Functional mechanisms underlie the emergence of a diverse range of plasticity phenomena

Diverse plasticity mechanisms are orchestrated to shape the spatiotemporal dynamics underlying brain functions. However, why these plasticity rules emerge and how their dynamics interact with neural activity to give rise to complex neural circuit dynamics remains largely unknown. Here we show that both Hebbian and homeostatic plasticity rules emerge from a functional perspective of neuronal dynamics whereby each neuron learns to encode its own activity in the population activity, so that the activity of the presynaptic neuron can be decoded from the activity of its postsynaptic neurons. We explain how a range of experimentally observed plasticity phenomena with widely separated time scales emerge from learning this encoding function, including STDP and its frequency dependence, and metaplasticity. We show that when implemented in neural circuits, these plasticity rules naturally give rise to essential neural response properties, including variable neural dynamics with balanced excitation and inhibition, and approximately log-normal distributions of synaptic strengths, while simultaneously encoding a complex real-world visual stimulus. These findings establish a novel function-based account of diverse plasticity mechanisms, providing a unifying framework relating plasticity, dynamics and neural computation.

[1]  Christian K. Machens,et al.  Learning optimal spike-based representations , 2012, NIPS.

[2]  W. Gerstner,et al.  Generalized Bienenstock-Cooper-Munro rule for spiking neurons that maximizes information transmission. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Jean-Pascal Pfister,et al.  STDP in Adaptive Neurons Gives Close-To-Optimal Information Transmission , 2010, Front. Comput. Neurosci..

[4]  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.

[5]  Wulfram Gerstner,et al.  Integrating Hebbian and homeostatic plasticity: the current state of the field and future research directions , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[7]  Vivien A. Casagrande,et al.  Biophysics of Computation: Information Processing in Single Neurons , 1999 .

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

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

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

[11]  Everton J. Agnes,et al.  Diverse synaptic plasticity mechanisms orchestrated to form and retrieve memories in spiking neural networks , 2015, Nature Communications.

[12]  John H. C. Palmer,et al.  Formation and Regulation of Dynamic Patterns in Two-Dimensional Spiking Neural Circuits with Spike-Timing-Dependent Plasticity , 2013, Neural Computation.

[13]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[14]  Y. Loewenstein,et al.  Multiplicative Dynamics Underlie the Emergence of the Log-Normal Distribution of Spine Sizes in the Neocortex In Vivo , 2011, The Journal of Neuroscience.

[15]  G. Buzsáki,et al.  The log-dynamic brain: how skewed distributions affect network operations , 2014, Nature Reviews Neuroscience.

[16]  W. Gerstner,et al.  The temporal paradox of Hebbian learning and homeostatic plasticity , 2017, Current Opinion in Neurobiology.

[17]  Pascal Vincent,et al.  Representation Learning: A Review and New Perspectives , 2012, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[18]  Niraj S. Desai,et al.  Homeostatic Plasticity and STDP: Keeping a Neuron's Cool in a Fluctuating World , 2010, Front. Syn. Neurosci..

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

[20]  Jinyuan Yan,et al.  Bow-tie signaling in c-di-GMP: Machine learning in a simple biochemical network , 2017, PLoS Comput. Biol..

[21]  Mark F Bear,et al.  Evidence for Altered NMDA Receptor Function as a Basis for Metaplasticity in Visual Cortex , 2003, The Journal of Neuroscience.

[22]  W. Senn,et al.  Matching Recall and Storage in Sequence Learning with Spiking Neural Networks , 2013, The Journal of Neuroscience.

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

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

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

[26]  Maxim Bazhenov,et al.  Homeostatic role of heterosynaptic plasticity: models and experiments , 2015, Front. Comput. Neurosci..

[27]  G. Turrigiano The dialectic of Hebb and homeostasis , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[28]  Jérémie Barral,et al.  Synaptic scaling rule preserves excitatory–inhibitory balance and salient neuronal network dynamics , 2016, Nature Neuroscience.

[29]  Wyeth Bair,et al.  Visual receptive field organization , 2005, Current Opinion in Neurobiology.

[30]  J. A. Henderson,et al.  Dynamical patterns underlying response properties of cortical circuits , 2018, Journal of The Royal Society Interface.

[31]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[32]  Mark F. Bear,et al.  The BCM theory of synapse modification at 30: interaction of theory with experiment , 2012, Nature Reviews Neuroscience.

[33]  John H. C. Palmer,et al.  Learning and executing goal-directed choices by internally generated sequences in spiking neural circuits , 2017, PLoS Comput. Biol..

[34]  Everton J. Agnes,et al.  Inhibitory Plasticity: Balance, Control, and Codependence. , 2017, Annual review of neuroscience.

[35]  Guigang Zhang,et al.  Deep Learning , 2016, Int. J. Semantic Comput..

[36]  Nitish Srivastava,et al.  Dropout: a simple way to prevent neural networks from overfitting , 2014, J. Mach. Learn. Res..

[37]  G D Lewen,et al.  Reproducibility and Variability in Neural Spike Trains , 1997, Science.

[38]  R. Froemke Plasticity of cortical excitatory-inhibitory balance. , 2015, Annual review of neuroscience.

[39]  Haim Sompolinsky,et al.  Computational neuroscience: beyond the local circuit , 2014, Current Opinion in Neurobiology.

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

[41]  T. Delbruck,et al.  > Replace This Line with Your Paper Identification Number (double-click Here to Edit) < 1 , 2022 .

[42]  John H. C. Palmer,et al.  Associative learning of classical conditioning as an emergent property of spatially extended spiking neural circuits with synaptic plasticity , 2014, Front. Comput. Neurosci..

[43]  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.

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

[45]  Michael Okun,et al.  Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities , 2008, Nature Neuroscience.

[46]  Wulfram Gerstner,et al.  Does computational neuroscience need new synaptic learning paradigms? , 2016, Current Opinion in Behavioral Sciences.

[47]  Rui Ponte Costa,et al.  Unified pre- and postsynaptic long-term plasticity enables reliable and flexible learning , 2015, eLife.

[48]  M. Bear,et al.  Experience-dependent modification of synaptic plasticity in visual cortex , 1996, Nature.

[49]  Pulin Gong,et al.  Propagating Waves Can Explain Irregular Neural Dynamics , 2015, The Journal of Neuroscience.

[50]  W. Gerstner,et al.  Hebbian plasticity requires compensatory processes on multiple timescales , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[51]  Christian K. Machens,et al.  Efficient codes and balanced networks , 2016, Nature Neuroscience.

[52]  W. Gerstner,et al.  Connectivity reflects coding: a model of voltage-based STDP with homeostasis , 2010, Nature Neuroscience.

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

[54]  Matthieu Gilson,et al.  Models of Metaplasticity: A Review of Concepts , 2015, Front. Comput. Neurosci..

[55]  W. Abraham,et al.  Mechanisms of heterosynaptic metaplasticity , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[56]  J. Pfister,et al.  A triplet spike-timing–dependent plasticity model generalizes the Bienenstock–Cooper–Munro rule to higher-order spatiotemporal correlations , 2011, Proceedings of the National Academy of Sciences.

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

[58]  Tobi Delbrück,et al.  A 128$\times$ 128 120 dB 15 $\mu$s Latency Asynchronous Temporal Contrast Vision Sensor , 2008, IEEE Journal of Solid-State Circuits.

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

[60]  Henning Sprekeler,et al.  Inhibitory Plasticity Balances Excitation and Inhibition in Sensory Pathways and Memory Networks , 2011, Science.

[61]  M. Poo,et al.  Calcium stores regulate the polarity and input specificity of synaptic modification , 2000, Nature.

[62]  Konrad P. Körding,et al.  Toward an Integration of Deep Learning and Neuroscience , 2016, bioRxiv.