Modeling brain activation patterns for the default and cognitive states

We argue that spatial patterns of cortical activation observed with EEG, MEG and fMRI might arise from spontaneous self-organisation of interacting populations of excitatory and inhibitory neurons. We examine the dynamical behavior of a mean-field cortical model that includes chemical and electrical (gap-junction) synapses, focusing on two limiting cases: the "slow-soma" limit with slow voltage feedback from soma to dendrite, and the "fast-soma" limit in which the feedback action of soma voltage onto dendrite reversal potentials is instantaneous. For slow soma-dendrite feedback, we find a low-frequency (approximately 1 Hz) dynamic Hopf instability, and a stationary Turing instability that catalyzes formation of patterned distributions of cortical firing-rate activity with pattern wavelength approximately 2 cm. Turing instability can only be triggered when gap-junction diffusion between inhibitory neurons is strong, but patterning is destroyed if the tonic level of subcortical excitation is raised sufficiently. Interaction between the Hopf and Turing instabilities may describe the non-cognitive background or "default" state of the brain, as observed by BOLD imaging. In the fast-soma limit, the model predicts a high-frequency Hopf (approximately 35 Hz) instability, and a traveling-wave gamma-band instability that manifests as a 2-D standing-wave pattern oscillating in place at approximately 30 Hz. Small levels of inhibitory diffusion enhance and broaden the definition of the gamma antinodal regions by suppressing higher-frequency spatial modes, but gamma emergence is not contingent on the presence of inhibitory gap junctions; higher levels of diffusion suppress gamma activity. Fast-soma instabilities are enhanced by increased subcortical stimulation. Prompt soma-dendrite feedback may be an essential component of the genesis and large-scale cortical synchrony of gamma activity observed at the point of cognition.

[1]  Enhua Shen,et al.  Advances in Cognitive Neurodynamics ICCN 2007 , 2008 .

[2]  D. Alistair Steyn-Ross,et al.  The K-complex and slow oscillation in terms of a mean-field cortical model , 2006, Journal of Computational Neuroscience.

[3]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[4]  W. Singer,et al.  Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology , 2006, Neuron.

[5]  J. Sleigh,et al.  The Sleep Cycle Modelled as a Cortical Phase Transition , 2005, Journal of biological physics.

[6]  M. Raichle Behind the scenes of functional brain imaging: a historical and physiological perspective. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[8]  H. Haken,et al.  Field Theory of Electromagnetic Brain Activity. , 1996, Physical review letters.

[9]  D A Steyn-Ross,et al.  Predictions and simulations of cortical dynamics during natural sleep using a continuum approach. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[10]  P. Somogyi,et al.  Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons , 2000, Nature Neuroscience.

[11]  P. Robinson,et al.  Prediction of electroencephalographic spectra from neurophysiology. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[12]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[13]  W. Senn,et al.  Dopamine increases the gain of the input–output response of rat prefrontal pyramidal neurons. J. Neurophysiol. (in press). doi: 10.1152/jn.01098.2007 [epub ahead of print , 2008 .

[14]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[15]  W. Singer,et al.  Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[16]  A. Zhabotinsky,et al.  Pattern formation arising from interactions between Turing and wave instabilities , 2002 .

[17]  D. Liley,et al.  Theoretical electroencephalogram stationary spectrum for a white-noise-driven cortex: evidence for a general anesthetic-induced phase transition. , 1999, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[18]  P. Fransson Spontaneous low‐frequency BOLD signal fluctuations: An fMRI investigation of the resting‐state default mode of brain function hypothesis , 2005, Human brain mapping.

[19]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[20]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[21]  Hannah Monyer,et al.  Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. Cross,et al.  Pattern formation outside of equilibrium , 1993 .

[23]  Karl J. Friston Functional and effective connectivity in neuroimaging: A synthesis , 1994 .

[24]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[25]  U. Habel,et al.  Neural correlates of working memory dysfunction in first-episode schizophrenia patients: An fMRI multi-center study , 2007, Schizophrenia Research.

[26]  B. Connors,et al.  A network of electrically coupled interneurons drives synchronized inhibition in neocortex , 2000, Nature Neuroscience.

[27]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[28]  D A Steyn-Ross,et al.  Toward a theory of the general-anesthetic-induced phase transition of the cerebral cortex. I. A thermodynamics analogy. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[29]  James J. Wright,et al.  Propagation and stability of waves of electrical activity in the cerebral cortex , 1997 .

[30]  W. Singer,et al.  Dysfunctional Long-Range Coordination of Neural Activity during Gestalt Perception in Schizophrenia , 2006, The Journal of Neuroscience.

[31]  J. Cowan,et al.  Large Scale Spatially Organized Activity in Neural Nets , 1980 .

[32]  Karl J. Friston Imaging neuroscience: principles or maps? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Donald O. Walter,et al.  Mass action in the nervous system , 1975 .

[34]  Peter A. Robinson,et al.  Visual gamma oscillations: waves, correlations, and other phenomena, including comparison with experimental data , 2007, Biological Cybernetics.

[35]  R. Bluhm,et al.  Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network. , 2007, Schizophrenia bulletin.

[36]  J. Sleigh,et al.  Toward a theory of the general-anesthetic-induced phase transition of the cerebral cortex. II. Numerical simulations, spectral entropy, and correlation times. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[37]  W. Singer,et al.  Gap Junctions among Dendrites of Cortical GABAergic Neurons Establish a Dense and Widespread Intercolumnar Network , 2006, The Journal of Neuroscience.

[38]  Fiona E. N. LeBeau,et al.  A model of gamma‐frequency network oscillations induced in the rat CA3 region by carbachol in vitro , 2000, The European journal of neuroscience.

[39]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[40]  D. Liley,et al.  Modeling electrocortical activity through improved local approximations of integral neural field equations. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[41]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[42]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[43]  Thomas Wennekers,et al.  Pattern formation in intracortical neuronal fields , 2003, Network.

[44]  R. Weiler,et al.  Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  F. H. Lopes da Silva,et al.  Model of brain rhythmic activity , 1974, Kybernetik.

[46]  N Kopell,et al.  Gap Junctions between Interneuron Dendrites Can Enhance Synchrony of Gamma Oscillations in Distributed Networks , 2001, The Journal of Neuroscience.

[47]  Hannah Monyer,et al.  A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[48]  M. Bennett,et al.  Electrical Coupling and Neuronal Synchronization in the Mammalian Brain , 2004, Neuron.

[49]  Jesper Tegnér,et al.  Electrotonic Signals along Intracellular Membranes May Interconnect Dendritic Spines and Nucleus , 2008, PLoS Comput. Biol..

[50]  David T. J. Liley,et al.  A continuum theory of electro-cortical activity , 1999, Neurocomputing.

[51]  S. Hestrin,et al.  A network of fast-spiking cells in the neocortex connected by electrical synapses , 1999, Nature.

[52]  B. Ermentrout Neural networks as spatio-temporal pattern-forming systems , 1998 .

[53]  W. Deng,et al.  Decreased Spontaneous Low-frequency BOLD Signal Fluctuation in First-episode Treatment-naive Schizophrenia * , 2007 .

[54]  Marcus T. Wilson,et al.  General Anesthetic-induced Seizures Can Be Explained by a Mean-field Model of Cortical Dynamics , 2006, Anesthesiology.

[55]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[56]  H. Markram The Blue Brain Project , 2006, Nature Reviews Neuroscience.

[57]  J. Cowan,et al.  A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue , 1973, Kybernetik.

[58]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[59]  P. Robinson,et al.  Mechanisms of cortical electrical activity and emergence of gamma rhythm. , 2000, Journal of theoretical biology.

[60]  J. J. Wright,et al.  Contribution of lateral interactions in V1 to organization of response properties , 2006, Vision Research.

[61]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[62]  A. M. Turing,et al.  The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[63]  C. L. Chapman,et al.  Toward an integrated continuum model of cerebral dynamics: the cerebral rhythms, synchronous oscillation and cortical stability. , 2001, Bio Systems.

[64]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[65]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[66]  J A Kelso,et al.  Spatiotemporal pattern formation in neural systems with heterogeneous connection topologies. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[67]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

[68]  Moira L Steyn-Ross,et al.  Gap junctions mediate large-scale Turing structures in a mean-field cortex driven by subcortical noise. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[69]  J. Fermaglich Electric Fields of the Brain: The Neurophysics of EEG , 1982 .

[70]  P. Robinson Patchy propagators, brain dynamics, and the generation of spatially structured gamma oscillations. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[71]  P. Glansdorff,et al.  Thermodynamic theory of structure, stability and fluctuations , 1971 .

[72]  Bressloff New mechanism for neural pattern formation. , 1996, Physical review letters.

[73]  Interacting Turing and Hopf Instabilities Drive Pattern Formation in a Noise-Driven Model Cortex , 2008 .

[74]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[75]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[76]  P. Robinson,et al.  Dynamics of large-scale brain activity in normal arousal states and epileptic seizures. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

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