Spike-timing-dependent synaptic plasticity and synaptic democracy in dendrites.

We explored in a computational study the effect of dendrites on excitatory synapses undergoing spike-timing-dependent plasticity (STDP), using both cylindrical dendritic models and reconstructed dendritic trees. We show that even if the initial strength, g(peak), of distal synapses is augmented in a location independent manner, the efficacy of distal synapses diminishes following STDP and proximal synapses would eventually dominate. Indeed, proximal synapses always win over distal synapses following linear STDP rule, independent of the initial synaptic strength distribution in the dendritic tree. This effect is more pronounced as the dendritic cable length increases but it does not depend on the dendritic branching structure. Adding a small multiplicative component to the linear STDP rule, whereby already strong synapses tend to be less potentiated than depressed (and vice versa for weak synapses) did partially "save" distal synapses from "dying out." Another successful strategy for balancing the efficacy of distal and proximal synapses following STDP is to increase the upper bound for the synaptic conductance (g(max)) with distance from the soma. We conclude by discussing an experiment for assessing which of these possible strategies might actually operate in dendrites.

[1]  P. J. Sjöström,et al.  Dendritic excitability and synaptic plasticity. , 2008, Physiological reviews.

[2]  Paul C. Bressloff,et al.  Modeling the role of lateral membrane diffusion in AMPA receptor trafficking along a spiny dendrite , 2008, Journal of Computational Neuroscience.

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

[4]  Roberto Araya,et al.  Sodium channels amplify spine potentials , 2007, Proceedings of the National Academy of Sciences.

[5]  Clifton C. Rumsey,et al.  Synaptic democracy in active dendrites. , 2006, Journal of neurophysiology.

[6]  Johannes J. Letzkus,et al.  Learning Rules for Spike Timing-Dependent Plasticity Depend on Dendritic Synapse Location , 2006, The Journal of Neuroscience.

[7]  Nicolangelo Iannella,et al.  Synaptic efficacy cluster formation across the dendrite via STDP , 2006, Neuroscience Letters.

[8]  P. J. Sjöström,et al.  A Cooperative Switch Determines the Sign of Synaptic Plasticity in Distal Dendrites of Neocortical Pyramidal Neurons , 2006, Neuron.

[9]  Johannes J. Letzkus,et al.  Requirement of dendritic calcium spikes for induction of spike‐timing‐dependent synaptic plasticity , 2006, The Journal of physiology.

[10]  Y. Dan,et al.  Spike timing-dependent plasticity: from synapse to perception. , 2006, Physiological reviews.

[11]  Idan Segev,et al.  The interplay between homeostatic synaptic plasticity and functional dendritic compartments. , 2006, Journal of neurophysiology.

[12]  Nelson Spruston,et al.  Distance-Dependent Differences in Synapse Number and AMPA Receptor Expression in Hippocampal CA1 Pyramidal Neurons , 2006, Neuron.

[13]  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.

[14]  G. Ascoli Mobilizing the base of neuroscience data: the case of neuronal morphologies , 2006, Nature Reviews Neuroscience.

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

[16]  Y. Dan,et al.  Spike-timing-dependent synaptic plasticity depends on dendritic location , 2005, Nature.

[17]  Florentin Wörgötter,et al.  Local learning rules: predicted influence of dendritic location on synaptic modification in spike-timing-dependent plasticity , 2005, Biological Cybernetics.

[18]  Takeshi Aihara,et al.  Spatial Localization of Synapses Required for Supralinear Summation of Action Potentials and EPSPs , 2004, Journal of Computational Neuroscience.

[19]  Arnd Roth,et al.  Rebuilding dendritic democracy. Focus on "equalization of synaptic efficacy by activity- and timing-dependent synaptic plasticity". , 2004, Journal of neurophysiology.

[20]  Clifton C. Rumsey,et al.  Equalization of synaptic efficacy by activity- and timing-dependent synaptic plasticity. , 2004, Journal of neurophysiology.

[21]  S. Siegelbaum,et al.  Hyperpolarization-activated cation currents: from molecules to physiological function. , 2003, Annual review of physiology.

[22]  Rafael Yuste,et al.  Systematic regulation of spine sizes and densities in pyramidal neurons. , 2003, Journal of neurobiology.

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

[24]  Patrick D Roberts,et al.  Stability of negative-image equilibria in spike-timing-dependent plasticity. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[25]  G. Bi,et al.  Temporal asymmetry in spike timing-dependent synaptic plasticity , 2002, Physiology & Behavior.

[26]  K. Holthoff,et al.  A problem with Hebb and local spikes , 2002, Trends in Neurosciences.

[27]  L. Cooper,et al.  A unified model of NMDA receptor-dependent bidirectional synaptic plasticity , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[30]  J. Magee,et al.  Distance-Dependent Increase in AMPA Receptor Number in the Dendrites of Adult Hippocampal CA1 Pyramidal Neurons , 2001, The Journal of Neuroscience.

[31]  L. Abbott,et al.  Cortical Development and Remapping through Spike Timing-Dependent Plasticity , 2001, Neuron.

[32]  Rajesh P. N. Rao,et al.  Spike-Timing-Dependent Hebbian Plasticity as Temporal Difference Learning , 2001, Neural Computation.

[33]  R. Kempter,et al.  Formation of temporal-feature maps by axonal propagation of synaptic learning , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[34]  T. Freund,et al.  Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells , 2001, Neuroscience.

[35]  M. Häusser,et al.  Propagation of action potentials in dendrites depends on dendritic morphology. , 2001, Journal of neurophysiology.

[36]  J E Rubin,et al.  Steady states in an iterative model for multiplicative spike-timing-dependent plasticity , 2001, Network.

[37]  J. Magee Dendritic integration of excitatory synaptic input , 2000, Nature Reviews Neuroscience.

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

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

[40]  P. Roberts,et al.  Modeling inhibitory plasticity in the electrosensory system of mormyrid electric fish. , 2000, Journal of neurophysiology.

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

[42]  J. Magee,et al.  Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons , 2000, Nature Neuroscience.

[43]  Daniel D. Lee,et al.  Equilibrium properties of temporally asymmetric Hebbian plasticity. , 2000, Physical review letters.

[44]  Patrick D. Roberts,et al.  Computational Consequences of Temporally Asymmetric Learning Rules: II. Sensory Image Cancellation , 2000, Journal of Computational Neuroscience.

[45]  D. Feldman,et al.  Timing-Based LTP and LTD at Vertical Inputs to Layer II/III Pyramidal Cells in Rat Barrel Cortex , 2000, Neuron.

[46]  J. Schiller,et al.  NMDA spikes in basal dendrites of cortical pyramidal neurons , 2000, Nature.

[47]  J. Leo van Hemmen,et al.  Modeling Synaptic Plasticity in Conjunction with the Timing of Pre- and Postsynaptic Action Potentials , 2000, Neural Computation.

[48]  B. Sakmann,et al.  Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex , 1999, Nature Neuroscience.

[49]  J. Magee Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons , 1999, Nature Neuroscience.

[50]  Jeffrey C. Magee,et al.  Dendritic I h normalizes temporal summation in hippocampal CA 1 neurons , 1999 .

[51]  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.

[52]  R. Huganir,et al.  Activity-Dependent Modulation of Synaptic AMPA Receptor Accumulation , 1998, Neuron.

[53]  Li I. Zhang,et al.  A critical window for cooperation and competition among developing retinotectal synapses , 1998, Nature.

[54]  R. Nicoll,et al.  Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Niraj S. Desai,et al.  Activity-dependent scaling of quantal amplitude in neocortical neurons , 1998, Nature.

[56]  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.

[57]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

[58]  V. Han,et al.  Synaptic plasticity in a cerebellum-like structure depends on temporal order , 1997, Nature.

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

[60]  M. Bear,et al.  Metaplasticity: the plasticity of synaptic plasticity , 1996, Trends in Neurosciences.

[61]  C. Koch,et al.  Amplification and linearization of distal synaptic input to cortical pyramidal cells. , 1994, Journal of neurophysiology.

[62]  Rafael Yuste,et al.  Ca2+ accumulations in dendrites of neocortical pyramidal neurons: An apical band and evidence for two functional compartments , 1994, Neuron.

[63]  J. Bower,et al.  Simulated responses of cerebellar Purkinje cells are independent of the dendritic location of granule cell synaptic inputs. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[64]  D. Whitteridge,et al.  An intracellular analysis of the visual responses of neurones in cat visual cortex. , 1991, The Journal of physiology.

[65]  R. Traub,et al.  A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. , 1991, Journal of neurophysiology.

[66]  M Marin-Padilla,et al.  Number and distribution of the apical dendritic spines of the layer V pyramidal cells in man , 1967, The Journal of comparative neurology.

[67]  W. Rall Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. , 1967, Journal of neurophysiology.

[68]  W. Rall Branching dendritic trees and motoneuron membrane resistivity. , 1959, Experimental neurology.

[69]  M. London,et al.  Dendritic computation. , 2005, Annual review of neuroscience.

[70]  B. Porr,et al.  Synaptic modifications depend on synapse location and activity: a biophysical model of STDP. , 2005, Bio Systems.

[71]  Abstracts of the 13th Annual Meeting of Israel Society for Neuroscience , 2005, Neural Plasticity.

[72]  Javier DeFelipe,et al.  Spine distribution in cortical pyramidal cells: a common organizational principle across species. , 2002, Progress in brain research.

[73]  K. Svoboda,et al.  Structure and function of dendritic spines. , 2002, Annual review of physiology.

[74]  Jeffrey C. Magee,et al.  Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons , 1999, Nature Neuroscience.