Emergence of binocular functional properties in a monocular neural circuit

Sensory circuits frequently integrate converging inputs while maintaining precise functional relationships between them. For example, in mammals with stereopsis, neurons at the first stages of binocular visual processing show a close alignment of receptive-field properties for each eye. Still, basic questions about the global wiring mechanisms that enable this functional alignment remain unanswered, including whether the addition of a second retinal input to an otherwise monocular neural circuit is sufficient for the emergence of these binocular properties. We addressed this question by inducing a de novo binocular retinal projection to the larval zebrafish optic tectum and examining recipient neuronal populations using in vivo two-photon calcium imaging. Notably, neurons in rewired tecta were predominantly binocular and showed matching direction selectivity for each eye. We found that a model based on local inhibitory circuitry that computes direction selectivity using the topographic structure of both retinal inputs can account for the emergence of this binocular feature.

[1]  W. Newsome,et al.  Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT. , 1986, Journal of neurophysiology.

[2]  Florian Engert,et al.  Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons , 2002, Nature.

[3]  Herwig Baier,et al.  Visuomotor Behaviors in Larval Zebrafish after GFP-Guided Laser Ablation of the Optic Tectum , 2003, The Journal of Neuroscience.

[4]  C. W. G Clifford,et al.  Fundamental mechanisms of visual motion detection: models, cells and functions , 2002, Progress in Neurobiology.

[5]  D. Hubel,et al.  Physiology of visual cells in mouse superior colliculus and correlation with somatosensory and auditory input , 1975, Nature.

[6]  W. B. Marks,et al.  Directionally selective visual units recorded in optic tectum of the goldfish. , 1973, Journal of neurophysiology.

[7]  M. Wallace,et al.  Integration of multiple sensory modalities in cat cortex , 2004, Experimental Brain Research.

[8]  C. Levinthal,et al.  Inhibitory mechanism in zebrafish optic tectum: Visual response properties of tectal cells altered by picrotoxin and bicuculline , 1983, Brain Research.

[9]  C. Blakemore,et al.  Development of cat visual cortex following rotation of one eye , 1975, Nature.

[10]  C. Holt,et al.  Ephrin-B2 and EphB1 Mediate Retinal Axon Divergence at the Optic Chiasm , 2003, Neuron.

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

[12]  B. Rohrer,et al.  Development of the retinotectal projection in zebrafish embryos under TTX-induced neural-impulse blockade , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  R. Sperry CHEMOAFFINITY IN THE ORDERLY GROWTH OF NERVE FIBER PATTERNS AND CONNECTIONS. , 1963, Proceedings of the National Academy of Sciences of the United States of America.

[14]  E I Knudsen,et al.  Computational maps in the brain. , 1987, Annual review of neuroscience.

[15]  Michael D. Abràmoff,et al.  Image processing with ImageJ , 2004 .

[16]  R. C. Emerson,et al.  Simple striate neurons in the cat. II. Mechanisms underlying directional asymmetry and directional selectivity. , 1977, Journal of neurophysiology.

[17]  C. Chien,et al.  astray, a Zebrafish roundabout Homolog Required for Retinal Axon Guidance , 2001, Science.

[18]  M. Law,et al.  Right and left eye bands in frogs with unilateral tectal ablations. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. Hubel,et al.  Binocular interaction in striate cortex of kittens reared with artificial squint. , 1965, Journal of neurophysiology.

[20]  S. Sharma Anomalous retinal projection after removal of contralateral optic tectum in adult goldfish. , 1973, Experimental neurology.

[21]  I. Ohzawa,et al.  Encoding of binocular disparity by complex cells in the cat's visual cortex. , 1996, Journal of neurophysiology.

[22]  M. Stryker,et al.  The role of visual experience in the development of columns in cat visual cortex. , 1998, Science.

[23]  R. K. Simpson Nature Neuroscience , 2022 .

[24]  D. Fitzpatrick,et al.  The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex , 2001, Nature.

[25]  L. C. Katz,et al.  Development of cortical circuits: Lessons from ocular dominance columns , 2002, Nature Reviews Neuroscience.

[26]  Pierre Vanderhaeghen,et al.  Mapping Labels in the Human Developing Visual System and the Evolution of Binocular Vision , 2005, The Journal of Neuroscience.

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

[28]  Stephen L. Johnson,et al.  nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. , 1999, Development.

[29]  M. Jacobson,et al.  Discontinuous mapping of retina onto tectum innervated by both eyes , 1975, Brain Research.

[30]  I. Ohzawa,et al.  Encoding of binocular disparity by simple cells in the cat's visual cortex. , 1996, Journal of neurophysiology.

[31]  Tobias Bonhoeffer,et al.  Development of identical orientation maps for two eyes without common visual experience , 1996, Nature.

[32]  H. Barlow,et al.  The mechanism of directionally selective units in rabbit's retina. , 1965, The Journal of physiology.

[33]  M. Cynader,et al.  Receptive-field organization of monkey superior colliculus. , 1972, Journal of neurophysiology.

[34]  P. Drapeau,et al.  In vivo recording from identifiable neurons of the locomotor network in the developing zebrafish , 1999, Journal of Neuroscience Methods.

[35]  E. S. Ruthazer,et al.  Control of Axon Branch Dynamics by Correlated Activity in Vivo , 2003, Science.

[36]  E. Knudsen Dynamic space codes in the superior colliculus , 1991, Current Opinion in Neurobiology.

[37]  P. O. Bishop,et al.  Binocular simple cells for local stereopsis: Comparison of receptive field organizations for the two eyes , 1984, Vision Research.

[38]  Bevil R. Conway,et al.  Applicability of white-noise techniques to analyzing motion responses. , 2010, Journal of neurophysiology.

[39]  P Sterling,et al.  Visual receptive fields in the superior colliculus of the cat. , 1969, Journal of neurophysiology.

[40]  M. Law,et al.  Eye-specific termination bands in tecta of three-eyed frogs. , 1978, Science.

[41]  B E Stein,et al.  Relationship between visual and tactile representations in cat superior colliculus. , 1976, Journal of neurophysiology.

[42]  C. Shatz,et al.  Transient period of correlated bursting activity during development of the mammalian retina , 1993, Neuron.

[43]  W. Newsome,et al.  Motion selectivity in macaque visual cortex. III. Psychophysics and physiology of apparent motion. , 1986, Journal of neurophysiology.

[44]  John G Flanagan,et al.  Neural map specification by gradients , 2006, Current Opinion in Neurobiology.

[45]  C. Niell,et al.  Functional Imaging Reveals Rapid Development of Visual Response Properties in the Zebrafish Tectum , 2005, Neuron.

[46]  K. Fujita [Two-photon laser scanning fluorescence microscopy]. , 2007, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[47]  S. Udin,et al.  Plasticity in the tectum of Xenopus laevis: binocular maps , 1999, Progress in Neurobiology.

[48]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[49]  Gail Mandel,et al.  Distribution of prospective glutamatergic, glycinergic, and GABAergic neurons in embryonic and larval zebrafish , 2004, The Journal of comparative neurology.

[50]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[51]  S. Easter,et al.  Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio) , 1994, The Journal of comparative neurology.

[52]  Rajesh P. N. Rao,et al.  Predictive learning of temporal sequences in recurrent neocortical circuits. , 2001, Novartis Foundation symposium.

[53]  M. Livingstone,et al.  Mechanisms of Direction Selectivity in Macaque V1 , 1998, Neuron.