Dynamical Synapses Enhance Neural Information Processing: Gracefulness, Accuracy, and Mobility

Experimental data have revealed that neuronal connection efficacy exhibits two forms of short-term plasticity: short-term depression (STD) and short-term facilitation (STF). They have time constants residing between fast neural signaling and rapid learning and may serve as substrates for neural systems manipulating temporal information on relevant timescales. This study investigates the impact of STD and STF on the dynamics of continuous attractor neural networks and their potential roles in neural information processing. We find that STD endows the network with slow-decaying plateau behaviors: the network that is initially being stimulated to an active state decays to a silent state very slowly on the timescale of STD rather than on that of neuralsignaling. This provides a mechanism for neural systems to hold sensory memory easily and shut off persistent activities gracefully. With STF, we find that the network can hold a memory trace of external inputs in the facilitated neuronal interactions, which provides a way to stabilize the network response to noisy inputs, leading to improved accuracy in population decoding. Furthermore, we find that STD increases the mobility of the network states. The increased mobility enhances the tracking performance of the network in response to time-varying stimuli, leading to anticipative neural responses. In general, we find that STD and STP tend to have opposite effects on network dynamics and complementary computational advantages, suggesting that the brain may employ a strategy of weighting them differentially depending on the computational purpose.

[1]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[2]  P C Bressloff,et al.  Oscillatory waves in inhomogeneous neural media. , 2003, Physical review letters.

[3]  Misha Tsodyks,et al.  The Emergence of Up and Down States in Cortical Networks , 2006, PLoS Comput. Biol..

[4]  Boris S. Gutkin,et al.  Turning On and Off with Excitation: The Role of Spike-Timing Asynchrony and Synchrony in Sustained Neural Activity , 2001, Journal of Computational Neuroscience.

[5]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[6]  H. Markram,et al.  The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[7]  R. Monasson,et al.  Crosstalk and transitions between multiple spatial maps in an attractor neural network model of the hippocampus: collective motion of the activity. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[8]  Y. Dan,et al.  An arithmetic rule for spatial summation of excitatory and inhibitory inputs in pyramidal neurons , 2009, Proceedings of the National Academy of Sciences.

[9]  S. Amari Dynamics of pattern formation in lateral-inhibition type neural fields , 1977, Biological Cybernetics.

[10]  Si Wu,et al.  Population Coding and Decoding in a Neural Field: A Computational Study , 2002, Neural Computation.

[11]  Xiao-Jing Wang Synaptic reverberation underlying mnemonic persistent activity , 2001, Trends in Neurosciences.

[12]  Paul C. Bressloff,et al.  Breathing Pulses in an Excitatory Neural Network , 2004, SIAM J. Appl. Dyn. Syst..

[13]  B L McNaughton,et al.  Path Integration and Cognitive Mapping in a Continuous Attractor Neural Network Model , 1997, The Journal of Neuroscience.

[14]  Jian-Young Wu,et al.  Propagating Waves of Activity in the Neocortex: What They Are, What They Do , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[15]  A. Baddeley Essentials of Human Memory , 1999 .

[16]  Janet Wiles,et al.  Self-sustained non-periodic activity in networks of spiking neurons: The contribution of local and long-range connections and dynamic synapses , 2010, NeuroImage.

[17]  Si Wu,et al.  A Moving Bump in a Continuous Manifold: A Comprehensive Study of the Tracking Dynamics of Continuous Attractor Neural Networks , 2008, Neural Computation.

[18]  H. Markram,et al.  t Synchrony Generation in Recurrent Networks with Frequency-Dependent Synapses , 2000, The Journal of Neuroscience.

[19]  K. Zhang,et al.  Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  P. Bressloff,et al.  Effects of synaptic depression and adaptation on spatiotemporal dynamics of an excitatory neuronal network , 2010 .

[21]  C. Stevens,et al.  Facilitation and depression at single central synapses , 1995, Neuron.

[22]  P. Dayan,et al.  Synapses with short-term plasticity are optimal estimators of presynaptic membrane potentials , 2010, Nature Neuroscience.

[23]  M. Tsodyks,et al.  Synaptic Theory of Working Memory , 2008, Science.

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

[25]  G. Elston,et al.  Pyramidal Cells, Patches, and Cortical Columns: a Comparative Study of Infragranular Neurons in TEO, TE, and the Superior Temporal Polysensory Area of the Macaque Monkey , 2000, The Journal of Neuroscience.

[26]  Paul C. Bressloff,et al.  Spatially structured oscillations in a two-dimensional excitatory neuronal network with synaptic depression , 2009, Journal of Computational Neuroscience.

[27]  D. Heeger Normalization of cell responses in cat striate cortex , 1992, Visual Neuroscience.

[28]  Mark C. W. van Rossum,et al.  Recurrent networks with short term synaptic depression , 2009, Journal of Computational Neuroscience.

[29]  Misha Tsodyks,et al.  Computation by Ensemble Synchronization in Recurrent Networks with Synaptic Depression , 2002, Journal of Computational Neuroscience.

[30]  Si Wu,et al.  Computing with Continuous Attractors: Stability and Online Aspects , 2005, Neural Computation.

[31]  Bard Ermentrout,et al.  Spatially Structured Activity in Synaptically Coupled Neuronal Networks: I. Traveling Fronts and Pulses , 2001, SIAM J. Appl. Math..

[32]  H. Markram,et al.  Redistribution of synaptic efficacy between neocortical pyramidal neurons , 1996, Nature.

[33]  D. Sagi,et al.  Excitatory-inhibitory network in the visual cortex: psychophysical evidence. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[34]  AmariShun-Ichi Dynamics of pattern formation in lateral-inhibition type neural fields , 1977 .

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

[36]  H. T. Blair,et al.  Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  Xiao-Jing Wang,et al.  Cannabinoid-mediated disinhibition and working memory: dynamical interplay of multiple feedback mechanisms in a continuous attractor model of prefrontal cortex. , 2007, Cerebral cortex.

[38]  C. Stevens,et al.  Heterogeneity of Release Probability, Facilitation, and Depletion at Central Synapses , 1997, Neuron.

[39]  Jacek M. Zurada,et al.  Neural networks with dynamic synapses for time-series prediction , 1998 .

[40]  Daniel D. Lee,et al.  Stability of the Memory of Eye Position in a Recurrent Network of Conductance-Based Model Neurons , 2000, Neuron.

[41]  Hilbert J. Kappen,et al.  Competition Between Synaptic Depression and Facilitation in Attractor Neural Networks , 2006, Neural Computation.

[42]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

[43]  A. Pouget,et al.  Reading population codes: a neural implementation of ideal observers , 1999, Nature Neuroscience.

[44]  J. M. Herrmann,et al.  Dynamical synapses causing self-organized criticality in neural networks , 2007, 0712.1003.

[45]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Max Welling,et al.  Herding dynamical weights to learn , 2009, ICML '09.

[47]  Masato Okada,et al.  Statistical mechanics of attractor neural network models with synaptic depression , 2009 .