The Epileptic Thalamocortical Network is a Macroscopic Self-Sustained Oscillator: Evidence from Frequency-Locking Experiments in Rat Brains

The rhythmic activity observed in nervous systems, in particular in epilepsies and Parkinson's disease, has often been hypothesized to originate from a macroscopic self-sustained neural oscillator. However, this assumption has not been tested experimentally. Here we support this viewpoint with in vivo experiments in a rodent model of absence seizures, by demonstrating frequency locking to external periodic stimuli and finding the characteristic Arnold tongue. This result has important consequences for developing methods for the control of brain activity, such as seizure cancellation.

[1]  Kiyoshi Kotani,et al.  Population dynamics of the modified theta model: macroscopic phase reduction and bifurcation analysis link microscopic neuronal interactions to macroscopic gamma oscillation , 2014, Journal of The Royal Society Interface.

[2]  Jose Luis Perez Velazquez,et al.  The Brain-Behavior Continuum: The Subtle Transition Between Sanity and Insanity , 2011 .

[3]  Roberto Fernández Galán,et al.  Phase response curves in the characterization of epileptiform activity , 2007, BMC Neuroscience.

[4]  C. Marsden,et al.  Physiological and pathological tremors and rhythmic central motor control. , 2000, Brain : a journal of neurology.

[5]  Peter A. Tass,et al.  A model of desynchronizing deep brain stimulation with a demand-controlled coordinated reset of neural subpopulations , 2003, Biological Cybernetics.

[6]  A. Benabid,et al.  Deep brain stimulation , 2004, Cell and Tissue Research.

[7]  M. Rosenblum,et al.  Delayed feedback control of collective synchrony: an approach to suppression of pathological brain rhythms. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[8]  Xiao-Jing Wang Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[9]  J. Winn,et al.  Brain , 1878, The Lancet.

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

[11]  J. Parra,et al.  Epilepsies as Dynamical Diseases of Brain Systems: Basic Models of the Transition Between Normal and Epileptic Activity , 2003, Epilepsia.

[12]  Ilʹi︠a︡ Izrailevich Blekhman,et al.  Synchronization in science and technology , 1988 .

[13]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[14]  Leonidas D. Iasemidis,et al.  Control of Synchronization of Brain Dynamics leads to Control of Epileptic Seizures in Rodents , 2009, Int. J. Neural Syst..

[15]  Leonidas D. Iasemidis,et al.  Control Aspects of a Theoretical Model for Epileptic Seizures , 2006, Int. J. Bifurc. Chaos.

[16]  S. Strogatz,et al.  Stability diagram for the forced Kuramoto model. , 2008, Chaos.

[17]  R. Morison,et al.  MECHANISM OF THALAMOCORTICAL AUGMENTATION AND REPETITION , 1943 .

[18]  S. Strogatz From Kuramoto to Crawford: exploring the onset of synchronization in populations of coupled oscillators , 2000 .

[19]  Peter A. Tass,et al.  Development of Therapeutic Brain Stimulation Techniques with Methods from Nonlinear Dynamics and Statistical Physics , 2006, Int. J. Bifurc. Chaos.

[20]  R. L. Stratonovich,et al.  Topics in the theory of random noise , 1967 .

[21]  D. Kullmann,et al.  Oscillatory dynamics in the hippocampus support dentate gyrus–CA3 coupling , 2012, Nature Neuroscience.

[22]  Hidetsugu Sakaguchi,et al.  Cooperative Phenomena in Coupled Oscillator Systems under External Fields , 1988 .

[23]  R. G. Medhurst,et al.  Topics in the Theory of Random Noise , 1969 .

[24]  F. L. D. Silva,et al.  Dynamics of non-convulsive epileptic phenomena modeled by a bistable neuronal network , 2004, Neuroscience.

[25]  F. A. Gibbs,et al.  Epilepsy: a paroxysmal cerebral dysrhythmia , 2002, Epilepsy & Behavior.

[26]  Christian Hauptmann,et al.  Effective desynchronization by nonlinear delayed feedback. , 2005, Physical review letters.

[27]  A. Pérez-Villalba Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[28]  Grigory V. Bordyugov,et al.  Entrainment between Heart Rate and Weak Noninvasive Forcing , 2000, Int. J. Bifurc. Chaos.

[29]  L. Glass Synchronization and rhythmic processes in physiology , 2001, Nature.

[30]  O. Snead,et al.  Functional contribution of specific brain areas to absence seizures: role of thalamic gap‐junctional coupling , 2006, The European journal of neuroscience.

[31]  Anne Beuter,et al.  Tremor: Is Parkinson's disease a dynamical disease? , 1995, Chaos.

[32]  R. Spigler,et al.  The Kuramoto model: A simple paradigm for synchronization phenomena , 2005 .

[33]  M. Kramer,et al.  Epilepsy as a Disorder of Cortical Network Organization , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[34]  Bard Ermentrout,et al.  Type I Membranes, Phase Resetting Curves, and Synchrony , 1996, Neural Computation.

[35]  Leon D. Iasemidis,et al.  Epileptic seizure prediction and control , 2003, IEEE Transactions on Biomedical Engineering.

[36]  X.L. Chen,et al.  Deep Brain Stimulation , 2013, Interventional Neurology.

[37]  E. Ott,et al.  Long time evolution of phase oscillator systems. , 2009, Chaos.

[38]  N. Kopell We Got Rhythm: Dynamical Systems of the Nervous System , 1999 .

[39]  P. Landa Nonlinear Oscillations and Waves in Dynamical Systems , 1996 .

[40]  Yoshiki Kuramoto,et al.  Chemical Oscillations, Waves, and Turbulence , 1984, Springer Series in Synergetics.