Is the Homunculus Aware of Sensory Adaptation?

Neural activity and perception are both affected by sensory history. The work presented here explores the relationship between the physiological effects of adaptation and their perceptual consequences. Perception is modeled as arising from an encoder-decoder cascade, in which the encoder is defined by the probabilistic response of a population of neurons, and the decoder transforms this population activity into a perceptual estimate. Adaptation is assumed to produce changes in the encoder, and we examine the conditions under which the decoder behavior is consistent with observed perceptual effects in terms of both bias and discriminability. We show that for all decoders, discriminability is bounded from below by the inverse Fisher information. Estimation bias, on the other hand, can arise for a variety of different reasons and can range from zero to substantial. We specifically examine biases that arise when the decoder is fixed, unaware of the changes in the encoding population (as opposed to aware of the adaptation and changing accordingly). We simulate the effects of adaptation on two well-studied sensory attributes, motion direction and contrast, assuming a gain change description of encoder adaptation. Although we cannot uniquely constrain the source of decoder bias, we find for both motion and contrast that an unaware decoder that maximizes the likelihood of the percept given by the preadaptation encoder leads to predictions that are consistent with behavioral data. This model implies that adaptation-induced biases arise as a result of temporary suboptimality of the decoder.

[1]  Joseph J Atick,et al.  Could information theory provide an ecological theory of sensory processing? , 2011, Network.

[2]  C. Clifford Perceptual adaptation: motion parallels orientation , 2002, Trends in Cognitive Sciences.

[3]  J. Gibson,et al.  ADAPTATION , AFTEREFFECT AND CONTRAST IN THE PERCEPTION OF TILTED LINES , 2004 .

[4]  H. Barlow,et al.  Adaptation to gratings: No compensatory advantages found , 1976, Vision Research.

[5]  Neil W. Roach,et al.  Asynchrony adaptation reveals neural population code for audio-visual timing , 2010, Proceedings of the Royal Society B: Biological Sciences.

[6]  M. Coltheart Visual feature-analyzers and after-effects of tilt and curvature. , 1971, Psychological review.

[7]  Derek H. Arnold,et al.  Orthogonal adaptation improves orientation discrimination , 2001, Vision Research.

[8]  N. Qian,et al.  Learning and adaptation in a recurrent model of V1 orientation selectivity. , 2003, Journal of neurophysiology.

[9]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[10]  M. Kendall Theoretical Statistics , 1956, Nature.

[11]  Robert Patterson,et al.  Direction-selective adaptation and simultaneous contrast induced by stereoscopic (cyclopean) motion , 1996, Vision Research.

[12]  Robert J. Snowden,et al.  Perceived contrast as a function of adaptation duration , 1994, Vision Research.

[13]  Justin L. Gardner Contrast adaptation and representation in human early visual cortex , 2006 .

[14]  J. Gibson,et al.  Adaptation, after-effect and contrast in the perception of tilted lines. I. Quantitative studies , 1937 .

[15]  Anthony J. Movshon,et al.  Optimal representation of sensory information by neural populations , 2006, Nature Neuroscience.

[16]  P. Dayan,et al.  Space and time in visual context , 2007, Nature Reviews Neuroscience.

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

[18]  M. Sur,et al.  Adaptation-Induced Plasticity of Orientation Tuning in Adult Visual Cortex , 2000, Neuron.

[19]  D. Regan,et al.  Postadaptation orientation discrimination. , 1985, Journal of the Optical Society of America. A, Optics and image science.

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

[21]  C. Blakemore,et al.  Size Adaptation: A New Aftereffect , 1969, Science.

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

[23]  J. Movshon,et al.  Adaptation changes the direction tuning of macaque MT neurons , 2004, Nature Neuroscience.

[24]  Rob R. de Ruyter van Steveninck,et al.  The metabolic cost of neural information , 1998, Nature Neuroscience.

[25]  S. Laughlin A Simple Coding Procedure Enhances a Neuron's Information Capacity , 1981, Zeitschrift fur Naturforschung. Section C, Biosciences.

[26]  Peter E. Latham,et al.  Narrow Versus Wide Tuning Curves: What's Best for a Population Code? , 1999, Neural Computation.

[27]  M W Oram,et al.  The temporal resolution of neural codes: does response latency have a unique role? , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[28]  Paul V McGraw,et al.  Perceived contrast following adaptation: the role of adapting stimulus visibility. , 2002, Spatial vision.

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

[30]  M. Meister,et al.  Dynamic predictive coding by the retina , 2005, Nature.

[31]  D. Tolhurst,et al.  Does a Bayesian model of V1 contrast coding offer a neurophysiological account of human contrast discrimination? , 2005, Vision Research.

[32]  Richard M. Lipkin,et al.  Adaptation across the Cortical Hierarchy: Low-Level Curve Adaptation Affects High-Level Facial-Expression Judgments , 2008, The Journal of Neuroscience.

[33]  C. Clifford,et al.  A functional angle on some after-effects in cortical vision , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  C. Bowd,et al.  Direction-selective Coding of Stereoscopic (Cyclopean) Motion , 1997, Vision Research.

[35]  Xiaohui Xie Threshold behaviour of the maximum likelihood method in population decoding , 2002, Network.

[36]  Rajesh P. N. Rao,et al.  Probabilistic Models of the Brain: Perception and Neural Function , 2002 .

[37]  Steven Kay,et al.  Fundamentals Of Statistical Signal Processing , 2001 .

[38]  M. Carrasco,et al.  Attention alters appearance , 2004, Nature Neuroscience.

[39]  Martin J. Wainwright,et al.  Visual adaptation as optimal information transmission , 1999, Vision Research.

[40]  K. H. Britten,et al.  Motion adaptation in area MT. , 2002, Journal of neurophysiology.

[41]  C. Clifford,et al.  Contrast adaptation may enhance contrast discrimination. , 2002, Spatial vision.

[42]  B. Dosher,et al.  The dynamics of perceptual learning: an incremental reweighting model. , 2005, Psychological review.

[43]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[44]  F. Heitger,et al.  The functional role of contrast adaptation , 1988, Vision Research.

[45]  H. Barlow Vision: A theory about the functional role and synaptic mechanism of visual after-effects , 1991 .

[46]  D. Bradley,et al.  Neural population code for fine perceptual decisions in area MT , 2005, Nature Neuroscience.

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

[48]  Keith Langley,et al.  Subtractive and divisive adaptation in visual motion computations , 2007, Vision Research.

[49]  R. Addams LI. An account of a peculiar optical phænomenon seen after having looked at a moving body , 1834 .

[50]  J. Ross,et al.  Perceived contrast following adaptation to gratings of different orientations , 1996, Vision Research.

[51]  Eero P. Simoncelli,et al.  Natural image statistics and divisive normalization: Modeling nonlinearity and adaptation in cortical neurons , 2002 .

[52]  M. Carrasco,et al.  How do attention and adaptation affect contrast sensitivity? , 2007, Journal of vision.

[53]  Stefan Treue,et al.  Different populations of neurons contribute to the detection and discrimination of visual motion , 2001, Vision Research.

[54]  R. Blake,et al.  Neural strength of visual attention gauged by motion adaptation , 1999, Nature Neuroscience.

[55]  J. J. Koenderink,et al.  Contrast adaptation and contrast gain control , 2004, Experimental Brain Research.

[56]  Maoz Shamir,et al.  The Scaling of Winner-Takes-All Accuracy with Population Size , 2006, Neural Computation.

[57]  Alan A. Stocker,et al.  Sensory Adaptation within a Bayesian Framework for Perception , 2005, NIPS.

[58]  R. Sekuler,et al.  Adaptation alters perceived direction of motion , 1976, Vision Research.

[59]  Ned Block,et al.  ATTENTION AND MENTAL PAINT , 2010 .

[60]  Benjamin T Backus,et al.  Illusory motion from change over time in the response to contrast and luminance. , 2005, Journal of vision.

[61]  Si Wu,et al.  Population Decoding Based on an Unfaithful Model , 1999, NIPS.

[62]  N. Sutherland Figural After-Effects and Apparent Size , 1961 .

[63]  Matteo Colombo How “Authentic Intentionality” can be Enabled: a Neurocomputational Hypothesis , 2010, Minds and Machines.

[64]  Justin L. Gardner,et al.  Contrast Adaptation and Representation in Human Early Visual Cortex , 2005, Neuron.

[65]  I. Dean,et al.  Neural population coding of sound level adapts to stimulus statistics , 2005, Nature Neuroscience.

[66]  H. Seung,et al.  Tilt aftereffect and adaptation-induced changes in orientation tuning in visual cortex. , 2005, Journal of neurophysiology.

[67]  Keith Langley,et al.  A parametric account of contrast adaptation on contrast perception. , 2002, Spatial vision.

[68]  S. Kay Fundamentals of statistical signal processing: estimation theory , 1993 .

[69]  Michael J. Berry,et al.  Adaptation of retinal processing to image contrast and spatial scale , 1997, Nature.

[70]  Herman P. Snippe,et al.  Parameter Extraction from Population Codes: A Critical Assessment , 1996, Neural Computation.

[71]  Si Wu,et al.  Attention Modulation of Neural Tuning Through Peak and Base Rate , 2001, Neural Computation.

[72]  Y. Frégnac,et al.  The “silent” surround of V1 receptive fields: theory and experiments , 2003, Journal of Physiology-Paris.

[73]  M. Ibbotson,et al.  Characterizing contrast adaptation in a population of cat primary visual cortical neurons using Fisher information. , 2007, Journal of the Optical Society of America. A, Optics, image science, and vision.

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

[75]  Eero P. Simoncelli,et al.  Noise characteristics and prior expectations in human visual speed perception , 2006, Nature Neuroscience.

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

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

[78]  Eero P. Simoncelli,et al.  Local velocity representation: evidence from motion adaptation , 1998, Vision Research.

[79]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[80]  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.

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

[82]  Roger W Li,et al.  Perceptual learning improves efficiency by re-tuning the decision 'template' for position discrimination , 2004, Nature Neuroscience.

[83]  COLIN BLAKEMORE,et al.  Perceptual Fading of a Stabilized Cortical Image , 1971, Nature.

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

[85]  A. Kohn Visual adaptation: physiology, mechanisms, and functional benefits. , 2007, Journal of neurophysiology.

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

[87]  Terrence J. Sejnowski,et al.  Neuronal Tuning: To Sharpen or Broaden? , 1999, Neural Computation.

[88]  M A Georgeson,et al.  The effect of spatial adaptation on perceived contrast. , 1985, Spatial vision.

[89]  P. Lennie,et al.  Rapid adaptation in visual cortex to the structure of images. , 1999, Science.

[90]  M. Carandini,et al.  A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. , 1997, Science.

[91]  Eero P. Simoncelli,et al.  Visual motion aftereffects arise from a cascade of two isomorphic adaptation mechanisms. , 2009, Journal of vision.

[92]  Adrienne L. Fairhall,et al.  Efficiency and ambiguity in an adaptive neural code , 2001, Nature.