Eye Smarter than Scientists Believed: Neural Computations in Circuits of the Retina

We rely on our visual system to cope with the vast barrage of incoming light patterns and to extract features from the scene that are relevant to our well-being. The necessary reduction of visual information already begins in the eye. In this review, we summarize recent progress in understanding the computations performed in the vertebrate retina and how they are implemented by the neural circuitry. A new picture emerges from these findings that helps resolve a vexing paradox between the retina's structure and function. Whereas the conventional wisdom treats the eye as a simple prefilter for visual images, it now appears that the retina solves a diverse set of specific tasks and provides the results explicitly to downstream brain areas.

[1]  J. B. Demb,et al.  Disinhibition Combines with Excitation to Extend the Operating Range of the OFF Visual Pathway in Daylight , 2008, The Journal of Neuroscience.

[2]  Markus Meister,et al.  Retina versus Cortex Contrast Adaptation in Parallel Visual Pathways , 2004, Neuron.

[3]  S Hecht,et al.  ENERGY AT THE THRESHOLD OF VISION. , 1941, Science.

[4]  G. Fain,et al.  Adaptation in vertebrate photoreceptors. , 2001, Physiological reviews.

[5]  Denis Fize,et al.  Speed of processing in the human visual system , 1996, Nature.

[6]  A. Hodgkin,et al.  Changes in time scale and sensitivity in the ommatidia of Limulus , 1964, The Journal of physiology.

[7]  Michael J. Berry,et al.  Synchronized Firing among Retinal Ganglion Cells Signals Motion Reversal , 2007, Neuron.

[8]  F. Werblin,et al.  Rapid global shifts in natural scenes block spiking in specific ganglion cell types , 2003, Nature Neuroscience.

[9]  Douglas S Kim,et al.  Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration , 2008, Nature Neuroscience.

[10]  I. Ohzawa,et al.  Contrast Gain Control in the Visual Cortex: Monocular Versus Binocular Mechanisms , 2000, The Journal of Neuroscience.

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

[12]  H. Wässle,et al.  Cone Contacts, Mosaics, and Territories of Bipolar Cells in the Mouse Retina , 2009, The Journal of Neuroscience.

[13]  J. Sanes,et al.  Molecular identification of a retinal cell type that responds to upward motion , 2008, Nature.

[14]  Kwoon Y. Wong,et al.  Ectopic retinal ON bipolar cell synapses in the OFF inner plexiform layer: Contacts with dopaminergic amacrine cells and melanopsin ganglion cells , 2009, The Journal of comparative neurology.

[15]  A. Hodgkin,et al.  The electrical response of turtle cones to flashes and steps of light , 1974, The Journal of physiology.

[16]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[17]  J. Stone,et al.  Properties of cat retinal ganglion cells: a comparison of W-cells with X- and Y-cells. , 1974, Journal of neurophysiology.

[18]  J. B. Demb,et al.  Contrast Adaptation in Subthreshold and Spiking Responses of Mammalian Y-Type Retinal Ganglion Cells , 2005, The Journal of Neuroscience.

[19]  Rava Azeredo da Silveira,et al.  Approach sensitivity in the retina processed by a multifunctional neural circuit , 2009, Nature Neuroscience.

[20]  J. L. Schnapf,et al.  Photovoltage of rods and cones in the macaque retina. , 1995, Science.

[21]  Jonathan B Demb,et al.  Cellular Mechanisms for Direction Selectivity in the Retina , 2007, Neuron.

[22]  H. Barlow,et al.  Responses to single quanta of light in retinal ganglion cells of the cat. , 1971, Vision research.

[23]  T H Bullock,et al.  Event-related potentials in the retina and optic tectum of fish. , 1990, Journal of neurophysiology.

[24]  H M Sakai,et al.  Response dynamics and receptive-field organization of catfish amacrine cells. , 1992, Journal of neurophysiology.

[25]  Sheila Nirenberg,et al.  Classification of retinal ganglion cells: a statistical approach. , 2003, Journal of neurophysiology.

[26]  Christopher L Passaglia,et al.  Complex temporal response patterns with a simple retinal circuit. , 2008, Journal of neurophysiology.

[27]  Tim Gollisch,et al.  Modeling convergent ON and OFF pathways in the early visual system , 2008, Biological Cybernetics.

[28]  K. Nakayama,et al.  Single visual neurons code opposing motion independent of direction. , 1983, Science.

[29]  M. Land Motion and vision: why animals move their eyes , 1999, Journal of Comparative Physiology A.

[30]  J. Ashmore,et al.  Absolute sensitivity of rod bipolar cells in a dark-adapted retina , 1976, Nature.

[31]  M. Meister,et al.  Fast and Slow Contrast Adaptation in Retinal Circuitry , 2002, Neuron.

[32]  Michael J. Berry,et al.  Detection and prediction of periodic patterns by the retina , 2007, Nature Neuroscience.

[33]  B. Boycott,et al.  Organization of the primate retina: electron microscopy , 1966, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[34]  R. Shapley,et al.  The effect of contrast on the transfer properties of cat retinal ganglion cells. , 1978, The Journal of physiology.

[35]  Michael J. Berry,et al.  Sophisticated temporal pattern recognition in retinal ganglion cells. , 2008, Journal of neurophysiology.

[36]  E J Chichilnisky,et al.  Behavioral / Systems / Cognitive Identification and Characterization of a Y-Like Primate Retinal Ganglion Cell Type , 2007 .

[37]  Kerry J. Kim,et al.  Temporal Contrast Adaptation in the Input and Output Signals of Salamander Retinal Ganglion Cells , 2001, The Journal of Neuroscience.

[38]  Stephen A. Baccus,et al.  Segregation of object and background motion in the retina , 2003, Nature.

[39]  E. Chichilnisky,et al.  Adaptation to Temporal Contrast in Primate and Salamander Retina , 2001, The Journal of Neuroscience.

[40]  F. Rieke,et al.  Selective Transmission of Single Photon Responses by Saturation at the Rod-to-Rod Bipolar Synapse , 2004, Neuron.

[41]  F. Rieke Temporal Contrast Adaptation in Salamander Bipolar Cells , 2001, The Journal of Neuroscience.

[42]  S. R. Y. Cajal La rétine des vertébrés , 1892 .

[43]  F. C. Volkmann Human visual suppression , 1986, Vision Research.

[44]  M. Tachibana,et al.  Synchronized retinal oscillations encode essential information for escape behavior in frogs , 2005, Nature Neuroscience.

[45]  N. Graham Visual Pattern Analyzers , 1989 .

[46]  B. Borghuis,et al.  Cellular Basis for Contrast Gain Control over the Receptive Field Center of Mammalian Retinal Ganglion Cells , 2007, The Journal of Neuroscience.

[47]  P. Sterling,et al.  Microcircuits for Night Vision in Mouse Retina , 2001, The Journal of Neuroscience.

[48]  H. Barlow,et al.  Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit , 1964, The Journal of physiology.

[49]  R. Shapley,et al.  X and Y cells in the lateral geniculate nucleus of macaque monkeys. , 1982, The Journal of physiology.

[50]  Ken-ichi Funahashi,et al.  On the approximate realization of continuous mappings by neural networks , 1989, Neural Networks.

[51]  A. Huberman,et al.  Architecture and Activity-Mediated Refinement of Axonal Projections from a Mosaic of Genetically Identified Retinal Ganglion Cells , 2008, Neuron.

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

[53]  C Blakemore,et al.  On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images , 1969, The Journal of physiology.

[54]  Jonathan Stone,et al.  Parallel Processing in the Visual System , 1983, Perspectives in Vision Research.

[55]  P. Lennie,et al.  Profound Contrast Adaptation Early in the Visual Pathway , 2004, Neuron.

[56]  Mark C. W. van Rossum,et al.  Noise removal at the rod synapse of mammalian retina , 1998, Visual Neuroscience.

[57]  R. Shapley,et al.  Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. , 1976, The Journal of physiology.

[58]  W. Levick Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit's retina , 1967, The Journal of physiology.

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

[60]  E. Chichilnisky,et al.  Precision of spike trains in primate retinal ganglion cells. , 2004, Journal of neurophysiology.

[61]  M. Carandini,et al.  The Statistical Computation Underlying Contrast Gain Control , 2006, The Journal of Neuroscience.

[62]  D. Baylor,et al.  Photoreceptor signals and vision. Proctor lecture. , 1987, Investigative ophthalmology & visual science.

[63]  E J Chichilnisky,et al.  Prediction and Decoding of Retinal Ganglion Cell Responses with a Probabilistic Spiking Model , 2005, The Journal of Neuroscience.

[64]  P. Sterling,et al.  Architecture of rod and cone circuits to the on-beta ganglion cell , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[65]  Stephen A. Baccus,et al.  Retinal Adaptation to Object Motion , 2007, Neuron.

[66]  D. Baylor,et al.  Two components of electrical dark noise in toad retinal rod outer segments. , 1980, The Journal of physiology.

[67]  Kenneth R Alexander,et al.  Is there an omitted stimulus response in the human cone flicker electroretinogram? , 2009, Visual Neuroscience.

[68]  Heinz Wässle,et al.  Parallel processing in the mammalian retina , 2004, Nature Reviews Neuroscience.

[69]  R. Masland,et al.  Spatial scale and cellular substrate of contrast adaptation by retinal ganglion cells , 2001, Nature Neuroscience.

[70]  Michael J. Berry,et al.  The Neural Code of the Retina , 1999, Neuron.

[71]  W. G. Owen,et al.  Temporal filtering in retinal bipolar cells. Elements of an optimal computation? , 1990, Biophysical journal.

[72]  D C Van Essen,et al.  Shifter circuits: a computational strategy for dynamic aspects of visual processing. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[73]  N. Kanwisher,et al.  Stages of processing in face perception: an MEG study , 2002, Nature Neuroscience.

[74]  Geng-Lin Li,et al.  Short-Term Depression at the Reciprocal Synapses between a Retinal Bipolar Cell Terminal and Amacrine Cells , 2007, The Journal of Neuroscience.

[75]  Rockefeller S.L. Young,et al.  Parallel Processing in the Visual System , 1984 .

[76]  J. Caldwell,et al.  New properties of rabbit retinal ganglion cells. , 1978, The Journal of physiology.

[77]  J. Pokorny,et al.  Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN , 2005, Nature.

[78]  C. Enroth-Cugell,et al.  Chapter 9 Visual adaptation and retinal gain controls , 1984 .

[79]  Barry B. Lee,et al.  Center surround receptive field structure of cone bipolar cells in primate retina , 2000, Vision Research.

[80]  B. Roska,et al.  Genetic address book for retinal cell types , 2009, Nature Neuroscience.

[81]  J. B. Demb,et al.  Presynaptic Mechanism for Slow Contrast Adaptation in Mammalian Retinal Ganglion Cells , 2006, Neuron.

[82]  H. K. Hartline,et al.  THE RESPONSES OF LIMULUS OPTIC NERVE FIBERS TO PATTERNS OF ILLUMINATION ON THE RECEPTOR MOSAIC , 1959, The Journal of general physiology.

[83]  Bruno A. Olshausen,et al.  A multiscale dynamic routing circuit for forming size- and position-invariant object representations , 1995, Journal of Computational Neuroscience.

[84]  P Sterling,et al.  Rod bipolar array in the cat retina: Pattern of input from rods and GABA‐accumulating amacrine cells , 1987, The Journal of comparative neurology.

[85]  Stephen A. Baccus,et al.  A Retinal Circuit That Computes Object Motion , 2008, The Journal of Neuroscience.

[86]  A Kawana,et al.  Short- and long-range synchronous activities in dimming detectors of the frog retina , 1999, Visual Neuroscience.

[87]  W. R. Taylor,et al.  Transmission of single photon signals through a binary synapse in the mammalian retina , 2004, Visual Neuroscience.

[88]  J. Victor The dynamics of the cat retinal X cell centre. , 1987, The Journal of physiology.

[89]  Michael B. Stadler,et al.  Molecular heterogeneity of developing retinal ganglion and amacrine cells revealed through single cell gene expression profiling , 2007, The Journal of comparative neurology.

[90]  F. Rieke,et al.  Bandpass Filtering at the Rod to Second-Order Cell Synapse in Salamander (Ambystoma tigrinum) Retina , 2003, The Journal of Neuroscience.

[91]  D. Baylor,et al.  The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. , 1984, The Journal of physiology.

[92]  O. Solnitzky The neuron. , 1953, Bulletin. Georgetown University. Medical Center.

[93]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[94]  J. B. Demb,et al.  Bipolar Cells Contribute to Nonlinear Spatial Summation in the Brisk-Transient (Y) Ganglion Cell in Mammalian Retina , 2001, The Journal of Neuroscience.

[95]  H. Wässle,et al.  The Primordial, Blue-Cone Color System of the Mouse Retina , 2005, The Journal of Neuroscience.

[96]  Tim Gollisch,et al.  Rapid Neural Coding in the Retina with Relative Spike Latencies , 2008, Science.

[97]  W. R. Taylor,et al.  New directions in retinal research , 2003, Trends in Neurosciences.

[98]  J. Diamond,et al.  Vesicle depletion and synaptic depression at a mammalian ribbon synapse. , 2006, Journal of neurophysiology.

[99]  H. Wässle,et al.  Immunocytochemical analysis of the mouse retina , 2000, The Journal of comparative neurology.

[100]  Michael J. Berry,et al.  Anticipation of moving stimuli by the retina , 1999, Nature.

[101]  H. Barlow Retinal noise and absolute threshold. , 1956, Journal of the Optical Society of America.

[102]  D. Dacey,et al.  Origins of perception : retinal ganglion cell diversity and the creation of parallel visual pathways , 2011 .

[103]  Guillaume S. Masson,et al.  Motion perception during saccadic eye movements , 2000, Nature Neuroscience.

[104]  P. Lennie,et al.  Pattern-selective adaptation in visual cortical neurones , 1979, Nature.

[105]  B. Sakitt Counting every quantum , 1972, The Journal of physiology.

[106]  J. B. Demb,et al.  Functional Circuitry of the Retinal Ganglion Cell's Nonlinear Receptive Field , 1999, The Journal of Neuroscience.

[107]  G D Field,et al.  Information processing in the primate retina: circuitry and coding. , 2007, Annual review of neuroscience.

[108]  F. Rieke,et al.  Nonlinear Signal Transfer from Mouse Rods to Bipolar Cells and Implications for Visual Sensitivity , 2002, Neuron.

[109]  J. Stone,et al.  Parametric and feature extraction analyses of the receptive fields of visual neurones. Two streams of thought in the study of a sensory pathway. , 1980, Brain, behavior and evolution.

[110]  R. Shapley,et al.  The nonlinear pathway of Y ganglion cells in the cat retina , 1979, The Journal of general physiology.

[111]  L. Lagnado,et al.  Synaptic Depression and the Kinetics of Exocytosis in Retinal Bipolar Cells , 2000, The Journal of Neuroscience.

[112]  R. Masland Neuronal diversity in the retina , 2001, Current Opinion in Neurobiology.

[113]  S. Bloomfield,et al.  Rod Vision: Pathways and Processing in the Mammalian Retina , 2001, Progress in Retinal and Eye Research.

[114]  Kurt Hornik,et al.  Multilayer feedforward networks are universal approximators , 1989, Neural Networks.

[115]  M. Tachibana,et al.  Light-evoked oscillatory discharges in retinal ganglion cells are generated by rhythmic synaptic inputs. , 2004, Journal of neurophysiology.

[116]  R. Born,et al.  Segregation of global and local motion processing in primate middle temporal visual area , 1993, Nature.

[117]  A. T. Smith,et al.  On the sensitivity of complex cells in feline striate cortex to relative motion , 2004, Experimental Brain Research.

[118]  Michael J. Berry,et al.  Role of eye movements in the retinal code for a size discrimination task. , 2007, Journal of neurophysiology.

[119]  C. Enroth-Cugell,et al.  The receptive‐field spatial structure of cat retinal Y cells. , 1987, The Journal of physiology.

[120]  D. Baylor,et al.  Responses of retinal rods to single photons. , 1979, The Journal of physiology.

[121]  R. Masland The fundamental plan of the retina , 2001, Nature Neuroscience.

[122]  Saskia E. J. de Vries,et al.  Retinal Ganglion Cells Can Rapidly Change Polarity from Off to On , 2007, PLoS biology.

[123]  L. Maffei,et al.  Neural Correlate of Perceptual Adaptation to Gratings , 1973, Science.

[124]  Arnaud Delorme,et al.  Spike-based strategies for rapid processing , 2001, Neural Networks.

[125]  D. Baylor,et al.  Visual transduction in cones of the monkey Macaca fascicularis. , 1990, The Journal of physiology.

[126]  Fred Rieke,et al.  Review the Challenges Natural Images Pose for Visual Adaptation , 2022 .

[127]  Samuel G. Solomon,et al.  Profound Contrast Adaptation Early in the Visual Pathway , 2004 .

[128]  D. Dacey,et al.  Colour coding in the primate retina: diverse cell types and cone-specific circuitry , 2003, Current Opinion in Neurobiology.

[129]  Michael J. Berry,et al.  Functional organization of ganglion cells in the salamander retina. , 2006, Journal of neurophysiology.

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

[131]  T H Bullock,et al.  Dynamic properties of human visual evoked and omitted stimulus potentials. , 1994, Electroencephalography and clinical neurophysiology.

[132]  M. Potter Short-term conceptual memory for pictures. , 1976, Journal of experimental psychology. Human learning and memory.

[133]  Barry B. Lee,et al.  Processing of Natural Temporal Stimuli by Macaque Retinal Ganglion Cells , 2002, The Journal of Neuroscience.

[134]  D. Hood,et al.  Lower-level visual processing and models of light adaptation. , 1998, Annual review of psychology.

[135]  D. Burr,et al.  Selective suppression of the magnocellular visual pathway during saccadic eye movements , 1994, Nature.

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

[137]  Eve Marder,et al.  Theory in motion , 1995, Current Opinion in Neurobiology.

[138]  Fan Gao,et al.  Functional Architecture of Synapses in the Inner Retina: Segregation of Visual Signals by Stratification of Bipolar Cell Axon Terminals , 2000, The Journal of Neuroscience.

[139]  D. Hubel,et al.  The role of fixational eye movements in visual perception , 2004, Nature Reviews Neuroscience.

[140]  W. Pitts,et al.  What the Frog's Eye Tells the Frog's Brain , 1959, Proceedings of the IRE.