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

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.

[1]  Eduardo D. Martín,et al.  Synaptically Released Acetylcholine Evokes Ca2+Elevations in Astrocytes in Hippocampal Slices , 2002, The Journal of Neuroscience.

[2]  Peter Gärdenfors,et al.  Conceptual spaces - the geometry of thought , 2000 .

[3]  Loredano Pollegioni,et al.  Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Todd A Fiacco,et al.  What Is the Role of Astrocyte Calcium in Neurophysiology? , 2008, Neuron.

[5]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[6]  G. Tononi.  Consciousness, information integration, and the brain. , 2005, Progress in brain research.

[7]  A. B. Bonds,et al.  Gamma oscillation maintains stimulus structure-dependent synchronization in cat visual cortex. , 2005, Journal of neurophysiology.

[8]  V. D. Sandberg,et al.  The Los Alamos Trapped Ion Quantum Computer Experiment , 1998 .

[9]  Vladimir Parpura,et al.  The trinity of Ca2+ sources for the exocytotic glutamate release from astrocytes , 2009, Neurochemistry International.

[10]  A. Charles,et al.  Glia-neuron intercellular calcium signaling. , 1994, Developmental neuroscience.

[11]  R. C. Reyes,et al.  Models of astrocytic Ca dynamics and epilepsy. , 2008, Drug discovery today. Disease models.

[12]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[13]  T. Takano,et al.  Astrocyte-mediated control of cerebral blood flow , 2006, Nature Neuroscience.

[14]  G. Perea,et al.  Properties of Synaptically Evoked Astrocyte Calcium Signal Reveal Synaptic Information Processing by Astrocytes , 2005, The Journal of Neuroscience.

[15]  E. Ben-Jacob,et al.  Coexistence of amplitude and frequency modulations in intracellular calcium dynamics. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[16]  Ole Jensen,et al.  Reading the hippocampal code by theta phase-locking , 2005, Trends in Cognitive Sciences.

[17]  M. C. Angulo,et al.  Glutamate Released from Glial Cells Synchronizes Neuronal Activity in the Hippocampus , 2004, The Journal of Neuroscience.

[18]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[19]  Michael M. Halassa,et al.  The tripartite synapse: roles for gliotransmission in health and disease. , 2007, Trends in molecular medicine.

[20]  S. Finkbeiner,et al.  Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. , 1990, Science.

[21]  A. Charles,et al.  Intercellular signaling in glial cells: Calcium waves and oscillations in response to mechanical stimulation and glutamate , 1991, Neuron.

[22]  Alfredo Pereira,et al.  Astrocyte-Trapped Calcium Ions: the Hypothesis of a Quantum-Like Conscious Protectorate , 2007 .

[23]  T. Pozzan,et al.  Intracellular Calcium Oscillations in Astrocytes: A Highly Plastic, Bidirectional Form of Communication between Neurons and Astrocytes In Situ , 1997, The Journal of Neuroscience.

[24]  J. Palva,et al.  New vistas for α-frequency band oscillations , 2007, Trends in Neurosciences.

[25]  K. McCarthy,et al.  Hippocampal Astrocytes In Situ Respond to Glutamate Released from Synaptic Terminals , 1996, The Journal of Neuroscience.

[26]  Hal Blumenfeld,et al.  Why do Seizures Cause Loss of Consciousness? , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[27]  Eric A Newman,et al.  Glial Cell Inhibition of Neurons by Release of ATP , 2003, The Journal of Neuroscience.

[28]  S. Goldman,et al.  Astrocyte-mediated potentiation of inhibitory synaptic transmission , 1998, Nature Neuroscience.

[29]  P. Gärdenfors.  Conceptual spaces as a framework for knowledge representation , 2004 .

[30]  H. Parri,et al.  Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation , 2001, Nature Neuroscience.

[31]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[32]  G. Tononi.  An information integration theory of consciousness , 2004, BMC Neuroscience.

[33]  Anil K Seth,et al.  Theories and measures of consciousness: an extended framework. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[34]  W. Singer,et al.  Relation between oscillatory activity and long-range synchronization in cat visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[35]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[36]  A. Roskies.  The Binding Problem , 1999, Neuron.

[37]  S. B. Kater,et al.  Evidence for glutamate-mediated activation of hippocampal neurons by glial calcium waves. , 1995, Journal of neurobiology.

[38]  Walter J. Jermakowicz,et al.  Neural networks a century after Cajal , 2007, Brain Research Reviews.

[39]  G. Perea,et al.  Astrocytes Potentiate Transmitter Release at Single Hippocampal Synapses , 2007, Science.

[40]  R. Dingledine,et al.  The glutamate receptor ion channels. , 1999, Pharmacological reviews.

[41]  S. Nadkarni,et al.  Spontaneous oscillations of dressed neurons: a new mechanism for epilepsy? , 2003, Physical review letters.

[42]  T. Fellin,et al.  Communication between neurons and astrocytes: relevance to the modulation of synaptic and network activity , 2009, Journal of neurochemistry.

[43]  Michael M. Halassa,et al.  Synaptic Islands Defined by the Territory of a Single Astrocyte , 2007, The Journal of Neuroscience.

[44]  Eric A Newman,et al.  Glial Cells Dilate and Constrict Blood Vessels: A Mechanism of Neurovascular Coupling , 2006, The Journal of Neuroscience.

[45]  B. J. Roth,et al.  A mathematical model of agonist-induced propagation of calcium waves in astrocytes. , 1995, Cell calcium.

[46]  Leif Hertz,et al.  Astrocytic involvement in learning and memory consolidation , 2008, Neuroscience & Biobehavioral Reviews.

[47]  James M. Robertson.  The Astrocentric Hypothesis: proposed role of astrocytes in consciousness and memory formation , 2002, Journal of Physiology-Paris.

[48]  Fang Liu,et al.  Glutamate-mediated astrocyte–neuron signalling , 1994, Nature.

[49]  J. Bhattacharya,et al.  Deconstructing Insight: EEG Correlates of Insightful Problem Solving , 2008, PloS one.

[50]  E. Bienenstock.  A model of neocortex , 1995 .

[51]  Michael M. Halassa,et al.  Astrocytic Modulation of Sleep Homeostasis and Cognitive Consequences of Sleep Loss , 2009, Neuron.

[52]  György Buzsáki,et al.  The structure of consciousness , 2007, Nature.

[53]  S. Gobbo,et al.  Neuronal Synchrony Mediated by Astrocytic Glutamate through Activation of Extrasynaptic NMDA Receptors , 2004, Neuron.

[54]  G. Rees,et al.  Neuroimaging: Decoding mental states from brain activity in humans , 2006, Nature Reviews Neuroscience.

[55]  A. Araque,et al.  Tripartite synapses: glia, the unacknowledged partner , 1999, Trends in Neurosciences.

[56]  Nikos K Logothetis,et al.  On the nature of the BOLD fMRI contrast mechanism. , 2004, Magnetic resonance imaging.

[57]  Peter A. Tass,et al.  Computational modeling of paroxysmal depolarization shifts in neurons induced by the glutamate release from astrocytes , 2008, Biological Cybernetics.

[58]  A. Treisman.  Solutions to the Binding Problem Progress through Controversy and Convergence , 1999, Neuron.

[59]  A. Araque,et al.  Glutamate‐dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons , 1998, The European journal of neuroscience.

[60]  M. C. Angulo,et al.  Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation , 2003, Nature Neuroscience.

[61]  J. Mostert,et al.  Dysfunctional astrocytes as key players in the pathogenesis of central nervous system disorders , 2008, Journal of the Neurological Sciences.

[62]  W. Singer,et al.  Temporal binding and the neural correlates of sensory awareness , 2001, Trends in Cognitive Sciences.

[63]  P. Laming,et al.  Potassium signalling in the brain: its role in behaviour , 2000, Neurochemistry International.

[64]  G. Buzsáki,et al.  Calcium Dynamics of Cortical Astrocytic Networks In Vivo , 2004, PLoS biology.

[65]  D. De Rossi,et al.  Erratum: Coexistence of amplitude and frequency modulations in intracellular calcium dynamics [Phys. Rev. E 77, 030903(R) (2008)] , 2008 .

[66]  H. Berg,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S7 Tables S1 to S3 References Movies S1 to S6 Tuned Responses of Astrocytes and Their Influence on Hemodynamic Signals in the Visual Cortex , 2022 .

[67]  David Lodge,et al.  Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-week old rat hippocampus , 2007, Neuropharmacology.

[68]  E. Rosch.  Cognitive Representations of Semantic Categories. , 1975 .

[69]  C. Steinhäuser,et al.  Ion channels in glial cells , 2000, Brain Research Reviews.

[70]  J. Filosa,et al.  Calcium Dynamics in Cortical Astrocytes and Arterioles During Neurovascular Coupling , 2004, Circulation research.

[71]  Mark Ellisman,et al.  Protoplasmic Astrocytes in CA1 Stratum Radiatum Occupy Separate Anatomical Domains , 2002, The Journal of Neuroscience.

[72]  Zubin Bhagwagar,et al.  Inflammation, Glutamate, and Glia in Depression: A Literature Review , 2008, CNS Spectrums.

[73]  E. Basar,et al.  Gamma, alpha, delta, and theta oscillations govern cognitive processes. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[74]  R. Caudle,et al.  Memory in astrocytes: a hypothesis , 2006, Theoretical Biology and Medical Modelling.

[75]  C. Monroe,et al.  Architecture for a large-scale ion-trap quantum computer , 2002, Nature.

[76]  William Wisden,et al.  From synapse to behavior: rapid modulation of defined neuronal types with engineered GABAA receptors , 2007, Nature Neuroscience.

[77]  G. Edelman,et al.  Visual binding through reentrant connectivity and dynamic synchronization in a brain-based device. , 2004, Cerebral cortex.

[78]  W. Singer,et al.  Synchronization of Neural Activity across Cortical Areas Correlates with Conscious Perception , 2007, The Journal of Neuroscience.

[79]  D. Rossi,et al.  Another BOLD role for astrocytes: coupling blood flow to neural activity , 2006, Nature Neuroscience.

[80]  Tullio Pozzan,et al.  Prostaglandins stimulate calcium-dependent glutamate release in astrocytes , 1998, Nature.

[81]  Eduardo Massad,et al.  The Brain: Fuzzy Arithmetic to Quantum Computing , 2004 .

[82]  G. Carmignoto,et al.  Astrocyte control of synaptic transmission and neurovascular coupling. , 2006, Physiological reviews.

[83]  T. Takano,et al.  An astrocytic basis of epilepsy , 2005, Nature Medicine.

[84]  Eugene M. Izhikevich,et al.  Polychronization: Computation with Spikes , 2006, Neural Computation.

[85]  Eshel Ben-Jacob,et al.  The Astrocyte as a Gatekeeper of Synaptic Information Transfer , 2006, Neural Computation.