Learning Probabilistic Inference through Spike-Timing-Dependent Plasticity123

Abstract Numerous experimental data show that the brain is able to extract information from complex, uncertain, and often ambiguous experiences. Furthermore, it can use such learnt information for decision making through probabilistic inference. Several models have been proposed that aim at explaining how probabilistic inference could be performed by networks of neurons in the brain. We propose here a model that can also explain how such neural network could acquire the necessary information for that from examples. We show that spike-timing-dependent plasticity in combination with intrinsic plasticity generates in ensembles of pyramidal cells with lateral inhibition a fundamental building block for that: probabilistic associations between neurons that represent through their firing current values of random variables. Furthermore, by combining such adaptive network motifs in a recursive manner the resulting network is enabled to extract statistical information from complex input streams, and to build an internal model for the distribution p* that generates the examples it receives. This holds even if p* contains higher-order moments. The analysis of this learning process is supported by a rigorous theoretical foundation. Furthermore, we show that the network can use the learnt internal model immediately for prediction, decision making, and other types of probabilistic inference.

[1]  R. Stickgold,et al.  Sleep-dependent memory triage: evolving generalization through selective processing , 2013, Nature Neuroscience.

[2]  W. Gerstner,et al.  Generalized Bienenstock-Cooper-Munro rule for spiking neurons that maximizes information transmission. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Linda B. Smith,et al.  The importance of shape in early lexical learning , 1988 .

[4]  Radford M. Neal Pattern Recognition and Machine Learning , 2007, Technometrics.

[5]  H. Kushner,et al.  Stochastic Approximation and Recursive Algorithms and Applications , 2003 .

[6]  F. Helmchen,et al.  Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex , 2013, Nature.

[7]  Simon Haykin,et al.  Neural Networks and Learning Machines , 2010 .

[8]  Miguel Á. Carreira-Perpiñán,et al.  On Contrastive Divergence Learning , 2005, AISTATS.

[9]  S. Denison,et al.  Probabilistic models, learning algorithms, and response variability: sampling in cognitive development , 2014, Trends in Cognitive Sciences.

[10]  Daniel Kersten,et al.  Bayesian models of object perception , 2003, Current Opinion in Neurobiology.

[11]  D. Knill,et al.  Apparent surface curvature affects lightness perception , 1991, Nature.

[12]  Wolfgang Maass,et al.  Bayesian Computation Emerges in Generic Cortical Microcircuits through Spike-Timing-Dependent Plasticity , 2013, PLoS Comput. Biol..

[13]  Geoffrey E. Hinton Training Products of Experts by Minimizing Contrastive Divergence , 2002, Neural Computation.

[14]  A. Polsky,et al.  Synaptic Integration in Tuft Dendrites of Layer 5 Pyramidal Neurons: A New Unifying Principle , 2009, Science.

[15]  Johannes J. Letzkus,et al.  Cortical feed-forward networks for binding different streams of sensory information , 2006, Nature Neuroscience.

[16]  Stefan Habenschuss,et al.  Stochastic Computations in Cortical Microcircuit Models , 2013, PLoS Comput. Biol..

[17]  Andreas Lüthi,et al.  Disinhibition, a Circuit Mechanism for Associative Learning and Memory , 2015, Neuron.

[18]  Wolfgang Maass,et al.  Neural Dynamics as Sampling: A Model for Stochastic Computation in Recurrent Networks of Spiking Neurons , 2011, PLoS Comput. Biol..

[19]  Wolfgang Jank,et al.  The EM Algorithm, Its Randomized Implementation and Global Optimization: Some Challenges and Opportunities for Operations Research , 2006 .

[20]  Nir Friedman,et al.  Probabilistic Graphical Models: Principles and Techniques - Adaptive Computation and Machine Learning , 2009 .

[21]  Paul Miller,et al.  Natural stimuli evoke dynamic sequences of states in sensory cortical ensembles , 2007, Proceedings of the National Academy of Sciences.

[22]  W. Senn,et al.  Matching Recall and Storage in Sequence Learning with Spiking Neural Networks , 2013, The Journal of Neuroscience.

[23]  Nir Friedman,et al.  Probabilistic Graphical Models - Principles and Techniques , 2009 .

[24]  Wei Ji Ma,et al.  Bayesian inference with probabilistic population codes , 2006, Nature Neuroscience.

[25]  Wolfgang Maass,et al.  Branch-Specific Plasticity Enables Self-Organization of Nonlinear Computation in Single Neurons , 2011, The Journal of Neuroscience.

[26]  Wulfram Gerstner,et al.  Variational Learning for Recurrent Spiking Networks , 2011, NIPS.

[27]  David Kappel,et al.  NEVESIM: event-driven neural simulation framework with a Python interface , 2014, Front. Neuroinform..

[28]  G. Stuart,et al.  Dependence of EPSP Efficacy on Synapse Location in Neocortical Pyramidal Neurons , 2002, Science.

[29]  Wulfram Gerstner,et al.  From Stochastic Nonlinear Integrate-and-Fire to Generalized Linear Models , 2011, NIPS.

[30]  Alexandre Pouget,et al.  Complex Inference in Neural Circuits with Probabilistic Population Codes and Topic Models , 2012, NIPS.

[31]  Geoffrey E. Hinton,et al.  The "wake-sleep" algorithm for unsupervised neural networks. , 1995, Science.

[32]  D. Debanne,et al.  Long-term plasticity of intrinsic excitability: learning rules and mechanisms. , 2003, Learning & memory.

[33]  P. J. Sjöström,et al.  Rate, Timing, and Cooperativity Jointly Determine Cortical Synaptic Plasticity , 2001, Neuron.

[34]  József Fiser,et al.  Spontaneous Cortical Activity Reveals Hallmarks of an Optimal Internal Model of the Environment , 2011, Science.

[35]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[36]  Radford M. Neal Connectionist Learning of Belief Networks , 1992, Artif. Intell..

[37]  Wolfgang Maass,et al.  Probabilistic Inference in General Graphical Models through Sampling in Stochastic Networks of Spiking Neurons , 2011, PLoS Comput. Biol..

[38]  Wolfgang Maass,et al.  Belief Propagation in Networks of Spiking Neurons , 2009, Neural Computation.

[39]  Daniel L. Schacter,et al.  The Seven Sins of Memory: How the Mind Forgets and Remembers , 2001 .

[40]  Yoshua Bengio,et al.  Towards Biologically Plausible Deep Learning , 2015, ArXiv.

[41]  Timothy D. Hanks,et al.  Probabilistic Population Codes for Bayesian Decision Making , 2008, Neuron.

[42]  Stefan Habenschuss,et al.  Emergence of Optimal Decoding of Population Codes Through STDP , 2013, Neural Computation.

[43]  H. Pashler,et al.  Measuring the Crowd Within , 2008, Psychological science.

[44]  J. Besag Statistical Analysis of Non-Lattice Data , 1975 .

[45]  Geoffrey E. Hinton,et al.  An Efficient Learning Procedure for Deep Boltzmann Machines , 2012, Neural Computation.

[46]  Yee Whye Teh,et al.  A Fast Learning Algorithm for Deep Belief Nets , 2006, Neural Computation.

[47]  J J Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Geoffrey E. Hinton,et al.  A Learning Algorithm for Boltzmann Machines , 1985, Cogn. Sci..

[49]  Wulfram Gerstner,et al.  Predicting spike timing of neocortical pyramidal neurons by simple threshold models , 2006, Journal of Computational Neuroscience.

[50]  Klaus Schuch,et al.  PCSIM: A Parallel Simulation Environment for Neural Circuits Fully Integrated with Python , 2008, Frontiers Neuroinformatics.

[51]  Shimon Ullman,et al.  Cortical Circuitry Implementing Graphical Models , 2009, Neural Computation.

[52]  Jean-Pascal Pfister,et al.  Optimal Spike-Timing-Dependent Plasticity for Precise Action Potential Firing in Supervised Learning , 2005, Neural Computation.

[53]  Lars E. Holzman,et al.  Neuronal integration of dynamic sources: Bayesian learning and Bayesian inference. , 2010, Chaos.

[54]  Wulfram Gerstner,et al.  Neuronal Dynamics: From Single Neurons To Networks And Models Of Cognition , 2014 .

[55]  Wolfgang Maass,et al.  Motif distribution, dynamical properties, and computational performance of two data-based cortical microcircuit templates , 2009, Journal of Physiology-Paris.

[56]  Naftali Tishby,et al.  Cortical activity flips among quasi-stationary states. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Rajesh P. N. Rao,et al.  Bayesian brain : probabilistic approaches to neural coding , 2006 .

[58]  A. Stone,et al.  The Seven Sins of Memory: How the Mind Forgets and Remembers , 2001 .

[59]  David Kappel,et al.  STDP Installs in Winner-Take-All Circuits an Online Approximation to Hidden Markov Model Learning , 2014, PLoS Comput. Biol..

[60]  A. Pouget,et al.  Marginalization in Neural Circuits with Divisive Normalization , 2011, The Journal of Neuroscience.

[61]  L. Pinneo On noise in the nervous system. , 1966, Psychological review.

[62]  Karl Steinbuch,et al.  Die Lernmatrix , 2004, Kybernetik.

[63]  J. Tenenbaum,et al.  Optimal Predictions in Everyday Cognition , 2006, Psychological science.

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

[65]  D. Rubin,et al.  Maximum likelihood from incomplete data via the EM - algorithm plus discussions on the paper , 1977 .

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

[67]  Robert H. Cudmore,et al.  Long-term potentiation of intrinsic excitability in LV visual cortical neurons. , 2004, Journal of neurophysiology.

[68]  Pico Caroni,et al.  Inhibitory microcircuit modules in hippocampal learning , 2015, Current Opinion in Neurobiology.

[69]  G. C. Wei,et al.  A Monte Carlo Implementation of the EM Algorithm and the Poor Man's Data Augmentation Algorithms , 1990 .

[70]  J J Hopfield,et al.  Neurons with graded response have collective computational properties like those of two-state neurons. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[71]  W. Newsome,et al.  Context-dependent computation by recurrent dynamics in prefrontal cortex , 2013, Nature.

[72]  Rajesh P. N. Rao Neural Models of Bayesian Belief Propagation , 2006 .

[73]  Xiao-Jing Wang,et al.  The importance of mixed selectivity in complex cognitive tasks , 2013, Nature.

[74]  J. Byrne,et al.  More than synaptic plasticity: role of nonsynaptic plasticity in learning and memory , 2010, Trends in Neurosciences.

[75]  S. Denison,et al.  Rational variability in children’s causal inferences: The Sampling Hypothesis , 2013, Cognition.

[76]  Kevin P. Murphy,et al.  Machine learning - a probabilistic perspective , 2012, Adaptive computation and machine learning series.

[77]  Sophie Denève,et al.  Bayesian Spiking Neurons II: Learning , 2008, Neural Computation.