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The role of neuron–glia interactions in the emergence of ultra-slow oscillations

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Abstract

Ultra-slow cortical oscillatory activity of 1–100 mHz has been recorded in human by electroencephalography and in dissociated cultures of cortical rat neurons, but the underlying mechanisms remain to be elucidated. This study presents a computational model of ultra-slow oscillatory activity based on the interaction between neurons and astrocytes. We predict that the frequency of these oscillations closely depends on activation of astrocytes in the network, which is reflected by oscillations of their intracellular calcium concentrations with periods between tens of seconds and minutes. An increase of intracellular calcium in astrocytes triggers the release of adenosine triphosphate from these cells which may alter transmission at nearby synapses by increasing or decreasing neurotransmitter release. These results provide theoretical support for the emerging awareness of astrocytes as active players in the regulation of neural activity and identify neuron–astrocyte interactions as a potential primary mechanism for the emergence of ultra-slow cortical oscillations.

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References

  • Amiri M, Bahrami F, Janahmadi M (2012) Functional contributions of astrocytes in synchronization of a neuronal network model. J Theor Biol 292:60–70

    Article  PubMed  Google Scholar 

  • Amiri M, Hosseinmardi N, Bahrami F, Janahmadi M (2013) Astrocyte-neuron interaction as a mechanism responsible for generation of neural synchrony: a study based on modeling and experiments. J Comput Neurosci 34:489–504

    Article  PubMed  Google Scholar 

  • Araque A, Carmignoto G, Haydon PG, Oliet SH, Robitaille R, Volterra A (2014) Gliotransmitters travel in time and space. Neuron 81:728–739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Attwell D, Buchan AM, Charpak S, Lauritzen M, MacVicar BA, Newman EA (2010) Glial and neuronal control of brain blood flow. Nature 468:232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azevedo FA et al (2009) Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol 513:532–541

    Article  PubMed  Google Scholar 

  • Bazargani N, Attwell D (2016) Astrocyte calcium signaling: the third wave. Nat Neurosci 19:182–189

    Article  CAS  PubMed  Google Scholar 

  • Bezzi P, Volterra A (2001) A neuron–glia signalling network in the active brain. Curr Opin Neurobiol 11:387–394

    Article  CAS  PubMed  Google Scholar 

  • Bowser DN, Khakh BS (2004) ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J Neurosci 24:8606–8620

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Brunel N (2000) Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons. J Comput Neurosci 8:183–208

    Article  CAS  PubMed  Google Scholar 

  • Brunel N, Hakim V (1999) Fast global oscillations in networks of integrate-and-fire neurons with low firing rates. Neural Comput 11:1621–1671

    Article  CAS  PubMed  Google Scholar 

  • Corner M, van der Togt C (2012) No phylogeny without ontogeny—a comparative and developmental search for the sources of sleep-like neural and behavioral rhythms. Neurosci Bull 28:25–38

    Article  PubMed  PubMed Central  Google Scholar 

  • De Pittà M, Brunel N (2016) Modulation of synaptic plasticity by glutamatergic gliotransmission: a modeling study. Neural Plast 2016

  • De Pitta M, Volman V, Berry H, Parpura V, Volterra A, Ben-Jacob E (2012) Computational quest for understanding the role of astrocyte signaling in synaptic transmission and plasticity. Front Comput Neurosci 6 (98)

  • De Young GW, Keizer J (1992) A single-pool inositol 1, 4, 5-trisphosphate-receptor-based model for agonist-stimulated oscillations in \(\text{ Ca }^{2+}\) concentration. Proc Natl Acad Sci 89:9895–9899

    Article  PubMed  PubMed Central  Google Scholar 

  • De Pittà M, Brunel N, Volterra A (2016) Astrocytes: orchestrating synaptic plasticity? Neuroscience 323:43–61

    Article  PubMed  Google Scholar 

  • Drew PJ, Duyn JH, Golanov E, Kleinfeld D (2008) Finding coherence in spontaneous oscillations. Nat Neurosci 11:991–993

    Article  CAS  PubMed  Google Scholar 

  • Fellin T (2009) Communication between neurons and astrocytes: relevance to the modulation of synaptic and network activity. J Neurochem 108:533–544

    Article  CAS  PubMed  Google Scholar 

  • Fellin T, Pascual O, Haydon PG (2006) Astrocytes coordinate synaptic networks: balanced excitation and inhibition. Physiology 21:208–215

    Article  CAS  PubMed  Google Scholar 

  • Fellin T, Ellenbogen JM, De Pittà M, Ben-Jacob E, Halassa MM (2012) Astrocyte regulation of sleep circuits: experimental and modeling perspectives. Front Comput Neurosci 6 (65)

  • Foskett JK, White C, Cheung K-H, Mak D-OD (2007) Inositol trisphosphate receptor \(\text{ Ca }^{2+}\) release channels. Physiol Rev 87:593–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giaume C, Koulakoff A, Roux L, Holcman D, Rouach N (2010) Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat Rev Neurosci 11:87–99

    Article  CAS  PubMed  Google Scholar 

  • Halassa MM, Haydon PG (2010) Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu Rev Physiol 72:335–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holt GR, Softky WR, Koch C, Douglas RJ (1996) Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J Neurophysiol 75:1806–1814

    CAS  PubMed  Google Scholar 

  • Hughes SW, Lőrincz ML, Parri HR, Crunelli V (2011) Infra-slow (\(<\) 0.1 Hz) oscillations in thalamic relay nuclei: basic mechanisms and significance to health and disease states. Progr Brain Res 193:145

    Article  Google Scholar 

  • Keizer J, Li Y, Stojilković S, Rinzel J (1995) InsP3-induced \(\text{ Ca }^{2+}\) excitability of the endoplasmic reticulum. Mol Biol cell 6:945–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koizumi S, Fujishita K, Tsuda M, Shigemoto-Mogami Y, Inoue K (2003) Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures. Proc Natl Acad Sci 100:11023–11028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lallouette J, De Pittà M, Ben-Jacob E, Berry H (2014) Sparse short-distance connections enhance calcium wave propagation in a 3D model of astrocyte networks. Front Comput Neurosci 8 (45)

  • Latham P, Richmond B, Nelson P, Nirenberg S (2000a) Intrinsic dynamics in neuronal networks. I. Theory J Neurophysiol 83:808–827

    CAS  PubMed  Google Scholar 

  • Latham P, Richmond B, Nirenberg S, Nelson P (2000b) Intrinsic dynamics in neuronal networks. II. Exp J Neurophysiol 83:828–835

    CAS  Google Scholar 

  • Li Y-X, Rinzel J (1994) Equations for \(\text{ InsP }^{3}\) receptor-mediated [\(\text{ Ca }^{2+} \text{ i }\) oscillations derived from a detailed kinetic model: a Hodgkin–Huxley like formalism. J Theor Biol 166:461–473

    Article  CAS  PubMed  Google Scholar 

  • Lőrincz ML, Geall F, Bao Y, Crunelli V, Hughes SW (2009) ATP-dependent infra-slow (\(<\) 0.1 Hz) oscillations in thalamic networks. PLoS ONE 4:e4447

    Article  PubMed  PubMed Central  Google Scholar 

  • Mok S, Nadasdy Z, Lim Y, Goh S (2012) Ultra-slow oscillations in cortical networks in vitro. Neuroscience 206:17–24

    Article  CAS  PubMed  Google Scholar 

  • Morris C, Lecar H (1981) Voltage oscillations in the barnacle giant muscle fiber. Biophys J 35:193–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nadkarni S, Jung P (2003) Spontaneous oscillations of dressed neurons: a new mechanism for epilepsy? Phys Rev Lett 91:268101

    Article  PubMed  Google Scholar 

  • Nadkarni S, Jung P (2004) Dressed neurons: modeling neural–glial interactions. Phys Biol 1:35

    Article  CAS  PubMed  Google Scholar 

  • Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26:523–530

    Article  CAS  PubMed  Google Scholar 

  • Pannasch U et al (2011) Astroglial networks scale synaptic activity and plasticity. Proc Natl Acad Sci 108:8467–8472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pasti L, Volterra A, Pozzan T, Carmignoto G (1997) Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J Neurosci 17:7817–7830

    CAS  PubMed  Google Scholar 

  • Picchioni D et al (2011) Infraslow EEG oscillations organize large-scale cortical–subcortical interactions during sleep: a combined EEG/fMRI study. Brain Res 1374:63–72

    Article  CAS  PubMed  Google Scholar 

  • Politi A, Gaspers LD, Thomas AP, Höfer T (2006) Models of IP3 and \(\text{ Ca }^{2+}\) oscillations: frequency encoding and identification of underlying feedbacks. Biophys J 90:3120–3133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poskanzer KE, Yuste R (2016) Astrocytes regulate cortical state switching in vivo. Proc Natl Acad Sci 113:E2675–E2684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Postnov D, Koreshkov R, Brazhe N, Brazhe A, Sosnovtseva O (2009) Dynamical patterns of calcium signaling in a functional model of neuron–astrocyte networks. J Biol Phys 35:425–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Potter SM, DeMarse TB (2001) A new approach to neural cell culture for long-term studies. J Neurosci Methods 110:17–24

    Article  CAS  PubMed  Google Scholar 

  • Prescott SA, Ratté S, De Koninck Y, Sejnowski TJ (2008) Pyramidal neurons switch from integrators in vitro to resonators under in vivo-like conditions. J Neurophysiol 100:3030–3042

    Article  PubMed  PubMed Central  Google Scholar 

  • Roux L, Benchenane K, Rothstein JD, Bonvento G, Giaume C (2011) Plasticity of astroglial networks in olfactory glomeruli. Proc Natl Acad Sci 108:18442–18446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sah P, Faber E (2002) Channels underlying neuronal calcium-activated potassium currents. Progr Neurobiol 66:345–353

    Article  CAS  Google Scholar 

  • Sasaki T, Ishikawa T, Abe R, Nakayama R, Asada A, Matsuki N, Ikegaya Y (2014) Astrocyte calcium signalling orchestrates neuronal synchronization in organotypic hippocampal slices. J Physiol 592:2771–2783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segev R, Shapira Y, Benveniste M, Ben-Jacob E (2001) Observations and modeling of synchronized bursting in two-dimensional neural networks. Phys Rev E 64:011920

    Article  CAS  Google Scholar 

  • Stiefel KM, Englitz B, Sejnowski TJ (2013) Origin of intrinsic irregular firing in cortical interneurons. Proc Natl Acad Sci 110:7886–7891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres A et al (2012) Extracellular \(\text{ Ca }^{2+}\) acts as a mediator of communication from neurons to glia. Sci signal 5:8

    Article  Google Scholar 

  • Volman V, Ben-Jacob E, Levine H (2007) The astrocyte as a gatekeeper of synaptic information transfer. Neural Comput 19:303–326

    Article  PubMed  Google Scholar 

  • Wagenaar D, DeMarse TB, Potter SM(2005) MEABench: a toolset for multi-electrode data acquisition and on-line analysis. In: 2nd international IEEE EMBS conference on neural engineering, 2005. Conference proceedings. IEEE, pp 518–521

  • Wallach G, Lallouette J, Herzog N, De Pittà M, Jacob EB, Berry H, Hanein Y (2014) Glutamate mediated astrocytic filtering of neuronal activity. PLoS Comput Biol 10:e1003964

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang et al (2003) ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40:971–982

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Fritz N, Ibarra C, Uhlén P (2011) Inositol 1, 4, 5-trisphosphate receptor subtype-specific regulation of calcium oscillations. Neurochem Res 36:1175–1185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu G, Li X, Pu J, Chen W, Luo Q (2010) Transient alterations in slow oscillations of hippocampal networks by low-frequency stimulations on multi-electrode arrays. Biomed Microdevices 12:153–158

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the Malaysian Ministry of Science Technology and Innovation (MOSTI) Flagship Program Project No. FP0911F001 and the UTAR Research Fund Project No. IPSR/ RMC / UTARRF/ 2016-C1/M1. We are also grateful to the two anonymous referees for their valuable comments that contributed to substantially improving our manuscript.

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Correspondence to Siow-Cheng Chan.

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Chan, SC., Mok, SY., Ng, D.WK. et al. The role of neuron–glia interactions in the emergence of ultra-slow oscillations. Biol Cybern 111, 459–472 (2017). https://doi.org/10.1007/s00422-017-0740-z

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  • DOI: https://doi.org/10.1007/s00422-017-0740-z

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