Finding neural assemblies with frequent item set mining

Cell assemblies, defined as groups of neurons exhibiting precise spike coordination, were proposed as a model of network processing in the cortex. Fortunately, in recent years considerable progress has been made in multi-electrode recordings, which enable recording massively parallel spike trains of hundred(s) of neurons simultaneously. However, due to the challenges inherent in multivariate approaches, most studies in favor of cortical cell assemblies still resorted to analyzing pairwise interactions. However, to recover the underlying correlation structures, higher-order correlations need to be identified directly. Inspired by the Accretion method proposed by Gerstein et al. (1978) we propose a new assembly detection method based on frequent item set mining (FIM). In contrast to Accretion, FIM searches effectively and without redundancy for individual spike patterns that exceed a given support threshold. We study different search methods, with which the space of potential cell assemblies may be explored, as well as different test statistics and subset conditions with which candidate assemblies may be assessed and filtered. It turns out that a core challenge of cell assembly detection is the problem of multiple testing, which causes a large number of false discoveries. Unfortunately, criteria that address individual candidate assemblies and try to assess them with statistical tests and/or subset conditions do not help much to tackle this problem. The core idea of our new method is that in order to cope with the multiple testing problem one has to shift the focus of statistical testing from specific assemblies (consisting of a specific set of neurons) to spike patterns of a certain size (i.e., with a certain number of neurons). This significantly reduces the number of necessary tests, thus alleviating the multiple testing problem. We demonstrate that our method is able to reliably suppress false discoveries, while it is still very sensitive in discovering synchronous activity. Since we exploit high-speed computational techniques from FIM for the tests, our method is also computationally efficient.

[1]  A. Aertsen,et al.  Representation of cooperative firing activity among simultaneously recorded neurons. , 1985, Journal of neurophysiology.

[2]  Christian Borgelt,et al.  Generation and Selection of Surrogate Methods for Correlation Analysis , 2010 .

[3]  Stefan Rotter,et al.  Higher-Order Statistics of Input Ensembles and the Response of Simple Model Neurons , 2003, Neural Computation.

[4]  Bart Goethals,et al.  Frequent Set Mining , 2010, Data Mining and Knowledge Discovery Handbook.

[5]  Vaughn L. Hetrick,et al.  Functional clustering algorithm for the analysis of dynamic network data. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[6]  Sonja Grün,et al.  Spatially organized spike correlation in cat visual cortex , 2007, Neurocomputing.

[7]  Sonja Grün,et al.  Data-driven significance estimation for precise spike correlation. , 2009, Journal of neurophysiology.

[8]  Peter E. Latham,et al.  Pairwise Maximum Entropy Models for Studying Large Biological Systems: When They Can Work and When They Can't , 2008, PLoS Comput. Biol..

[9]  M. Nicolelis,et al.  Reconstructing the Engram: Simultaneous, Multisite, Many Single Neuron Recordings , 1997, Neuron.

[10]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[11]  C. Bonferroni Il calcolo delle assicurazioni su gruppi di teste , 1935 .

[12]  Sonja Grün,et al.  Detecting synfire chains in parallel spike data , 2012, Journal of Neuroscience Methods.

[13]  Christian Borgelt,et al.  Frequent item set mining , 2012, WIREs Data Mining Knowl. Discov..

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

[15]  Jonathon Shlens,et al.  The Structure of Multi-Neuron Firing Patterns in Primate Retina , 2006, The Journal of Neuroscience.

[16]  Sonja Grün,et al.  Higher-Order Correlations in Non-Stationary Parallel Spike Trains: Statistical Modeling and Inference , 2009, Front. Comput. Neurosci..

[17]  Christian Borgelt,et al.  Efficient Identification of Assembly Neurons within Massively Parallel Spike Trains , 2009, Comput. Intell. Neurosci..

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

[19]  W. Singer,et al.  Integrator or coincidence detector? The role of the cortical neuron revisited , 1996, Trends in Neurosciences.

[20]  Stefano Pezzuto,et al.  This is an Open Access article distributed under the terms of the Creative Commons Attribution-Noncommercial License, which permits unrestricted use, distribution, and reproduction in any noncommercial medium, provided the original work is properly cited. , 2009 .

[21]  Sonja Grün,et al.  CuBIC: cumulant based inference of higher-order correlations in massively parallel spike trains , 2009, Journal of Computational Neuroscience.

[22]  Roman Borisyuk,et al.  Statistical technique for analysing functional connectivity of multiple spike trains , 2011, Journal of Neuroscience Methods.

[23]  Sonja Grün,et al.  Long-Term Modifications in Motor Cortical Dynamics Induced by Intensive Practice , 2009, The Journal of Neuroscience.

[24]  Sonja Grün,et al.  Noise Suppression and Surplus Synchrony by Coincidence Detection , 2012, PLoS Comput. Biol..

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

[26]  Emery N. Brown,et al.  State-Space Analysis of Time-Varying Higher-Order Spike Correlation for Multiple Neural Spike Train Data , 2012, PLoS Comput. Biol..

[27]  Wolf Singer,et al.  Detecting Multineuronal Temporal Patterns in Parallel Spike Trains , 2012, Front. Neuroinform..

[28]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[29]  W. Singer,et al.  Stimulus dependent intercolumnar synchronization of single unit responses in cat area 17. , 1995, Neuroreport.

[30]  Matthew Sperrin,et al.  Multiple Testing Procedures with Applications to Genomics , 2010 .

[31]  Gordon Pipa,et al.  NeuroXidence: reliable and efficient analysis of an excess or deficiency of joint-spike events , 2009, Journal of Computational Neuroscience.

[32]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[33]  Das Amrita,et al.  Mining Association Rules between Sets of Items in Large Databases , 2013 .

[34]  M. Abeles Role of the cortical neuron: integrator or coincidence detector? , 1982, Israel journal of medical sciences.

[35]  G. Buzsáki Large-scale recording of neuronal ensembles , 2004, Nature Neuroscience.

[36]  A. Aertsen,et al.  Dynamics of neuronal interactions in monkey cortex in relation to behavioural events , 1995, Nature.

[37]  Stefan Rotter,et al.  Single-trial estimation of neuronal firing rates: From single-neuron spike trains to population activity , 1999, Journal of Neuroscience Methods.

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

[39]  R. Fisher Statistical methods for research workers , 1927, Protoplasma.

[40]  Tomasz Imielinski,et al.  Mining association rules between sets of items in large databases , 1993, SIGMOD Conference.

[41]  George L. Gerstein,et al.  Identification of functionally related neural assemblies , 1978, Brain Research.

[42]  H. Abdi The Bonferonni and Šidák Corrections for Multiple Comparisons , 2006 .

[43]  Christian Borgelt,et al.  Statistical evaluation of synchronous spike patterns extracted by frequent item set mining , 2013, Front. Comput. Neurosci..

[44]  Neil Salkind Encyclopedia of Measurement and Statistics , 2006 .

[45]  Sonja Grün,et al.  Analysis of Parallel Spike Trains , 2010 .

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

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

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

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

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

[51]  Michael J. Berry,et al.  Weak pairwise correlations imply strongly correlated network states in a neural population , 2005, Nature.

[52]  G. Buzsáki,et al.  Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex , 2008, Nature Neuroscience.