Immunohistochemical identification and synaptic inputs to the diffuse bipolar cell type DB1 in macaque retina

Journal of Comparative Neurology

Volumn 519, Issue 18, 2011, Pages 3640-3656

  Puthussery, Theresa ^a   Gayet Primo, Jacqueline ^a   Taylor, W Rowland ^a   Haverkamp, Silke ^b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

Amacrine cell; Blue cone input; Cone photoreceptors; Glutamate receptors; Glycine receptor; OFF cone bipolar cells; Secretagogin

Indexed keywords

4 AMINOBUTYRIC ACID; CALCIUM BINDING PROTEIN; DOPAMINE; GLUTAMATE RECEPTOR; GLYCINE RECEPTOR; GLYCINE RECEPTOR ALPHA 1 SUBUNIT; SECRETAGOGIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CONTACT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; MACACA; NONHUMAN; PRIORITY JOURNAL; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA CONE; RETINA INNER PLEXIFORM LAYER; RETINA ROD; SYNAPSE; SYNAPTIC TRANSMISSION;

AMACRINE CELLS; ANIMALS; BIOLOGICAL MARKERS; CALCIUM-BINDING PROTEINS; IMMUNOHISTOCHEMISTRY; MACACA FASCICULARIS; MICROSCOPY, IMMUNOELECTRON; NEURAL PATHWAYS; PHOTORECEPTOR CELLS, VERTEBRATE; PRESYNAPTIC TERMINALS; RECEPTORS, GLUTAMATE; RETINA; RETINAL BIPOLAR CELLS; SYNAPSES;

EID: 80054708518     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22756     Document Type: Article

References (70)

1. Adamus G, Amundson D. 1996. Epitope recognition of recoverin in cancer associated retinopathy: evidence for calcium-dependent conformational epitopes. J Neurosci Res 45: 863-872.
2. Bloomfield SA, Dacheux RF. 2001. Rod vision: pathways and processing in the mammalian retina. Prog Retin Eye Res 20: 351-384.
3. Bordt AS, Hoshi H, Yamada ES, Perryman-Stout WC, Marshak DW. 2006. Synaptic input to OFF parasol ganglion cells in macaque retina. J Comp Neurol 498: 46-57.
4. Boycott BB, Hopkins JM. 1993. Cone synapses of a flat diffuse cone bipolar cell in the primate retina. J Neurocytol 22: 765-778.
5. Boycott BB, Wässle H. 1991. Morphological classification of bipolar cells of the primate retina. Eur J Neurosci 3: 1069-1088.
6. Brandstätter JH, Koulen P, Wässle H. 1997. Selective synaptic distribution of kainate receptor subunits in the two plexiform layers of the rat retina. J Neurosci 17: 9298-9307.
7. Breuninger T, Puller C, Haverkamp S, Euler T. 2011. Chromatic bipolar cell pathways in the mouse retina. J Neurosci 31: 6504-6517.
8. Calkins DJ, Tsukamoto Y, Sterling P. 1998 Microcircuitry and mosaic of a blue-yellow ganglion cell in the primate retina. J Neurosci 18: 3373-3385.
9. Dacey DM, Packer OS. 2003. Colour coding in the primate retina: diverse cell types and cone-specific circuitry. Curr Opin Neurobiol 13: 421-427.
10. Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, Pokorny J, Yau KW, Gamlin, PD. 2005. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433: 749-754.
11. DeVries SH. 2000. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28: 847-856.
12. Dhingra A, Sulaiman P, Xu Y, Fina ME, Veh RW, Vardi N. 2008. Probing neurochemical structure and function of retinal ON bipolar cells with a transgenic mouse. J Comp Neurol 510: 484-496.
13. Dowling JE, Boycott BB. 1966. Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci 166: 80-111.
14. Drenckhahn D, Holbach M, Ness W, Schmitz F, Anderson LV. 1996. Dystrophin and the dystrophin-associated glycoprotein, beta-dystroglycan, co-localize in photoreceptor synaptic complexes of the human retina. Neuroscience 73: 605-612.
15. Dumitrescu ON, Pucci FG, Wong KY, Berson DM. 2009. Ectopic retinal ON bipolar cell synapses in the OFF inner plexiform layer: contacts with dopaminergic amacrine cells and melanopsin ganglion cells. J Comp Neurol 517: 226-244.
16. Fyk-Kolodziej B, Qin P, Pourcho RG. 2003. Identification of a cone bipolar cell in cat retina which has input from both rod and cone photoreceptors. J Comp Neurol 464: 104-113.
17. Ghosh KK, Grünert U. 1999. Synaptic input to small bistratified (blue-ON) ganglion cells in the retina of a new world monkey, the marmoset Callithrix jacchus. J Comp Neurol 413: 417-428.
18. Ghosh KK, Bujan S, Haverkamp S, Feigenspan A, Wässle H. 2004. Types of bipolar cells in the mouse retina. J Comp Neurol 469: 70-82.
19. Gong J, Jellali A, Mutterer J, Sahel JA, Rendon A, Picaud S. 2006. Distribution of vesicular glutamate transporters in rat and human retina. Brain Res 1082: 73-85.
20. Grant GB, Dowling JE. 1995. A glutamate-activated chloride current in cone-driven ON bipolar cells of the white perch retina. J Neurosci 15: 3852-3862.
21. Grünert U, Wässle H. 1990. GABA-like immunoreactivity in the macaque monkey retina: a light and electron microscopic study. J Comp Neurol 297: 509-524.
22. Grünert U, Wässle H. 1996. Glycine receptors in the rod pathway of the macaque monkey retina. Vis Neurosci 13: 101-115.
23. Grünert U, Martin PR, Wässle H. 1994. Immunocytochemical analysis of bipolar cells in the macaque monkey retina. J Comp Neurol 348: 607-627.
24. Grünert U, Jusuf PR, Lee SC, Nguyen DT. 2011. Bipolar input to melanopsin containing ganglion cells in primate retina. Vis Neurosci 28: 39-50.
25. Hack I, Peichl L, Brandstätter JH. 1999. An alternative pathway for rod signals in the rodent retina: rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. Proc Natl Acad Sci U S A 96: 14130-14135.
26. Haverkamp S, Grünert U, Wässle H. 2000. The cone pedicle, a complex synapse in the retina. Neuron 27: 85-95.
27. Haverkamp S, Grünert U, Wässle H. 2001a. The synaptic architecture of AMPA receptors at the cone pedicle of the primate retina. J Neurosci 21: 2488-2500.
28. Haverkamp S, Grünert U, Wässle H. 2001b. Localization of kainate receptors at the cone pedicles of the primate retina. J Comp Neurol 436: 471-486.
29. Haverkamp S, Specht D, Majumdar S, Zaidi NF, Brandstätter JH, Wasco W, Wässle H, Tom Dieck S. 2008. Type 4 OFF cone bipolar cells of the mouse retina express calsenilin and contact cones as well as rods. J Comp Neurol 507: 1087-1101.
30. Hokoc JN, Mariani AP. 1987. Tyrosine hydroxylase immunoreactivity in the rhesus monkey retina reveals synapses from bipolar cells to dopaminergic amacrine cells. J Neurosci 7: 2785-2793.
31. Hoshi H, Liu WL, Massey SC, Mills SL. 2009. ON inputs to the OFF layer: bipolar cells that break the stratification rules of the retina. J Neurosci 29: 8875-8883.
32. Huang L, Shanker YG, Dubauskaite J, Zheng JZ, Yan W, Rosenzweig S, Spielman AI, Max M, Margolskee RF. 1999. Ggamma13 colocalizes with gustducin in taste receptor cells and mediates IP3 responses to bitter denatonium. Nat Neurosci 2: 1055-1062.
33. 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.
34. Jacoby RA, Marshak DW. 2000. Synaptic connections of DB3 diffuse bipolar cell axons in macaque retina. J Comp Neurol 416: 19-29.
35. Jacoby RA, Wiechmann AF, Amara SG, Leighton BH, Marshak DW. 2000. Diffuse bipolar cells provide input to OFF parasol ganglion cells in the macaque retina. J Comp Neurol 416: 6-18.
36. Johnson J, Tian N, Caywood MS, Reimer RJ, Edwards RH, Copenhagen DR. 2003. Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. J Neurosci 23: 518-529.
37. Jusuf PR, Haverkamp S, Grünert U. 2005. Localization of glycine receptor alpha subunits on bipolar and amacrine cells in primate retina. J Comp Neurol 488: 113-128.
38. Kalloniatis M, Marc RE, Murry RF. 1996. Amino acid signatures in the primate retina. J Neurosci 16: 6807-6829.
39. Kolb H. 1970. Organization of the outer plexiform layer of the primate retina: electron microscopy of Golgi-impregnated cells. Philos Trans R Soc Lond B 258: 261-283.
40. Kolb H, Zhang L, Dekorver L, Cuenca N. 2002. A new look at calretinin-immunoreactive amacrine cell types in the monkey retina. J Comp Neurol 453: 168-184.
41. Lee SC, Grünert U. 2007. Connections of diffuse bipolar cells in primate retina are biased against S-cones. J Comp Neurol 502: 126-140.
42. Li W, DeVries SH. 2006. Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Nat Neurosci 9: 669-675.
43. Li W, Keung JW, Massey SC. 2004. Direct synaptic connections between rods and OFF cone bipolar cells in the rabbit retina. J Comp Neurol 474: 1-12.
44. Li W, Chen S, DeVries SH. 2010. A fast rod photoreceptor signaling pathway in the mammalian retina. Nat Neurosci 13: 414-416.
45. Mariani AP, Hokoc JN. 1988. Two types of tyrosine hydroxylase-immunoreactive amacrine cell in the rhesus monkey retina. J Comp Neurol 276: 81-91.
46. Martin PR, Grünert U. 1999. Analysis of the short wavelength-sensitive ("blue") cone mosaic in the primate retina: comparison of New World and Old World monkeys. J Comp Neurol 406: 1-14.
47. Mataruga A, Kremmer E, Muller F. 2007. Type 3a and type 3b OFF cone bipolar cells provide for the alternative rod pathway in the mouse retina. J Comp Neurol 502: 1123-1137.
48. Milam AH, Dacey DM, Dizhoor AM. 1993. Recoverin immunoreactivity in mammalian cone bipolar cells. Vis Neurosci 10: 1-12.
49. Molnar A, Hsueh HA, Roska B, Werblin FS. 2009. Crossover inhibition in the retina: circuitry that compensates for nonlinear rectifying synaptic transmission. J Comput Neurosci 27: 569-590.
50. Nasu-Nishimura Y, Hurtado D, Braud S, Tang TT, Isaac JT, Roche KW. 2006. Identification of an endoplasmic reticulum-retention motif in an intracellular loop of the kainate receptor subunit KA2. J Neurosci 26: 7014-7021.
51. Park SA, Yin H, Bhattarai JP, Park SJ, Lee JC, Kim CJ, Han SK. 2010. Postnatal change of GluR5 kainate receptor expression in the substantia gelatinosa neuron of the trigeminal subnucleus caudalis in mice. Brain Res 1346: 52-61.
52. Pfeiffer F, Simler R, Grenningloh G, Betz H. 1984. Monoclonal antibodies and peptide mapping reveal structural similarities between the subunits of the glycine receptor of rat spinal cord. Proc Natl Acad Sci U S A 81: 7224-7227.
53. Pow DV, Hendrickson AE. 1999. Distribution of the glycine transporter glyt-1 in mammalian and nonmammalian retinae. Vis Neurosci 16: 231-239.
54. Puller C, Haverkamp S. 2011. Cell-type-specific localization of protocadherin beta16 at AMPA and AMPA/Kainate receptor-containing synapses in the primate retina. J Comp Neurol 519: 467-479.
55. Puller C, Haverkamp S, Grünert U. 2007. OFF midget bipolar cells in the retina of the marmoset, Callithrix jacchus, express AMPA receptors. J Comp Neurol 502: 442-454.
56. Puller C, Ondreka K, Haverkamp S. 2011. Bipolar cells of the ground squirrel retina. J Comp Neurol 519: 759-774.
57. Puthussery T, Gayet-Primo J, Taylor WR. 2010. Localization of the calcium-binding protein secretagogin in cone bipolar cells of the mammalian retina. J Comp Neurol 518: 513-525.
58. Ren Z, Riley NJ, Garcia EP, Sanders JM, Swanson GT, Marshall J. 2003. Multiple trafficking signals regulate kainate receptor KA2 subunit surface expression. J Neurosci 23: 6608-6616.
59. Rogstam A, Linse S, Lindqvist A, James P, Wagner L, Berggard T. 2007. Binding of calcium ions and SNAP-25 to the hexa EF-hand protein secretagogin. Biochem J 401: 353-363.
60. Schroder S, Hoch W, Becker CM, Grenningloh G, Betz H. 1991. Mapping of antigenic epitopes on the alpha 1 subunit of the inhibitory glycine receptor. Biochemistry 30: 42-47.
61. Tsukamoto Y, Morigiwa K, Ueda M, Sterling P. 2001. Microcircuits for night vision in mouse retina. J Neurosci 21: 8616-8623.
62. Vardi N. 1998. Alpha subunit of Go localizes in the dendritic tips of ON bipolar cells. J Comp Neurol 395: 43-52.
63. Wagner L, Oliyarnyk O, Gartner W, Nowotny P, Groeger M, Kaserer K, Waldhausl W, Pasternack MS. 2000. Cloning and expression of secretagogin, a novel neuroendocrine- and pancreatic islet of Langerhans-specific Ca2+-binding protein. J Biol Chem 275: 24740-24751.
64. Wang Y, Macke JP, Merbs SL, Zack DJ, Klaunberg B, Bennett J, Gearhart J, Nathans J. 1992. A locus control region adjacent to the human red and green visual pigment genes. Neuron 9: 429-440.
65. Wässle H, Chun MH. 1988. Dopaminergic and indoleamine-accumulating amacrine cells express GABA-like immunoreactivity in the cat retina. J Neurosci 8: 3383-3394.
66. Wässle H, Riemann HJ. 1978. The mosaic of nerve cells in the mammalian retina. Proc R Soc Lond B Biol Sci 200: 441-461.
67. Wässle H, Grünert U, Martin PR, Boycott BB. 1994. Immunocytochemical characterization and spatial distribution of midget bipolar cells in the macaque monkey retina. Vision Res 34: 561-579.
68. Wässle H, Grünert U, Chun MH, Boycott BB. 1995. The rod pathway of the macaque monkey retina: identification of AII-amacrine cells with antibodies against calretinin. J Comp Neurol 361: 537-551.
69. Winsky L, Isaacs KR, Jacobowitz DM. 1996. Calretinin mRNA and immunoreactivity in the medullary reticular formation of the rat: colocalization with glutamate receptors. Brain Res 741: 123-133.
70. Zhang DQ, Zhou TR, McMahon DG. 2007. Functional heterogeneity of retinal dopaminergic neurons underlying their multiple roles in vision. J Neurosci 27: 692-699.