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On the role of synchrony for neuron–astrocyte interactions and perceptual conscious processing

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Abstract

Recent research on brain correlates of cognitive processes revealed the occurrence of global synchronization during conscious processing of sensory stimuli. In spite of technological progress in brain imaging, an explanation of the computational role of synchrony is still a highly controversial issue. In this study, we depart from an analysis of the usage of blood-oxygen-level-dependent functional magnetic resonance imaging for the study of cognitive processing, leading to the identification of evoked local field potentials as the vehicle for sensory patterns that compose conscious episodes. Assuming the “astrocentric hypothesis” formulated by James M. Robertson (astrocytes being the final stage of conscious processing), we propose that the role of global synchrony in perceptual conscious processing is to induce the transfer of information patterns embodied in local field potentials to astrocytic calcium waves, further suggesting that these waves are responsible for the “binding” of spatially distributed patterns into unitary conscious episodes.

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References

  1. Robertson, J.M.: The astrocentric hypothesis: proposed role of astrocytes in consciousness and memory formation. J. Physiol. (Paris) 96, 251–255 (2002). doi:10.1016/S0928-4257(02)00013-X

    Article  Google Scholar 

  2. Perea, G., Araque, A.: Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J. Neurosci. 25, 2192–2203 (2005). doi:10.1523/JNEUROSCI.3965-04.2005

    Article  Google Scholar 

  3. Halassa, M.M., Fellin, T., Takano, H., Dong, J.H., Haydon, P.G.: Synaptic islands defined by the territory of a single astrocyte. J. Neurosci. 27, 6473–6477 (2007). doi:10.1523/JNEUROSCI.1419-07.2007

    Article  Google Scholar 

  4. Haydon, P.G., Carmignoto, G.: Astrocyte control of synaptic transmission and neurovascular coupling. Physiol. Rev. 86, 1009–1031 (2006). doi:10.1152/physrev.00049.2005

    Article  Google Scholar 

  5. Bushong, E.A., Martone, M.E., Jones, Y.Z., Ellisman, M.H.: Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J. Neurosci. 22, 183–192 (2002)

    Google Scholar 

  6. Agulhon, C., Petravicz, J., McMullen, A.B., Sweger, E.J., Minton, S.K., Taves, S.R., Casper, K.B., Fiacco, T.A., McCarthy, K.D.: What is the role of astrocyte calcium in neurophysiology? Neuron 59, 932–946 (2008). doi:10.1016/j.neuron.2008.09.004

    Article  Google Scholar 

  7. Araque, A., Parpura, V., Sanzgiri, R.P., Haydon, P.G.: Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 22, 208–215 (1999). doi:10.1016/S0166-2236(98)01349-6

    Article  Google Scholar 

  8. Araque, A., Martín, E.D., Perea, G., Arellano, J.I., Buño, W.: Synaptically released acetylcholine evokes Ca2 +  elevations in astrocytes in hippocampal slices. J. Neurosci. 22, 2443–2450 (2002)

    Google Scholar 

  9. Kang, J., Jiang, L., Goldman, S.A., Nedergaard, M.: Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat. Neurosci. 1, 683–692 (1998). doi:10.1038/3684

    Article  Google Scholar 

  10. Perea, G., Araque, A.: Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J. Neurosci. 25, 2192–2203 (2005). doi:10.1523/JNEUROSCI.3965-04.2005

    Article  Google Scholar 

  11. Cornell-Bell, A.H., Finkbeiner, S.M., Cooper, M.S., Smith, S.J.: Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470–473 (1990). doi:10.1126/science.1967852

    Article  ADS  Google Scholar 

  12. Charles, A.C., Merrill, J.E., Dirksen, E.R., Sanderson, M.J.: Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron 6, 983–992 (1991). doi:10.1016/0896-6273(91)90238-U

    Article  Google Scholar 

  13. Porter, J.T., McCarthy, K.D.: Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J. Neurosci. 16, 5073–5081 (1996)

    Google Scholar 

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

    Google Scholar 

  15. Verkhratsky, A., Steinhauser, C.: Ion channels in glial cells. Brain Res. Rev. 32, 380–412 (2000). doi:10.1016/S0165-0173(99)00093-4

    Article  Google Scholar 

  16. Reyes, R.C., Parpura, V.: The trinity of Ca2 +  sources for the exocytotic glutamate release from astrocytes. Neurochem. Int. (2009, in press). doi:10.1016/j.neuint.2008.12.018

    Google Scholar 

  17. De Pittà, M., Volman, V., Levine, H., Pioggia, G., De Rossi, D., Ben-Jacob, E.: Coexistence of amplitude and frequency modulations in intracellular calcium dynamics. Phys. Rev. E 77, 030903-R (2008)

    Google Scholar 

  18. Mothet, J.P., Pollegioni, L., Ouanounou, G., Martineau, M., Fossier, P., Baux, G.: Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter d-serine. Proc. Natl. Acad. Sci. U. S. A. 102, 5606–5611 (2005). doi:10.1073/pnas.0408483102

    Article  ADS  Google Scholar 

  19. Newman, E.A.: Glial cell inhibition of neurons by release of ATP. J. Neurosci. 23, 1659–1666 (2003)

    Google Scholar 

  20. Charles, A.C.: Glia-neuron intercellular calcium signaling. Dev. Neurosci. 16, 196–206 (1994). doi:10.1159/000112107

    Article  Google Scholar 

  21. Parpura, V., Basarsky, T.A., Liu, F., Jeftinija, K., Jeftinija, S., Haydon, P.G.: Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744–747 (1994). doi:10.1038/369744a0

    Article  ADS  Google Scholar 

  22. Hassinger, T.D., Atkinson, P.B., Strecker, G.J., Whalen, L.R., Dudek, F.E., Kossel, A.H., Kater, S.B.: Evidence for glutamate-mediated activation of hippocampal neurons by glial calcium waves. J. Neurobiol. 28, 159–170 (1995). doi:10.1002/neu.480280204

    Article  Google Scholar 

  23. Bezzi, P., Carmignoto, G., Pasti, L., Vesce, S., Rossi, D., Rizzini, B.L., Pozzan, T., Volterra, A.: Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391, 281–285 (1998). doi:10.1038/34651

    Article  ADS  Google Scholar 

  24. Fellin, T., Pascual, O., Gobbo, S., Pozzan, T., Haydon, P.G., Carmignoto, G.: Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43, 729–743 (2004). doi:10.1016/j.neuron.2004.08.011

    Article  Google Scholar 

  25. Bartlett, T.E., Bannister, N.J., Collet, V.J., Dargan, S.L., Massey, P.V., Bortolotto, Z.A., Fitzjohn, S.M., Bashir, Z.I., Collingridge, G.L., Lodge, D.: Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-week old rat hippocampus. Neuropharmacology 52, 60–70 (2007). doi:10.1016/j.neuropharm.2006.07.013

    Article  Google Scholar 

  26. Dingledine, R., Borges, K., Bowie, D., Traynelis, S.F.: The glutamate receptor ion channels. Pharmacol. Rev. 51, 7–61 (1999)

    Google Scholar 

  27. Araque, A., Parpura, V., Sanzgiri, R.P., Haydon, P.G.: Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur. J. Neurosci. 10, 2129–2142 (1998). doi:10.1046/j.1460-9568.1998.00221.x

    Article  Google Scholar 

  28. Parri, H.R., Gould, T.M., Crunelli, V.: Spontaneous astrocytic Ca2 +  oscillations in situ drive NMDAR-mediated neuronal excitation. Nat. Neurosci. 4, 803–812 (2001). doi:10.1038/90507

    Article  Google Scholar 

  29. Angulo, M.C., Kozlov, A.S., Charpak, S., Audinat, E.: Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J. Neurosci. 24, 6920–6927 (2004). doi:10.1523/JNEUROSCI.0473-04.2004

    Article  Google Scholar 

  30. Fellin, T.: Communication between neurons and astrocytes: relevance to the modulation of synaptic and network activity. J. Neurochem. 108, 533–544 (2009). doi:10.1111/j.1471-4159.2008.05830.x

    Article  Google Scholar 

  31. Volman, V., Ben-Jacob, E., Levine, H.: The astrocyte as a gatekeeper of synaptic information transfer. Neural Comput. 19, 303–326 (2007). doi:10.1162/neco.2007.19.2.303

    Article  MATH  MathSciNet  Google Scholar 

  32. Perea, G., Araque, A.: Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317, 1083–1086 (2007). doi:10.1126/science.1144640

    Article  ADS  Google Scholar 

  33. Gibbs, M.E., Hutchinson, D., Hertz, L.: Astrocytic involvement in learning and memory consolidation. Neurosci. Biobehav. Rev. 32, 927–944 (2008). doi:10.1016/j.neubiorev.2008.02.001

    Article  Google Scholar 

  34. Caudle, R.M.: Memory in astrocytes: a hypothesis. Theor. Biol. Med. Model. 3, 2 (2006). doi:10.1186/1742-4682-3-2

    Article  Google Scholar 

  35. Schummers, J., Yu, H., Sur, M.: Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320, 1638–1643 (2008). doi:10.1126/science.1156120

    Article  ADS  Google Scholar 

  36. Tian, G., Azmi, H., Takano, T., Xu, Q., Peng, W., Lin, J., Oberheim, N., Lou, N., Wang, X., Zielke, H., Kang, J., Nedergaard, M.: An astrocytic basis of epilepsy. Nat. Med. 11, 973–981 (2005)

    Google Scholar 

  37. Silchenko, A.N., Tass, P.A.: Computational modeling of paroxysmal depolarization shifts in neurons induced by the glutamate release from astrocytes. Biol. Cybern. 98, 61–74 (2008). doi:10.1007/s00422-007-0196-7

    Article  MATH  Google Scholar 

  38. Halassa, M., Florian, C., Fellin, T., Munoz, J., Lee, S., Abel, T., Haydon, P., Frank, M.: Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61, 213–219 (2009). doi:10.1016/j.neuron.2008.11.024

    Article  Google Scholar 

  39. Pereira Jr., A.: Astrocyte-trapped calcium ions: the hypothesis of a quantum-like conscious protectorate. Quantum Biosystems 2, 80–92 (2007)

    Google Scholar 

  40. Wulff, P., Goetz, T., Leppä, E., Linden, A.M., Renzi, M., Swinny, J.D., Vekovischeva, O.Y., Sieghart, W., Somogyi, P., Korpi, E.R., Farrant, M., Wisden, W.: From synapse to behavior: rapid modulation of defined neuronal types with engineered GABAA receptors. Nat. Neurosci. 10, 923–929 (2007). doi:10.1038/nn1927

    Article  Google Scholar 

  41. Logothetis, N.K., Wandell, B.A.: Interpreting the BOLD signal. Annu. Rev. Physiol. 66, 735–769 (2004). doi:10.1146/annurev.physiol.66.082602.092845

    Article  Google Scholar 

  42. Logothetis, N.K., Pfeuffer, J.: On the nature of BOLD fMRI contrast mechanism. Magn. Reson. Imaging 22, 1517–1531 (2004). doi:10.1016/j.mri.2004.10.018

    Article  Google Scholar 

  43. Logothetis, N.K., Pauls, J., Augath, M., Trinath, T., Oeltermann, A.: Neurophysiological investigation of the basis of the fMRI signal. Nature 412, 150–157 (2001). doi:10.1038/35084005

    Article  ADS  Google Scholar 

  44. Zonta, M., Angulo, M.C., Gobbo, S., Rosengarten, B., Hossmann, K.A., Pozzan, T., Carmignoto, G.: Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat. Neurosci. 6, 43–50 (2003). doi:10.1038/nn980

    Article  Google Scholar 

  45. Filosa, J.A., Bonev, A.D., Nelson, M.T.: Calcium dynamics in cortical astrocytes and arterioles during neurovascular coupling. Circ. Res. 95, e73–e81 (2004). doi:10.1161/01.RES.0000148636.60732.2e

    Article  Google Scholar 

  46. Metea, M.R., Newman, E.A.: Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J. Neurosci. 26, 2862–2870 (2006). doi:10.1523/JNEUROSCI.4048-05.2006

    Article  Google Scholar 

  47. Takano, T., Tian, G.F., Peng, W., Lou, N., Libionka, W., Han, X., Nedergaard, M.: Astrocyte-mediated control of cerebral blood flow. Nat. Neurosci. 9, 159–161 (2006). doi:10.1038/nn1623

    Article  Google Scholar 

  48. Haynes, J.D., Rees, G.: Decoding mental states from brain activity in humans. Nat. Rev. Neurosci. 7, 523–534 (2006). doi:10.1038/nrn1931

    Article  Google Scholar 

  49. Kamitani, Y., Tong, F.: Decoding the visual and subjective contents of the human brain. Nat. Neurosci. 8, 679–685 (2005). doi:10.1038/nn1444

    Article  Google Scholar 

  50. Rosch, E.: Cognitive representations of semantic categories. J. Exp. Psychol. (Gen.) 104, 192–233 (1975). doi:10.1037/0096-3445.104.3.192

    Article  Google Scholar 

  51. Gärdenfors, P.: Conceptual Spaces: The Geometry of Thought. MIT Press, Cambridge (2000)

    Google Scholar 

  52. Gärdenfors, P.: Conceptual spaces as a framework for knowledge representations. Mind Matter 2, 9–27 (2004)

    Google Scholar 

  53. Niessing, J., Ebisch, B., Schmidt, K.E., Niessing, M., Singer, W., Galuske, R.A.: Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309, 948–951 (2005). doi:10.1126/science.1110948

    Article  ADS  Google Scholar 

  54. Jermakowicz, W.J., Casagrande, V.A.: Neural networks a century after Cajal. Brain Res. Rev. 55, 264–284 (2007). doi:10.1016/j.brainresrev.2007.06.003

    Article  Google Scholar 

  55. Samonds, J.M., Bonds, A.B.: Gamma oscillation maintains stimulus structure-dependent synchronization in cat visual cortex. J. Neurophysiol. 93, 223–236 (2005). doi:10.1152/jn.00548.2004

    Article  Google Scholar 

  56. Izhikevich, E.: Polychronization: computation with spikes. Neural Comput. 18, 245–282 (2006). doi:10.1162/089976606775093882

    Article  MATH  MathSciNet  Google Scholar 

  57. Abeles, M.: Corticonics: Neural Circuits of the Cerebral Cortex. Cambridge University Press, New York (1991)

    Google Scholar 

  58. Treisman, A.: Solutions to the binding problem: progress through controversy and convergence. Neuron 24, 105–110 (1999). doi:10.1016/S0896-6273(00)80826-0

    Article  Google Scholar 

  59. Buzsáki, G.: The structure of consciousness. Nature 446, 267 (2007). doi:10.1038/446267a

    Article  ADS  Google Scholar 

  60. Roskies, A.L.: The binding problem. Neuron 24, 7–9 (1999). doi:10.1016/S0896-6273(00)80817-X

    Article  Google Scholar 

  61. Seth, A.K., McKinstry, J.L., Edelman, G.M., Krichmar, J.L.: Visual binding through reentrant connectivity and dynamic synchronization in a brain-based device. Cereb. Cortex 14, 1185–1199 (2004). doi:10.1093/cercor/bhh079

    Article  Google Scholar 

  62. Bienenstock, E.: A model of neocortex. Network: Comput. Neural Syst. 6, 179–224 (1995)

    Article  MATH  Google Scholar 

  63. Seth, A.K., Izhikevich, E., Reeke, G.N., Edelman, G.M.: Theories and measures of consciousness: an extended framework. Proc. Natl. Acad. Sci. U. S. A. 103, 10799–10804 (2006). doi:10.1073/pnas.0604347103

    Article  ADS  Google Scholar 

  64. Nadkarni, S., Jung, P.: Spontaneous oscillations of dressed neurons: a new mechanism for epilepsy? Phys. Rev. Lett. 91, 268101 (2003). doi:10.1103/PhysRevLett.91.268101

    Article  ADS  Google Scholar 

  65. Basar, E., Basar-Eroglu, S., Karaka, S., Schurmann, M.: Gamma, alpha, delta, and theta oscillations govern cognitive processes. Int. J. Psychophysiol. 39, 241–248 (1991). doi:10.1016/S0167-8760(00)00145-8

    Article  Google Scholar 

  66. Blumenfeld, H., Taylor, J.: Why do seizures cause loss of consciousness? Neurosci. 9, 301–310 (2003). doi:10.1177/1073858403255624

    Article  Google Scholar 

  67. König, P., Engel, A.K., Singer, W.: Relation between oscillatory activity and long-range synchronization in cat visual cortex. Proc. Natl. Acad. Sci. U. S. A. 92, 290–294 (1995). doi:10.1073/pnas.92.1.290

    Article  ADS  Google Scholar 

  68. Engel, A.K., Singer, W.: Temporal binding and the neural correlates of sensory awareness. Trends Cogn. Sci. 5, 16–25 (2001). doi:10.1016/S1364-6613(00)01568-0

    Article  Google Scholar 

  69. Melloni, L., Molina, C., Pena, M., Torres, D., Singer, W., Rodriguez, E.: Synchronization of neural activity across cortical areas correlates with conscious perception. J. Neurosci. 27, 2858–2865 (2007). doi:10.1523/JNEUROSCI.4623-06.2007

    Article  Google Scholar 

  70. Palva, S., Palva, J.M.: New vistas for alpha-frequency band oscillations. Trends Neurosci. 30, 150–158 (2007). doi:10.1016/j.tins.2007.02.001

    Article  Google Scholar 

  71. Sandkühler, S., Bhattacharya, J.: Deconstructing insight: EEG correlates of insightful problem solving. PLoS One 3, e1459 (2008). doi:10.1371/journal.pone.0001459

    Article  ADS  Google Scholar 

  72. Jensen, O.: Reading the hippocampal code by theta phase-locking. Trends Cogn. Sci. 9, 551–554 (2005). doi:10.1016/j.tics.2005.10.003

    Article  Google Scholar 

  73. Tononi, G.: An information integration theory of consciousness. BMC Neurosci. 5, 42 (2004). doi:10.1186/1471-2202-5-42

    Article  Google Scholar 

  74. Tononi, G.: Consciousness, information integration, and the brain. Prog. Brain Res. 150, 109–126 (2005). doi:10.1016/S0079-6123(05)50009-8

    Article  Google Scholar 

  75. Rocha, A., Massad, E., Pereira, A. Jr.: The Brain: From Fuzzy Grammar to Quantum Computing. Springer, Berlin (2005)

    MATH  Google Scholar 

  76. Kielpinski, D., Monroe, C., Wineland, D.J.: Architecture for a large-scale ion-trap quantum computer. Nature 417, 709–711 (2002)

    Article  ADS  Google Scholar 

  77. Hughes, R.J., James, D.F.V., Gomez, J.J., Gulley, M.S., Holzscheiter, M.H., Kwiat, P.G., Lamoreaux, S.K., Peterson, C.G., Sandberg, V.D., Schauer, M.M., Simmons, C.M., Thorburn, C.E., Tupa, D., Wang, P.Z.,White, A.G.: The Los Alamos trapped ion quantum computer experiment. Prog. Phys. 46, 329–361 (1998)

    Google Scholar 

  78. Reyes, R.C., Parpura, V.: Models of astrocytic Ca2 +  dynamics and epilepsy. Drug Discov. Today 5, 13–18 (2008)

    Google Scholar 

  79. Hirase, H., Qian, L., Barthó, P., Buzsáki, G.: Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol. 4, e96 (2004). doi:10.1371/journal.pbio.0020096

    Article  Google Scholar 

  80. Roth, B.J., Yagodin, S.V., Holtzclaw, L., Russell, J.T.: A mathematical model of agonist-induced propagation of calcium waves in astrocytes. Cell Calcium 17, 53–64 (1995). doi:10.1016/0143-4160(95)90102-7

    Article  Google Scholar 

  81. Halassa, M.M., Fellin, T., Haydon, P.G.: The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol. Med. 13, 54–63 (2007). doi:10.1016/j.molmed.2006.12.005

    Article  Google Scholar 

  82. McNally, L., Bhagwagar, Z., Hannestad, J.: Inflammation, glutamate, and glia in depression: a literature review. CNS Spectr. 13, 501–510 (2008)

    Google Scholar 

  83. De Keyser, J., Mostert, J.P., Koch, M.W.: Dysfunctional astrocytes as key players in the pathogenesis of central nervous system disorders. J. Neurol. Sci. 267, 3–16 (2008). doi:10.1016/j.jns.2007.08.044

    Article  Google Scholar 

  84. Laming, P.R.: Potassium signaling in the brain: its role in behaviour. Neurochem. Int. 36, 271–290 (2000). doi:10.1016/S0197-0186(99)00136-9

    Article  ADS  Google Scholar 

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Acknowledgements

The authors thank the Brazilian National Research Council (CNPQ) for a grant conceded to APJ; Dr. Bernard Baars, for discussion of an early draft of this paper in his Advanced Seminar (an activity of Consciousness: the Webcourse, supported by the Univ. of Arizona), and two anonymous reviewers for their constructive criticisms and suggestions.

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  1. Institute of Biosciences, São Paulo State University (UNESP), Botucatu, SP, Brasil

    Alfredo Pereira Jr.

  2. University of Marília (Unimar), Marília, SP, Brasil

    Fábio Augusto Furlan

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Pereira, A., Furlan, F.A. On the role of synchrony for neuron–astrocyte interactions and perceptual conscious processing. J Biol Phys 35, 465–480 (2009). https://doi.org/10.1007/s10867-009-9147-y

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