Delay- and coupling-induced firing patterns in oscillatory neural loops.

For a feedforward loop of oscillatory Hodgkin-Huxley neurons interacting via excitatory chemical synapses, we show that a great variety of spatiotemporal periodic firing patterns can be encoded by properly chosen communication delays and synaptic weights, which contributes to the concept of temporal coding by spikes. These patterns can be obtained by a modulation of the multiple coexisting stable in-phase synchronized states or traveling waves propagating along or against the direction of coupling. We derive explicit conditions for the network parameters allowing us to achieve a desired pattern. Interestingly, whereas the delays directly affect the time differences between spikes of interacting neurons, the synaptic weights control the phase differences. Our results show that already such a simple neural circuit may unfold an impressive spike coding capability.

[1]  Khashayar Pakdaman,et al.  Transient oscillations in continuous-time excitatory ring neural networks with delay , 1997 .

[2]  C. Hammond,et al.  Latest view on the mechanism of action of deep brain stimulation , 2008, Movement disorders : official journal of the Movement Disorder Society.

[3]  Y. Dan,et al.  Spike timing-dependent plasticity: a Hebbian learning rule. , 2008, Annual review of neuroscience.

[4]  Evgueniy V. Lubenov,et al.  Decoupling through Synchrony in Neuronal Circuits with Propagation Delays , 2008, Neuron.

[5]  Jack D. Cowan,et al.  DYNAMICS OF SELF-ORGANIZED DELAY ADAPTATION , 1999 .

[6]  D. Hansel,et al.  Phase Dynamics for Weakly Coupled Hodgkin-Huxley Neurons , 1993 .

[7]  T. Sejnowski,et al.  Regulation of spike timing in visual cortical circuits , 2008, Nature Reviews Neuroscience.

[8]  Wei Zou,et al.  Splay States in a Ring of Coupled Oscillators: From Local to Global Coupling , 2009, SIAM J. Appl. Dyn. Syst..

[9]  Rajarshi Roy,et al.  Isochronal synchrony and bidirectional communication with delay-coupled nonlinear oscillators. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[10]  J. J. Hopfield,et al.  Pattern recognition computation using action potential timing for stimulus representation , 1995, Nature.

[11]  Steve M. Potter,et al.  Long-Term Activity-Dependent Plasticity of Action Potential Propagation Delay and Amplitude in Cortical Networks , 2008, PloS one.

[12]  Foss,et al.  Multistability and delayed recurrent loops. , 1996, Physical review letters.

[13]  Charles J. Wilson,et al.  Activity Patterns in a Model for the Subthalamopallidal Network of the Basal Ganglia , 2002, The Journal of Neuroscience.

[14]  S Yanchuk,et al.  Synchronizing distant nodes: a universal classification of networks. , 2010, Physical review letters.

[15]  Marc Timme,et al.  Breaking synchrony by heterogeneity in complex networks. , 2003, Physical review letters.

[16]  Raymond Kapral,et al.  Spatial and temporal structure in systems of coupled nonlinear oscillators , 1984 .

[17]  C. Mirasso,et al.  Chaos synchronization and spontaneous symmetry-breaking in symmetrically delay-coupled semiconductor lasers. , 2001, Physical review letters.

[18]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[19]  L. Glass,et al.  Instabilities of a propagating pulse in a ring of excitable media. , 1993, Physical review letters.

[20]  Bruno Cessac,et al.  Overview of facts and issues about neural coding by spikes , 2010, Journal of Physiology-Paris.

[21]  Edward Ott,et al.  Desynchronization waves and localized instabilities in oscillator arrays. , 2004, Physical review letters.

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

[23]  André Longtin,et al.  Noise-induced stabilization of bumps in systems with long-range spatial coupling , 2001 .

[24]  Christian Leibold,et al.  Spiking neurons learning phase delays: how mammals may develop auditory time-difference sensitivity. , 2005, Physical review letters.

[25]  M. Timme,et al.  Designing complex networks , 2006, q-bio/0606041.

[26]  Mary Silber,et al.  Feedback control of travelling wave solutions of the complex Ginzburg–Landau equation , 2003, nlin/0308021.

[27]  Frank Pasemann,et al.  Characterization of periodic attractors in neural ring networks , 1995, Neural Networks.

[28]  Vicente Pérez-Muñuzuri,et al.  Interaction of chaotic rotating waves in coupled rings of chaotic cells , 1999 .

[29]  G. Deuschl,et al.  Pathophysiology of Parkinson's disease: From clinical neurology to basic neuroscience and back , 2002, Movement disorders : official journal of the Movement Disorder Society.

[30]  György Buzsáki,et al.  Neural Syntax: Cell Assemblies, Synapsembles, and Readers , 2010, Neuron.

[31]  C. Postlethwaite,et al.  Spatial and temporal feedback control of traveling wave solutions of the two-dimensional complex Ginzburg-Landau equation. , 2006, nlin/0701007.

[32]  Wulfram Gerstner,et al.  A neuronal learning rule for sub-millisecond temporal coding , 1996, Nature.

[33]  T. Tsumoto,et al.  Change of conduction velocity by regional myelination yields constant latency irrespective of distance between thalamus and cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Haim Sompolinsky,et al.  Traveling Waves and the Processing of Weakly Tuned Inputs in a Cortical Network Module , 2004, Journal of Computational Neuroscience.

[35]  P. Brown,et al.  Different functional loops between cerebral cortex and the subthalmic area in Parkinson's disease. , 2006, Cerebral cortex.

[36]  M. C. Soriano,et al.  Dynamics, correlation scaling, and synchronization behavior in rings of delay-coupled oscillators. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[37]  Michael Schmitt,et al.  On the Complexity of Learning for Spiking Neurons with Temporal Coding , 1999, Inf. Comput..

[38]  P König,et al.  Direct physiological evidence for scene segmentation by temporal coding. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Rajarshi Roy,et al.  Crowd synchrony and quorum sensing in delay-coupled lasers. , 2010, Physical review letters.

[40]  D. Kleinfeld,et al.  Traveling Electrical Waves in Cortex Insights from Phase Dynamics and Speculation on a Computational Role , 2001, Neuron.

[41]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[42]  Hiroaki Daido STRANGE WAVES IN COUPLED-OSCILLATOR ARRAYS: MAPPING APPROACH , 1997 .

[43]  Kazuyuki Aihara,et al.  Dynamical Cell Assembly Hypothesis -- Theoretical Possibility of Spatio-temporal Coding in the Cortex , 1996, Neural Networks.

[44]  Martin Schneider,et al.  Activity-Dependent Development of Axonal and Dendritic Delays, or, Why Synaptic Transmission Should Be Unreliable , 2002, Neural Computation.

[45]  P. Bressloff,et al.  DYNAMICS OF A RING OF PULSE-COUPLED OSCILLATORS : GROUP THEORETIC APPROACH , 1997 .

[46]  D. Debanne,et al.  Release-Dependent Variations in Synaptic Latency: A Putative Code for Short- and Long-Term Synaptic Dynamics , 2007, Neuron.

[47]  S Yanchuk,et al.  Periodic patterns in a ring of delay-coupled oscillators. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[48]  Matthias Wolfrum,et al.  Destabilization patterns in chains of coupled oscillators. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.