Coherence resonance in bursting neural networks.

Synchronized neural bursts are one of the most noticeable dynamic features of neural networks, being essential for various phenomena in neuroscience, yet their complex dynamics are not well understood. With extrinsic electrical and optical manipulations on cultured neural networks, we demonstrate that the regularity (or randomness) of burst sequences is in many cases determined by a (few) low-dimensional attractor(s) working under strong neural noise. Moreover, there is an optimal level of noise strength at which the regularity of the interburst interval sequence becomes maximal-a phenomenon of coherence resonance. The experimental observations are successfully reproduced through computer simulations on a well-established neural network model, suggesting that the same phenomena may occur in many in vivo as well as in vitro neural networks.

[1]  Lief E. Fenno,et al.  Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins , 2011, Nature Methods.

[2]  Eric Vanden-Eijnden,et al.  Two distinct mechanisms of coherence in randomly perturbed dynamical systems. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[3]  L. M. Ward,et al.  Synchronous neural oscillations and cognitive processes , 2003, Trends in Cognitive Sciences.

[4]  D. McCormick,et al.  On the cellular and network bases of epileptic seizures. , 2001, Annual review of physiology.

[5]  Yasuhiko Jimbo,et al.  Analytical characterization of spontaneous firing in networks of developing rat cultured cortical neurons. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[6]  J. Kurths,et al.  Coherence Resonance in a Noise-Driven Excitable System , 1997 .

[7]  Eugene M. Izhikevich,et al.  Simple model of spiking neurons , 2003, IEEE Trans. Neural Networks.

[8]  Mark D. McDonnell,et al.  The benefits of noise in neural systems: bridging theory and experiment , 2011, Nature Reviews Neuroscience.

[9]  Wim L. C. Rutten,et al.  Long-term characterization of firing dynamics of spontaneous bursts in cultured neural networks , 2004, IEEE Transactions on Biomedical Engineering.

[10]  Rachel Kuske,et al.  Noise-Induced Coherence and Network Oscillations in a Reduced Bursting Model , 2006, Bulletin of mathematical biology.

[11]  Yuzuru Takamura,et al.  Investigating neuronal activity with planar microelectrode arrays: achievements and new perspectives. , 2005, Journal of bioscience and bioengineering.

[12]  Lutz Schimansky-Geier,et al.  Maximizing spike train coherence or incoherence in the leaky integrate-and-fire model. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[13]  Jan Stegenga,et al.  Network bursts in cortical cultures are best simulated using pacemaker neurons and adaptive synapses , 2010, Biological Cybernetics.

[14]  D Popivanov,et al.  Tracking EEG signal dynamics during mental tasks. A combined linear/nonlinear approach. , 1998, IEEE engineering in medicine and biology magazine : the quarterly magazine of the Engineering in Medicine & Biology Society.

[15]  A. Longtin.  AUTONOMOUS STOCHASTIC RESONANCE IN BURSTING NEURONS , 1997 .

[16]  B H Jansen,et al.  Quantitative analysis of electroencephalograms: is there chaos in the future? , 1991, International journal of bio-medical computing.

[17]  Jyh-Jang Sun,et al.  Three Patterns of Oscillatory Activity Differentially Synchronize Developing Neocortical Networks In Vivo , 2009, The Journal of Neuroscience.

[18]  Fabrizio Gabbiani,et al.  Burst firing in sensory systems , 2004, Nature Reviews Neuroscience.

[19]  Karl Deisseroth,et al.  Optogenetics in Neural Systems , 2011, Neuron.

[20]  W. Freeman,et al.  How brains make chaos in order to make sense of the world , 1987, Behavioral and Brain Sciences.

[21]  M. Steriade.  Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. , 1997, Cerebral cortex.

[22]  Michael J. O'Donovan,et al.  The Role of Activity-Dependent Network Depression in the Expression and Self-Regulation of Spontaneous Activity in the Developing Spinal Cord , 2001, The Journal of Neuroscience.

[23]  Joon Ho Choi,et al.  Dynamic transitions among multiple oscillators of synchronized bursts in cultured neural networks , 2014 .

[24]  A. Faisal,et al.  Noise in the nervous system , 2008, Nature Reviews Neuroscience.

[25]  Joon Ho Choi,et al.  Modulating the precision of recurrent bursts in cultured neural networks. , 2012, Physical review letters.

[26]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[27]  E. Vaadia,et al.  Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates , 1998, Trends in Neurosciences.

[28]  J. Pine.  Recording action potentials from cultured neurons with extracellular microcircuit electrodes , 1980, Journal of Neuroscience Methods.

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

[30]  Ivan Cohen,et al.  Threshold Behavior in the Initiation of Hippocampal Population Bursts , 2006, Neuron.

[31]  Kevin L. Briggman,et al.  Multifunctional pattern-generating circuits. , 2008, Annual review of neuroscience.

[32]  H. Robinson,et al.  Spontaneous periodic synchronized bursting during formation of mature patterns of connections in cortical cultures , 1996, Neuroscience Letters.

[33]  Jin Hee Hong,et al.  Serotonin-2C receptor involved serotonin-induced Ca2+ mobilisations in neuronal progenitors and neurons in rat suprachiasmatic nucleus , 2014, Scientific Reports.

[34]  Alexander B. Neiman,et al.  COHERENCE RESONANCE AT NOISY PRECURSORS OF BIFURCATIONS IN NONLINEAR DYNAMICAL SYSTEMS , 1997 .

[35]  R. Segev,et al.  Long term behavior of lithographically prepared in vitro neuronal networks. , 2002, Physical review letters.