Identification of Multiple Noise Sources Improves Estimation of Neural Responses across Stimulus Conditions

Most models of neural responses are constructed to capture the average response to inputs but poorly reproduce the observed response variability. The origins and structure of this variability have significant implications for how information is encoded and processed in the nervous system. Here, we present a new modeling framework that better captures observed features of neural response variability across stimulus conditions by incorporating multiple sources of noise. We use this model to fit responses of retinal ganglion cells at two different ambient light levels and demonstrate that it captures the full distribution of responses. The model reveals light level-dependent changes that could not be seen with previous models. It shows both large changes in rectification of nonlinear circuit elements and systematic differences in the contributions of different noise sources under different conditions. This modeling framework is general and can be applied to a variety of systems outside the retina.

[1]  E J Chichilnisky,et al.  Prediction and Decoding of Retinal Ganglion Cell Responses with a Probabilistic Spiking Model , 2005, The Journal of Neuroscience.

[2]  E. Chichilnisky,et al.  Temporal resolution of single photon responses in primate rod photoreceptors and limits imposed by cellular noise , 2018, bioRxiv.

[3]  Maxwell H. Turner,et al.  Direction-Selective Circuits Shape Noise to Ensure a Precise Population Code , 2016, Neuron.

[4]  Eero P. Simoncelli,et al.  Inference of Nonlinear Spatial Subunits by Spike-Triggered Clustering in Primate Retina , 2018, bioRxiv.

[5]  M. Freed,et al.  Synaptic noise is an information bottleneck in the inner retina during dynamic visual stimulation , 2014, The Journal of physiology.

[6]  Eero P. Simoncelli,et al.  Modeling the Impact of Common Noise Inputs on the Network Activity of Retinal Ganglion Cells Action Editor: Brent Doiron , 2022 .

[7]  M. Carandini,et al.  The Nature of Shared Cortical Variability , 2015, Neuron.

[8]  Fred Rieke,et al.  Network Variability Limits Stimulus-Evoked Spike Timing Precision in Retinal Ganglion Cells , 2006, Neuron.

[9]  D. Debanne,et al.  Action-potential propagation gated by an axonal IA-like K+ conductance in hippocampus , 1997, Nature.

[10]  Rubén Moreno-Bote,et al.  Poisson-Like Spiking in Circuits with Probabilistic Synapses , 2014, PLoS Comput. Biol..

[11]  Steven W. Flavell,et al.  Feedback from Network States Generates Variability in a Probabilistic Olfactory Circuit , 2015, Cell.

[12]  M. Vorobyev,et al.  Receptor noise as a determinant of colour thresholds , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[13]  Mohsen Jamali,et al.  Coding of envelopes by correlated but not single-neuron activity requires neural variability , 2015, Proceedings of the National Academy of Sciences.

[14]  Eero P. Simoncelli,et al.  Spatio-temporal correlations and visual signalling in a complete neuronal population , 2008, Nature.

[15]  Eero P. Simoncelli,et al.  Spike-triggered neural characterization. , 2006, Journal of vision.

[16]  Michael J. Berry,et al.  Selectivity for multiple stimulus features in retinal ganglion cells. , 2006, Journal of neurophysiology.

[17]  T. Komiyama,et al.  Dynamic Sensory Representations in the Olfactory Bulb: Modulation by Wakefulness and Experience , 2012, Neuron.

[18]  P. Bays Spikes not slots: noise in neural populations limits working memory , 2015, Trends in Cognitive Sciences.

[19]  Eero P. Simoncelli,et al.  Inference of Nonlinear Spatial Subunits in Primate Retina with Spike-Triggered Clustering , 2018 .

[20]  Eero P. Simoncelli,et al.  Partitioning neuronal variability , 2014, Nature Neuroscience.

[21]  Adrienne L Fairhall,et al.  Two-Dimensional Time Coding in the Auditory Brainstem , 2005, The Journal of Neuroscience.

[22]  E J Chichilnisky,et al.  A simple white noise analysis of neuronal light responses , 2001, Network.

[23]  D. Butts,et al.  Tuning Curves, Neuronal Variability, and Sensory Coding , 2006, PLoS biology.

[24]  Kerry J. Kim,et al.  Temporal Contrast Adaptation in the Input and Output Signals of Salamander Retinal Ganglion Cells , 2001, The Journal of Neuroscience.

[25]  F. Rieke,et al.  The impact of photoreceptor noise on retinal gain controls , 2006, Current Opinion in Neurobiology.

[26]  Eero P. Simoncelli,et al.  Spatiotemporal Elements of Macaque V1 Receptive Fields , 2005, Neuron.

[27]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[28]  Jonathan W. Pillow,et al.  Capturing the Dynamical Repertoire of Single Neurons with Generalized Linear Models , 2016, Neural Computation.

[29]  J. L. Schnapf,et al.  Noise and light adaptation in rods of the macaque monkey , 2000, Visual Neuroscience.

[30]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  Chethan Pandarinath,et al.  Ganglion Cell Adaptability: Does the Coupling of Horizontal Cells Play a Role? , 2008, PloS one.

[32]  Wulfram Gerstner,et al.  Predicting spike timing of neocortical pyramidal neurons by simple threshold models , 2006, Journal of Computational Neuroscience.

[33]  E.J. Chichilnisky,et al.  Cone photoreceptor contributions to noise and correlations in the retinal output , 2011, Nature Neuroscience.

[34]  R. Reid,et al.  Low Response Variability in Simultaneously Recorded Retinal, Thalamic, and Cortical Neurons , 2000, Neuron.

[35]  R. Reid,et al.  Predicting Every Spike A Model for the Responses of Visual Neurons , 2001, Neuron.

[36]  A. Pouget,et al.  Neural correlations, population coding and computation , 2006, Nature Reviews Neuroscience.

[37]  G. J. Tomko,et al.  Neuronal variability: non-stationary responses to identical visual stimuli. , 1974, Brain research.

[38]  William N. Grimes,et al.  The Synaptic and Circuit Mechanisms Underlying a Change in Spatial Encoding in the Retina , 2014, Neuron.

[39]  G Buchsbaum,et al.  Rate of quantal transmitter release at the mammalian rod synapse. , 1994, Biophysical journal.

[40]  H. Barlow Retinal noise and absolute threshold. , 1956, Journal of the Optical Society of America.

[41]  Uri T Eden,et al.  A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. , 2005, Journal of neurophysiology.

[42]  Alexander S. Ecker,et al.  The Effect of Noise Correlations in Populations of Diversely Tuned Neurons , 2011, The Journal of Neuroscience.

[43]  Fred Rieke,et al.  Synaptic Rectification Controls Nonlinear Spatial Integration of Natural Visual Inputs , 2016, Neuron.

[44]  Eero P. Simoncelli,et al.  Biases in white noise analysis due to non-Poisson spike generation , 2003, Neurocomputing.

[45]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

[46]  F. Rieke,et al.  Nonlinear Signal Transfer from Mouse Rods to Bipolar Cells and Implications for Visual Sensitivity , 2002, Neuron.

[47]  Peter Dayan,et al.  The Effect of Correlated Variability on the Accuracy of a Population Code , 1999, Neural Computation.

[48]  Fred Rieke,et al.  Origin and Impact of Phototransduction Noise in Primate Cone Photoreceptors , 2013, Nature Neuroscience.

[49]  Tatyana O Sharpee,et al.  Critical and maximally informative encoding between neural populations in the retina , 2014, Proceedings of the National Academy of Sciences.

[50]  Jianhua Lin,et al.  Divergence measures based on the Shannon entropy , 1991, IEEE Trans. Inf. Theory.

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

[52]  S. Wu,et al.  Connexin 36 and rod bipolar cell independent rod pathways drive retinal ganglion cells and optokinetic reflexes , 2016, Vision Research.

[53]  Peter Sterling,et al.  Loss of Sensitivity in an Analog Neural Circuit , 2009, The Journal of Neuroscience.

[54]  Michael J. Berry,et al.  Refractoriness and Neural Precision , 1997, The Journal of Neuroscience.

[55]  Liam Paninski,et al.  Statistical models for neural encoding, decoding, and optimal stimulus design. , 2007, Progress in brain research.

[56]  F. Jäkel,et al.  Spatial four-alternative forced-choice method is the preferred psychophysical method for naïve observers. , 2006, Journal of vision.

[57]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[58]  Michael J. Berry,et al.  The structure and precision of retinal spike trains. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[59]  A. Pouget,et al.  Variance as a Signature of Neural Computations during Decision Making , 2011, Neuron.

[60]  P Lennie,et al.  The control of retinal ganglion cell discharge by receptive field surrounds. , 1975, The Journal of physiology.

[61]  S. Laughlin,et al.  Ion-Channel Noise Places Limits on the Miniaturization of the Brain’s Wiring , 2005, Current Biology.

[62]  H. L. Bryant,et al.  Spike initiation by transmembrane current: a white‐noise analysis. , 1976, The Journal of physiology.

[63]  A. Pouget,et al.  Information-limiting correlations , 2014, Nature Neuroscience.

[64]  M A Freed,et al.  Parallel Cone Bipolar Pathways to a Ganglion Cell Use Different Rates and Amplitudes of Quantal Excitation , 2000, The Journal of Neuroscience.

[65]  W. Gerstner,et al.  Parameter extraction and classification of three cortical neuron types reveals two distinct adaptation mechanisms. , 2012, Journal of neurophysiology.

[66]  Eric Shea-Brown,et al.  How Do Efficient Coding Strategies Depend on Origins of Noise in Neural Circuits? , 2016, PLoS Comput. Biol..