Development and plasticity of outer retinal circuitry following genetic removal of horizontal cells

Journal of Neuroscience

Volumn 33, Issue 45, 2013, Pages 17847-17862

  Keeley, Patrick W ^a   Luna, Gabriel ^a   Fariss, Robert N ^f   Skyles, Kimberly A ^a   Madsen, Nils R ^a   Raven, Mary A ^a   Poché, Ross A ^c   Swindell, Eric C ^d   Jamrich, Milan ^c   Oh, Edwin C ^e   Swaroop, Anand ^f   Fisher, Steven K ^a,b   Reese, Benjamin E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

^f NATIONAL EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL MIGRATION; DENDRITE; ELECTRON MICROSCOPY; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MOUSE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; RETINA; RETINA BIPOLAR GANGLION CELL; RETINA CONE; RETINA HORIZONTAL NERVE CELL; RETINA ROD;

ANIMALS; FEMALE; MICE; MICE, TRANSGENIC; NEURONAL PLASTICITY; RETINAL HORIZONTAL CELLS; RETINAL NEURONS; SYNAPSES; VISUAL PATHWAYS;

EID: 84887065413     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1373-13.2013     Document Type: Article

References (52)

1. Bayley PR, Morgans CW (2007) Rod bipolar cells and horizontal cells form displaced synaptic contacts with rods in the outer nuclear layer of the nob2 retina. J Comp Neurol 500:286-298. CrossRef Medline
2. Betley JN, Wright CV, Kawaguchi Y, Erdélyi F, Szabó G, Jessell TM, Kaltschmidt JA (2009) Stringent specificity in the construction of a GABAergic presynaptic inhibitory circuit. Cell 139:161-174. CrossRef Medline
3. Blanks JC, Johnson LV (1983) Selective lectin binding of the developing mouse retina. J Comp Neurol 221:31-41. CrossRef Medline
4. Chang B, Heckenlively JR, Bayley PR, Brecha NC, Davisson MT, Hawes NL, Hirano AA, Hurd RE, Ikeda A, Johnson BA, McCall MA, Morgans CW, Nusinowitz S, Peachey NS, Rice DS, Vessey KA, Gregg RG (2006) The nob2 mouse, a null mutation in Cacna1f: anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses. Vis Neurosci 23:11-24. CrossRef Medline
5. Dalva MB, McClelland AC, Kayser MS (2007) Cell adhesion molecules: signalling functions at the synapse. Nat Rev Neurosci 8:206-220. CrossRef Medline
6. Dick O, Tom Dieck S, Altrock WD, Ammermüller J, Weiler R, Garner CC, Gundelfinger ED, Brandstätter JH (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37:775-786. CrossRef Medline
7. Fisher SK, Lewis GP (2003) Müller cell and neuronal remodeling in retinal detachment and reattachment and their potential consequences for visual recovery: a review and reconsideration of recent data. Vision Res 43:887-897. CrossRef Medline
8. Fisher SK, Lewis GP, Linberg KA, Verardo MR (2005) Cellular remodeling in mammalian retina: results from studies of experimental retinal detachment. Prog Ret Eye Res 24:395-431. CrossRef Medline
9. Fox K, Wong RO (2005) A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48:465-477. CrossRef Medline
10. Frotscher M, Zhao S, Förster E (2007) Development of cell and fiber layers in the dentate gyrus. Prog Brain Res 163:133-142. CrossRef Medline
11. Fuerst PG, Bruce F, Tian M, Wei W, Elstrott J, Feller MB, Erskine L, Singer JH, Burgess RW (2009) DSCAM and DSCAML1 function in self-avoidance in multiple cell types in the developing mouse retina. Neuron 64:484-497. CrossRef Medline
12. 2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nat Neurosci 7:1079-1087. CrossRef Medline
13. Haverkamp S, Grünert U, Wässle H (2001) The synaptic architecture of AMPA receptors at the cone pedicle of the primate retina. J Neurosci 21:2488-2500.
14. Huang L, Max M, Margolskee RF, Su H, Masland RH, Euler T (2003) G protein subunit G gamma 13 is coexpressed with G alpha o, G beta 3, and G beta 4 in retinal ON bipolar cells. J Comp Neurol 455:1-10. CrossRef Medline
15. Huberman AD, Clandinin TR, Baier H (2010) Molecular and cellular mechanisms of lamina-specific axon targeting. Cold Spring Harb Perspect Biol 2:a001743. CrossRef Medline
16. Huckfeldt RM, Schubert T, Morgan JL, Godinho L, Di Cristo G, Huang ZJ, Wong RO (2009) Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions. Nat Neurosci 12:35-43. CrossRef Medline
17. Keeley PW, Reese BE (2010) Role of afferents in the differentiation of bipolar cells in the mouse retina. J Neurosci 30:1677-1685. CrossRef Medline
18. Keeley PW, Sliff BJ, Lee SC, Fuerst PG, Burgess RW, Eglen SJ, Reese BE (2012) Neuronal clustering and fasciculation phenotype in Dscam-and Bax-deficient mouse retinas. J Comp Neurol 520:1349-1364. CrossRef Medline
19. Kremer JR, Mastronarde DN, McIntosh RJ (1996) Computer visualization of three-dimensional image data using iMod. J Struct Biol 116:71-76. CrossRef Medline
20. Kwan KM, Behringer RR (2002) Conditional inactivation of Lim1 function. Genesis 32:118-120. CrossRef Medline
21. Lee SC, Cowgill EJ, Al-Nabulsi A, Quinn EJ, Evans SM, Reese BE (2011) Homotypic regulation of neuronal morphology and connectivity in the mouse retina. J Neurosci 31:14126-14133. CrossRef Medline
22. Lewis GP, Linberg KA, Fisher SK (1998) Neurite outgrowth from bipolar and horizontal cells after experimental retinal detachment. Invest Ophthalmol Vis Sci 39:424-434.
23. Medline
24. Liets LC, Eliasieh K, van der List DA, Chalupa LM (2006) Dendrites of rod bipolar cells sprout in normal aging retina. Proc Natl Acad Sci U S A 103:12156-12160. CrossRef Medline
25. Mansergh F, Orton NC, Vessey JP, Lalonde MR, Stell WK, Tremblay F, Barnes S, Rancourt DE, Bech-Hansen NT (2005) Mutation of the calcium channel gene Cacna1f disrupts calcium signaling, synaptic transmission and cellular organization in mouse retina. Hum Mol Genet 14:3035-3046. CrossRef Medline
26. Marc RE, Jones BW, Watt CB, Strettoi E (2003) Neural remodeling in retinal degeneration. Prog Ret Eye Res 22:607-655. CrossRef Medline
27. Matsuoka RL, Chivatakarn O, Badea TC, Samuels IS, Cahill H, Katayama K, Kumar SR, Suto F, Chédotal A, Peachey NS, Nathans J, Yoshida Y, Giger RJ, Kolodkin AL (2011a) Class 5 transmembrane semaphorins control selective Mammalian retinal lamination and function. Neuron 71:460-473. CrossRef Medline
28. Matsuoka RL, Nguyen-Ba-Charvet KT, Parray A, Badea TC, Chédotal A, Kolodkin AL (2011b) Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 470:259-263. CrossRef Medline
29. Matsuoka RL, Jiang Z, Samuels IS, Nguyen-Ba-Charvet KT, Sun LO, Peachey NS, Chédotal A, Yau KW, Kolodkin AL (2012) Guidancecue control of horizontal cell morphology, lamination, and synapse formation in the mammalian outer retina. J Neurosci 32:6859-6868. CrossRef Medline
30. Mears AJ, Kondo M, Swain PK, Takada Y, Bush RA, Saunders TL, Sieving PA, Swaroop A (2001) Nrl is required for rod photoreceptor development. Nat Genet 29:447-452. CrossRef Medline
31. Morgan JL, Dhingra A, Vardi N, Wong RO (2006) Axons and dendrites originate from neuroepithelial-like processes of retinal bipolar cells. Nat Neurosci 9:85-92. CrossRef Medline
32. Poché RA, Kwan KM, Raven MA, Furuta Y, Reese BE, Behringer RR (2007) Lim1 is essential for the correct laminar positioning of retinal horizontal cells. J Neurosci 27:14099-14107. CrossRef Medline
33. Poché RA, Raven MA, Kwan KM, Furuta Y, Behringer RR, Reese BE (2008) Somal positioning and dendritic growth of horizontal cells are regulated by interactions with homotypic neighbors. Eur J Neurosci 27:1607-1614. CrossRef Medline
34. Raisman G (1994) Plasticity of adult central fibre tracts. Prog Brain Res 100:195-201. CrossRef Medline
35. Raven MA, Stagg SB, Nassar H, Reese BE (2005) Developmental improvement in the regularity and packing of mouse horizontal cells: implications for mechanisms underlying mosaic pattern formation. Vis Neurosci 22: 569-573. CrossRef Medline
36. Raven MA, Orton NC, Nassar H, Williams GA, Stell WK, Jacobs GH, Bech-Hansen NT, Reese BE (2008) Early afferent signaling in the outer plexiform layer regulates development of horizontal cell morphology. J Comp Neurol 506:745-758. CrossRef Medline
37. Reese BE, Raven MA, Stagg SB (2005) Afferents and homotypic neighbors regulate horizontal cell morphology, connectivity, and retinal coverage. J Neurosci 25:2167-2175. CrossRef Medline
38. Sanes JR, Yamagata M (2009) Many paths to synaptic specificity. Annu Rev Cell Dev Biol 25:161-195. CrossRef Medline
39. Schubert T, Huckfeldt RM, Parker E, Campbell JE, Wong RO (2010) Assembly of the outer retina in the absence of GABA synthesis in horizontal cells. Neural Dev 5:15. CrossRef Medline
40. Sherry DM, Wang MM, Bates J, Frishman LJ (2003) Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol 465:480-498. CrossRef Medline
41. Sonntag S, Dedek K, Dorgau B, Schultz K, Schmidt KF, Cimiotti K, Weiler R, Löwel S, Willecke K, Janssen-Bienhold U (2012) Ablation of retinal horizontal cells from adult mice leads to rod degeneration and remodeling in the outer retina. J Neurosci 32:10713-10724. CrossRef Medline
42. Sotelo C, Dusart I (2009) Intrinsic versus extrinsic determinants during the development of Purkinje cell dendrites. Neuroscience 162:589-600. CrossRef Medline
43. Soto F, Watkins KL, Johnson RE, Schottler F, Kerschensteiner D (2013) NGL-2 regulates pathway-specific neurite growth and lamination, syn-apse formation, and signal transmission in the retina. J Neurosci 33: 11949-11959. CrossRef Medline
44. Specht D, Tom Dieck S, Ammermüller J, Regus-Leidig H, Gundelfinger ED, Brandstätter JH (2007) Structural and functional remodeling in the retina of a mouse with a photoreceptor synaptopathy: plasticity in the rod and degeneration in the cone system. Eur J Neurosci 26:2506-2515. CrossRef Medline
45. Swindell EC, Bailey TJ, Loosli F, Liu C, Amaya-Manzanares F, Mahon KA,Wittbrodt J, Jamrich M (2006) Rx-Cre, a tool for inactivation of gene expression in the developing retina. Genesis 44:361-363. CrossRef Medline
46. Trevarrow B, Marks DL, Kimmel CB (1990) Organization of hindbrain segments in the zebrafish embryo. Neuron 4:669-679. CrossRef Medline
47. Wieloch T, Nikolich K (2006) Mechanisms of neural plasticity following brain injury. Curr Opin Neurobiol 16:258-264. CrossRef Medline
48. Wong RO, Ghosh A (2002) Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 3:803-812. CrossRef Medline
49. Wu F, Li R, Umino Y, Kaczynski TJ, Sapkota D, Li S, Xiang M, Fliesler SJ, Sherry DM, Gannon M, Solessio E, Mu X (2013) Onecut1 is essential for horizontal cell genesis and retinal integrity. J Neurosci 33:13053-13065, 13065a. CrossRef Medline
50. Yamagata M, Sanes JR (2008) Dscam and Sidekick proteins direct laminaspecific synaptic connections in vertebrate retina. Nature 451:465-469. CrossRef Medline
51. Yamagata M, Sanes JR (2012) Expanding the Ig superfamily code for laminar specificity in retina: expression and role of contactins. J Neurosci 32:14402-14414. CrossRef Medline
52. Young RW (1985) Cell differentiation in the mouse retina. Anat Rec 212: 199-205. Medline