Establishing Wiring Specificity in Visual System Circuits: From the Retina to the Brain.

The retina is a tremendously complex image processor, containing numerous cell types that form microcircuits encoding different aspects of the visual scene. Each microcircuit exhibits a distinct pattern of synaptic connectivity. The developmental mechanisms responsible for this patterning are just beginning to be revealed. Furthermore, signals processed by different retinal circuits are relayed to specific, often distinct, brain regions. Thus, much work has focused on understanding the mechanisms that wire retinal axonal projections to their appropriate central targets. Here, we highlight recently discovered cellular and molecular mechanisms that together shape stereotypic wiring patterns along the visual pathway, from within the retina to the brain. Although some mechanisms are common across circuits, others play unconventional and circuit-specific roles. Indeed, the highly organized connectivity of the visual system has greatly facilitated the discovery of novel mechanisms that establish precise synaptic connections within the nervous system.

[1]  J. B. Demb,et al.  Functional Circuitry of the Retina. , 2015, Annual review of vision science.

[2]  Alon Poleg-Polsky,et al.  Species-specific wiring for direction selectivity in the mammalian retina , 2016, Nature.

[3]  M. Stratton,et al.  Mutations in FRMD7, a newly identified member of the FERM family, cause X-linked idiopathic congenital nystagmus , 2006, Nature Genetics.

[4]  H. Kolb The inner plexiform layer in the retina of the cat: electron microscopic observations , 1979, Journal of neurocytology.

[5]  P. Detwiler,et al.  Directionally selective calcium signals in dendrites of starburst amacrine cells , 2002, Nature.

[6]  Samer Hattar,et al.  Central projections of melanopsin‐expressing retinal ganglion cells in the mouse , 2006, The Journal of comparative neurology.

[7]  D. I. Vaney,et al.  Chapter 2 The mosaic of amacrine cells in the mammalian retina , 1990 .

[8]  R. Wong,et al.  Neurotransmission selectively regulates synapse formation in parallel circuits in vivo , 2009, Nature.

[9]  F. Rieke,et al.  Interplay of Cell-Autonomous and Nonautonomous Mechanisms Tailors Synaptic Connectivity of Converging Axons In Vivo , 2014, Neuron.

[10]  W. Harris,et al.  Cellular Requirements for Building a Retinal Neuropil , 2013, Cell reports.

[11]  Phong L. Nguyen,et al.  Cadherin-6 Mediates Axon-Target Matching in a Non-Image-Forming Visual Circuit , 2011, Neuron.

[12]  E. Gundelfinger,et al.  Molecular dissection of the photoreceptor ribbon synapse , 2005, The Journal of cell biology.

[13]  Masahito Yamagata,et al.  Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina , 2008, Nature.

[14]  A. Litke,et al.  Corticothalamic Axons Are Essential for Retinal Ganglion Cell Axon Targeting to the Mouse Dorsal Lateral Geniculate Nucleus , 2016, The Journal of Neuroscience.

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

[16]  Erika D Eggers,et al.  Multiple pathways of inhibition shape bipolar cell responses in the retina , 2010, Visual Neuroscience.

[17]  Patricia Gaspar,et al.  Structural Requirement of TAG-1 for Retinal Ganglion Cell Axons and Myelin in the Mouse Optic Nerve , 2008, The Journal of Neuroscience.

[18]  Carol A. Mason,et al.  Slit1 and Slit2 Cooperate to Prevent Premature Midline Crossing of Retinal Axons in the Mouse Visual System , 2002, Neuron.

[19]  R. Wong,et al.  Diverse Strategies Engaged in Establishing Stereotypic Wiring Patterns among Neurons Sharing a Common Input at the Visual System's First Synapse , 2012, The Journal of Neuroscience.

[20]  S. Haverkamp,et al.  Morphology and connectivity of the small bistratified A8 amacrine cell in the mouse retina , 2015, The Journal of comparative neurology.

[21]  L. Chalupa,et al.  Depletion of Cholinergic Amacrine Cells by a Novel Immunotoxin Does Not Perturb the Formation of Segregated On and Off Cone Bipolar Cell Projections , 2002, The Journal of Neuroscience.

[22]  Benjamin Sivyer,et al.  Direction selectivity in the retina: symmetry and asymmetry in structure and function , 2012, Nature Reviews Neuroscience.

[23]  Masahito Yamagata,et al.  SIDEKICK 2 DIRECTS FORMATION OF A RETINAL CIRCUIT THAT DETECTS DIFFERENTIAL MOTION , 2015, Nature.

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

[25]  Andreas Hierlemann,et al.  Congenital Nystagmus Gene FRMD7 Is Necessary for Establishing a Neuronal Circuit Asymmetry for Direction Selectivity , 2016, Neuron.

[26]  Josh L. Morgan,et al.  Axons and dendrites originate from neuroepithelial-like processes of retinal bipolar cells , 2006, Nature Neuroscience.

[27]  J. Sanes,et al.  Type II Cadherins Guide Assembly of a Direction-Selective Retinal Circuit , 2014, Cell.

[28]  Fred Rieke,et al.  The spatial structure of a nonlinear receptive field , 2012, Nature Neuroscience.

[29]  N. Kamasawa,et al.  The Auxiliary Calcium Channel Subunit α2δ4 Is Required for Axonal Elaboration, Synaptic Transmission, and Wiring of Rod Photoreceptors , 2017, Neuron.

[30]  Samer Hattar,et al.  Architecture of retinal projections to the central circadian pacemaker , 2016, Proceedings of the National Academy of Sciences.

[31]  Ben A. Barres,et al.  Transgenic Mice Reveal Unexpected Diversity of On-Off Direction-Selective Retinal Ganglion Cell Subtypes and Brain Structures Involved in Motion Processing , 2011, The Journal of Neuroscience.

[32]  E. Weeber,et al.  ApoER2 Function in the Establishment and Maintenance of Retinal Synaptic Connectivity , 2011, The Journal of Neuroscience.

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

[34]  B. Völgyi,et al.  Convergence and Segregation of the Multiple Rod Pathways in Mammalian Retina , 2004, The Journal of Neuroscience.

[35]  T. Curran,et al.  The Reelin Pathway Modulates the Structure and Function of Retinal Synaptic Circuitry , 2001, Neuron.

[36]  B. Reese,et al.  Role of Afferents in the Differentiation of Bipolar Cells in the Mouse Retina , 2010, The Journal of Neuroscience.

[37]  M. A. Raven,et al.  Afferent Control of Horizontal Cell Morphology Revealed by Genetic Respecification of Rods and Cones , 2007, The Journal of Neuroscience.

[38]  M. Feller Retinal waves are likely to instruct the formation of eye-specific retinogeniculate projections , 2009, Neural Development.

[39]  Edward M. Callaway,et al.  A dedicated circuit linking direction selective retinal ganglion cells to primary visual cortex , 2014, Nature.

[40]  Heinz Wässle,et al.  Characterization of the glycinergic input to bipolar cells of the mouse retina , 2006, The European journal of neuroscience.

[41]  Botond Roska,et al.  The First Stage of Cardinal Direction Selectivity Is Localized to the Dendrites of Retinal Ganglion Cells , 2013, Neuron.

[42]  B. Chauhan,et al.  The retino–retinal projection: Tracing retinal ganglion cells projecting to the contralateral retina , 2015, Neuroscience Letters.

[43]  Bart G Borghuis,et al.  Excitatory Synaptic Inputs to Mouse On-Off Direction-Selective Retinal Ganglion Cells Lack Direction Tuning , 2014, The Journal of Neuroscience.

[44]  C. Mason,et al.  The optic chiasm as a midline choice point , 2004, Current Opinion in Neurobiology.

[45]  Joshua H. Singer,et al.  Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors , 2006, Nature.

[46]  E. Hartveit,et al.  Electrical synapses between AII amacrine cells in the retina: Function and modulation , 2012, Brain Research.

[47]  Tom Maniatis,et al.  PROTOCADHERINS MEDIATE DENDRITIC SELF-AVOIDANCE IN THE MAMMALIAN NERVOUS SYSTEM , 2012, Nature.

[48]  E. V. Famiglietti,et al.  Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction , 1991, The Journal of comparative neurology.

[49]  W. Taylor,et al.  Time course of EPSCs in ON‐type starburst amacrine cells is independent of dendritic location , 2016, The Journal of physiology.

[50]  A. Harvey,et al.  Seeing with Two Eyes: Integration of Binocular Retinal Projections in the Brain , 2013 .

[51]  R. Weiler,et al.  Expression and Localization of Connexins in the Outer Retina of the Mouse , 2015, Journal of Molecular Neuroscience.

[52]  P. Reynolds,et al.  The expanding family of FERM proteins. , 2013, The Biochemical journal.

[53]  Onkar S Dhande,et al.  Genetic Dissection of Retinal Inputs to Brainstem Nuclei Controlling Image Stabilization , 2013, The Journal of Neuroscience.

[54]  Onkar S. Dhande,et al.  Functional Assembly of Accessory Optic System Circuitry Critical for Compensatory Eye Movements , 2015, Neuron.

[55]  Y. Tsukamoto,et al.  Some OFF bipolar cell types make contact with both rods and cones in macaque and mouse retinas , 2014, Front. Neuroanat..

[56]  Y. Tsukamoto,et al.  Effects of mGluR6-deficiency on photoreceptor ribbon synapse formation: Comparison of electron microscopic analysis of serial sections with random sections , 2013, Visual Neuroscience.

[57]  Erika D Eggers,et al.  Presynaptic inhibition differentially shapes transmission in distinct circuits in the mouse retina , 2007, The Journal of physiology.

[58]  H. Wässle,et al.  GABAA and GABAC receptors on mammalian rod bipolar cells , 1998, The Journal of comparative neurology.

[59]  Brian Barton,et al.  fMRI of the rod scotoma elucidates cortical rod pathways and implications for lesion measurements , 2015, Proceedings of the National Academy of Sciences.

[60]  Hiroshi Ishikane,et al.  Identification of Retinal Ganglion Cells and Their Projections Involved in Central Transmission of Information about Upward and Downward Image Motion , 2009, PloS one.

[61]  B. Völgyi,et al.  The diverse functional roles and regulation of neuronal gap junctions in the retina , 2009, Nature Reviews Neuroscience.

[62]  Carol A. Mason,et al.  Retinal axon growth at the optic chiasm: to cross or not to cross. , 2008, Annual review of neuroscience.

[63]  H. Wässle,et al.  Glycine receptors of A-type ganglion cells of the mouse retina , 2007, Visual Neuroscience.

[64]  Michal Rivlin-Etzion,et al.  On and Off Retinal Circuit Assembly by Divergent Molecular Mechanisms , 2013, Science.

[65]  H. Holländer,et al.  A small population of retinal ganglion cells projecting to the retina of the other eye , 2004, Experimental Brain Research.

[66]  M. Feller,et al.  An Asymmetric Increase in Inhibitory Synapse Number Underlies the Development of a Direction Selective Circuit in the Retina , 2015, The Journal of Neuroscience.

[67]  T. Jessell,et al.  Optic Chiasm Presentation of Semaphorin6D in the Context of Plexin-A1 and Nr-CAM Promotes Retinal Axon Midline Crossing , 2012, Neuron.

[68]  Jianhua Cang,et al.  Developmental mechanisms of topographic map formation and alignment. , 2013, Annual review of neuroscience.

[69]  L. Chalupa,et al.  Segregation of On and Off Bipolar Cell Axonal Arbors in the Absence of Retinal Ganglion Cells , 2000, The Journal of Neuroscience.

[70]  W. Taylor,et al.  Direction selectivity in the retina , 2002, Current Opinion in Neurobiology.

[71]  Herwig Baier,et al.  The Retinal Projectome Reveals Brain-Area-Specific Visual Representations Generated by Ganglion Cell Diversity , 2014, Current Biology.

[72]  J. Simpson The accessory optic system. , 1984, Annual review of neuroscience.

[73]  J. Sanes,et al.  Expanding the Ig Superfamily Code for Laminar Specificity in Retina: Expression and Role of Contactins , 2012, The Journal of Neuroscience.

[74]  H Nawa,et al.  Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. , 1993, The Journal of biological chemistry.

[75]  Wallace B. Thoreson,et al.  Lateral interactions in the outer retina , 2012, Progress in Retinal and Eye Research.

[76]  S. Nakanishi,et al.  A Novel Connection between Rods and ON Cone Bipolar Cells Revealed by Ectopic Metabotropic Glutamate Receptor 7 (mGluR7) in mGluR6-Deficient Mouse Retinas , 2007, The Journal of Neuroscience.

[77]  M. Feller,et al.  DSCAM and DSCAML1 Function in Self-Avoidance in Multiple Cell Types in the Developing Mouse Retina , 2009, Neuron.

[78]  S. Haverkamp,et al.  Calcium Channel-Dependent Molecular Maturation of Photoreceptor Synapses , 2013, PloS one.

[79]  Kiely N. James,et al.  Mechanism for Selective Synaptic Wiring of Rod Photoreceptors into the Retinal Circuitry and Its Role in Vision , 2015, Neuron.

[80]  Ji-Jie Pang,et al.  Rod, M‐cone and M/S‐cone inputs to hyperpolarizing bipolar cells in the mouse retina , 2012, The Journal of physiology.

[81]  Daniel Kerschensteiner,et al.  NGL-2 Regulates Pathway-Specific Neurite Growth and Lamination, Synapse Formation, and Signal Transmission in the Retina , 2013, The Journal of Neuroscience.

[82]  K. Yau,et al.  Guidance-Cue Control of Horizontal Cell Morphology, Lamination, and Synapse Formation in the Mammalian Outer Retina , 2012, The Journal of Neuroscience.

[83]  J. Nathans,et al.  Class 5 Transmembrane Semaphorins Control Selective Mammalian Retinal Lamination and Function , 2011, Neuron.

[84]  N. Vardi,et al.  Lack of mGluR6‐related cascade elements leads to retrograde trans‐synaptic effects on rod photoreceptor synapses via matrix‐associated proteins , 2016, The European journal of neuroscience.

[85]  Frank S. Werblin,et al.  Mechanisms and circuitry underlying directional selectivity in the retina , 2002, Nature.

[86]  M. Feller,et al.  Genetic Identification of an On-Off Direction- Selective Retinal Ganglion Cell Subtype Reveals a Layer-Specific Subcortical Map of Posterior Motion , 2009, Neuron.

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

[88]  M. Bickford,et al.  Retinal and Tectal “Driver-Like” Inputs Converge in the Shell of the Mouse Dorsal Lateral Geniculate Nucleus , 2015, The Journal of Neuroscience.

[89]  Adam Bleckert,et al.  A Role for Synaptic Input Distribution in a Dendritic Computation of Motion Direction in the Retina , 2016, Neuron.

[90]  Mu-ming Poo,et al.  Turning of Retinal Growth Cones in a Netrin-1 Gradient Mediated by the Netrin Receptor DCC , 1997, Neuron.

[91]  Helga Kolb,et al.  The connections between horizontal cells and photoreceptors in the retina of the cat: Electron microscopy of Golgi preparations , 1974, The Journal of comparative neurology.

[92]  Kwok-Fai So,et al.  Frizzled3 Shapes the Development of Retinal Rod Bipolar Cells. , 2016, Investigative ophthalmology & visual science.

[93]  Dimitar Kostadinov,et al.  Protocadherin-dependent dendritic self-avoidance regulates neural connectivity and circuit function , 2015, eLife.

[94]  W. Guido Refinement of the retinogeniculate pathway , 2008, The Journal of physiology.

[95]  D. Mastronarde,et al.  Exploring the retinal connectome , 2011, Molecular vision.

[96]  Helga Kolb,et al.  Rod and Cone Pathways in the Inner Plexiform Layer of Cat Retina , 1974, Science.

[97]  Y. Tsukamoto,et al.  Functional allocation of synaptic contacts in microcircuits from rods via rod bipolar to AII amacrine cells in the mouse retina , 2013, The Journal of comparative neurology.

[98]  S. Takeda,et al.  Post-translational Maturation of Dystroglycan Is Necessary for Pikachurin Binding and Ribbon Synaptic Localization* , 2010, The Journal of Biological Chemistry.

[99]  Takashi Fujikado,et al.  Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation , 2008, Nature Neuroscience.

[100]  H. Baier,et al.  Molecular and cellular mechanisms of lamina-specific axon targeting. , 2010, Cold Spring Harbor perspectives in biology.

[101]  M. A. Raven,et al.  Development and Plasticity of Outer Retinal Circuitry Following Genetic Removal of Horizontal Cells , 2013, The Journal of Neuroscience.

[102]  Adam Bleckert,et al.  Visual Space Is Represented by Nonmatching Topographies of Distinct Mouse Retinal Ganglion Cell Types , 2014, Current Biology.

[103]  Onkar S. Dhande,et al.  Contributions of Retinal Ganglion Cells to Subcortical Visual Processing and Behaviors. , 2015, Annual review of vision science.

[104]  Balázs Rózsa,et al.  Single-cell–initiated monosynaptic tracing reveals layer-specific cortical network modules , 2015, Science.

[105]  B. Roska,et al.  Adeno-associated virus-RNAi of GlyRα1 and characterization of its synapse-specific inhibition in OFF alpha transient retinal ganglion cells. , 2014, Journal of neurophysiology.

[106]  S. Wu,et al.  Connexin 36 and rod bipolar cell independent rod pathways drive retinal ganglion cells and optokinetic reflexes , 2016, Vision Research.

[107]  W. R. Taylor,et al.  The role of starburst amacrine cells in visual signal processing , 2012, Visual Neuroscience.

[108]  Srinivas C. Turaga,et al.  Space-time wiring specificity supports direction selectivity in the retina , 2014, Nature.

[109]  Satchidananda Panda,et al.  Melanopsin Contributions to Irradiance Coding in the Thalamo-Cortical Visual System , 2010, PLoS biology.

[110]  F. Werblin,et al.  Directional Selectivity Is Formed at Multiple Levels by Laterally Offset Inhibition in the Rabbit Retina , 2005, Neuron.

[111]  Jianhua Cang,et al.  Neurons in the Most Superficial Lamina of the Mouse Superior Colliculus Are Highly Selective for Stimulus Direction , 2015, The Journal of Neuroscience.

[112]  Michael S. Deiner,et al.  Netrin-1 and DCC Mediate Axon Guidance Locally at the Optic Disc: Loss of Function Leads to Optic Nerve Hypoplasia , 1997, Neuron.

[113]  Xiaofeng Ma,et al.  Spontaneous Activity Promotes Synapse Formation in a Cell-Type-Dependent Manner in the Developing Retina , 2012, The Journal of Neuroscience.

[114]  C. Ruhrberg,et al.  VEGF Signaling through Neuropilin 1 Guides Commissural Axon Crossing at the Optic Chiasm , 2011, Neuron.

[115]  J. S. Lauritzen,et al.  The AII amacrine cell connectome: a dense network hub , 2014, Front. Neural Circuits.

[116]  M. Meister,et al.  A neuronal circuit for colour vision based on rod–cone opponency , 2016, Nature.

[117]  L. P. Morin,et al.  Retinofugal projections in the mouse , 2014, The Journal of comparative neurology.

[118]  M. Fox,et al.  Multiple Retinal Axons Converge onto Relay Cells in the Adult Mouse Thalamus , 2015, Cell reports.

[119]  Daniel R. Berger,et al.  The Fuzzy Logic of Network Connectivity in Mouse Visual Thalamus , 2016, Cell.

[120]  Glen T. Prusky,et al.  Melanopsin-Expressing Retinal Ganglion-Cell Photoreceptors: Cellular Diversity and Role in Pattern Vision , 2010, Neuron.

[121]  M. Crair,et al.  Structural organization and function of mouse photoreceptor ribbon synapses involve the immunoglobulin protein synaptic cell adhesion molecule 1 , 2014, The Journal of comparative neurology.

[122]  J. Sanes,et al.  Chemoaffinity Revisited: Dscams, Protocadherins, and Neural Circuit Assembly , 2010, Cell.

[123]  Phong L. Nguyen,et al.  Contactin-4 Mediates Axon-Target Specificity and Functional Development of the Accessory Optic System , 2015, Neuron.

[124]  M. Kondo,et al.  Presynaptic Dystroglycan–Pikachurin Complex Regulates the Proper Synaptic Connection between Retinal Photoreceptor and Bipolar Cells , 2012, The Journal of Neuroscience.

[125]  B. Roska,et al.  Rods in daylight act as relay cells for cone-driven horizontal cell–mediated surround inhibition , 2014, Nature Neuroscience.

[126]  F. Rieke,et al.  Neurotransmission plays contrasting roles in the maturation of inhibitory synapses on axons and dendrites of retinal bipolar cells , 2015, Proceedings of the National Academy of Sciences.

[127]  R. Wong,et al.  Developmental Regulation and Activity-Dependent Maintenance of GABAergic Presynaptic Inhibition onto Rod Bipolar Cell Axonal Terminals , 2013, Neuron.

[128]  R. Wong,et al.  Sensory Experience Shapes the Development of the Visual System’s First Synapse , 2013, Neuron.

[129]  Kevin L. Briggman,et al.  Wiring specificity in the direction-selectivity circuit of the retina , 2011, Nature.

[130]  C. Chiao,et al.  Cx36 expression in the AII‐mediated rod pathway is activity dependent in the developing rabbit retina , 2016, Developmental neurobiology.

[131]  E. Strettoi,et al.  Recruitment of the Rod Pathway by Cones in the Absence of Rods , 2004, The Journal of Neuroscience.

[132]  Phong L. Nguyen,et al.  Birthdate and outgrowth timing predict cellular mechanisms of axon target matching in the developing visual pathway. , 2014, Cell reports.

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

[134]  Kiely N. James,et al.  Ephrin‐as are required for the topographic mapping but not laminar choice of physiologically distinct RGC types , 2015, Developmental neurobiology.

[135]  H. Wässle,et al.  GABAA Receptor subunits have differential distributions in the rat retinae: In situ hybridization and immunohistochemistry , 1995, The Journal of comparative neurology.

[136]  B. Boycott,et al.  Dendritic territories of cat retinal ganglion cells , 1981, Nature.

[137]  Lynda Erskine,et al.  The retinal ganglion cell axon's journey: insights into molecular mechanisms of axon guidance. , 2007, Developmental biology.

[138]  Tudor C. Badea,et al.  Transmembrane semaphorin signaling controls laminar stratification in the mammalian retina , 2010, Nature.

[139]  W. Guido,et al.  Reelin Is Required for Class-Specific Retinogeniculate Targeting , 2011, The Journal of Neuroscience.

[140]  Botond Roska,et al.  Ambient Illumination Toggles a Neuronal Circuit Switch in the Retina and Visual Perception at Cone Threshold , 2013, Neuron.

[141]  J. Sanes,et al.  Laminar Restriction of Retinal Ganglion Cell Dendrites and Axons: Subtype-Specific Developmental Patterns Revealed with Transgenic Markers , 2010, The Journal of Neuroscience.

[142]  Herwig Baier,et al.  Synaptic laminae in the visual system: molecular mechanisms forming layers of perception. , 2013, Annual review of cell and developmental biology.

[143]  C. Sabatti,et al.  Robust discrimination between self and non-self neurites requires thousands of Dscam1 isoforms , 2009, Nature.

[144]  F. Rieke,et al.  Complex Inhibitory Microcircuitry Regulates Retinal Signaling near Visual Threshold All Experiments Were Performed in Accordance with Protocols Approved by Institutional Animal Care and Use Committees at The , 2022 .

[145]  R. Wong,et al.  Supplemental Information Development of Cell Type-Specific Connectivity Patterns of Converging Excitatory Axons in the Retina , 2011 .

[146]  R. Wong,et al.  Functional architecture of the retina: Development and disease , 2014, Progress in Retinal and Eye Research.

[147]  Masahito Yamagata,et al.  Retinal Ganglion Cells with Distinct Directional Preferences Differ in Molecular Identity, Structure, and Central Projections , 2011, The Journal of Neuroscience.

[148]  D. Schreiner,et al.  Combinatorial homophilic interaction between γ-protocadherin multimers greatly expands the molecular diversity of cell adhesion , 2010, Proceedings of the National Academy of Sciences.

[149]  J. Sanes,et al.  The types of retinal ganglion cells: current status and implications for neuronal classification. , 2015, Annual review of neuroscience.