Noisy Synaptic Conductance: Bug or a Feature?

More often than not, action potentials fail to trigger neurotransmitter release. And even when neurotransmitter is released, the resulting change in synaptic conductance is highly variable. Given the energetic cost of generating and propagating action potentials, and the importance of information transmission across synapses, this seems both wasteful and inefficient. However, synaptic noise arising from variable transmission can improve, in certain restricted conditions, information transmission. Under broader conditions, it can improve information transmission per release, a quantity that is relevant given the energetic constraints on computing in the brain. Here we discuss the role, both positive and negative, synaptic noise plays in information transmission and computation in the brain.

[1]  Alexandre Pouget,et al.  A probabilistic approach to demixing odors , 2016, Nature Neuroscience.

[2]  S. Redman Quantal analysis of synaptic potentials in neurons of the central nervous system. , 1990, Physiological reviews.

[3]  Dominique M. Durand,et al.  Enhancement of information transmission of sub-threshold signals applied to distal positions of dendritic trees in hippocampal CA1 neuron models with stochastic resonance , 2010, Biological Cybernetics.

[4]  Raymond J. Dolan,et al.  Information theory, novelty and hippocampal responses: unpredicted or unpredictable? , 2005, Neural Networks.

[5]  N. Stocks,et al.  Suprathreshold stochastic resonance in multilevel threshold systems , 2000, Physical review letters.

[6]  Haim Sompolinsky,et al.  Chaotic Balanced State in a Model of Cortical Circuits , 1998, Neural Computation.

[7]  M L Hines,et al.  Neuron: A Tool for Neuroscientists , 2001, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[8]  Christof Koch,et al.  Detecting and Estimating Signals over Noisy and Unreliable Synapses: Information-Theoretic Analysis , 2001, Neural Computation.

[9]  D. Rusakov,et al.  Receptor actions of synaptically released glutamate: the role of transporters on the scale from nanometers to microns. , 2008, Biophysical journal.

[10]  L. Abbott,et al.  Redundancy Reduction and Sustained Firing with Stochastic Depressing Synapses , 2002, The Journal of Neuroscience.

[11]  J. Borst The low synaptic release probability in vivo , 2010, Trends in Neurosciences.

[12]  J J Jack,et al.  Quantal analysis of excitatory synaptic mechanisms in the mammalian central nervous system. , 1990, Cold Spring Harbor symposia on quantitative biology.

[13]  K. Svoboda,et al.  Facilitation at single synapses probed with optical quantal analysis , 2002, Nature Neuroscience.

[14]  József Fiser,et al.  Perceptual Decision-Making as Probabilistic Inference by Neural Sampling , 2014, Neuron.

[15]  Keiichi Kitajo,et al.  Behavioral stochastic resonance within the human brain. , 2003, Physical review letters.

[16]  Xiao-Jing Wang,et al.  Mean-Driven and Fluctuation-Driven Persistent Activity in Recurrent Networks , 2007, Neural Computation.

[17]  S. D. Meriney,et al.  Are unreliable release mechanisms conserved from NMJ to CNS? , 2013, Trends in Neurosciences.

[18]  Mark S. Cembrowski,et al.  Single excitatory axons form clustered synapses onto CA1 pyramidal cell dendrites , 2018, Nature Neuroscience.

[19]  J. Zylberberg,et al.  Mechanisms of Persistent Activity in Cortical Circuits: Possible Neural Substrates for Working Memory. , 2017, Annual review of neuroscience.

[20]  William B Levy,et al.  Energy-Efficient Neuronal Computation via Quantal Synaptic Failures , 2002, The Journal of Neuroscience.

[21]  Kelvin E. Jones,et al.  Neuronal variability: noise or part of the signal? , 2005, Nature Reviews Neuroscience.

[22]  Daniel Choquet,et al.  Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors , 2004, Nature Neuroscience.

[23]  T. Sejnowski,et al.  Independent Sources of Quantal Variability at Single Glutamatergic Synapses , 2003, The Journal of Neuroscience.

[24]  A. Pouget,et al.  Not Noisy, Just Wrong: The Role of Suboptimal Inference in Behavioral Variability , 2012, Neuron.

[25]  A. Pouget,et al.  Probabilistic Synapses , 2014, 1410.1029.

[26]  J. Hounsgaard,et al.  Voltage fluctuations in neurons: signal or noise? , 2011, Physiological reviews.

[27]  D. Rusakov,et al.  Cannabinoid- and lysophosphatidylinositol-sensitive receptor GPR55 boosts neurotransmitter release at central synapses , 2013, Proceedings of the National Academy of Sciences.

[28]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[29]  M. London,et al.  Sensitivity to perturbations in vivo implies high noise and suggests rate coding in cortex , 2010, Nature.

[30]  Laurence Aitchison,et al.  With or without you: predictive coding and Bayesian inference in the brain , 2017, Current Opinion in Neurobiology.

[31]  L. Savtchenko,et al.  Central Synapses Release a Resource-Efficient Amount of Glutamate , 2012, Nature Neuroscience.

[32]  Nicolette Ognjanovski,et al.  Resonance with subthreshold oscillatory drive organizes activity and optimizes learning in neural networks , 2018, Proceedings of the National Academy of Sciences.

[33]  Qiming Pei,et al.  Effects of noise and synaptic weight on propagation of subthreshold excitatory postsynaptic current signal in a feed-forward neural network , 2018, Nonlinear Dynamics.

[34]  D. Knill,et al.  The Bayesian brain: the role of uncertainty in neural coding and computation , 2004, Trends in Neurosciences.

[35]  A. Zador Impact of synaptic unreliability on the information transmitted by spiking neurons. , 1998, Journal of neurophysiology.

[36]  Alan F. Murray,et al.  Synaptic weight noise during multilayer perceptron training: fault tolerance and training improvements , 1993, IEEE Trans. Neural Networks.

[37]  T W Berger,et al.  Novel expression mechanism for synaptic potentiation: alignment of presynaptic release site and postsynaptic receptor. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[38]  W. Stacey,et al.  Synaptic noise improves detection of subthreshold signals in hippocampal CA1 neurons. , 2001, Journal of neurophysiology.

[39]  L. Savtchenko,et al.  Moderate AMPA receptor clustering on the nanoscale can efficiently potentiate synaptic current , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  Ralf Wessel,et al.  Cortical Circuit Dynamics Are Homeostatically Tuned to Criticality In Vivo , 2019, Neuron.

[41]  T. Bliss,et al.  Optical Quantal Analysis Reveals a Presynaptic Component of LTP at Hippocampal Schaffer-Associational Synapses , 2003, Neuron.

[42]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[43]  Michele Migliore,et al.  Role of an A-Type K+ Conductance in the Back-Propagation of Action Potentials in the Dendrites of Hippocampal Pyramidal Neurons , 1999, Journal of Computational Neuroscience.

[44]  Stefano Allesina,et al.  The Song Overlap Null model Generator (SONG): a new tool for distinguishing between random and non-random song overlap , 2016 .

[45]  Mark D. McDonnell,et al.  The benefits of noise in neural systems: bridging theory and experiment , 2011, Nature Reviews Neuroscience.

[46]  Stefan Glasauer,et al.  Short-term synaptic depression can increase the rate of information transfer at a release site , 2019, PLoS Comput. Biol..

[47]  Mark S. Goldman,et al.  Enhancement of Information Transmission Efficiency by Synaptic Failures , 2004, Neural Computation.

[48]  R. Tsien,et al.  Variability of Neurotransmitter Concentration and Nonsaturation of Postsynaptic AMPA Receptors at Synapses in Hippocampal Cultures and Slices , 1999, Neuron.

[49]  A. Pouget,et al.  Probabilistic brains: knowns and unknowns , 2013, Nature Neuroscience.

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

[51]  L. Pinneo On noise in the nervous system. , 1966, Psychological review.

[52]  Lav R. Varshney,et al.  Optimal Information Storage in Noisy Synapses under Resource Constraints , 2006, Neuron.

[53]  B. Gustafsson,et al.  Paired-Pulse Plasticity at the Single Release Site Level: An Experimental and Computational Study , 2001, The Journal of Neuroscience.

[54]  Thomas A. Blanpied,et al.  A transsynaptic nanocolumn aligns neurotransmitter release to receptors , 2016, Nature.

[55]  Daniel Choquet,et al.  Super-Resolution Imaging Reveals That AMPA Receptors Inside Synapses Are Dynamically Organized in Nanodomains Regulated by PSD95 , 2013, The Journal of Neuroscience.

[56]  Daniel Choquet,et al.  New Concepts in Synaptic Biology Derived from Single-Molecule Imaging , 2008, Neuron.

[57]  Alan F. Murray,et al.  Analogue Synaptic Noise - Implications And Learning Improvements , 1993, Int. J. Neural Syst..

[58]  P. Latham,et al.  The idiosyncratic nature of confidence , 2017, Nature Human Behaviour.

[59]  J. Marvin,et al.  Multiplex imaging relates quantal glutamate release to presynaptic Ca2+ homeostasis at multiple synapses in situ , 2019, Nature Communications.