Temporal sequence learning in winner-take-all networks of spiking neurons demonstrated in a brain-based device

Animal behavior often involves a temporally ordered sequence of actions learned from experience. Here we describe simulations of interconnected networks of spiking neurons that learn to generate patterns of activity in correct temporal order. The simulation consists of large-scale networks of thousands of excitatory and inhibitory neurons that exhibit short-term synaptic plasticity and spike-timing dependent synaptic plasticity. The neural architecture within each area is arranged to evoke winner-take-all (WTA) patterns of neural activity that persist for tens of milliseconds. In order to generate and switch between consecutive firing patterns in correct temporal order, a reentrant exchange of signals between these areas was necessary. To demonstrate the capacity of this arrangement, we used the simulation to train a brain-based device responding to visual input by autonomously generating temporal sequences of motor actions.

[1]  Leonardo Fogassi,et al.  Neuronal Chains for Actions in the Parietal Lobe: A Computational Model , 2011, PloS one.

[2]  Emilio Salinas,et al.  Rank-Order-Selective Neurons Form a Temporal Basis Set for the Generation of Motor Sequences , 2009, The Journal of Neuroscience.

[3]  Eugene M Izhikevich,et al.  Hybrid spiking models , 2010, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

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

[5]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

[6]  G. Edelman Group selection and phasic reentrant signaling a theory of higher brain function , 1982 .

[7]  J. Tanji Sequential organization of multiple movements: involvement of cortical motor areas. , 2001, Annual review of neuroscience.

[8]  Bjarne Stroustrup,et al.  C++ Programming Language , 1986, IEEE Softw..

[9]  Eugene M. Izhikevich,et al.  Simple model of spiking neurons , 2003, IEEE Trans. Neural Networks.

[10]  Ueli Rutishauser,et al.  State-Dependent Computation Using Coupled Recurrent Networks , 2008, Neural Computation.

[11]  Dean V Buonomano,et al.  Embedding Multiple Trajectories in Simulated Recurrent Neural Networks in a Self-Organizing Manner , 2009, The Journal of Neuroscience.

[12]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[13]  Jun Tanji,et al.  Covert representation of second-next movement in the pre-supplementary motor area of monkeys. , 2009, Journal of neurophysiology.

[14]  G. Edelman,et al.  Large-scale model of mammalian thalamocortical systems , 2008, Proceedings of the National Academy of Sciences.

[15]  Bruno B Averbeck,et al.  Parallel processing of serial movements in prefrontal cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Gerald M Edelman,et al.  Learning in and from Brain-Based Devices , 2007, Science.

[17]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[18]  G. Edelman,et al.  The Mindful Brain: Cortical Organization and the Group-Selective Theory of Higher Brain Function , 1978 .

[19]  S. Nelson,et al.  The NMDA-to-AMPA ratio at synapses onto layer 2/3 pyramidal neurons is conserved across prefrontal and visual cortices. , 2003, Journal of neurophysiology.

[20]  Michael J. Gutnick,et al.  NMDA Receptors in Layer 4 Spiny Stellate Cells of the Mouse Barrel Cortex Contain the NR2C Subunit , 2006, The Journal of Neuroscience.

[21]  Gerald M. Edelman,et al.  Versatile networks of simulated spiking neurons displaying winner-take-all behavior , 2013, Front. Comput. Neurosci..

[22]  Jeffrey L. Krichmar,et al.  Embodied models of delayed neural responses: Spatiotemporal categorization and predictive motor control in brain based devices , 2008, Neural Networks.

[23]  Daniel Bullock,et al.  Learning and production of movement sequences: behavioral, neurophysiological, and modeling perspectives. , 2004, Human movement science.

[24]  Bard Ermentrout,et al.  A model for complex sequence learning and reproduction in neural populations , 2011, Journal of Computational Neuroscience.