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Monitoring Interneuron–Astrocyte Signaling and Its Consequences on Synaptic Transmission

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Astrocytes

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1938))

Abstract

Whole-cell patch clamp allows the characterization of synaptic transmission in neurons. It is possible to manipulate astrocytic activity and record how these glial cells affect neuronal networks. Here we describe the methodology to monitor the endogenously activation of astrocytes by inhibitory synaptic activity. Afterward, such glial activation will let us study the consequences of interneuron–astrocyte signaling on excitatory neurotransmission at hippocampal synapses.

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References

  1. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117(4):500–544

    Article  CAS  Google Scholar 

  2. Sakmann a B, Neher E (1984) Patch clamp techniques for studying ionic channels in excitable membranes. Annu Rev Physiol 46(1):455–472

    Article  Google Scholar 

  3. Neher E, Sakmann B (1976) Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature 260:799

    Article  CAS  Google Scholar 

  4. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391(2):85–100

    Article  CAS  Google Scholar 

  5. Henneberger C, Rusakov DA (2012) Monitoring local synaptic activity with astrocytic patch pipettes. Nat Protoc 7(12):2171–2179

    Article  CAS  Google Scholar 

  6. Ma B, Xu G, Wang W, Enyeart JJ, Zhou M (2014) Dual patch voltage clamp study of low membrane resistance astrocytes in situ. Mol Brain 7:18

    Article  Google Scholar 

  7. Perea G, Araque A (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317(5841):1083–1086

    Article  CAS  Google Scholar 

  8. Perea G, Araque A (2005) Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci 25(9):2192–2203

    Article  CAS  Google Scholar 

  9. Sontheimer H (1994) Voltage-dependent ion channels in glial cells. Glia 11(2):156–172

    Article  CAS  Google Scholar 

  10. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A, Feldmeyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, Kisvarday ZF, Lambolez B, Lewis DA, Marin O, Markram H, Munoz A, Packer A, Petersen CC, Rockland KS, Rossier J, Rudy B, Somogyi P, Staiger JF, Tamas G, Thomson AM, Toledo-Rodriguez M, Wang Y, West DC, Yuste R (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9(7):557–568

    Article  CAS  Google Scholar 

  11. Perea G, Gomez R, Mederos S, Covelo A, Ballesteros JJ, Schlosser L, Hernandez-Vivanco A, Martin-Fernandez M, Quintana R, Rayan A, Diez A, Fuenzalida M, Agarwal A, Bergles DE, Bettler B, Manahan-Vaughan D, Martin ED, Kirchhoff F, Araque A (2016) Activity-dependent switch of GABAergic inhibition into glutamatergic excitation in astrocyte-neuron networks. Elife 5:e20362

    Article  Google Scholar 

  12. Douglas RM (1998) In: Shepherd GM (ed) KAC the synaptic organization of the brain. Oxford Univ Press, Oxford, pp 459–511

    Google Scholar 

  13. Gupta A, Wang Y, Markram H (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287(5451):273–278

    Article  CAS  Google Scholar 

  14. Navarrete M, Araque A (2010) Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron 68(1):113–126

    Article  CAS  Google Scholar 

  15. Navarrete M, Perea G, Fernandez de Sevilla D, Gomez-Gonzalo M, Nunez A, Martin ED, Araque A (2012) Astrocytes mediate in vivo cholinergic-induced synaptic plasticity. PLoS Biol 10(2):e1001259

    Article  CAS  Google Scholar 

  16. Paredes RM, Etzler JC, Watts LT, Zheng W, Lechleiter JD (2008) Chemical calcium indicators. Methods 46(3):143–151

    Article  CAS  Google Scholar 

  17. Thomas D, Tovey SC, Collins TJ, Bootman MD, Berridge MJ, Lipp P (2000) A comparison of fluorescent Ca2+ indicator properties and their use in measuring elementary and global Ca2+ signals. Cell Calcium 28(4):213–223

    Article  CAS  Google Scholar 

  18. Hennig GW, Gould TW, Koh SD, Corrigan RD, Heredia DJ, Shonnard MC, Smith TK (2015) Use of genetically encoded calcium indicators (GECIs) combined with advanced motion tracking techniques to examine the behavior of neurons and glia in the enteric nervous system of the intact murine colon. Front Cell Neurosci 9:436

    Article  Google Scholar 

  19. Pérez Koldenkova V, Nagai T (2013) Genetically encoded Ca2+ indicators: properties and evaluation. Biochim Biophys Acta 1833(7):1787–1797

    Article  Google Scholar 

  20. Mariotti L, Losi G, Lia A, Melone M, Chiavegato A, Gomez-Gonzalo M, Sessolo M, Bovetti S, Forli A, Zonta M, Requie LM, Marcon I, Pugliese A, Viollet C, Bettler B, Fellin T, Conti F, Carmignoto G (2018) Interneuron-specific signaling evokes distinctive somatostatin-mediated responses in adult cortical astrocytes. Nat Commun 9(1):82

    Article  Google Scholar 

  21. Araque A, Martin ED, Perea G, Arellano JI, Buno W (2002) Synaptically released acetylcholine evokes Ca2+ elevations in astrocytes in hippocampal slices. J Neurosci 22(7):2443–2450

    Article  CAS  Google Scholar 

  22. Nimmerjahn A, Kirchhoff F, Kerr JN, Helmchen F (2004) Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 1(1):31–37

    Article  CAS  Google Scholar 

  23. Shigetomi E, Kracun S, Sofroniew MV, Khakh BS (2010) A genetically targeted optical sensor to monitor calcium signals in astrocyte processes. Nat Neurosci 13(6):759–766

    Article  CAS  Google Scholar 

  24. Serrano A, Haddjeri N, Lacaille JC, Robitaille R (2006) GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J Neurosci 26(20):5370–5382

    Article  CAS  Google Scholar 

  25. Poskanzer KE, Yuste R (2011) Astrocytic regulation of cortical UP states. Proc Natl Acad Sci U S A 108(45):18453–18458

    Article  CAS  Google Scholar 

  26. Gould T, Chen L, Emri Z, Pirttimaki T, Errington AC, Crunelli V, Parri HR (2014) GABA(B) receptor-mediated activation of astrocytes by gamma-hydroxybutyric acid. Philos Trans R Soc Lond B Biol Sci 369(1654):20130607

    Article  Google Scholar 

  27. Mori T, Tanaka K, Buffo A, Wurst W, Kuhn R, Gotz M (2006) Inducible gene deletion in astroglia and radial glia--a valuable tool for functional and lineage analysis. Glia 54(1):21–34

    Article  Google Scholar 

  28. Haller C, Casanova E, Muller M, Vacher CM, Vigot R, Doll T, Barbieri S, Gassmann M, Bettler B (2004) Floxed allele for conditional inactivation of the GABAB(1) gene. Genesis 40(3):125–130

    Article  CAS  Google Scholar 

  29. Tanaka Y, Tanaka Y, Furuta T, Yanagawa Y, Kaneko T (2008) The effects of cutting solutions on the viability of GABAergic interneurons in cerebral cortical slices of adult mice. J Neurosci Methods 171(1):118–125

    Article  CAS  Google Scholar 

  30. Moyer JR Jr, Brown TH (1998) Methods for whole-cell recording from visually preselected neurons of perirhinal cortex in brain slices from young and aging rats. J Neurosci Methods 86(1):35–54

    Article  Google Scholar 

  31. Kroner S, Krimer LS, Lewis DA, Barrionuevo G (2007) Dopamine increases inhibition in the monkey dorsolateral prefrontal cortex through cell type-specific modulation of interneurons. Cereb Cortex 17(5):1020–1032

    Article  Google Scholar 

  32. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW (2000) Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20(9):3354–3368

    Article  CAS  Google Scholar 

  33. Kaiser T, Ting JT, Monteiro P, Feng G (2016) Transgenic labeling of parvalbumin-expressing neurons with tdTomato. Neuroscience 321:236–245

    Article  CAS  Google Scholar 

  34. Maximiliano José N, Hashikawa Y, Rudy B (2018) Diversity and connectivity of layer 5 somatostatin-expressing interneurons in the mouse barrel cortex. J Neurosci 38(7):1622–1633

    Article  Google Scholar 

  35. Bindocci E, Savtchouk I, Liaudet N, Becker D, Carriero G, Volterra A (2017) Three-dimensional Ca(2+) imaging advances understanding of astrocyte biology. Science 356(6339):eaai8185

    Article  Google Scholar 

  36. Di Castro MA, Chuquet J, Liaudet N, Bhaukaurally K, Santello M, Bouvier D, Tiret P, Volterra A (2011) Local Ca2+ detection and modulation of synaptic release by astrocytes. Nat Neurosci 14(10):1276–1284

    Article  Google Scholar 

  37. Li X, Zima AV, Sheikh F, Blatter LA, Chen J (2005) Endothelin-1-induced arrhythmogenic Ca2+ signaling is abolished in atrial myocytes of inositol-1,4,5-trisphosphate(IP3)-receptor type 2-deficient mice. Circ Res 96(12):1274–1281

    Article  CAS  Google Scholar 

  38. Petravicz J, Fiacco TA, McCarthy KD (2008) Loss of IP3 receptor-dependent Ca2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. J Neurosci 28(19):4967–4973

    Article  CAS  Google Scholar 

  39. Klapoetke NC, Murata Y, Kim SS, Pulver SR, Birdsey-Benson A, Cho YK, Morimoto TK, Chuong AS, Carpenter EJ, Tian Z, Wang J, Xie Y, Yan Z, Zhang Y, Chow BY, Surek B, Melkonian M, Jayaraman V, Constantine-Paton M, Wong GK, Boyden ES (2014) Independent optical excitation of distinct neural populations. Nat Methods 11(3):338–346

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by PhD fellowship program (MINECO, BES-2014-067594) to S.M; and MINECO grants (BFU2016-75107-P) to G.P.

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Authors and Affiliations

  1. Neuron-Glia Networks Lab, Instituto Cajal (CSIC), Madrid, Spain

    Sara Mederos & Gertrudis Perea

Authors
  1. Sara Mederos
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  2. Gertrudis Perea
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Corresponding author

Correspondence to Gertrudis Perea .

Editor information

Editors and Affiliations

  1. Department of Psychiatry and Psychotherapy, University of Regensburg, Regensburg, Germany

    Barbara Di Benedetto

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Mederos, S., Perea, G. (2019). Monitoring Interneuron–Astrocyte Signaling and Its Consequences on Synaptic Transmission. In: Di Benedetto, B. (eds) Astrocytes. Methods in Molecular Biology, vol 1938. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-9068-9_9

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  • DOI: https://doi.org/10.1007/978-1-4939-9068-9_9

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  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-9067-2

  • Online ISBN: 978-1-4939-9068-9

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