Decorrelation of Spiking Variability and Improved Information Transfer Through Feedforward Divisive Normalization

Response variability is often positively correlated in pairs of similarly tuned neurons in the visual cortex. Many authors have considered correlated variability to prevent postsynaptic neurons from averaging across large groups of inputs to obtain reliable stimulus estimates. However, a simple average of variability ignores nonlinearities in cortical signal integration. This study shows that feedforward divisive normalization of a neuron's inputs effectively decorrelates their variability. Furthermore, we show that optimal linear estimates of a stimulus parameter that are based on normalized inputs are more accurate than those based on nonnormalized inputs, due partly to reduced correlations, and that these estimates improve with increasing population size up to several thousand neurons. This suggests that neurons may possess a simple mechanism for substantially decorrelating noise in their inputs. Further work is needed to reconcile this conclusion with past evidence that correlated noise impairs visual perception.

[1]  P. Goldman-Rakic,et al.  Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. , 2002, Journal of neurophysiology.

[2]  A. P. Georgopoulos,et al.  Variability and Correlated Noise in the Discharge of Neurons in Motor and Parietal Areas of the Primate Cortex , 1998, The Journal of Neuroscience.

[3]  Piet Van Mieghem,et al.  Emergence of Modular Structure in a Large-Scale Brain Network with Interactions between Dynamics and Connectivity , 2010, Front. Comput. Neurosci..

[4]  Emilio Salinas,et al.  Vector reconstruction from firing rates , 1994, Journal of Computational Neuroscience.

[5]  Néstor Parga,et al.  Auto- and crosscorrelograms for the spike response of leaky integrate-and-fire neurons with slow synapses. , 2006, Physical review letters.

[6]  G. DeAngelis,et al.  Contribution of Middle Temporal Area to Coarse Depth Discrimination: Comparison of Neuronal and Psychophysical Sensitivity , 2003, The Journal of Neuroscience.

[7]  T. Albright,et al.  Efficient Discrimination of Temporal Patterns by Motion-Sensitive Neurons in Primate Visual Cortex , 1998, Neuron.

[8]  Nicholas L. Port,et al.  Erratum: Variability and correlated noise in the discharge of neurons in motor and parietal areas of the primate cortex (Journal of Neuroscience (February, 1998) (1161-1170)) , 1998 .

[9]  Christof Koch,et al.  Temporal Precision of Spike Trains in Extrastriate Cortex of the Behaving Macaque Monkey , 1999, Neural Computation.

[10]  J. Movshon,et al.  Dynamics of Suppression in Macaque Primary Visual Cortex , 2006, The Journal of Neuroscience.

[11]  Tomaso A. Poggio,et al.  A Canonical Neural Circuit for Cortical Nonlinear Operations , 2008, Neural Computation.

[12]  P. L. V. Kan,et al.  Response covariance in cat visual cortex , 2004, Experimental Brain Research.

[13]  J. Maunsell,et al.  Attention improves performance primarily by reducing interneuronal correlations , 2009, Nature Neuroscience.

[14]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[15]  Eero P. Simoncelli,et al.  Natural signal statistics and sensory gain control , 2001, Nature Neuroscience.

[16]  R. Navarro,et al.  Optimal coding through divisive normalization models of V1 neurons , 2003, Network.

[17]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  S. Prescott,et al.  Gain control of firing rate by shunting inhibition: Roles of synaptic noise and dendritic saturation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. Ringach Population coding under normalization , 2010, Vision Research.

[20]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

[21]  Eric Shea-Brown,et al.  Stimulus-Dependent Correlations and Population Codes , 2008, Neural Computation.

[22]  Chris Eliasmith,et al.  Neural Engineering: Computation, Representation, and Dynamics in Neurobiological Systems , 2004, IEEE Transactions on Neural Networks.

[23]  M. Gazzaniga The cognitive neurosciences, 3rd edition , 2004 .

[24]  M. A. Smith,et al.  The Role of Correlations in Direction and Contrast Coding in the Primary Visual Cortex , 2007, The Journal of Neuroscience.

[25]  Nicholas J. Priebe,et al.  Estimating Target Speed from the Population Response in Visual Area MT , 2004, The Journal of Neuroscience.

[26]  J. Ko Sensory discrimination: neural processes preceding discrimination decision. , 1980 .

[27]  S. Treue,et al.  Misperceptions of speed are accounted for by the responses of neurons in macaque cortical area MT. , 2011, Journal of neurophysiology.

[28]  Angelo Arleo,et al.  Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity , 2000, Biological Cybernetics.

[29]  G. Orban,et al.  Human velocity and direction discrimination measured with random dot patterns , 1988, Vision Research.

[30]  Jude F. Mitchell,et al.  Spatial Attention Decorrelates Intrinsic Activity Fluctuations in Macaque Area V4 , 2009, Neuron.

[31]  J. Movshon,et al.  Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex , 1997, The Journal of Neuroscience.

[32]  R. Silver,et al.  Shunting Inhibition Modulates Neuronal Gain during Synaptic Excitation , 2003, Neuron.

[33]  Eero P. Simoncelli,et al.  A model of neuronal responses in visual area MT , 1998, Vision Research.

[34]  B. Cumming,et al.  Macaque V2 Neurons, But Not V1 Neurons, Show Choice-Related Activity , 2006, The Journal of Neuroscience.

[35]  W. Newsome,et al.  Estimates of the Contribution of Single Neurons to Perception Depend on Timescale and Noise Correlation , 2009, The Journal of Neuroscience.

[36]  W. Bair,et al.  Correlated Firing in Macaque Visual Area MT: Time Scales and Relationship to Behavior , 2001, The Journal of Neuroscience.

[37]  H. O. Lancaster Some properties of the bivariate normal distribution considered in the form of a contingency table , 1957 .

[38]  D. G. Albrecht,et al.  Cortical neurons: Isolation of contrast gain control , 1992, Vision Research.

[39]  E. Seidemann,et al.  Optimal decoding of correlated neural population responses in the primate visual cortex , 2006, Nature Neuroscience.

[40]  M. Carandini,et al.  Summation and division by neurons in primate visual cortex. , 1994, Science.

[41]  P. Dayan,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S9 References the Asynchronous State in Cortical Circuits , 2022 .

[42]  Jaime de la Rocha,et al.  Supplementary Information for the article ‘ Correlation between neural spike trains increases with firing rate ’ , 2007 .

[43]  M. A. Smith,et al.  Spatial and Temporal Scales of Neuronal Correlation in Primary Visual Cortex , 2008, The Journal of Neuroscience.

[44]  Xin Huang,et al.  Noise correlations in cortical area MT and their potential impact on trial-by-trial variation in the direction and speed of smooth-pursuit eye movements. , 2009, Journal of neurophysiology.

[45]  J. Movshon,et al.  The statistical reliability of signals in single neurons in cat and monkey visual cortex , 1983, Vision Research.

[46]  J A Solomon,et al.  Model of visual contrast gain control and pattern masking. , 1997, Journal of the Optical Society of America. A, Optics, image science, and vision.

[47]  H. Sompolinsky,et al.  Population coding in neuronal systems with correlated noise. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[48]  Pieter R. Roelfsema,et al.  Noise Correlations Have Little Influence on the Coding of Selective Attention in Area V1 , 2008, Cerebral cortex.

[49]  Brent Doiron,et al.  Subtractive and Divisive Inhibition: Effect of Voltage-Dependent Inhibitory Conductances and Noise , 2001, Neural Computation.

[50]  A. Parker,et al.  The Precision of Single Neuron Responses in Cortical Area V1 during Stereoscopic Depth Judgments , 2000, The Journal of Neuroscience.

[51]  R. Navarro,et al.  Optimal coding through divisive normalization models of V1 neurons. , 2003 .

[52]  K. O. Johnson,et al.  Sensory discrimination: neural processes preceding discrimination decision. , 1980, Journal of neurophysiology.

[53]  Michael Rudolph,et al.  A Fast-Conducting, Stochastic Integrative Mode for Neocortical Neurons InVivo , 2003, The Journal of Neuroscience.

[54]  Alexander S. Ecker,et al.  Decorrelated Neuronal Firing in Cortical Microcircuits , 2010, Science.

[55]  A. Destexhe Kinetic Models of Synaptic Transmission , 1997 .

[56]  Robert Rosenbaum,et al.  Frontiers in Computational Neuroscience Computational Neuroscience , 2022 .

[57]  Timothy D. Hanks,et al.  Bounded Integration in Parietal Cortex Underlies Decisions Even When Viewing Duration Is Dictated by the Environment , 2008, The Journal of Neuroscience.

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

[59]  Bryan P. Tripp,et al.  A Search For Principles of Basal Ganglia Function , 2009 .

[60]  Romain Brette,et al.  Generation of Correlated Spike Trains , 2009, Neural Computation.

[61]  R. Rebonato,et al.  The Most General Methodology to Create a Valid Correlation Matrix for Risk Management and Option Pricing Purposes , 2011 .

[62]  M. Carandini,et al.  A Synaptic Explanation of Suppression in Visual Cortex , 2002, The Journal of Neuroscience.

[63]  Frances S. Chance,et al.  Drivers and modulators from push-pull and balanced synaptic input. , 2005, Progress in brain research.

[64]  Mike W Oram,et al.  Visual stimulation decorrelates neuronal activity. , 2011, Journal of neurophysiology.

[65]  D. Heeger Normalization of cell responses in cat striate cortex , 1992, Visual Neuroscience.

[66]  J. Donoghue,et al.  Neuronal Interactions Improve Cortical Population Coding of Movement Direction , 1999, The Journal of Neuroscience.

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

[68]  M. Carandini Receptive fields and suppressive fields in the early visual system , 2004 .

[69]  Bartlett W. Mel,et al.  Arithmetic of Subthreshold Synaptic Summation in a Model CA1 Pyramidal Cell , 2003, Neuron.

[70]  John H. R. Maunsell,et al.  Dynamics of neuronal responses in macaque MT and VIP during motion detection , 2002, Nature Neuroscience.

[71]  W. Newsome,et al.  Correlation between Speed Perception and Neural Activity in the Middle Temporal Visual Area , 2005, The Journal of Neuroscience.

[72]  J L Gallant,et al.  Sparse coding and decorrelation in primary visual cortex during natural vision. , 2000, Science.

[73]  T. Sejnowski,et al.  Impact of Correlated Synaptic Input on Output Firing Rate and Variability in Simple Neuronal Models , 2000, The Journal of Neuroscience.

[74]  W. Bialek,et al.  Naturalistic stimuli increase the rate and efficiency of information transmission by primary auditory afferents , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[76]  A. Aertsen,et al.  Dynamics of neuronal interactions in monkey cortex in relation to behavioural events , 1995, Nature.

[77]  A. Parker,et al.  Sense and the single neuron: probing the physiology of perception. , 1998, Annual review of neuroscience.

[78]  Christof Koch,et al.  Shunting Inhibition Does Not Have a Divisive Effect on Firing Rates , 1997, Neural Computation.

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

[80]  M. A. Smith,et al.  Correlations and brain states: from electrophysiology to functional imaging , 2009, Current Opinion in Neurobiology.

[81]  Valentin Dragoi,et al.  Adaptive coding of visual information in neural populations , 2008, Nature.

[82]  Frances S. Chance,et al.  Gain Modulation from Background Synaptic Input , 2002, Neuron.

[83]  Si Wu,et al.  Population Coding and Decoding in a Neural Field: A Computational Study , 2002, Neural Computation.

[84]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[85]  Haim Sompolinsky,et al.  Implications of Neuronal Diversity on Population Coding , 2006, Neural Computation.

[86]  W. Bialek,et al.  Time Course of Information about Motion Direction in Visual Area MT of Macaque Monkeys , 2004, The Journal of Neuroscience.

[87]  James J DiCarlo,et al.  Multiple Object Response Normalization in Monkey Inferotemporal Cortex , 2005, The Journal of Neuroscience.

[88]  G. DeAngelis,et al.  A Logarithmic, Scale-Invariant Representation of Speed in Macaque Middle Temporal Area Accounts for Speed Discrimination Performance , 2005, The Journal of Neuroscience.

[89]  Haim Sompolinsky,et al.  Nonlinear Population Codes , 2004, Neural Computation.

[90]  M. Carandini Amplification of Trial-to-Trial Response Variability by Neurons in Visual Cortex , 2004, PLoS biology.

[91]  M. Carandini,et al.  Suppression without Inhibition in Visual Cortex , 2002, Neuron.

[92]  E T Rolls,et al.  Correlations and the encoding of information in the nervous system , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[93]  E. Seidemann,et al.  Linking Neuronal and Behavioral Performance in a Reaction-Time Visual Detection Task , 2007, The Journal of Neuroscience.