Light-induced changes in spike synchronization between coupled ON direction selective ganglion cells in the mammalian retina

Journal of Neuroscience

Volumn 26, Issue 16, 2006, Pages 4206-4215

  Ackert, Jessica M ^a   Wu, Synphen H ^a   Lee, Jacob C ^a   Abrams, Joseph ^a   Hu, Edward H ^a   Perlman, Ido ^b   Bloomfield, Stewart A ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Coupling; Ganglion cells; Gap junctions; Inhibition; Retina; Synchrony

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

ACCESSORY NERVE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL STRUCTURE; CELL SYNCHRONIZATION; CONTROLLED STUDY; GAP JUNCTION; LATENT PERIOD; LIGHT EXPOSURE; MAMMAL CELL; NERVE CELL; NONHUMAN; OPTOKINETIC STIMULATION; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RETINA AMACRINE CELL; SIGNAL TRANSDUCTION; SPIKE WAVE; VISUAL STIMULATION; VISUAL SYSTEM; ACTION POTENTIAL; ANIMAL; COMPARATIVE STUDY; CYTOLOGY; IN VITRO STUDY; METHODOLOGY; PHOTOSTIMULATION; PHYSIOLOGY; RABBIT; RETINA; RETINA GANGLION CELL; TIME;

ACTION POTENTIALS; ANIMALS; PHOTIC STIMULATION; RABBITS; RETINA; RETINAL GANGLION CELLS; TIME FACTORS; VISUAL PATHWAYS;

EID: 33646461416     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0496-06.2006     Document Type: Article

References (68)

1. Alonso JM, Usrey WM, Reid RC (1996) Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383:815-819.
2. Amthor FR, Takahashi ES, Oyster CW (1989) Morphologies of rabbit retinal ganglion cells with complex receptive fields. J Comp Neurol 280:97-121.
3. Arnett D, Spraker TE (1981) Cross-correlation analysis of the maintained discharge of rabbit retinal ganglion cells. J Physiol (Lond) 317:29-47.
4. Barlow HB, Hill RM, Levick WR (1964) Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. J Physiol (Lond) 173:377-407.
5. Beyer EC, Paul DL, Goodenough DA (1990) Connexin family of gap junction proteins. J Membr Biol 116:87-194.
6. Bloomfield SA (1992) Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. J Neurophysiol 68:711-725.
7. Bloomfield SA, Miller RF (1986) A functional organization of ON and OFF pathways in the rabbit retina. J Neurosci 6:1-13.
8. Bloomfield SA, Xin D (1997) A comparison of receptive-field and tracer-coupling size of amacrine and ganglion cells in the rabbit retina. Vis Neurosci 14:1153-1165.
9. Bloomfield SA, Xin D, Osborne T (1997) Light-induced modulation of coupling between AII amacrine cells in the rabbit retina. Vis Neurosci 14:565-576.
10. Brivanlou IH, Warland DK, Meister M (1998) Mechanisms of concerted firing among retinal ganglion cells. Neuron 20:527-539.
11. Buhl EH, Peichl L (1986) Morphology of rabbit retinal ganglion cells projecting to the medial terminal nucleus of the accessory optic system. J Comp Neurol 253:163-174.
12. Caldwell JH, Daw NW, Wyatt HJ (1978) Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. J Physiol (Lond) 276:277-298.
13. Castelo-Branco M, Neuenschwander S, Singer W (1998) Synchronization of visual responses between cortex, lateral geniculate nucleus, and retina in the anesthetized cat. J Neurosci 18:6395-6410.
14. Dacey DM (1989) Axon-bearing amacrine cells of the macaque monkey retina. J Comp Neurol 284:275-293.
15. Dartnell HJA (1968) The photosensitivities of visual pigments in the presence of hydroxylamine. Vis Res 8:339-358.
16. Davidson JS, Baumgarten IM (1988) Glycyrrhetinic acid derivatives: a novel class of inhibitors of gap-junctional intercellular communication. Structure-activity relationships. J Pharm Exp Ther 246:1104-1107.
17. DeMonasterio FM (1978) Spectral interactions in horizontal and ganglion cells of the isolated and arterially-perfused rabbit retina. Brain Res 150:239-258.
18. DeVries SH (1999) Correlated firing in rabbit retinal ganglion cells. J Neurophysiol 81:908-920.
19. DeVries SH, Schwartz EA (1989) Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. J Physiol (Lond) 414:351-375.
20. Dodt E, Elenius V (1960) Changes in threshold during dark adaptation measured with orange and blue lights in cats and rabbits. Experimentia 16:313-314.
21. Dong W, Sun W, Zhang Y, Chen X, He S (2004) Dendritic relationship between starburst amacrine cells and direction-selective ganglion cells in the rabbit retina. J Physiol (Lond) 556:11-17.
22. Euler T, Detwiler PB, Denk W (2002) Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418:845-851.
23. Famiglietti EV (1992a) Polyaxonal amacrine cells of rabbit retina: morphology and stratification of PA1 cells. J Comp Neurol 316:406-421.
24. Famiglietti EV (1992b) Polyaxonal amacrine cells of rabbit retina: size and distribution of PA2, PA3, and PA4 cells. Light and electron microscopic studies with a functional interpretation. J Comp Neurol 316:422-446.
25. Fried SI, Munch TA, Werblin FS (2002) Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420:411-414.
26. Fried SI, Munch TA, Werblin FS (2005) Directional selectivity is formed at multiple levels by laterally offset inhibition in the rabbit retina. Neuron 46:117-127.
27. Goodenough DA, Goliger JA, Paul DL (1996) Connexins, connexons, and intercellular communication. Annu Rev Biochem 65:475-502.
28. He S, Masland RH (1998) ON direction-selective ganglion cells in the rabbit retina: dendritic morphology and pattern of fasciculation. Vis Neurosci 15:369-375.
29. Hu EH, Bloomfield SA (2003) Gap junctional coupling underlies the short-latency synchrony of retinal alpha ganglion cells. J Neurosci 23:6768-6777.
30. Hu EH, Dacheux RF, Bloomfield SA (2000) A flattened retina-eyecup preparation suitable for electrophysiological studies of neurons visualized with trans-scleral infrared illumination. J Neurosci Methods 103:209-216.
31. Kittila CA, Massey SC (1997) Pharmacology of directionally selective ganglion cells in the rabbit retina. J Neurophysiol 77:675-689.
32. Kogo N, Rubio DM, Ariel M (1998) Direction tuning of individual retinal inputs to the turtle accessory optic system. J Neurosci 18:2673-2684.
33. Kumar NM, Gilula NB (1996) The gap junction communication channel. Cell 84:381-388.
34. Lang EJ (2002) GABAergic and glutamatergic modulation of spontaneous and motor-cortex-evoked complex spike activity. J Neurophysiol 87:1993-2008.
35. Lang EJ, Sugihara I, Llinás R (1996) GABAergic modulation of complex spike activity by the cerebellar nucleoolivary pathway in rat. J Neurophysiol 76:255-275.
36. Liebman PA, Entine G (1964) Sensitive low-light-level microspectrophotometer: detection of photosensitive pigments of retinal cones. J Opt Soc Am 54:1451-1459.
37. Mangel SC, Dowling JE (1985) Responsiveness and receptive field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science 229:1107-1109.
38. Mastronarde DN (1983) Interactions between ganglion cells in cat retina. J Neurophysiol 49:350-365.
39. Meister M, Berry MJ (1999) The neural code of the retina. Neuron 22:435-450.
40. Meister M, Lagnado L, Baylor DA (1995) Concerted signaling by retinal ganglion cells. Science 270:1207-1210.
41. Miller RF, Bloomfield SA (1983) Electroanatomy of a unique amacrine cell in the rabbit retina. Proc Natl Acad Sci USA 80:3069-3073.
42. Nelson R, Famiglietti EV, Kolb H (1978) Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in cat retina. J Neurophysiol 41:472-483.
43. Neuenschwander S, Castelo-Branco M, Singer W (1999) Synchronous oscillations in the cat retina. Vis Res 39:2485-2497.
44. Nuboer JFW (1971) Photometry in rabbits. Doc Ophthal 30:259-278.
45. Oyster CW (1968) The analysis of image motion by the rabbit retina. J Physiol (Lond) 199:613-635.
46. Oyster CW, Simpson JI, Takahashi ES, Soodak RE (1980) Retinal ganglion cells projecting to the rabbit accessory optic system. J Comp Neurol 190:49-61.
47. Petit-Jacques J, Völgyi B, Rudy B, Bloomfield SA (2005) Spontaneous oscillatory activity of starburst amacrine cells in the mouse retina. J Neurophysiol 94:1770-1780.
48. Prince JH, McConnell DG (1964) Retinal and optic nerve. In: The rabbit in eye research (Prince JH, ed), pp 385-448. Springfield, IL: Charles C. Thomas.
49. Pu ML, Amthor FR (1990) Dendritic morphologies of retinal ganglion cells projecting to the nucleus of the optic tract in the rabbit. J Comp Neurol 302:657-674.
50. Rodriguez E, George N, Lachaux JP, Martinerie J, Renault B, Varela FJ (1999) Perception's shadow: long-distance synchronization of human brain activity. Nature 397:430-433.
51. Rosenberg AF, Ariel M (1991) Electrophysiological evidence for a direct projection of direction-selective retinal ganglion cells to the turtle's accessory optic system. J Neurophysiol 65:1022-1033.
52. Sáez JC, Berthoud VM, Branes MC, Martinez AD, Beyer EC (2003) Plasma membrane channels formed by connexins: their regulation and functions. Physiol Rev 83:1359-1400.
53. Schnitzer MJ, Meister M (2003) Multineuronal firing patterns in the signal from eye to brain. Neuron 37:499-511.
54. Simpson JI (1984) The accessory optic system. Annu Rev Neurosci 7:13-41.
55. Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24:49-65.
56. Singer W, Engel AK, Kreiter AK, Munk MHJ, Neuenschwander S, Roefselma PR (1997) Neuronal assemblies: necessity, signature and detectability. Trends Cognit Sci 1:252-261.
57. Solessio E, Vigh J, Cuenca N, Rapp K, Lasater EM (2002) Membrane properties of an unusual intrinsically oscillating, wide-field teleost retinal amacrine cell. J Physiol (Lond) 544:831-847.
58. Soodak RE, Simpson JI (1988) The accessory optic system of rabbit. I. Basic visual response properties. J Neurophysiol 60:2037-2054.
59. Spira ME, Spray DC, Bennett MV (1980) Synaptic organization of expansion motoneurons of Navanax inermis. Brain Res 195:241-269.
60. Stahl JS (2004) Using eye movements to assess brain function in mice. Vis Res 44:3401-3410.
61. Umino O, Lee Y, Dowling JE (1991) Effects of light stimuli on the release of dopamine from interplexiform cells in the white perch retina. Vis Neurosci 7:451-458.
62. Usrey WM, Reid RD (1999) Synchronous activity in the visual system. Annu Rev Physiol 61:435-456.
63. Vaney DI (1991) Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neurosci Lett 125:187-190.
64. Vaney DI (1994) Patterns of neuronal coupling in the retina. Prog Retina Eye Res 13:301-355.
65. Völgyi B, Xin D, Amarillo Y, Bloomfield SA (2001) Morphology and physiology of the polyaxonal amacrine cells in the rabbit retina. J Comp Neurol 440:109-125.
66. Wässle H, Reimann HJ (1978) The mosaic of nerve cells in mammalian retina. Proc R Soc Lond B Biol Sci 200:441-461.
67. Xin D, Bloomfield SA (1997) Tracer coupling pattern of amacrine and ganglion cells in the rabbit retina. J Comp Neurol 383:512-528.
68. Xin D, Bloomfield SA (1999) Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. J Comp Neurol 405:75-87.