Population Coding with Motion Energy Filters: The Impact of Correlations

The codes obtained from the responses of large populations of neurons are known as population codes. Several studies have shown that the amount of information conveyed by such codes, and the format of this information, is highly dependent on the pattern of correlations. However, very little is known about the impact of response correlations (as found in actual cortical circuits) on neural coding. To address this problem, we investigated the properties of population codes obtained from motion energy filters, which provide one of the best models for motion selectivity in early visual areas. It is therefore likely that the correlations that arise among energy filters also arise among motion-selective neurons. We adopted an ideal observer approach to analyze filter responses to three sets of images: noisy sine gratings, random dots kinematograms, and images of natural scenes. We report that in our model, the structure of the population code varies with the type of image. We also show that for all sets of images, correlations convey a large fraction of the information: 40% to 90% of the total information. Moreover, ignoring those correlations when decoding leads to considerable information lossfrom 50% to 93%, depending on the image type. Finally we show that it is important to consider a large population of motion energy filters in order to see the impact of correlations. Study of pairs of neurons, as is often done experimentally, can underestimate the effect of correlations.

[1]  Miguel P. Eckstein,et al.  Detection and contrast discrimination of moving signals in uncorrelated Gaussian noise , 1996, Medical Imaging.

[2]  Haim Sompolinsky,et al.  The Effect of Correlations on the Fisher Information of Population Codes , 1998, NIPS.

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

[4]  D. Pollen,et al.  Spatial and temporal frequency selectivity of neurones in visual cortical areas V1 and V2 of the macaque monkey. , 1985, The Journal of physiology.

[5]  M P Eckstein,et al.  Role of knowledge in human visual temporal integration in spatiotemporal noise. , 1996, Journal of the Optical Society of America. A, Optics, image science, and vision.

[6]  Russell L. De Valois,et al.  PII: S0042-6989(00)00210-8 , 2000 .

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

[8]  S. Watamaniuk Ideal observer for discrimination of the global direction of dynamic random-dot stimuli. , 1993, Journal of the Optical Society of America. A, Optics and image science.

[9]  R. Zemel,et al.  Inference and computation with population codes. , 2003, Annual review of neuroscience.

[10]  B L Whitsel,et al.  Variability in somatosensory cortical neuron discharge: effects on capacity to signal different stimulus conditions using a mean rate code. , 1978, Journal of neurophysiology.

[11]  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.

[12]  P. Latham,et al.  Synergy, Redundancy, and Independence in Population Codes, Revisited , 2005, The Journal of Neuroscience.

[13]  S. Panzeri,et al.  An exact method to quantify the information transmitted by different mechanisms of correlational coding. , 2003, Network.

[14]  E H Adelson,et al.  Spatiotemporal energy models for the perception of motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

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

[16]  P. Latham,et al.  Retinal ganglion cells act largely as independent encoders , 2001, Nature.

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

[18]  D. Perrett,et al.  The `Ideal Homunculus': decoding neural population signals , 1998, Trends in Neurosciences.

[19]  S. Treue,et al.  The response of neurons in areas V1 and MT of the alert rhesus monkey to moving random dot patterns , 2005, Experimental Brain Research.

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

[21]  R. Vogels,et al.  Population coding of stimulus orientation by striate cortical cells , 1990, Biological Cybernetics.

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

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

[24]  J. V. van Hateren,et al.  Independent component filters of natural images compared with simple cells in primary visual cortex , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

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

[27]  Christoph von der Malsburg,et al.  The Correlation Theory of Brain Function , 1994 .

[28]  A. Pouget,et al.  Tuning curve sharpening for orientation selectivity: coding efficiency and the impact of correlations , 2004, Nature Neuroscience.

[29]  Daeyeol Lee,et al.  Neural Noise and Movement-Related Codes in the Macaque Supplementary Motor Area , 2003, The Journal of Neuroscience.

[30]  Z L Lu,et al.  Perceptual learning reflects external noise filtering and internal noise reduction through channel reweighting. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[31]  D. Field,et al.  The structure and symmetry of simple-cell receptive-field profiles in the cat’s visual cortex , 1986, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[32]  J. Robson Spatial and Temporal Contrast-Sensitivity Functions of the Visual System , 1966 .

[33]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of striate cortical neurones , 1975, Nature.

[34]  E. Salinas How Behavioral Constraints May Determine Optimal Sensory Representations , 2006, PLoS biology.

[35]  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.

[36]  J. A. Movshon,et al.  The dependence of response amplitude and variance of cat visual cortical neurones on stimulus contrast , 1981, Experimental Brain Research.

[37]  Si Wu,et al.  Population Coding with Correlation and an Unfaithful Model , 2001, Neural Computation.

[38]  Stefano Panzeri,et al.  Objective assessment of the functional role of spike train correlations using information measures , 2001 .

[39]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[40]  H Barlow,et al.  Redundancy reduction revisited , 2001, Network.

[41]  A J Ahumada,et al.  Model of human visual-motion sensing. , 1985, Journal of the Optical Society of America. A, Optics and image science.

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

[43]  Peter E. Latham,et al.  Optimal computation with attractor networks , 2003, Journal of Physiology-Paris.

[44]  I. Ohzawa,et al.  Receptive-field dynamics in the central visual pathways , 1995, Trends in Neurosciences.

[45]  A. Pouget,et al.  Reading population codes: a neural implementation of ideal observers , 1999, Nature Neuroscience.

[46]  M. Paradiso,et al.  A theory for the use of visual orientation information which exploits the columnar structure of striate cortex , 2004, Biological Cybernetics.

[47]  Johan A. K. Suykens,et al.  Least Squares Support Vector Machines , 2002 .

[48]  Leonard E. White,et al.  Mapping multiple features in the population response of visual cortex , 2003, Nature.

[49]  Heekuck Oh,et al.  Neural Networks for Pattern Recognition , 1993, Adv. Comput..

[50]  Peter E. Latham,et al.  Statistically Efficient Estimation Using Population Coding , 1998, Neural Computation.

[51]  P. Latham,et al.  Population coding in the retina , 1998, Current Opinion in Neurobiology.

[52]  H Barlow,et al.  Correspondence Noise and Signal Pooling in the Detection of Coherent Visual Motion , 1997, The Journal of Neuroscience.

[53]  Sheila Nirenberg,et al.  Decoding neuronal spike trains: How important are correlations? , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Si Wu,et al.  Information processing in a neuron ensemble with the multiplicative correlation structure , 2004, Neural Networks.

[55]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[56]  J Zhang,et al.  On the directional selectivity of cells in the visual cortex to drifting dot patterns , 1994, Visual Neuroscience.

[57]  Michael J. Berry,et al.  Synergy, Redundancy, and Independence in Population Codes , 2003, The Journal of Neuroscience.