Active efficient coding explains the development of binocular vision and its failure in amblyopia

The development of vision during the first months of life is an active process that comprises the learning of appropriate neural representations and the learning of accurate eye movements. While it has long been suspected that the two learning processes are coupled, there is still no widely accepted theoretical framework describing this joint development. Here we propose a computational model of the development of active binocular vision to fill this gap. The model is based on a new formulation of the Active Efficient Coding theory, which proposes that eye movements, as well as stimulus encoding, are jointly adapted to maximize the overall coding efficiency of the system. Under healthy conditions, the model self-calibrates to perform accurate vergence and accommodation eye movements. It exploits disparity cues to deduce the direction of defocus, which leads to coordinated vergence and accommodation responses. In a simulated anisometropic case, where the refraction power of the two eyes differs, an amblyopia-like state develops, in which the foveal region of one eye is suppressed due to inputs from the other eye. After correcting for refraction errors, the model can only reach healthy performance levels if receptive fields are still plastic, in line with findings on a critical period for binocular vision development. Overall, our model offers a unifying conceptual framework for understanding the development of binocular vision under healthy conditions and in amblyopia. Significance Statement Brains must operate in an energy efficient manner. The efficient coding hypothesis states that sensory systems achieve this by adapting neural representations to the statistics of sensory input signals. Importantly, however, these statistics are influenced by the organism’s behavior and how it samples information from the environment. Therefore, optimal performance requires jointly optimizing neural representations and behavior, a theory called Active Efficient Coding. Here we test the plausibility of this theory by proposing a computational model of the development of binocular vision. The model explains the development of accurate binocular vision under healthy conditions. In the case of refractive errors, however, the model develops an amblyopia-like state and predicts conditions for successful treatment.

[1]  Michael J. Berry,et al.  Predictive information in a sensory population , 2013, Proceedings of the National Academy of Sciences.

[2]  S. Gallagher,et al.  Accommodative Function in Individuals with Autism Spectrum Disorder. , 2018, Optometry and vision science : official publication of the American Academy of Optometry.

[3]  Metzinger Thomas,et al.  Philosophy and Predictive Processing , 2017 .

[4]  Robert F Hess,et al.  Regional Extent of Peripheral Suppression in Amblyopia. , 2017, Investigative ophthalmology & visual science.

[5]  C Blakemore,et al.  Experimental analysis of amblyopia and strabismus. , 1974, The British journal of ophthalmology.

[6]  S. Morad,et al.  Ceramide-orchestrated signalling in cancer cells , 2012, Nature Reviews Cancer.

[7]  H. B. Barlow,et al.  Possible Principles Underlying the Transformations of Sensory Messages , 2012 .

[8]  Karl J. Friston The free-energy principle: a unified brain theory? , 2010, Nature Reviews Neuroscience.

[9]  Caroline E. Robertson,et al.  Sensory perception in autism , 2017, Nature Reviews Neuroscience.

[10]  T Rowan Candy,et al.  Cues for the control of ocular accommodation and vergence during postnatal human development. , 2008, Journal of vision.

[11]  Alfred O. Hero,et al.  Bounds on Variance for Unimodal Distributions , 2015, IEEE Transactions on Information Theory.

[12]  Megumi Hatori,et al.  The role of arrestin In melanopsin function , 2009 .

[13]  Jochen Triesch,et al.  Joint Learning of Binocularly Driven Saccades and Vergence by Active Efficient Coding , 2017, Front. Neurorobot..

[14]  Shalabh Bhatnagar,et al.  Natural actor-critic algorithms , 2009, Autom..

[15]  K J Ciuffreda,et al.  Dynamic vergence eye movements in strabismus and amblyopia: symmetric vergence. , 1980, Investigative ophthalmology & visual science.

[16]  Michael P Stryker,et al.  Amblyopia: New molecular/pharmacological and environmental approaches. , 2018, Visual neuroscience.

[17]  M. Meister,et al.  Decorrelation and efficient coding by retinal ganglion cells , 2012, Nature Neuroscience.

[18]  Louis Sokoloff,et al.  Circulation and Energy Metabolism of the Brain , 1999 .

[19]  D. N. Spinelli,et al.  Visual Experience Modifies Distribution of Horizontally and Vertically Oriented Receptive Fields in Cats , 1970, Science.

[20]  David C. Knill,et al.  Stereopsis and amblyopia: A mini-review , 2015, Vision Research.

[21]  Yu Zhao,et al.  A unified model of the joint development of disparity selectivity and vergence control , 2012, 2012 IEEE International Conference on Development and Learning and Epigenetic Robotics (ICDL).

[22]  David R Williams,et al.  Accommodation with higher-order monochromatic aberrations corrected with adaptive optics. , 2006, Journal of the Optical Society of America. A, Optics, image science, and vision.

[23]  P O Hoyer,et al.  Independent component analysis applied to feature extraction from colour and stereo images , 2000, Network.

[24]  David M. Hoffman,et al.  Vergence-accommodation conflicts hinder visual performance and cause visual fatigue. , 2008, Journal of vision.

[25]  Michael C. Frank Language as a link between exact number and approximate magnitude , 2010 .

[26]  Joseph J. Atick,et al.  What Does the Retina Know about Natural Scenes? , 1992, Neural Computation.

[27]  Luke E. Hallum,et al.  Altered Balance of Receptive Field Excitation and Suppression in Visual Cortex of Amblyopic Macaque Monkeys , 2017, The Journal of Neuroscience.

[28]  Jürgen Schmidhuber,et al.  Driven by Compression Progress: A Simple Principle Explains Essential Aspects of Subjective Beauty, Novelty, Surprise, Interestingness, Attention, Curiosity, Creativity, Art, Science, Music, Jokes , 2008, ABiALS.

[29]  Thomas Kohnen,et al.  Dynamics of Interocular Suppression in Amblyopic Children during Electronically Monitored Occlusion Therapy: First Insight , 2016, Strabismus.

[30]  P. Molinoff,et al.  Basic Neurochemistry: Molecular, Cellular and Medical Aspects , 1989 .

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

[32]  Peter Dayan,et al.  Sparse Coding Can Predict Primary Visual Cortex Receptive Field Changes Induced by Abnormal Visual Input , 2013, PLoS Comput. Biol..

[33]  Rahul Narain,et al.  Blur and the perception of depth at occlusions. , 2016, Journal of vision.

[34]  Manuela Chessa,et al.  A cortical model for binocular vergence control without explicit calculation of disparity , 2010, Neurocomputing.

[35]  Jochen Triesch,et al.  An active-efficient-coding model of optokinetic nystagmus. , 2016, Journal of vision.

[36]  M. Stryker,et al.  Development and Plasticity of the Primary Visual Cortex , 2012, Neuron.

[37]  Andrea Canessa,et al.  The Active Side of Stereopsis: Fixation Strategy and Adaptation to Natural Environments , 2017, Scientific Reports.

[38]  T Rowan Candy,et al.  The effect of lens-induced anisometropia on accommodation and vergence during human visual development. , 2011, Investigative ophthalmology & visual science.

[39]  Ronald E. Gangnon,et al.  Successful treatment of anisometropic amblyopia with spectacles alone. , 2006, Journal of AAPOS : the official publication of the American Association for Pediatric Ophthalmology and Strabismus.

[40]  Bruce J W Evans,et al.  Monovision: a review , 2007, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[41]  A Bradley,et al.  Contrast sensitivity in anisometropic amblyopia. , 1981, Investigative ophthalmology & visual science.

[42]  T Rowan Candy,et al.  Accommodative and vergence responses to conflicting blur and disparity stimuli during development. , 2009, Journal of vision.

[43]  David J. Heeger,et al.  A Model of Binocular Rivalry and Cross-orientation Suppression , 2013, PLoS Comput. Biol..

[44]  D. Hubel,et al.  SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE. , 1963, Journal of neurophysiology.

[45]  Y. C. Pati,et al.  Orthogonal matching pursuit: recursive function approximation with applications to wavelet decomposition , 1993, Proceedings of 27th Asilomar Conference on Signals, Systems and Computers.

[46]  Sonja B. Hofer,et al.  Synaptic organization of visual space in primary visual cortex , 2017, Nature.

[47]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[48]  Thomas M. Cover,et al.  Elements of Information Theory: Cover/Elements of Information Theory, Second Edition , 2005 .

[49]  D. Heeger,et al.  Inter-ocular contrast normalization in human visual cortex. , 2009, Journal of vision.

[50]  Michael S. Lewicki,et al.  Efficient coding of natural sounds , 2002, Nature Neuroscience.

[51]  T. Rowan Candy,et al.  Eye Movements , Strabismus , Amblyopia , and Neuro-Ophthalmology Accommodative Performance of Children With Unilateral Amblyopia , 2015 .

[52]  A. Kraskov,et al.  Estimating mutual information. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[53]  Andriana Olmos,et al.  A biologically inspired algorithm for the recovery of shading and reflectance images , 2004 .

[54]  T. Rowan Candy,et al.  Accommodation and vergence latencies in human infants , 2008, Vision Research.

[55]  Yu Zhao,et al.  Self-calibrating smooth pursuit through active efficient coding , 2015, Robotics Auton. Syst..

[56]  A. Dekaban,et al.  Changes in brain weights during the span of human life: Relation of brain weights to body heights and body weights , 1978, Annals of neurology.

[57]  Stéphane Mallat,et al.  Matching pursuits with time-frequency dictionaries , 1993, IEEE Trans. Signal Process..

[58]  Philipp Sterzer,et al.  Priming in a shape task but not in a category task under continuous flash suppression. , 2016, Journal of vision.

[59]  J. B. Levitt,et al.  Relation between patterns of intrinsic lateral connectivity, ocular dominance, and cytochrome oxidase-reactive regions in macaque monkey striate cortex. , 1996, Cerebral cortex.

[60]  Ronald E Gangnon,et al.  Successful treatment of anisometropic amblyopia with spectacles alone. , 2006, Journal of AAPOS : the official publication of the American Association for Pediatric Ophthalmology and Strabismus.

[61]  Eero P. Simoncelli,et al.  Natural image statistics and neural representation. , 2001, Annual review of neuroscience.

[62]  Randolph Blake,et al.  Selective losses in binocular vision in anisometropic amblyopes , 1986, Vision Research.

[63]  Michael X Repka,et al.  Treatment of anisometropic amblyopia in children with refractive correction. , 2006, Ophthalmology.

[64]  Robert F. Hess,et al.  Amblyopia and the binocular approach to its therapy , 2015, Vision Research.

[65]  Kathryn J. Saunders,et al.  Determining the relative contribution of retinal disparity and blur cues to ocular accommodation in Down syndrome , 2017, Scientific reports.

[66]  David J. Field,et al.  Sparse coding with an overcomplete basis set: A strategy employed by V1? , 1997, Vision Research.

[67]  E. Adelson,et al.  The Plenoptic Function and the Elements of Early Vision , 1991 .

[68]  J. Movshon,et al.  Visual neural development. , 1981, Annual review of psychology.

[69]  Dana H. Ballard,et al.  Animate Vision , 1991, Artif. Intell..

[70]  J. Stone,et al.  Physiological normality of the retinal in visually deprived cats. , 1973, Brain research.