Detecting synfire chains in parallel spike data

The synfire chain model of brain organization has received much theoretical attention since its introduction (Abeles, 1982, 1991). However there has been no convincing experimental demonstration of synfire chains due partly to limitations of recording technology but also due to lack of appropriate analytic methods for large scale recordings of parallel spike trains. We have previously published one such method based on intersection of the neural populations active at two different times (Schrader et al., 2008). In the present paper we extend this analysis to deal with higher firing rates and noise levels, and develop two additional tools based on properties of repeating firing patterns. All three measures show characteristic signatures if synfire chains underlie the recorded data. However we demonstrate that the detection of repeating firing patterns alone (as used in several papers) is not enough to infer the presence of synfire chains. Positive results from all three measures are needed.

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

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

[3]  D. Georgescauld Local Cortical Circuits, An Electrophysiological Study , 1983 .

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

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

[6]  Markus Diesmann,et al.  A Compositionality Machine Realized by a Hierarchic Architecture of Synfire Chains , 2011, Front. Comput. Neurosci..

[7]  M. Abeles,et al.  Detecting precise firing sequences in experimental data , 2001, Journal of Neuroscience Methods.

[8]  David W. Tank,et al.  Regression-Based Identification of Behavior-Encoding Neurons During Large-Scale Optical Imaging of Neural Activity at Cellular Resolution , 2010, Journal of neurophysiology.

[9]  Debprakash Patnaik,et al.  Inferring neuronal network connectivity from spike data: A temporal data mining approach , 2008, Sci. Program..

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

[11]  Yoram Ben-Shaul,et al.  Temporally precise cortical firing patterns are associated with distinct action segments. , 2006, Journal of neurophysiology.

[12]  A Aertsen,et al.  Propagation of synchronous spiking activity in feedforward neural networks , 1996, Journal of Physiology-Paris.

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

[14]  Markus Diesmann,et al.  High-capacity embedding of synfire chains in a cortical network model , 2012, Journal of Computational Neuroscience.

[15]  Sonja Grün,et al.  Detecting synfire chain activity using massively parallel spike train recording. , 2008, Journal of neurophysiology.

[16]  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.

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

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

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

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

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

[22]  P. S. Sastry,et al.  Conditional Probability-Based Significance Tests for Sequential Patterns in Multineuronal Spike Trains , 2008, Neural Computation.

[23]  Atsushi Miyawaki,et al.  Innovations in the Imaging of Brain Functions using Fluorescent Proteins , 2005, Neuron.

[24]  Thomas Knöpfel,et al.  Optical recordings of membrane potential using genetically targeted voltage-sensitive fluorescent proteins. , 2003, Methods.

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

[26]  Asohan Amarasingham,et al.  At what time scale does the nervous system operate? , 2003, Neurocomputing.

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

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

[29]  J. Knott The organization of behavior: A neuropsychological theory , 1951 .

[30]  Ad Aertsen,et al.  Propagation of cortical synfire activity: survival probability in single trials and stability in the mean , 2001, Neural Networks.

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

[32]  Akira Date,et al.  On the temporal resolution of neural activity , 1998 .

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

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

[35]  Z. Nadasdy,et al.  Neurons of the cerebral cortex exhibit precise interspike timing in correspondence to behavior. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[37]  Diesmann Markus Random compositional networks of synfire chains dynamically self-tune to the critical state for ongoing percolation of activity , 2010 .

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

[39]  Christian Borgelt,et al.  Complexity distribution as a measure for assembly size and temporal precision , 2010, Neural Networks.

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

[41]  Sonja Grün,et al.  Frontiers in Computational Neuroscience , 2022 .

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

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

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

[45]  B J Richmond,et al.  Stochastic nature of precisely timed spike patterns in visual system neuronal responses. , 1999, Journal of neurophysiology.

[46]  G. Buzsáki,et al.  Sequential structure of neocortical spontaneous activity in vivo , 2007, Proceedings of the National Academy of Sciences.

[47]  Markus Diesmann,et al.  High storage capacity of synfire chains in large-scale cortical networks of conductance-based spiking neurons , 2010, BMC Neuroscience.

[48]  Markus Diesmann,et al.  Synchronization and rate dynamics in embedded synfire chains: effect of network heterogeneity and feedback , 2009, BMC Neuroscience.

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