Detecting synfire chain activity using massively parallel spike train recording.

The synfire chain model has been proposed as the substrate that underlies computational processes in the brain and has received extensive theoretical study. In this model cortical tissue is composed of a superposition of feedforward subnetworks (chains) each capable of transmitting packets of synchronized spikes with high reliability. Computations are then carried out by interactions of these chains. Experimental evidence for synfire chains has so far been limited to inference from detection of a few repeating spatiotemporal neuronal firing patterns in multiple single-unit recordings. Demonstration that such patterns actually come from synfire activity would require finding a meta organization among many detected patterns, as yet an untried approach. In contrast we present here a new method that directly visualizes the repetitive occurrence of synfire activity even in very large data sets of multiple single-unit recordings. We achieve reliability and sensitivity by appropriately averaging over neuron space (identities) and time. We test the method with data from a large-scale balanced recurrent network simulation containing 50 randomly activated synfire chains. The sensitivity is high enough to detect synfire chain activity in simultaneous single-unit recordings of 100 to 200 neurons from such data, enabling application to experimental data in the near future.

[1]  Steve M. Potter,et al.  Precisely timed spatiotemporal patterns of neural activity in dissociated cortical cultures , 2007, Neuroscience.

[2]  Marc-Oliver Gewaltig,et al.  NEST (NEural Simulation Tool) , 2007, Scholarpedia.

[3]  Prof. Dr. Valentino Braitenberg,et al.  Anatomy of the Cortex , 1991, Studies of Brain Function.

[4]  Nicolas Brunel,et al.  Dynamics of Sparsely Connected Networks of Excitatory and Inhibitory Spiking Neurons , 2000, Journal of Computational Neuroscience.

[5]  L. Abbott,et al.  Neural network dynamics. , 2005, Annual review of neuroscience.

[6]  R N Lemon,et al.  Synchronization in monkey motor cortex during a precision grip task. I. Task-dependent modulation in single-unit synchrony. , 2001, Journal of neurophysiology.

[7]  R N Lemon,et al.  Precise spatiotemporal repeating patterns in monkey primary and supplementary motor areas occur at chance levels. , 2000, Journal of neurophysiology.

[8]  E. Callaway,et al.  Excitatory cortical neurons form fine-scale functional networks , 2005, Nature.

[9]  John P. Donoghue,et al.  Connecting cortex to machines: recent advances in brain interfaces , 2002, Nature Neuroscience.

[10]  D. R. Euston,et al.  Fast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep , 2007, Science.

[11]  Masataka Goto,et al.  A chorus section detection method for musical audio signals and its application to a music listening station , 2006, IEEE Transactions on Audio, Speech, and Language Processing.

[12]  Sooyoung Chung,et al.  Highly ordered arrangement of single neurons in orientation pinwheels , 2006, Nature.

[13]  Sidarta Ribeiro,et al.  Multielectrode recordings: the next steps , 2002, Current Opinion in Neurobiology.

[14]  Moshe Abeles,et al.  On Embedding Synfire Chains in a Balanced Network , 2003, Neural Computation.

[15]  Yuji Ikegaya,et al.  Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity , 2004, Science.

[16]  Sonja Grün,et al.  Unitary Events in Multiple Single-Neuron Spiking Activity: I. Detection and Significance , 2002, Neural Computation.

[17]  G L Gerstein,et al.  Detecting spatiotemporal firing patterns among simultaneously recorded single neurons. , 1988, Journal of neurophysiology.

[18]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

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

[20]  P. M. D. Lorenzo,et al.  Across unit patterns in the neural response to taste: vector space analysis. , 1989 .

[21]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[22]  M. Abeles Local Cortical Circuits: An Electrophysiological Study , 1982 .

[23]  D. Amit,et al.  Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. , 1997, Cerebral cortex.

[24]  P. J. Sjöström,et al.  Correction: Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS Biology.

[25]  Markus Diesmann,et al.  Exact Subthreshold Integration with Continuous Spike Times in Discrete-Time Neural Network Simulations , 2007, Neural Computation.

[26]  Professor Moshe Abeles,et al.  Local Cortical Circuits , 1982, Studies of Brain Function.

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

[28]  Markus Diesmann,et al.  The mechanism of synchronization in feed-forward neuronal networks , 2008 .

[29]  B. Sakmann,et al.  The Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex , 2000, The Journal of Neuroscience.

[30]  Jürgen Kurths,et al.  Recurrence plots for the analysis of complex systems , 2009 .

[31]  John F. Kalaska,et al.  Spatial coding of movement: A hypothesis concerning the coding of movement direction by motor cortical populations , 1983 .

[32]  Marc-Oliver Gewaltig,et al.  Efficient Parallel Simulation of Large-Scale Neuronal Networks on Clusters of Multiprocessor Computers , 2007, Euro-Par.

[33]  George L Gerstein,et al.  Searching for significance in spatio-temporal firing patterns. , 2004, Acta neurobiologiae experimentalis.

[34]  Daniel Lehmann,et al.  Modeling Compositionality by Dynamic Binding of Synfire Chains , 2004, Journal of Computational Neuroscience.

[35]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

[36]  E. Vaadia,et al.  Spatiotemporal structure of cortical activity: properties and behavioral relevance. , 1998, Journal of neurophysiology.

[37]  J. Csicsvari,et al.  Massively parallel recording of unit and local field potentials with silicon-based electrodes. , 2003, Journal of neurophysiology.

[38]  Sonja Grün,et al.  Robustness of the significance of spike synchrony with respect to sorting errors , 2006, Journal of Computational Neuroscience.

[39]  George L. Gerstein,et al.  Cross-correlation measures of unresolved multi-neuron recordings , 2000, Journal of Neuroscience Methods.

[40]  D. J. Warren,et al.  High-resolution two-dimensional spatial mapping of cat striate cortex using a 100-microelectrode array , 2001, Neuroscience.

[41]  Norio Matsuki,et al.  Metastability of Active CA 3 Networks , 2007 .

[42]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

[43]  D. Schild,et al.  Principles of odor coding and a neural network for odor discrimination. , 1988, Biophysical journal.

[44]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[45]  Stefan Rotter,et al.  Correlations and Population Dynamics in Cortical Networks , 2008, Neural Computation.

[46]  Sooyoung Chung,et al.  Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex , 2005, Nature.

[47]  N. Matsuki,et al.  Metastability of Active CA3 Networks , 2007, The Journal of Neuroscience.

[48]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

[49]  Paul H. E. Tiesinga,et al.  A New Correlation-Based Measure of Spike Timing Reliability , 2002, Neurocomputing.

[50]  Stefan Rotter,et al.  Exact digital simulation of time-invariant linear systems with applications to neuronal modeling , 1999, Biological Cybernetics.

[51]  M. A. Smith,et al.  Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque , 2005, The Journal of Neuroscience.

[52]  Markus Diesmann,et al.  Activity dynamics and propagation of synchronous spiking in locally connected random networks , 2003, Biological Cybernetics.

[53]  J. Griffith,et al.  Functional Coupling between Cells in the Visual Cortex of the Unrestrained Cat , 1963, Nature.

[54]  DiesmannMarkus,et al.  Unitary events in multiple single-neuron spiking activity , 2002 .

[55]  E. Vaadia,et al.  Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. , 1993, Journal of neurophysiology.

[56]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[57]  Daniel Lehmann,et al.  A Model for Representing the Dynamics of a System of Synfire Chains , 2005, Journal of Computational Neuroscience.