Brain Structure and Function

, Volume 222, Issue 1, pp 651–659 | Cite as

Unitary GABAergic volume transmission from individual interneurons to astrocytes in the cerebral cortex

  • Márton Rózsa
  • Judith Baka
  • Sándor Bordé
  • Balázs Rózsa
  • Gergely Katona
  • Gábor Tamás
Short Communication

Abstract

Communication between individual GABAergic cells and their target neurons is mediated by synapses and, in the case of neurogliaform cells (NGFCs), by unitary volume transmission. Effects of non-synaptic volume transmission might involve non-neuronal targets, and astrocytes not receiving GABAergic synapses but expressing GABA receptors are suitable for evaluating this hypothesis. Testing several cortical interneuron types in slices of the rat cerebral cortex, we show selective unitary transmission from NGFCs to astrocytes with an early, GABAA receptor and GABA transporter-mediated component and a late component that results from the activation of GABA transporters and neuronal GABAB receptors. We could not detect Ca2+ influx in astrocytes associated with unitary GABAergic responses. Our experiments identify a presynaptic cell-type-specific, GABA-mediated communication pathway from individual neurons to astrocytes, assigning a role for unitary volume transmission in the control of ionic and neurotransmitter homeostasis.

Keywords

Interneuron GABAA GABAB Neocortex 

Notes

Acknowledgments

This work was supported by the ERC INTERIMPACT project and the Hungarian Academy of Sciences (G.T.).

References

  1. Agnati LF, Leo G, Zanardi A et al (2006) Volume transmission and wiring transmission from cellular to molecular networks: history and perspectives. Acta Physiol 187:329–344. doi:10.1111/j.1748-1716.2006.01579.x CrossRefGoogle Scholar
  2. Amzica F, Massimini M, Manfridi A (2002) Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo. J Neurosci 22:1042–1053PubMedGoogle Scholar
  3. Ballanyi K, Grafe P, ten Bruggencate G (1987) Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices. J Physiol 382:159–174CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barbour B, Häusser M (1997) Intersynaptic diffusion of neurotransmitter. Trends Neurosci 20:377–384. doi:10.1016/S0166-2236(96)20050-5 CrossRefPubMedGoogle Scholar
  5. Bergles DE, Roberts JD, Somogyi P, Jahr CE (2000) Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:187–191. doi:10.1038/35012083 CrossRefPubMedGoogle Scholar
  6. 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 22:73–86. doi:10.1016/j.ijdevneu.2003.12.008 CrossRefPubMedGoogle Scholar
  7. Cahoy JD, Emery B, Kaushal A et al (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264–278. doi:10.1523/JNEUROSCI.4178-07.2008 CrossRefPubMedGoogle Scholar
  8. Capogna M (2011) Neurogliaform cells and other interneurons of stratum lacunosum-moleculare gate entorhinal-hippocampal dialogue. J Physiol 589:1875–1883. doi:10.1113/jphysiol.2010.201004 CrossRefPubMedGoogle Scholar
  9. Chittajallu R, Pelkey KA, McBain CJ (2013) Neurogliaform cells dynamically regulate somatosensory integration via synapse-specific modulation. Nat Neurosci 16:13–15. doi:10.1038/nn.3284 CrossRefPubMedGoogle Scholar
  10. Craig MT, McBain CJ (2014) The emerging role of GABAB receptors as regulators of network dynamics: fast actions from a “slow” receptor? Curr Opin Neurobiol 26:15–21. doi:10.1016/j.conb.2013.10.002 CrossRefPubMedGoogle Scholar
  11. Craig MT, Mayne EW, Bettler B et al (2013) Distinct roles of GABAB1a- and GABAB1b-containing GABAB receptors in spontaneous and evoked termination of persistent cortical activity. J Physiol 591:835–843. doi:10.1113/jphysiol.2012.248088 CrossRefPubMedGoogle Scholar
  12. Di Castro MA, Chuquet J, Liaudet N et al (2011) Local Ca2+ detection and modulation of synaptic release by astrocytes. Nat Neurosci 14:1276–1284. doi:10.1038/nn.2929 CrossRefPubMedGoogle Scholar
  13. Doengi M, Hirnet D, Coulon P et al (2009) GABA uptake-dependent Ca2+ signaling in developing olfactory bulb astrocytes. Proc Natl Acad Sci 106:17570–17575. doi:10.1073/pnas.0809513106 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Dy JG, Brodley CE (2004) Feature selection for unsupervised learning. J Mach Learn Res 5:845–889Google Scholar
  15. Egawa K, Yamada J, Furukawa T et al (2013) Cl homeodynamics in gap junction-coupled astrocytic networks on activation of GABAergic synapses. J Physiol 591:3901–3917. doi:10.1113/jphysiol.2013.257162 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Eulenburg V, Gomeza J (2010) Neurotransmitter transporters expressed in glial cells as regulators of synapse function. Brain Res Rev 63:103–112. doi:10.1016/j.brainresrev.2010.01.003 CrossRefPubMedGoogle Scholar
  17. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: phasic and tonic activation of GABAA receptors. Nat Rev Neurosci 6:215–229. doi:10.1038/nrn1625 CrossRefPubMedGoogle Scholar
  18. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470. doi:10.1002/(SICI)1098-1063(1996)6:4<347:AID-HIPO1>3.0.CO;2-I CrossRefPubMedGoogle Scholar
  19. Fritschy J-M, Sidler C, Parpan F et al (2004) Independent maturation of the GABA(B) receptor subunits GABA(B1) and GABA(B2) during postnatal development in rodent brain. J Comp Neurol 477:235–252. doi:10.1002/cne.20188 CrossRefPubMedGoogle Scholar
  20. Gentet LJ, Avermann M, Matyas F et al (2010) Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 65:422–435. doi:10.1016/j.neuron.2010.01.006 CrossRefPubMedGoogle Scholar
  21. Grosche J, Matyash V, Möller T et al (1999) Microdomains for neuron–glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci 2:139–143. doi:10.1038/5692 CrossRefPubMedGoogle Scholar
  22. Haustein MD, Kracun S, Lu X-H et al (2014) Conditions and constraints for astrocyte calcium signaling in the hippocampal mossy fiber pathway. Neuron 82:413–429. doi:10.1016/j.neuron.2014.02.041 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hibino H, Inanobe A, Furutani K et al (2010) Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev 90:291–366. doi:10.1152/physrev.00021.2009 CrossRefPubMedGoogle Scholar
  24. Kaila K, Lamsa K, Smirnov S et al (1997) Long-lasting GABA-mediated depolarization evoked by high-frequency stimulation in pyramidal neurons of rat hippocampal slice is attributable to a network-driven, bicarbonate-dependent K+ transient. J Neurosci 17:7662–7672PubMedGoogle Scholar
  25. Kang J, Jiang L, Goldman SA, Nedergaard M (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1:683–692. doi:10.1038/3684 CrossRefPubMedGoogle Scholar
  26. Katona G, Szalay G, Maák P et al (2012) Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes. Nat Methods 9:201–208. doi:10.1038/nmeth.1851 CrossRefPubMedGoogle Scholar
  27. Kaupmann K, Huggel K, Heid J et al (1997) Expression cloning of GABA(B) receptors uncovers similarity to metabotropic glutamate receptors. Nature 386:239–246. doi:10.1038/386239a0 CrossRefPubMedGoogle Scholar
  28. Kettenmann H, Backus KH, Schachner M (1984) Aspartate, glutamate and gamma-aminobutyric acid depolarize cultured astrocytes. Neurosci Lett 52:25–29. doi:10.1016/0304-3940(84)90345-8 CrossRefPubMedGoogle Scholar
  29. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53–57. doi:10.1126/science.1149381 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129:1045–1056CrossRefPubMedPubMedCentralGoogle Scholar
  31. Li Y, Dong M, Hua J (2008) Localized feature selection for clustering. Pattern Recognit Lett 29:10–18. doi:10.1016/j.patrec.2007.08.012 CrossRefGoogle Scholar
  32. Lin S, Bergles DE (2004) Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nat Neurosci 7:24–32. doi:10.1038/nn1162 CrossRefPubMedGoogle Scholar
  33. López-Bendito G, Shigemoto R, Kulik A et al (2004) Distribution of metabotropic GABA receptor subunits GABAB1a/b and GABAB2 in the rat hippocampus during prenatal and postnatal development. Hippocampus 14:836–848. doi:10.1002/hipo.10221 CrossRefPubMedGoogle Scholar
  34. 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 B Biol Sci 369:20130609. doi:10.1098/rstb.2013.0609 CrossRefGoogle Scholar
  35. Luján R, Shigemoto R (2006) Localization of metabotropic GABA receptor subunits GABAB1 and GABAB2 relative to synaptic sites in the rat developing cerebellum. Eur J Neurosci 23:1479–1490. doi:10.1111/j.1460-9568.2006.04669.x CrossRefPubMedGoogle Scholar
  36. Ma B-F, Xie M-J, Zhou M (2012) Bicarbonate efflux via GABAA receptors depolarizes membrane potential and inhibits two-pore domain potassium channels of astrocytes in rat hippocampal slices. Glia 60:1761–1772. doi:10.1002/glia.22395 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Ma B, Xu G, Wang W et al (2014) Dual patch voltage clamp study of low membrane resistance astrocytes in situ. Mol Brain 7:18. doi:10.1186/1756-6606-7-18 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Mann EO, Kohl MM, Paulsen O (2009) Distinct roles of GABAA and GABAB receptors in balancing and terminating persistent cortical activity. J Neurosci 29:7513–7518. doi:10.1523/JNEUROSCI.6162-08.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Markram H, Toledo-Rodriguez M, Wang Y et al (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793–807. doi:10.1038/nrn1519 CrossRefPubMedGoogle Scholar
  40. Martin SC, Steiger JL, Gravielle MC et al (2004) Differential expression of gamma-aminobutyric acid type B receptor subunit mRNAs in the developing nervous system and receptor coupling to adenylyl cyclase in embryonic neurons. J Comp Neurol 473:16–29. doi:10.1002/cne.20094 CrossRefPubMedGoogle Scholar
  41. McLachlan GJ, Peel DA (2000) Finite mixture models. Wiley, New YorkCrossRefGoogle Scholar
  42. Meier SD, Kafitz KW, Rose CR (2008) Developmental profile and mechanisms of GABA-induced calcium signaling in hippocampal astrocytes. Glia 56:1127–1137. doi:10.1002/glia.20684 CrossRefPubMedGoogle Scholar
  43. Miles R, Wong RK (1984) Unitary inhibitory synaptic potentials in the guinea-pig hippocampus in vitro. J Physiol 356:97–113CrossRefPubMedPubMedCentralGoogle Scholar
  44. Mishima T, Hirase H (2010) In vivo intracellular recording suggests that gray matter astrocytes in mature cerebral cortex and hippocampus are electrophysiologically homogeneous. J Neurosci 30:3093–3100. doi:10.1523/JNEUROSCI.5065-09.2010 CrossRefPubMedGoogle Scholar
  45. Nilsson M, Eriksson PS, Rönnbäck L, Hansson E (1993) GABA induces Ca2+ transients in astrocytes. Neuroscience 54:605–614. doi:10.1016/0306-4522(93)90232-5 CrossRefPubMedGoogle Scholar
  46. Oláh S, Füle M, Komlósi G et al (2009) Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461:1278–1281. doi:10.1038/nature08503 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Oldfield CS, Marty A, Stell BM (2010) Interneurons of the cerebellar cortex toggle Purkinje cells between up and down states. Proc Natl Acad Sci 107:13153–13158. doi:10.1073/pnas.1002082107 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Otis TS, Staley KJ, Mody I (1991) Perpetual inhibitory activity in mammalian brain slices generated by spontaneous GABA release. Brain Res 545:142–150CrossRefPubMedGoogle Scholar
  49. Porter JT, McCarthy KD (1997) Astrocytic neurotransmitter receptors in situ and in vivo. Prog Neurobiol 51:439–455. doi:10.1016/S0301-0082(96)00068-8 CrossRefPubMedGoogle Scholar
  50. Pouille F, Scanziani M (2004) Routing of spike series by dynamic circuits in the hippocampus. Nature 429:717–723. doi:10.1038/nature02615 CrossRefPubMedGoogle Scholar
  51. Serrano A (2006) GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J Neurosci 26:5370–5382. doi:10.1523/JNEUROSCI.5255-05.2006 CrossRefPubMedGoogle Scholar
  52. Simon A, Oláh S, Molnár G et al (2005) Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J Neurosci 25:6278–6285. doi:10.1523/JNEUROSCI.1431-05.2005 CrossRefPubMedGoogle Scholar
  53. Sun W, McConnell E, Pare J-F et al (2013) Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 339(80):197–200. doi:10.1126/science.1226740 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Tamas G (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299(80):1902–1905. doi:10.1126/science.1082053 CrossRefPubMedGoogle Scholar
  55. Thomson AM, Bannister AP, Mercer A, Morris OT (2002) Target and temporal pattern selection at neocortical synapses. Philos Trans R Soc B Biol Sci 357:1781–1791. doi:10.1098/rstb.2002.1163 CrossRefGoogle Scholar
  56. Velez-Fort M, Audinat E, Angulo MC (2012) Central role of GABA in Neuron–Glia Interactions. Neurosci 18:237–250. doi:10.1177/1073858411403317 Google Scholar
  57. Viitanen T, Ruusuvuori E, Kaila K, Voipio J (2010) The K+-Cl cotransporter KCC2 promotes GABAergic excitation in the mature rat hippocampus. J Physiol 588:1527–1540. doi:10.1113/jphysiol.2009.181826 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Vizi ES, Kiss JP (1998) Neurochemistry and pharmacology of the major hippocampal transmitter systems: synaptic and nonsynaptic interactions. Hippocampus 8:566–607. doi:10.1002/(SICI)1098-1063(1998)8:6<566:AID-HIPO2>3.0.CO;2-W CrossRefPubMedGoogle Scholar
  59. Vizi ES, Kiss JP, Lendvai B (2004) Nonsynaptic communication in the central nervous system. Neurochem Int 45:443–451. doi:10.1016/j.neuint.2003.11.016 CrossRefPubMedGoogle Scholar
  60. Volterra A, Liaudet N, Savtchouk I (2014) Astrocyte Ca2+ signalling: an unexpected complexity. Nat Rev Neurosci 15:327–335. doi:10.1038/nrn3725 CrossRefPubMedGoogle Scholar
  61. Wang F, Xu Q, Wang W et al (2012) Bergmann glia modulate cerebellar Purkinje cell bistability via Ca2+-dependent K+ uptake. Proc Natl Acad Sci 109:7911–7916. doi:10.1073/pnas.1120380109 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Williams SR, Mitchell SJ (2008) Direct measurement of somatic voltage clamp errors in central neurons. Nat Neurosci 11:790–798. doi:10.1038/nn.2137 CrossRefPubMedGoogle Scholar
  63. Zhou M (2005) Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. J Neurophysiol 95:134–143. doi:10.1152/jn.00570.2005 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Márton Rózsa
    • 1
  • Judith Baka
    • 1
  • Sándor Bordé
    • 1
  • Balázs Rózsa
    • 2
  • Gergely Katona
    • 2
  • Gábor Tamás
    • 1
  1. 1.MTA-SZTE Research Group for Cortical Microcircuits, Department of Anatomy, Physiology and NeuroscienceUniversity of SzegedSzegedHungary
  2. 2.Two-Photon Imaging Center, Institute of Experimental MedicineHungarian Academy of SciencesBudapestHungary

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