Making a visual map: mechanisms and molecules

Current Opinion in Neurobiology

Volumn 19, Issue 2, 2009, Pages 174-180

  Clandinin, Thomas R ^a   Feldheim, David A ^b  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN;

AUTOCRINE EFFECT; CELL ADHESION; CELL INTERACTION; CELL PROLIFERATION; DENDRITE; MOLECULAR BIOLOGY; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVE GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; REGULATORY MECHANISM; RETINA DEVELOPMENT; REVIEW; SIGNAL TRANSDUCTION; TARGET CELL; VERTEBRATE; VISUAL CORTEX; VISUAL NERVOUS SYSTEM;

ANIMALS; BRAIN; NEURONS; RETINA; TIME FACTORS; VISUAL PATHWAYS; VISUAL PERCEPTION;

EID: 67651049541     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2009.04.011     Document Type: Review

References (37)

1. Huang Z., and Kunes S. Hedgehog, transmitted along retinal axons, triggers neurogenesis in the developing visual centers of the Drosophila brain. Cell 86 (1996) 411-422
2. Huang Z., Shilo B.Z., and Kunes S. A retinal axon fascicle uses spitz, an EGF receptor ligand, to construct a synaptic cartridge in the brain of Drosophila. Cell 95 (1998) 693-703
3. Umetsu D., Murakami S., Sato M., and Tabata T. The highly ordered assembly of retinal axons and their synaptic partners is regulated by Hedgehog/Single-minded in the Drosophila visual system. Development 133 (2006) 791-800
4. Sato M., Umetsu D., Murakami S., Yasugi T., and Tabata T. DWnt4 regulates the dorsoventral specificity of retinal projections in the Drosophila melanogaster visual system. Nat Neurosci 9 (2006) 67-75
5. Tomasi T., Hakeda-Suzuki S., Ohler S., Schleiffer A., and Suzuki T. The transmembrane protein Golden goal regulates R8 photoreceptor axon-axon and axon-target interactions. Neuron 57 (2008) 691-704
6. Kirschfeld K. The projection of the optical environment on the screen of the rhabdomere in the compound eye of the Musca. Exp Brain Res 3 (1967) 248-270
7. Braitenberg V. Patterns of projection in the visual system of the fly. 1. Retina-lamina projections. Exp Brain Res 3 (1967) 271-298
8. Clandinin T.R., and Zipursky S.L. Afferent growth cone interactions control synaptic specificity in the Drosophila visual system. Neuron 28 (2000) 427-436
9. Hiesinger P.R., Zhai R.G., Zhou Y., Koh T.W., Mehta S.Q., Schulze K.L., Cao Y., Verstreken P., Clandinin T.R., Fischbach K.F., et al. Activity-independent prespecification of synaptic partners in the visual map of Drosophila. Curr Biol 16 (2006) 1835-1843
10. Lee R.C., Clandinin T.R., Lee C.H., Chen P.L., Meinertzhagen I.A., and Zipursky S.L. The protocadherin Flamingo is required for axon target selection in the Drosophila visual system. Nat Neurosci 6 (2003) 557-563
11. Chen P.L., and Clandinin T.R. The cadherin Flamingo mediates level-dependent interactions that guide photoreceptor target choice in Drosophila. Neuron 58 (2008) 26-33. The non-classical cadherin Flamingo is required for R1-R6 axons to choose appropriate target columns within the developing Drosophila lamina. Using a series of somatic mosaic studies, this work demonstrates that Flamingo mediates cell-cell interactions between growth cones within the same ommatidial bundle, and that relative differences in Flamingo levels between neighboring growth cones determine subsequent outgrowth trajectory.
12. Bazigou E., Apitz H., Johansson J., Loren C.E., Hirst E.M., Chen P.L., Palmer R.H., and Salecker I. Anterograde Jelly belly and Alk receptor tyrosine kinase signaling mediates retinal axon targeting in Drosophila. Cell 128 (2007) 961-975
13. Huberman A.D., Manu M., Koch S.M., Susman M.W., Lutz A.B., Ullian E.M., Baccus S.A., and Barres B.A. Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59 (2008) 425-438. A transgenic line of mice that expresses GFP in a complete mosaic of transient OFF-alpha RGCs is described. This class of RGCs projects exclusively to the SC and LGN and are restricted to a specific lamina in each of these targets. In addition, the axons are also organized into columns in the SC. Column structure, but not lamination, become blurred when spontaneous activity patterns are disrupted suggesting that lamina choice is independent of activity for this cell type. This is the first example of a study examining the development of a genetically identified visual projection in mammals.
14. Pfeiffenberger C., Yamada J., and Feldheim D.A. Ephrin-As and patterned retinal activity act together in the development of topographic maps in the primary visual system. J Neurosci 26 (2006) 12873-12884
15. Cang J., Wang L., Stryker M.P., and Feldheim D.A. Roles of ephrin-as and structured activity in the development of functional maps in the superior colliculus. J Neurosci 28 (2008) 11015-11023. A method of Fourier imaging of intrinsic signals was used to visualize the functional maps in the mouse SC in wild type, ephrin-A tko mice, and mice missing ephrin-As plus the β2 subunit of the nACh receptor (the mice have altered patterns of spontaneous retinal activity). In the absence of ephrin-As, functional maps are disrupted selectively along the N-T mapping axis, and are discontinuous, with patches of SC responding to topographically incorrect locations. Removal of ephrin-As and β2 results in a near absence of map, selectively along the N-T axis. These results are consistent with a computational model that includes graded guidance cues, axon-axon competition and activity-dependent mechanisms in mapping.
16. Rashid T., Upton A.L., Blentic A., Ciossek T., Knoll B., Thompson I.D., and Drescher U. Opposing gradients of Ephrin-As and EphA7 in the superior colliculus are essential for topographic mapping in the mammalian visual system. Neuron 47 (2005) 57-69
17. Lim Y.S., McLaughlin T., Sung T.C., Santiago A., Lee K.F., and O'Leary D.D. p75(NTR) mediates ephrin-A reverse signaling required for axon repulsion and mapping. Neuron 59 (2008) 746-758. The low affinity neurotrophin receptor, p75, was identified as a co-receptor required for ephrin-A reverse signaling by retinal ganglion cells. Retinal axons require p75 for EphA7 repulsion in vitro and nasal axons make topographic mapping errors in p75 mutant mice.
18. Marler K.J., Becker-Barroso E., Martinez A., Llovera M., Wentzel C., Poopalasundaram S., Hindges R., Soriano E., Comella J., and Drescher U. A TrkB/EphrinA interaction controls retinal axon branching and synaptogenesis. J Neurosci 28 (2008) 12700-12712. A novel cis interaction between ephrin-A5 and TrkB on RGC axons was discovered. Data presented suggest that this interaction contributes to the control of axon branching of RGC axons and is also involved in branching and synaptogenesis of hippocampal neurons.
19. Brown A., Yates P.A., Burrola P., Ortuno D., Vaidya A., Jessell T.M., Pfaff S.L., O'Leary D.D.M., and Lemke G. Topographic mapping from the retina to the midbrain is controlled by relative but not absolute levels of EphA receptor signaling. Cell 102 (2000) 77-88
20. Gosse N.J., Nevin L.M., and Baier H. Retinotopic order in the absence of axon competition. Nature 452 (2008) 892-895
21. Millard S.S., Flanagan J.J., Pappu K.S., Wu W., and Zipursky S.L. Dscam2 mediates axonal tiling in the Drosophila visual system. Nature 447 (2007) 720-724. A member of the Ig Superfamily, DSCAM2, was knocked out and shown to play a role in restricting the axons of a specific subtype of lamina neuron to single columns in the medulla. Biochemical analysis demonstrated that this protein mediates homophillic interactions, and single-cell somatic mosaic analysis determined that this protein has both cell-autonomous and non-autonomous effects on neighboring terminals. This paper proposed that homophillic, repulsive interactions between neighboring growth cones underlies the phenomenon of axon tiling in this context.
22. Ting C.Y., Herman T., Yonekura S., Gao S., Wang J., Serpe M., O'Connor M.B., Zipursky S.L., and Lee C.H. Tiling of r7 axons in the Drosophila visual system is mediated both by transduction of an activin signal to the nucleus and by mutual repulsion. Neuron 56 (2007) 793-806. Activin-mediated signals are required to restrict the terminals of R7 photoreceptors to single columns in the medulla. Genetic studies of multiple signaling components reveal that this pathway functions in autocrine fashion, requires transmitting a signal from the growth cone to the nucleus, and acts by reducing growth cone motility. This work thus demonstrates the importance of both cell-intrinsic and extrinsic cues in achieving axon tiling.
23. Fuerst P.G., Koizumi A., Masland R.H., and Burgess R.W. Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 451 (2008) 470-474. A DSCAM mutant mouse was identified and shown to have tiling defects consistent with the idea that DSCAM is a homophillic repellent molecule. DSCAM is normally expressed in subsets of neurons in the retina including two types of amacrine cells. In DSCAM mutants these cells have altered spacing and dendritic morphologies. This is the first example of a genetic perturbation that affects tiling in the vertebrate visual system.
24. Lin B., Wang S.W., and Masland R.H. Retinal ganglion cell type, size, and spacing can be specified independent of homotypic dendritic contacts. Neuron 43 (2004) 475-485
25. Huckfeldt R.M., Schubert T., Morgan J.L., Godinho L., Di Cristo G., Huang Z.J., and Wong R.O. Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions. Nat Neurosci 12 (2009) 35-43
26. Petrovic M., and Hummel T. Temporal identity in axonal target layer recognition. Nature 456 (2008) 800-803. Mutations in the transcription factor sequoia disrupt the layer-specific targeting decisions made by R7 and R8 photoreceptor axons. Sequoia is expressed in a temporally dynamic pattern as these cells differentiate, being expressed first in R8, and then in R7. Altering this temporal sequence of expression, causing R7 and R8 axons to express sequoia simultaneously directs R7 and R8 axons to the same layer, an effect that is dependent on the classical cadherin, N-cadherin. This work suggests that dynamic regulation of competence to respond to a relatively generic adhesive factor can drive lamination.
27. Lee C.H., Herman T., Clandinin T.R., Lee R., and Zipursky S.L. N-cadherin regulates target specificity in the Drosophila visual system. Neuron 30 (2001) 437-450
28. Nern A., Zhu Y., and Zipursky S.L. Local N-cadherin interactions mediate distinct steps in the targeting of lamina neurons. Neuron 58 (2008) 34-41
29. Morey M., Yee S.K., Herman T., Nern A., Blanco E., and Zipursky S.L. Coordinate control of synaptic-layer specificity and rhodopsins in photoreceptor neurons. Nature 456 (2008) 795-799
30. Shinza-Kameda M., Takasu E., Sakurai K., Hayashi S., and Nose A. Regulation of layer-specific targeting by reciprocal expression of a cell adhesion molecule, capricious. Neuron 49 (2006) 205-213
31. Liu X., Grishanin R.N., Tolwani R.J., Renteria R.C., Xu B., Reichardt L.F., and Copenhagen D.R. Brain-derived neurotrophic factor and TrkB modulate visual experience-dependent refinement of neuronal pathways in retina. J Neurosci 27 (2007) 7256-7267
32. Tian N., and Copenhagen D.R. Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron 39 (2003) 85-96
33. Nevin L.M., Taylor M.R., and Baier H. Hardwiring of fine synaptic layers in the zebrafish visual pathway. Neural Dev 3 (2008) 36
34. Mumm J.S., Williams P.R., Godinho L., Koerber A., Pittman A.J., Roeser T., Chien C.B., Baier H., and Wong R.O. In vivo imaging reveals dendritic targeting of laminated afferents by zebrafish retinal ganglion cells. Neuron 52 (2006) 609-621
35. Yamagata M., and Sanes J.R. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451 (2008) 465-469. Four closely related IGG super family members are expressed in overlapping and distinct subsets of interneurons and RGCs in the retina. Loss and gain of function perturbations resulted in predictable changes in retinal lamination that are consistent with these molecules acting as homophilic adhesion molecules. This work suggests that there is a combinatorial cell-adhesion code that is used to direct pre- and post-synaptic partners to their proper lamina
36. Yonehara K., Shintani T., Suzuki R., Sakuta H., Takeuchi Y., Nakamura-Yonehara K., and Noda M. Expression of SPIG1 reveals development of a retinal ganglion cell subtype projecting to the medial terminal nucleus in the mouse. PLoS ONE 3 (2008) e1533
37. Kim I.J., Zhang Y., Yamagata M., Meister M., and Sanes J.R. Molecular identification of a retinal cell type that responds to upward motion. Nature 452 (2008) 478-482