Beyond STDP—towards diverse and functionally relevant plasticity rules

Synaptic plasticity, induced by the close temporal association of two neural signals, supports associative forms of learning. However, the millisecond timescales for association often do not match the much longer delays for behaviorally relevant signals that supervise learning. In particular, information about the behavioral outcome of neural activity can be delayed, leading to a problem of temporal credit assignment. Recent studies suggest that synaptic plasticity can have temporal rules that not only accommodate the delays relevant to the circuit, but also be precisely tuned to the behavior the circuit supports. These discoveries highlight the diversity of plasticity rules, whose temporal requirements may depend on circuit delays and the contingencies of behavior.

[1]  Stephanie E Palmer,et al.  Learning to make external sensory stimulus predictions using internal correlations in populations of neurons , 2017, Proceedings of the National Academy of Sciences.

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

[3]  Susumu Tonegawa,et al.  Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons , 2015, Nature Neuroscience.

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

[5]  W. Gerstner,et al.  Spike-Timing-Dependent Plasticity: A Comprehensive Overview , 2012, Front. Syn. Neurosci..

[6]  Toshiki Tazoe,et al.  Spike-Timing-Dependent Plasticity in Lower-Limb Motoneurons after 1 Human Spinal Cord Injury , 2017 .

[7]  N. Spruston,et al.  Questions about STDP as a General Model of Synaptic Plasticity , 2010, Front. Syn. Neurosci..

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

[9]  Jackie Schiller,et al.  The Many Worlds of Plasticity Rules , 2018, Trends in Neurosciences.

[10]  W. Gerstner,et al.  Neuromodulated Spike-Timing-Dependent Plasticity, and Theory of Three-Factor Learning Rules , 2016, Front. Neural Circuits.

[11]  J. Wickens,et al.  Timing is not Everything: Neuromodulation Opens the STDP Gate , 2010, Front. Syn. Neurosci..

[12]  D. Johnston,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997 .

[13]  W. Schultz,et al.  Sequential neuromodulation of Hebbian plasticity offers mechanism for effective reward-based navigation , 2017, eLife.

[14]  M. Bear,et al.  A Cholinergic Mechanism for Reward Timing within Primary Visual Cortex , 2013, Neuron.

[15]  Su Z. Hong,et al.  Distinct Eligibility Traces for LTP and LTD in Cortical Synapses , 2015, Neuron.

[16]  G. Bi,et al.  Gain in sensitivity and loss in temporal contrast of STDP by dopaminergic modulation at hippocampal synapses , 2009, Proceedings of the National Academy of Sciences.

[17]  Gayle M. Wittenberg,et al.  Spike Timing Dependent Plasticity: A Consequence of More Fundamental Learning Rules , 2010, Front. Comput. Neurosci..

[18]  Nicolangelo Iannella,et al.  Modulating STDP Balance Impacts the Dendritic Mosaic , 2017, Front. Comput. Neurosci..

[19]  Z. Josh Huang,et al.  A Cortico-Hippocampal Learning Rule Shapes Inhibitory Microcircuit Activity to Enhance Hippocampal Information Flow , 2013, Neuron.

[20]  Sho Yagishita,et al.  A critical time window for dopamine actions on the structural plasticity of dendritic spines , 2014, Science.

[21]  Tomoki Fukai,et al.  Detailed dendritic excitatory/inhibitory balance through heterosynaptic spike-timing-dependent plasticity , 2016 .

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

[23]  J. Albus A Theory of Cerebellar Function , 1971 .

[24]  M. R. Mehta,et al.  Role of experience and oscillations in transforming a rate code into a temporal code , 2002, Nature.

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

[26]  Joshua L. Plotkin,et al.  Dopamine and synaptic plasticity in dorsal striatal circuits controlling action selection , 2009, Current Opinion in Neurobiology.

[27]  R. F. Thompson,et al.  Temporal specificity of long-term depression in parallel fiber--Purkinje synapses in rat cerebellar slice. , 1995, Learning & memory.

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

[29]  M. Kilgard,et al.  Cortical map reorganization enabled by nucleus basalis activity. , 1998, Science.

[30]  Harel Z. Shouval,et al.  The Role of Multiple Neuromodulators in Reinforcement Learning That Is Based on Competition between Eligibility Traces , 2016, Front. Synaptic Neurosci..

[31]  Beatriz E. P. Mizusaki,et al.  Functional consequences of pre- and postsynaptic expression of synaptic plasticity , 2016, bioRxiv.

[32]  Huibert D. Mansvelder,et al.  Distributed Network Actions by Nicotine Increase the Threshold for Spike-Timing-Dependent Plasticity in Prefrontal Cortex , 2007, Neuron.

[33]  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.

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

[35]  Martin K. Schwarz,et al.  Adrenergic Gate Release for Spike Timing-Dependent Synaptic Potentiation , 2017, Neuron.

[36]  P. Redgrave,et al.  Cortico-Striatal Spike-Timing Dependent Plasticity After Activation of Subcortical Pathways , 2010, Front. Syn. Neurosci..

[37]  Giacomo Koch,et al.  Spike-timing-dependent plasticity in the human dorso-lateral prefrontal cortex , 2016, NeuroImage.

[38]  N. Spruston,et al.  Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity , 2005, Nature Neuroscience.

[39]  D. Feldman The Spike-Timing Dependence of Plasticity , 2012, Neuron.

[40]  Wulfram Gerstner,et al.  Frontiers in Synaptic Neuroscience Synaptic Neuroscience , 2022 .

[41]  Gerald M. Rubin,et al.  Heterosynaptic Plasticity Underlies Aversive Olfactory Learning in Drosophila , 2015, Neuron.

[42]  Toshiki Tazoe,et al.  Spike-timing-dependent plasticity in lower-limb motoneurons after human spinal cord injury. , 2017, Journal of neurophysiology.

[43]  Mark S. Cembrowski,et al.  Spatial Gene-Expression Gradients Underlie Prominent Heterogeneity of CA1 Pyramidal Neurons , 2016, Neuron.

[44]  D. Feldman,et al.  Spike Timing-Dependent Synaptic Depression in the In Vivo Barrel Cortex of the Rat , 2007, The Journal of Neuroscience.

[45]  P. Greengard,et al.  Dichotomous Dopaminergic Control of Striatal Synaptic Plasticity , 2008, Science.

[46]  J. Kerr,et al.  Dopamine Receptor Activation Is Required for Corticostriatal Spike-Timing-Dependent Plasticity , 2008, The Journal of Neuroscience.

[47]  Martina Sgritta,et al.  Hebbian Spike-Timing Dependent Plasticity at the Cerebellar Input Stage , 2017, The Journal of Neuroscience.

[48]  G. Rubin,et al.  The neuronal architecture of the mushroom body provides a logic for associative learning , 2014, eLife.

[49]  Paola Cognigni,et al.  Do the right thing: neural network mechanisms of memory formation, expression and update in Drosophila , 2018, Current Opinion in Neurobiology.

[50]  David H. Brann,et al.  Input-Timing-Dependent Plasticity in the Hippocampal CA2 Region and Its Potential Role in Social Memory , 2019, Neuron.

[51]  G. Stuart,et al.  Dendritic small conductance calcium-activated potassium channels activated by action potentials suppress EPSPs and gate spike-timing dependent synaptic plasticity , 2017, eLife.

[52]  E. Meloni,et al.  Coactivation of Thalamic and Cortical Pathways Induces Input Timing-Dependent Plasticity in Amygdala , 2011, Nature Neuroscience.

[53]  G. Laurent,et al.  Corrigendum: Conditional modulation of spike-timing-dependent plasticity for olfactory learning , 2012, Nature.

[54]  M. Merzenich,et al.  Cortical remodelling induced by activity of ventral tegmental dopamine neurons , 2001, Nature.

[55]  S. Siegelbaum,et al.  A Role for Synaptic Inputs at Distal Dendrites: Instructive Signals for Hippocampal Long-Term Plasticity , 2007, Neuron.

[56]  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.

[57]  A. Holtmaat,et al.  Sensory-evoked LTP driven by dendritic plateau potentials in vivo , 2014, Nature.

[58]  Y. Frégnac,et al.  Temporal constraints in associative synaptic plasticity in hippocampus and neocortex. , 1995, Canadian journal of physiology and pharmacology.

[59]  D. Debanne,et al.  Asynchronous pre- and postsynaptic activity induces associative long-term depression in area CA1 of the rat hippocampus in vitro. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Wulfram Gerstner,et al.  A History of Spike-Timing-Dependent Plasticity , 2011, Front. Syn. Neurosci..

[61]  J. Knott The organization of behavior: A neuropsychological theory , 1951 .

[62]  Wulfram Gerstner,et al.  Multicontact Co-operativity in Spike-Timing–Dependent Structural Plasticity Stabilizes Networks , 2016, Cerebral cortex.

[63]  J. Raymond,et al.  Timing Rules for Synaptic Plasticity Matched to Behavioral Function , 2016, Neuron.

[64]  Shih-Chii Liu,et al.  Perceptron learning rule derived from spike-frequency adaptation and spike-time-dependent plasticity , 2010, Proceedings of the National Academy of Sciences.

[65]  Walter Senn,et al.  Spatio-Temporal Credit Assignment in Neuronal Population Learning , 2011, PLoS Comput. Biol..

[66]  Daniel A. Dombeck,et al.  Increased Prevalence of Calcium Transients across the Dendritic Arbor during Place Field Formation , 2017, Neuron.

[67]  Heydar Davoudi,et al.  Selective Activation of a Putative Reinforcement Signal Conditions Cued Interval Timing in Primary Visual Cortex , 2015, Current Biology.

[68]  Johannes C. Dahmen,et al.  Stimulus-Timing-Dependent Plasticity of Cortical Frequency Representation , 2008, The Journal of Neuroscience.

[69]  Y. Humeau,et al.  Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition , 2003, Nature Neuroscience.

[70]  David A. Smith,et al.  Temporal covariance of pre- and postsynaptic activity regulates functional connectivity in the visual cortex. , 1994, Journal of neurophysiology.

[71]  Katie C. Bittner,et al.  Behavioral time scale synaptic plasticity underlies CA1 place fields , 2017, Science.

[72]  L. Abbott,et al.  Extending the effects of spike-timing-dependent plasticity to behavioral timescales. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[73]  E. Izhikevich Solving the distal reward problem through linkage of STDP and dopamine signaling , 2007, BMC Neuroscience.

[74]  D. Marr A theory of cerebellar cortex , 1969, The Journal of physiology.

[75]  S. Nelson,et al.  Strength through Diversity , 2008, Neuron.

[76]  W. Schultz,et al.  Retroactive modulation of spike timing-dependent plasticity by dopamine , 2015, eLife.

[77]  Wade G. Regehr,et al.  Timing dependence of the induction of cerebellar LTD , 2008, Neuropharmacology.

[78]  Yukio Nishimura,et al.  Spike-Timing-Dependent Plasticity in Primate Corticospinal Connections Induced during Free Behavior , 2013, Neuron.

[79]  Daniel A. Dombeck,et al.  Calcium transient prevalence across the dendritic arbor predicts place field properties , 2014, Nature.