Reconciling the STDP and BCM Models of Synaptic Plasticity in a Spiking Recurrent Neural Network

Rate-coded Hebbian learning, as characterized by the BCM formulation, is an established computational model of synaptic plasticity. Recently it has been demonstrated that changes in the strength of synapses in vivo can also depend explicitly on the relative timing of pre- and postsynaptic firing. Computational modeling of this spike-timing-dependent plasticity (STDP) has demonstrated that it can provide inherent stability or competition based on local synaptic variables. However, it has also been demonstrated that these properties rely on synaptic weights being either depressed or unchanged by an increase in mean stochastic firing rates, which directly contradicts empirical data. Several analytical studies have addressed this apparent dichotomy and identified conditions under which distinct and disparate STDP rules can be reconciled with rate-coded Hebbian learning. The aim of this research is to verify, unify, and expand on these previous findings by manipulating each element of a standard computational STDP model in turn. This allows us to identify the conditions under which this plasticity rule can replicate experimental data obtained using both rate and temporal stimulation protocols in a spiking recurrent neural network. Our results describe how the relative scale of mean synaptic weights and their dependence on stochastic pre- or postsynaptic firing rates can be manipulated by adjusting the exact profile of the asymmetric learning window and temporal restrictions on spike pair interactions respectively. These findings imply that previously disparate models of rate-coded autoassociative learning and temporally coded heteroassociative learning, mediated by symmetric and asymmetric connections respectively, can be implemented in a single network using a single plasticity rule. However, we also demonstrate that forms of STDP that can be reconciled with rate-coded Hebbian learning do not generate inherent synaptic competition, and thus some additional mechanism is required to guarantee long-term input-output selectivity.

[1]  Neil Burgess,et al.  Computational models of the spatial and mnemonic functions of the hippocampus , 2006 .

[2]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

[3]  Y. Dan,et al.  Spike-timing-dependent synaptic modification induced by natural spike trains , 2002, Nature.

[4]  S. Wang,et al.  Dissection of bidirectional synaptic plasticity into saturable unidirectional processes. , 2005, Journal of neurophysiology.

[5]  M. Bear,et al.  Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Mark C. W. van Rossum,et al.  Stable Hebbian Learning from Spike Timing-Dependent Plasticity , 2000, The Journal of Neuroscience.

[7]  Davide Badoni,et al.  Spike-Driven Synaptic Plasticity: Theory, Simulation, VLSI Implementation , 2000, Neural Computation.

[8]  W. Abraham Metaplasticity: tuning synapses and networks for plasticity , 2008, Nature Reviews Neuroscience.

[9]  Johannes J. Letzkus,et al.  Dendritic mechanisms controlling spike-timing-dependent synaptic plasticity , 2007, Trends in Neurosciences.

[10]  Yoko Yamaguchi,et al.  Neural dynamics of the cognitive map in the hippocampus , 2007, Cognitive Neurodynamics.

[11]  Motonobu Hattori,et al.  Hippocampal memory modification induced by pattern completion and spike-timing dependent synaptic plasticity , 2005, Int. J. Neural Syst..

[12]  D. Debanne,et al.  Long‐term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures , 1998, The Journal of physiology.

[13]  M. Bear,et al.  A biophysically-based neuromorphic model of spike rate- and timing-dependent plasticity , 2011, Proceedings of the National Academy of Sciences.

[14]  S. Wang,et al.  Malleability of Spike-Timing-Dependent Plasticity at the CA3–CA1 Synapse , 2006, The Journal of Neuroscience.

[15]  A. Burkitt,et al.  Learning the structure of correlated synaptic subgroups using stable and competitive spike-timing-dependent plasticity. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[16]  M. Richard Theories of Hippocampal Function , 2006 .

[17]  Mu-ming Poo,et al.  Spike Train Timing-Dependent Associative Modification of Hippocampal CA3 Recurrent Synapses by Mossy Fibers , 2004, Neuron.

[18]  M. Frerking,et al.  Spike timing in CA3 pyramidal cells during behavior: implications for synaptic transmission. , 2005, Journal of neurophysiology.

[19]  R. Miles,et al.  Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea‐pig in vitro. , 1990, The Journal of physiology.

[20]  Mark C. W. van Rossum,et al.  Memory retention and spike-timing-dependent plasticity. , 2009, Journal of neurophysiology.

[21]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[22]  Wulfram Gerstner,et al.  Phenomenological models of synaptic plasticity based on spike timing , 2008, Biological Cybernetics.

[23]  Sandro Romani,et al.  Learning in realistic networks of spiking neurons and spike‐driven plastic synapses , 2005, The European journal of neuroscience.

[24]  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.

[25]  T. Bliss,et al.  The Hippocampus Book , 2006 .

[26]  D. Amaral,et al.  Historical Perspective: Proposed Functions, Biological Characteristics, and Neurobiological Models of the Hippocampus , 2009 .

[27]  S. Wang,et al.  Graded bidirectional synaptic plasticity is composed of switch-like unitary events. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[28]  S. Kaplan The Physiology of Thought , 1950 .

[29]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[30]  David W. Nauen,et al.  Coactivation and timing-dependent integration of synaptic potentiation and depression , 2005, Nature Neuroscience.

[31]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[32]  L. Abbott,et al.  Competitive Hebbian learning through spike-timing-dependent synaptic plasticity , 2000, Nature Neuroscience.

[33]  R. Malenka,et al.  Synaptic scaling mediated by glial TNF-α , 2006, Nature.

[34]  Daniel J. Amit,et al.  Spike-Driven Synaptic Dynamics Generating Working Memory States , 2003, Neural Computation.

[35]  Y. Dan,et al.  Contribution of individual spikes in burst-induced long-term synaptic modification. , 2006, Journal of neurophysiology.

[36]  Haim Sompolinsky,et al.  Learning Input Correlations through Nonlinear Temporally Asymmetric Hebbian Plasticity , 2003, The Journal of Neuroscience.

[37]  S. J. Martin,et al.  Synaptic plasticity and memory: an evaluation of the hypothesis. , 2000, Annual review of neuroscience.

[38]  Niraj S. Desai,et al.  Homeostatic plasticity in the CNS: synaptic and intrinsic forms , 2003, Journal of Physiology-Paris.

[39]  Lubica Benusková,et al.  STDP rule endowed with the BCM sliding threshold accounts for hippocampal heterosynaptic plasticity , 2007, Journal of Computational Neuroscience.

[40]  David B. Grayden,et al.  Spike-Timing-Dependent Plasticity: The Relationship to Rate-Based Learning for Models with Weight Dynamics Determined by a Stable Fixed Point , 2004, Neural Computation.

[41]  Guo-Qiang Bi,et al.  Spatiotemporal specificity of synaptic plasticity: cellular rules and mechanisms , 2002, Biological Cybernetics.

[42]  E. Rolls,et al.  A computational theory of hippocampal function, and empirical tests of the theory , 2006, Progress in Neurobiology.

[43]  W. Gerstner,et al.  Triplets of Spikes in a Model of Spike Timing-Dependent Plasticity , 2006, The Journal of Neuroscience.

[44]  Marco Idiart,et al.  Memory retrieval time and memory capacity of the CA3 network: role of gamma frequency oscillations. , 2007, Learning & memory.

[45]  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.

[46]  Walter Senn,et al.  Beyond spike timing: the role of nonlinear plasticity and unreliable synapses , 2002, Biological Cybernetics.

[47]  Wulfram Gerstner,et al.  Intrinsic Stabilization of Output Rates by Spike-Based Hebbian Learning , 2001, Neural Computation.

[48]  J. Nadal,et al.  What can we learn from synaptic weight distributions? , 2007, Trends in Neurosciences.

[49]  Edmund T. Rolls,et al.  Memory, Attention, and Decision-Making , 2007 .

[50]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

[51]  Eugene M. Izhikevich,et al.  Which model to use for cortical spiking neurons? , 2004, IEEE Transactions on Neural Networks.

[52]  Eugene M. Izhikevich,et al.  Relating STDP to BCM , 2003, Neural Computation.

[53]  Thomas P. Trappenberg,et al.  Computational consequences of experimentally derived spike-time and weight dependent plasticity rules , 2007, Biological Cybernetics.

[54]  D. Debanne,et al.  Heterogeneity of Synaptic Plasticity at Unitary CA3–CA1 and CA3–CA3 Connections in Rat Hippocampal Slice Cultures , 1999, The Journal of Neuroscience.

[55]  Jean-Pascal Pfister,et al.  Optimality Model of Unsupervised Spike-Timing-Dependent Plasticity: Synaptic Memory and Weight Distribution , 2007, Neural Computation.

[56]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. , 1973, Experimental neurology.

[57]  P. Dayan,et al.  Matching storage and recall: hippocampal spike timing–dependent plasticity and phase response curves , 2005, Nature Neuroscience.

[58]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[59]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.