Five key factors determining pairwise correlations in visual cortex

The responses of cortical neurons to repeated presentation of a stimulus are highly variable, yet correlated. These “noise correlations” reflect a low-dimensional structure of population dynamics. Here, we examine noise correlations in 22,705 pairs of neurons in primary visual cortex (V1) of anesthetized cats, during ongoing activity and in response to artificial and natural visual stimuli. We measured how noise correlations depend on 11 factors. Because these factors are themselves not independent, we distinguished their influences using a nonlinear additive model. The model revealed that five key factors play a predominant role in determining pairwise correlations. Two of these are distance in cortex and difference in sensory tuning: these are known to decrease correlation. A third factor is firing rate: confirming most earlier observations, it markedly increased pairwise correlations. A fourth factor is spike width: cells with a broad spike were more strongly correlated amongst each other. A fifth factor is spike isolation: neurons with worse isolation were more correlated, even if they were recorded on different electrodes. For pairs of neurons with poor isolation, this last factor was the main determinant of correlations. These results were generally independent of stimulus type and timescale of analysis, but there were exceptions. For instance, pairwise correlations depended on difference in orientation tuning more during responses to gratings than to natural stimuli. These results consolidate disjoint observations in a vast literature on pairwise correlations and point towards regularities of population coding in sensory cortex.

[1]  M. Carandini,et al.  Cortical State Determines Global Variability and Correlations in Visual Cortex , 2015, The Journal of Neuroscience.

[2]  Alexander S. Ecker,et al.  State Dependence of Noise Correlations in Macaque Primary Visual Cortex , 2014, Neuron.

[3]  Adam Kohn,et al.  Laminar dependence of neuronal correlations in visual cortex. , 2013, Journal of neurophysiology.

[4]  Valentin Dragoi,et al.  Correlated Variability in Laminar Cortical Circuits , 2012, Neuron.

[5]  M. Corbetta,et al.  Large-scale cortical correlation structure of spontaneous oscillatory activity , 2012, Nature Neuroscience.

[6]  M. Cohen,et al.  Measuring and interpreting neuronal correlations , 2011, Nature Neuroscience.

[7]  P. J. Sjöström,et al.  Functional specificity of local synaptic connections in neocortical networks , 2011, Nature.

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

[9]  Matteo Carandini,et al.  Coding of stimulus sequences by population responses in visual cortex , 2009, Nature Neuroscience.

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

[11]  M. Carandini,et al.  Neuronal Selectivity and Local Map Structure in Visual Cortex , 2008, Neuron.

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

[13]  Eric Shea-Brown,et al.  Correlation and synchrony transfer in integrate-and-fire neurons: basic properties and consequences for coding. , 2008, Physical review letters.

[14]  Robert A. Frazor,et al.  Standing Waves and Traveling Waves Distinguish Two Circuits in Visual Cortex , 2007, Neuron.

[15]  Eric Shea-Brown,et al.  Universal properties of correlation transfer in integrate-and-fire neurons , 2007, q-bio/0703037.

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

[17]  Michael J. Berry,et al.  Weak pairwise correlations imply strongly correlated network states in a neural population , 2005, Nature.

[18]  M. A. Smith,et al.  Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque , 2005, The Journal of Neuroscience.

[19]  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.

[20]  Jessy D. Dorn,et al.  Estimating membrane voltage correlations from extracellular spike trains. , 2003, Journal of neurophysiology.

[21]  Maria V. Sanchez-Vives,et al.  Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. , 2003, Journal of neurophysiology.

[22]  F. Mechler,et al.  Independent and Redundant Information in Nearby Cortical Neurons , 2001, Science.

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

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

[25]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

[26]  Christopher K. I. Williams Prediction with Gaussian Processes: From Linear Regression to Linear Prediction and Beyond , 1999, Learning in Graphical Models.

[27]  J. Alonso,et al.  Functional connectivity between simple cells and complex cells in cat striate cortex , 1998, Nature Neuroscience.

[28]  Purvis Bedenbaugh,et al.  Multiunit Normalized Cross Correlation Differs from the Average Single-Unit Normalized Correlation , 1997, Neural Computation.

[29]  J. Hertz,et al.  Adjacent visual cortical complex cells share about 20% of their stimulus-related information. , 1996, Cerebral cortex.

[30]  Sompolinsky,et al.  Theory of correlations in stochastic neural networks. , 1994, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

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

[32]  Stefan Sperlich,et al.  Generalized Additive Models , 2014 .

[33]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  K. Tanaka,et al.  Organization of cat visual cortex as investigated by cross-correlation technique. , 1981, Journal of neurophysiology.

[35]  K. Tanaka,et al.  Cross-Correlation Analysis of Interneuronal Connectivity in cat visual cortex. , 1981, Journal of neurophysiology.

[36]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[37]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. I. The single spike train. , 1967, Biophysical journal.

[38]  M. Volgushev,et al.  Long-range correlation of the membrane potential in neocortical neurons during slow oscillation. , 2011, Progress in brain research.

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

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

[41]  Konrad P. Körding,et al.  The world from a cat’s perspective – statistics of natural videos , 2003, Biological Cybernetics.

[42]  Maneesh Sahani,et al.  How Linear are Auditory Cortical Responses? , 2002, NIPS.

[43]  BsnNr C. Srorn,et al.  CLASSIFYING SIMPLE AND COMPLEX CELLS ON THE BASIS OF RESPONSE MODULATION , 2002 .

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

[45]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.