Skip to main content
SpringerLink
Log in

Diversity of synaptic astrocyte–neuron signaling

  • Review article
  • Published:
e-Neuroforum

Abstract

Fast signal exchange between neurons and astrocytes at the synaptic level has attracted considerable attention. Astrocytes often respond with Ca2+ transients to widely different neuronal synaptic activity. At the same time, astrocyte Ca2+ elevations trigger profound and diverse changes of both excitatory and inhibitory synaptic transmission. Here, we briefly review examples of the heterogeneity of Ca2+-dependent astrocyte–neuron communication in the rodent hippocampus and discuss mechanisms that could maintain specificity of synaptic astrocyte–neuron signaling in the face of its diversity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Anders S, Minge D, Griemsmann S, Herde MK, Steinhäuser C, Henneberger C (2014) Spatial properties of astrocyte gap junction coupling in the rat hippocampus. Philos Trans R Soc Lond B Biol Sci 369:20130600

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Andersson M, Hanse E (2010) Astrocytes impose postburst depression of release probability at hippocampal glutamate synapses. J Neurosci 30:5776–5780

    Article  CAS  PubMed  Google Scholar 

  3. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22:208–215

    Article  CAS  PubMed  Google Scholar 

  4. Benfenati V, Amiry-Moghaddam M, Caprini M, Mylonakou MN, Rapisarda C, Ottersen OP, Ferroni S (2007) Expression and functional characterization of transient receptor potential vanilloid-related channel 4 (TRPV4) in rat cortical astrocytes. Neuroscience 148:876–892

    Article  CAS  PubMed  Google Scholar 

  5. Bernardinelli Y, Randall J, Janett E, Nikonenko I, König S, Jones EV, Flores CE, Murai KK, Bochet CG, Holtmaat A, Muller D (2014) Activity-dependent structural plasticity of perisynaptic astrocytic domains promotes excitatory synapse stability. Curr Biol 24:1679–1688

    Article  CAS  PubMed  Google Scholar 

  6. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183–192

    CAS  PubMed  Google Scholar 

  7. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247:470–473

    Article  CAS  PubMed  Google Scholar 

  8. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105

    Article  CAS  PubMed  Google Scholar 

  9. Delekate A, Füchtemeier M, Schumacher T, Ulbrich C, Foddis M, Petzold GC (2014) Metabotropic P2Y1 receptor signalling mediates astrocytic hyperactivity in vivo in an Alzheimer’s disease mouse model. Nat Commun 5:5422

    Article  PubMed  Google Scholar 

  10. 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 14:1276–1284

    Article  CAS  PubMed  Google Scholar 

  11. Dunn KM, Hill-Eubanks DC, Liedtke WB, Nelson MT (2013) TRPV4 channels stimulate Ca2+-induced Ca2+ release in astrocytic endfeet and amplify neurovascular coupling responses. Proc Natl Acad Sci U S A 110:6157–6162

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Henneberger C, Medvedev NI, Stuart MG, Rusakov DA (2008). LTP induction changes the morphology of astrocytes in the CA1 region of the hippocampus in vitro. In Society for neuroscience meeting. Washington, p 242.7/I2

  13. Henneberger C, Papouin T, Oliet SHR, Rusakov DA (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463:232–236

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Kanemaru K, Sekiya H, Xu M, Satoh K, Kitajima N, Yoshida K, Okubo Y, Sasaki T, Moritoh S, Hasuwa H, Mimura M, Horikawa K, Matsui K, Nagai T, Iino M, Tanaka KF (2014) In vivo visualization of subtle, transient, and local activity of astrocytes using an ultrasensitive Ca2+ indicator. Cell Rep 8:311–318

    Article  CAS  PubMed  Google Scholar 

  15. Kang J, Jiang L, Goldman SA, Nedergaard M (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1:683–692

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  17. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53–57

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Losi G, Mariotti L, Carmignoto G (2014) GABAergic interneuron to astrocyte signalling: a neglected form of cell communication in the brain. Philos Trans R Soc Lond B Biol Sci 369:20130609

    Article  CAS  PubMed  Google Scholar 

  19. Matyash V, Kettenmann H (2010) Heterogeneity in astrocyte morphology and physiology. Brain Res Rev 63:2–10

    Article  CAS  PubMed  Google Scholar 

  20. Medvedev N, Popov V, Henneberger C, Kraev I, Rusakov DA, Stewart MG (2014) Glia selectively approach synapses on thin dendritic spines. Philos Trans R Soc Lond B Biol Sci 369:20140047

    Article  PubMed Central  PubMed  Google Scholar 

  21. Meier SD, Kafitz KW, Rose CR (2008) Developmental profile and mechanisms of GABA-induced calcium signaling in hippocampal astrocytes. Glia 56:1127–1137

    Article  PubMed  Google Scholar 

  22. Meyer D, Bonhoeffer T, Scheuss V (2014) Balance and stability of synaptic structures during synaptic plasticity. Neuron 82:430–443

    Article  CAS  PubMed  Google Scholar 

  23. Navarrete M, Araque A (2008) Endocannabinoids mediate neuron–astrocyte communication. Neuron 57:883–893

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  25. Navarrete M, Perea G, de Sevilla DF, Gómez-Gonzalo M, Núñez A, Martín ED, Araque A (2012) Astrocytes mediate in vivo cholinergic-induced synaptic plasticity. PLoS Biol 10:e1001259

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Nett WJ, Oloff SH, McCarthy KD (2002) Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity. J Neurophysiol 87:528–537

    PubMed  Google Scholar 

  27. Nuriya M, Yasui M (2013) Endfeet serve as diffusion-limited subcellular compartments in astrocytes. J Neurosci 33:3692–3698

    Article  CAS  PubMed  Google Scholar 

  28. Oliet SH, Piet R, Poulain DA (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292:923–926

    Article  CAS  PubMed  Google Scholar 

  29. Panatier A, Theodosis DT, Mothet J-P, Touquet B, Pollegioni L, Poulain DA, Oliet SHR (2006) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125:775–784

    Article  CAS  PubMed  Google Scholar 

  30. Panatier A, Vallée J, Haber M, Murai KK, Lacaille J-C, Robitaille R (2011) Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146:785–798

    Article  CAS  PubMed  Google Scholar 

  31. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyte–neuron signalling. Nature 369:744–747

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  33. Perez-Alvarez A, Navarrete M, Covelo A, Martin ED, Araque A (2014) Structural and functional plasticity of astrocyte processes and dendritic spine interactions. J Neurosci 34:12738–12744

    Article  CAS  PubMed  Google Scholar 

  34. Petzold GC, Murthy VN (2011) Role of astrocytes in neurovascular coupling. Neuron 71:782–797

    Article  CAS  PubMed  Google Scholar 

  35. Porter JT, McCarthy KD (1996) Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J Neurosci 16:5073–5081

    CAS  PubMed  Google Scholar 

  36. Rusakov DA, Bard L, Stewart MG, Henneberger C (2014) Diversity of astroglial functions alludes to subcellular specialisation. Trends Neurosci 37:228–242

    Article  CAS  PubMed  Google Scholar 

  37. Santello M, Bezzi P, Volterra A (2011) TNFa controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69:988–1001

    Article  CAS  PubMed  Google Scholar 

  38. Sasaki T, Beppu K, Tanaka KF, Fukazawa Y, Shigemoto R, Matsui K (2012) Application of an optogenetic byway for perturbing neuronal activity via glial photostimulation. Proc Natl Acad Sci U S A 109:20720–20725

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Srinivasan R, Huang BS, Venugopal S, Johnston AD, Chai H, Zeng H, Golshani P, Khakh BS (2015) Ca2+ signaling in astrocytes from Ip3r2(−/−) mice in brain slices and during startle responses in vivo. Nat Neurosci 18:708–717

    Article  CAS  PubMed  Google Scholar 

  40. Sun W, McConnell E, Pare J-F, Xu Q, Chen M, Peng W, Lovatt D, Han X, Smith Y, Nedergaard M (2013) Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 339:197–200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. Tang W, Szokol K, Jensen V, Enger R, Trivedi CA, Hvalby Ø, Helm PJ, Looger LL, Sprengel R, Nagelhus EA (2015) Stimulation-evoked Ca2+ signals in astrocytic processes at hippocampal CA3–CA1 synapses of adult mice are modulated by glutamate and ATP. J Neurosci 35:3016–3021

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19:6897–6906

    CAS  PubMed  Google Scholar 

  43. Wang F, Smith NA, Xu Q, Fujita T, Baba A, Matsuda T, Takano T, Bekar L, Nedergaard M (2012). Astrocytes modulate neural network activity by Ca2+-dependent uptake of extracellular K+. Sci Signal 5:ra26

    PubMed Central  PubMed  Google Scholar 

  44. 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 560:122–131

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Work was supported by DFG (SFB1089 B03 to Christian Henneberger, SPP1757 HE6949/1 to Christian Henneberger, PE1193/2-1 to Gabor C. Petzold), NRW-Rückkehrerprogramm (Christian Henneberger), Human Frontiers Science Program (Christian Henneberger), Else-Kröner Fresenius Foundation (Gabor C. Petzold), Network Of Centres Of Excellence In Neurodegeneration—CoEN (Gabor C. Petzold) and the DZNE (Gabor C. Petzold).

Author information

Authors and Affiliations

  1. Institute of Cellular Neurosciences, University of Bonn Medical School, Sigmund-Freud-Str. 25, 53105, Bonn, Germany

    Christian Henneberger

  2. UCL Institute of Neurology, London, UK

    Christian Henneberger

  3. German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany

    Gabor C. Petzold

Authors
  1. Christian Henneberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gabor C. Petzold
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christian Henneberger.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Henneberger, C., Petzold, G. Diversity of synaptic astrocyte–neuron signaling. e-Neuroforum 6, 79–83 (2015). https://doi.org/10.1007/s13295-015-0011-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13295-015-0011-1

Keywords

Search

Navigation