholar 

  67. Paukert M, Bergles DE (2006) Synaptic communication between neurons and NG2 + cells. Curr Opin Neurobiol 16:515–521

    Article  CAS  PubMed  Google Scholar 

  68. Dimou L, Gallo V (2015) NG2-glia and their functions in the central nervous system. Glia 63:1429–1451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Haas B, Schipke CG, Peters O, Sohl G, Willecke K, Kettenmann H (2006) Activity-dependent ATP-waves in the mouse neocortex are independent from astrocytic calcium waves. Cereb Cortex 16:237–246

    Article  PubMed  Google Scholar 

  70. Ransom BR, Kettenmann H (1990) Electrical coupling, without dye coupling, between mammalian astrocytes and oligodendrocytes in cell culture. Glia 3:258–266

    Article  CAS  PubMed  Google Scholar 

  71. Wasseff SK, Scherer SS (2011) Cx32 and Cx47 mediate oligodendrocyte:astrocyte and oligodendrocyte:oligodendrocyte gap junction coupling. Neurobiol Dis 42:506–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Wigley R, Hamilton N, Nishiyama A, Kirchhoff F, Butt AM (2007) Morphological and physiological interactions of NG2-glia with astrocytes and neurons. J Anat 210:661–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Kettenmann H, Ransom BR (1988) Electrical coupling between astrocytes and between oligodendrocytes studied in mammalian cell cultures. Glia 1:64–73

    Article  CAS  PubMed  Google Scholar 

  74. Kirischuk S, Kettenmann H, Verkhratsky A (1997) Na+/Ca2+ exchanger modulates kainate-triggered Ca2+ signaling in Bergmann glial cells in situ. Faseb J 11:566–572

    CAS  PubMed  Google Scholar 

  75. Rojas H, Colina C, Ramos M, Benaim G, Jaffe EH, Caputo C, DiPolo R (2007) Na+ entry via glutamate transporter activates the reverse Na+/Ca2+ exchange and triggers Ca(i)2+-induced Ca2+ release in rat cerebellar Type-1 astrocytes. J Neurochem 100:1188–1202

    Article  CAS  PubMed  Google Scholar 

  76. Reyes RC, Verkhratsky A, Parpura V (2012) Plasmalemmal Na+/Ca2+ exchanger modulates Ca2+-dependent exocytotic release of glutamate from rat cortical astrocytes. ASN Neuro. doi:10.1042/AN20110059

    PubMed  PubMed Central  Google Scholar 

  77. Friess M, Hammann J, Unichenko P, Luhmann HJ, White R, Kirischuk S (2016) Intracellular ion signaling influences myelin basic protein synthesis in oligodendrocyte precursor cells. Cell Calcium 60:322–330

    Article  CAS  PubMed  Google Scholar 

  78. Tong XP, Li XY, Zhou B, Shen W, Zhang ZJ, Xu TL, Duan S (2009) Ca(2+) signaling evoked by activation of Na(+) channels and Na(+)/Ca(2+) exchangers is required for GABA-induced NG2 cell migration. J Cell Biol 186:113–128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Matute C, Domercq M, Perez-Samartin A, Ransom BR (2013) Protecting white matter from stroke injury. Stroke 44:1204–1211

    Article  PubMed  Google Scholar 

  80. Borges K, Kettenmann H (1995) Blockade of K+ channels induced by AMPA/kainate receptor activation in mouse oligodendrocyte precursor cells is mediated by Na+ entry. J Neurosci Res 42:579–593

    Article  CAS  PubMed  Google Scholar 

  81. Knutson P, Ghiani CA, Zhou JM, Gallo V, McBain CJ (1997) K+ channel expression and cell proliferation are regulated by intracellular sodium and membrane depolarization in oligodendrocyte progenitor cells. J Neurosci 17:2669–2682

    CAS  PubMed  Google Scholar 

  82. Schröder W, Seifert G, Huttmann K, Hinterkeuser S, Steinhauser C (2002) AMPA receptor-mediated modulation of inward rectifier K+ channels in astrocytes of mouse hippocampus. Mol Cell Neurosci 19:447–458

    Article  PubMed  Google Scholar 

  83. Magistretti PJ (2006) Neuron-glia metabolic coupling and plasticity. J Exp Biol 209:2304–2311

    Article  CAS  PubMed  Google Scholar 

  84. Brown AM, Ransom BR (2007) Astrocyte glycogen and brain energy metabolism. Glia 55:1263–1271

    Article  PubMed  Google Scholar 

  85. Brown AM, Sickmann HM, Fosgerau K, Lund TM, Schousboe A, Waagepetersen HS, Ransom BR (2005) Astrocyte glycogen metabolism is required for neural activity during aglycemia or intense stimulation in mouse white matter. J Neurosci Res 79:74–80

    Article  CAS  PubMed  Google Scholar 

  86. Funfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS, Edgar J, Brinkmann BG, Kassmann CM, Tzvetanova ID, Mobius W, Diaz F, Meijer D, Suter U, Hamprecht B, Sereda MW, Moraes CT, Frahm J, Goebbels S, Nave KA (2012) Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485:517–521

    PubMed  PubMed Central  Google Scholar 

  87. Hirrlinger J, Nave KA (2014) Adapting brain metabolism to myelination and long-range signal transduction. Glia 62:1749–1761

    Article  PubMed  Google Scholar 

  88. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, Liu Y, Tsingalia A, Jin L, Zhang PW, Pellerin L, Magistretti PJ, Rothstein JD (2012) Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487:443–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C (2008) Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322:1551–1555

    Article  CAS  PubMed  Google Scholar 

  90. Pannasch U, Rouach N (2013) Emerging role for astroglial networks in information processing: from synapse to behavior. Trends Neurosci 36:405–417

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Deutsche Forschungsgemeinschaft (SPP1757 “Glial Heterogeneity”, Ro2327/8 − 1). We thank Simone Durry for excellent technical assistance. The authors thank Dr. Gerald Seifert and Prof. Christian Steinhäuser, University of Bonn, Germany, as well as Prof. Nikolaj Klöcker, Heinrich Heine University Duesseldorf, Germany, for providing transgenic reporter animals (hGFAP-GFP, PLP-GFP, NG2-EYFP).

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  1. Institute of Neurobiology, Faculty of Mathematics and Natural Sciences, Heinrich Heine University Düsseldorf, Universitätsstrasse 1, 40225, Düsseldorf, Germany

    Behrouz Moshrefi-Ravasdjani, Evelyn L. Hammel, Karl W. Kafitz & Christine R. Rose

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  1. Behrouz Moshrefi-Ravasdjani
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  2. Evelyn L. Hammel
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Correspondence to Christine R. Rose.

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This study was carried out in strict accordance with the institutional guidelines of the Heinrich Heine University Düsseldorf, as well as the European Community Council Directive (86/609/EEC). All experiments were communicated to and approved by the Animal Welfare Office at the Animal Care and Use Facility of the Heinrich Heine University Düsseldorf (institutional act number: O52/05), following the recommendation of the European Commission (published in: Euthanasia of experimental animals, Luxembourg: Office for Official Publications of the European Communities, 1997; ISBN 92–827–9694-9).

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Moshrefi-Ravasdjani, B., Hammel, E.L., Kafitz, K.W. et al. Astrocyte Sodium Signalling and Panglial Spread of Sodium Signals in Brain White Matter. Neurochem Res 42, 2505–2518 (2017). https://doi.org/10.1007/s11064-017-2197-9

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