Nothing Special   »   [go: up one dir, main page]

skip to main content
article

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

Published: 01 December 2017 Publication History

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.

References

[1]
Amiri M, Bahrami F, Janahmadi M (2012) Functional contributions of astrocytes in synchronization of a neuronal network model. J Theor Biol 292:60-70.
[2]
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.
[3]
Araque A, Carmignoto G, Haydon PG, Oliet SH, Robitaille R, Volterra A (2014) Gliotransmitters travel in time and space. Neuron 81:728-739.
[4]
Attwell D, Buchan AM, Charpak S, Lauritzen M, MacVicar BA, Newman EA (2010) Glial and neuronal control of brain blood flow. Nature 468:232.
[5]
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.
[6]
Bazargani N, Attwell D (2016) Astrocyte calcium signaling: the third wave. Nat Neurosci 19:182-189.
[7]
Bezzi P, Volterra A (2001) A neuron-glia signalling network in the active brain. Curr Opin Neurobiol 11:387-394.
[8]
Bowser DN, Khakh BS (2004) ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J Neurosci 24:8606-8620.
[9]
Brown AM, Ransom BR (2007) Astrocyte glycogen and brain energy metabolism. Glia 55:1263-1271.
[10]
Brunel N (2000) Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons. J Comput Neurosci 8:183-208.
[11]
Brunel N, Hakim V (1999) Fast global oscillations in networks of integrate-and-fire neurons with low firing rates. Neural Comput 11:1621-1671.
[12]
Corner M, van der Togt C (2012) No phylogeny without ontogeny--a comparative and developmental search for the sources of sleeplike neural and behavioral rhythms. Neurosci Bull 28:25-38.
[13]
De Pittà M, Brunel N (2016) Modulation of synaptic plasticity by glutamatergic gliotransmission: a modeling study. Neural Plast 2016.
[14]
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).
[15]
De Young GW, Keizer J (1992) A single-pool inositol 1, 4, 5- trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca 2+ concentration. Proc Natl Acad Sci 89:9895-9899.
[16]
De Pittà M, Brunel N, Volterra A (2016) Astrocytes: orchestrating synaptic plasticity? Neuroscience 323:43-61.
[17]
Drew PJ, Duyn JH, Golanov E, Kleinfeld D (2008) Finding coherence in spontaneous oscillations. Nat Neurosci 11:991-993.
[18]
Fellin T (2009) Communication between neurons and astrocytes: relevance to the modulation of synaptic and network activity. J Neurochem 108:533-544.
[19]
Fellin T, Pascual O, Haydon PG (2006) Astrocytes coordinate synaptic networks: balanced excitation and inhibition. Physiology 21:208-215.
[20]
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).
[21]
Foskett JK, White C, Cheung K-H, Mak D-OD (2007) Inositol trisphosphate receptor Ca 2+ release channels. Physiol Rev 87:593-658.
[22]
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.
[23]
Halassa MM, Haydon PG (2010) Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu Rev Physiol 72:335-355.
[24]
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.
[25]
Hughes SW, Lorincz 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.
[26]
Keizer J, Li Y, Stojilkovic S, Rinzel J (1995) InsP3-induced Ca 2+ excitability of the endoplasmic reticulum. Mol Biol cell 6:945-951.
[27]
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.
[28]
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).
[29]
Latham P, Richmond B, Nelson P, Nirenberg S (2000a) Intrinsic dynamics in neuronal networks. I. Theory J Neurophysiol 83:808-827.
[30]
Latham P, Richmond B, Nirenberg S, Nelson P (2000b) Intrinsic dynamics in neuronal networks. II. Exp J Neurophysiol 83:828-835.
[31]
Li Y-X, Rinzel J (1994) Equations for InsP3 receptor-mediated [Ca 2+i oscillations derived from a detailed kinetic model: a Hodgkin-Huxley like formalism. J Theor Biol 166:461-473.
[32]
Lorincz 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.
[33]
Mok S, Nadasdy Z, Lim Y, Goh S (2012) Ultra-slow oscillations in cortical networks in vitro. Neuroscience 206:17-24.
[34]
Morris C, Lecar H (1981) Voltage oscillations in the barnacle giant muscle fiber. Biophys J 35:193-213.
[35]
Nadkarni S, Jung P (2003) Spontaneous oscillations of dressed neurons: a new mechanism for epilepsy? Phys Rev Lett 91:268101.
[36]
Nadkarni S, Jung P (2004) Dressed neurons: modeling neural-glial interactions. Phys Biol 1:35.
[37]
Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26:523-530.
[38]
Pannasch U et al (2011) Astroglial networks scale synaptic activity and plasticity. Proc Natl Acad Sci 108:8467-8472.
[39]
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.
[40]
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.
[41]
Politi A, Gaspers LD, Thomas AP, Höfer T (2006) Models of IP3 and Ca 2+ oscillations: frequency encoding and identification of underlying feedbacks. Biophys J 90:3120-3133.
[42]
Poskanzer KE, Yuste R (2011) Astrocytic regulation of cortical UP states. Proc Natl Acad Sci 108:18453-18458.
[43]
Poskanzer KE, Yuste R (2016) Astrocytes regulate cortical state switching in vivo. Proc Natl Acad Sci 113:E2675-E2684.
[44]
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.
[45]
Potter SM, DeMarse TB (2001) A new approach to neural cell culture for long-term studies. J Neurosci Methods 110:17-24.
[46]
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.
[47]
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.
[48]
Sah P, Faber E (2002) Channels underlying neuronal calcium-activated potassium currents. Progr Neurobiol 66:345-353.
[49]
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.
[50]
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.
[51]
Stiefel KM, Englitz B, Sejnowski TJ (2013) Origin of intrinsic irregular firing in cortical interneurons. Proc Natl Acad Sci 110:7886-7891.
[52]
Torres A et al (2012) Extracellular Ca 2+ acts as a mediator of communication from neurons to glia. Sci signal 5:8.
[53]
Volman V, Ben-Jacob E, Levine H (2007) The astrocyte as a gatekeeper of synaptic information transfer. Neural Comput 19:303-326.
[54]
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.
[55]
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.
[56]
Zhang et al (2003) ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40:971-982.
[57]
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.
[58]
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.

Cited By

View all
  • (2019)Spatiotemporal model of tripartite synapse with perinodal astrocytic processJournal of Computational Neuroscience10.1007/s10827-019-00734-448:1(1-20)Online publication date: 3-Dec-2019
  1. The role of neuron---glia interactions in the emergence of ultra-slow oscillations

      Recommendations

      Comments

      Please enable JavaScript to view thecomments powered by Disqus.

      Information & Contributors

      Information

      Published In

      cover image Biological Cybernetics
      Biological Cybernetics  Volume 111, Issue 5-6
      December 2017
      137 pages

      Publisher

      Springer-Verlag

      Berlin, Heidelberg

      Publication History

      Published: 01 December 2017

      Author Tags

      1. Cortical culture
      2. Neuron---glia interactions
      3. Ultra-slow oscillations

      Qualifiers

      • Article

      Contributors

      Other Metrics

      Bibliometrics & Citations

      Bibliometrics

      Article Metrics

      • Downloads (Last 12 months)0
      • Downloads (Last 6 weeks)0
      Reflects downloads up to 01 Dec 2024

      Other Metrics

      Citations

      Cited By

      View all
      • (2019)Spatiotemporal model of tripartite synapse with perinodal astrocytic processJournal of Computational Neuroscience10.1007/s10827-019-00734-448:1(1-20)Online publication date: 3-Dec-2019

      View Options

      View options

      Login options

      Media

      Figures

      Other

      Tables

      Share

      Share

      Share this Publication link

      Share on social media