Ephrin-As and Neural Activity Are Required for Eye-specific Patterning During Retinogeniculate Mapping

Overview

Journal Nat Neurosci

Date 2005 Jul 19

PMID 16025107

Citations 113

Authors

Cory Pfeiffenberger

Tyler Cutforth

Georgia Woods

Jena Yamada

Rene C Renteria

David R Copenhagen

John G Flanagan

David A Feldheim

Affiliations

Soon will be listed here.

Abstract

In mammals, retinal ganglion cell (RGC) projections initially intermingle and then segregate into a stereotyped pattern of eye-specific layers in the dorsal lateral geniculate nucleus (dLGN). Here we found that in mice deficient for ephrin-A2, ephrin-A3 and ephrin-A5, eye-specific inputs segregated but the shape and location of eye-specific layers were profoundly disrupted. In contrast, mice that lacked correlated retinal activity did not segregate eye-specific inputs. Inhibition of correlated neural activity in ephrin mutants led to overlapping retinal projections that were located in inappropriate regions of the dLGN. Thus, ephrin-As and neural activity act together to control patterning of eye-specific retinogeniculate layers.

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References

Williams S, Mann F, Erskine L, Sakurai T, Wei S, Rossi D . Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron. 2003; 39(6):919-35. DOI: 10.1016/j.neuron.2003.08.017. View

Feldheim D, Vanderhaeghen P, Hansen M, Frisen J, Lu Q, Barbacid M . Topographic guidance labels in a sensory projection to the forebrain. Neuron. 1999; 21(6):1303-13. DOI: 10.1016/s0896-6273(00)80650-9. View

Feldheim D, Nakamoto M, Osterfield M, Gale N, DeChiara T, Rohatgi R . Loss-of-function analysis of EphA receptors in retinotectal mapping. J Neurosci. 2004; 24(10):2542-50. PMC: 6729493. DOI: 10.1523/JNEUROSCI.0239-03.2004. View

Vanderhaeghen P, Polleux F . Developmental mechanisms patterning thalamocortical projections: intrinsic, extrinsic and in between. Trends Neurosci. 2004; 27(7):384-91. DOI: 10.1016/j.tins.2004.05.009. View

Gartz Hanson M, Landmesser L . Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron. 2004; 43(5):687-701. DOI: 10.1016/j.neuron.2004.08.018. View

Crowley J, Katz L . Development of ocular dominance columns in the absence of retinal input. Nat Neurosci. 1999; 2(12):1125-30. DOI: 10.1038/16051. View

Flanagan J . In situ analysis of embryos with receptor or ligand fusion protein probes. Curr Biol. 2000; 10(2):R52-3. DOI: 10.1016/s0960-9822(00)00293-1. View

Chapman B . Necessity for afferent activity to maintain eye-specific segregation in ferret lateral geniculate nucleus. Science. 2000; 287(5462):2479-82. PMC: 2637940. DOI: 10.1126/science.287.5462.2479. View

Feldheim D, Kim Y, Bergemann A, Frisen J, Barbacid M, Flanagan J . Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron. 2000; 25(3):563-74. DOI: 10.1016/s0896-6273(00)81060-0. View

10.

Huh G, Boulanger L, Du H, Riquelme P, Brotz T, Shatz C . Functional requirement for class I MHC in CNS development and plasticity. Science. 2000; 290(5499):2155-9. PMC: 2175035. DOI: 10.1126/science.290.5499.2155. View

11.

Rossi F, Pizzorusso T, Porciatti V, Marubio L, Maffei L, Changeux J . Requirement of the nicotinic acetylcholine receptor beta 2 subunit for the anatomical and functional development of the visual system. Proc Natl Acad Sci U S A. 2001; 98(11):6453-8. PMC: 33489. DOI: 10.1073/pnas.101120998. View

12.

Pham T, Rubenstein J, Silva A, Storm D, Stryker M . The CRE/CREB pathway is transiently expressed in thalamic circuit development and contributes to refinement of retinogeniculate axons. Neuron. 2001; 31(3):409-20. DOI: 10.1016/s0896-6273(01)00381-6. View

13.

Stellwagen D, Shatz C . An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron. 2002; 33(3):357-67. DOI: 10.1016/s0896-6273(02)00577-9. View

14.

Crowley J, Katz L . Ocular dominance development revisited. Curr Opin Neurobiol. 2002; 12(1):104-9. DOI: 10.1016/s0959-4388(02)00297-0. View

15.

Muir-Robinson G, Hwang B, Feller M . Retinogeniculate axons undergo eye-specific segregation in the absence of eye-specific layers. J Neurosci. 2002; 22(13):5259-64. PMC: 6758243. DOI: 20026563. View

16.

Hindges R, McLaughlin T, Genoud N, Henkemeyer M, OLeary D . EphB forward signaling controls directional branch extension and arborization required for dorsal-ventral retinotopic mapping. Neuron. 2002; 35(3):475-87. DOI: 10.1016/s0896-6273(02)00799-7. View

17.

Huberman A, Stellwagen D, Chapman B . Decoupling eye-specific segregation from lamination in the lateral geniculate nucleus. J Neurosci. 2002; 22(21):9419-29. PMC: 2662346. View

18.

Adams D, Horton J . Capricious expression of cortical columns in the primate brain. Nat Neurosci. 2003; 6(2):113-4. DOI: 10.1038/nn1004. View

19.

McLaughlin T, Hindges R, OLeary D . Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr Opin Neurobiol. 2003; 13(1):57-69. DOI: 10.1016/s0959-4388(03)00014-x. View

20.

Demas J, Eglen S, Wong R . Developmental loss of synchronous spontaneous activity in the mouse retina is independent of visual experience. J Neurosci. 2003; 23(7):2851-60. PMC: 6742078. View