Cellular basis for contrast gain control over the receptive field center of mammalian retinal ganglion cells

Journal of Neuroscience

Volumn 27, Issue 10, 2007, Pages 2636-2645

  Beaudoin, Deborah L ^a   Borghuis, Bart G ^b   Demb, Jonathan B ^a,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Adaptation; Amacrine cell; Bipolar cell; Intracellular recording; Vision; Whole cell recording

Indexed keywords

CALCIUM; NEUROTRANSMITTER RECEPTOR;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL TYPE; CONTROLLED STUDY; GUINEA PIG; IN VITRO STUDY; MEMBRANE CURRENT; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; RETINA AMACRINE CELL; RETINA GANGLION CELL; RETINA RECEPTIVE FIELD; SPIKE WAVE; VISUAL STIMULATION; VOLTAGE CLAMP;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; AMACRINE CELLS; ANIMALS; CALCIUM; CONTRAST SENSITIVITY; ELECTROPHYSIOLOGY; GUINEA PIGS; MEMBRANE POTENTIALS; NEURAL INHIBITION; PHOTIC STIMULATION; PHOTORECEPTORS, VERTEBRATE; RETINAL BIPOLAR CELLS; RETINAL GANGLION CELLS; SYNAPSES; VISUAL FIELDS;

EID: 33847768951     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4610-06.2007     Document Type: Article

References (60)

1. Akopian A, Witkovsky P (2001) Intracellular calcium reduces light-induced excitatory post-synaptic responses in salamander retinal ganglion cells. J Physiol (Lond) 532:43-53.
2. Baccus SA, Meister M (2002) Fast and slow contrast adaptation in retinal circuitry. Neuron 36:909-919.
3. Baccus SA, Meister M (2004) Retina versus cortex; contrast adaptation in parallel visual pathways. Neuron 42:5-7.
4. Benardete EA, Kaplan E (1999) The dynamics of primate M retinal ganglion cells. Vis Neurosci 16:355-368.
5. Benardete EA, Kaplan E, Knight BW (1992) Contrast gain control in the primate retina: P cells are not X-like, some M cells are. Vis Neurosci 8:483-486.
6. Bonin V, Mante V, Carandini M (2005) The suppressive field of neurons in lateral geniculate nucleus. J Neurosci 25:10844-10856.
7. Bonin V, Mante V, Carandini M (2006) The statistical computation underlying contrast gain control. J Neurosci 26:6346-6353.
8. Bormann J, Hamill OP, Sakmann B (1987) Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. J Physiol (Lond) 385:243-286.
9. Brown SP, Masland RH (2001) Spatial scale and cellular substrate of contrast adaptation by retinal ganglion cells. Nat Neurosci 4:44-51.
10. Carandini M, Demb JB, Mante V, Tolhurst DJ, Dan Y, Olshausen BA, Gallant JL, Rust NC (2005) Do we know what the early visual system does? J Neurosci 25:10577-10597.
11. Chander D, Chichilnisky EJ (2001) Adaptation to temporal contrast in primate and salamander retina. J Neurosci 21:9904-9916.
12. Chichilnisky EJ (2001) A simple white noise analysis of neuronal light responses. Network 12:199-213.
13. Cohen E, Sterling P (1992) Parallel circuits from cones to the On-beta ganglion cell. Eur J Neurosci 4:506-520.
14. Cohen ED (2000) Light-evoked excitatory synaptic currents of X-type retinal ganglion cells. J Neurophysiol 83:3217-3229.
15. Cook PB, McReynolds JS (1998) Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells. Nat Neurosci 1:714-719.
16. Dacey D, Packer OS, Diller L, Brainard D, Peterson B, Lee B (2000) Center surround receptive field structure of cone bipolar cells in primate retina. Vision Res 40:1801-1811.
17. Dacey DM, Lee BB, Stafford DK, Pokorny J, Smith VC (1996) Horizontal cells of the primate retina: cone specificity without spectral opponency. Science 271:656-659.
18. Demb JB (2002) Multiple mechanisms for contrast adaptation in the retina. Neuron 36:781-783.
19. Demb JB, Haarsma L, Freed MA, Sterling P (1999) Functional circuitry of the retinal ganglion cell's nonlinear receptive field. J Neurosci 19:9756-9767.
20. Demb JB, Zaghloul K, Haarsma L, Sterling P (2001) Bipolar cells contribute to nonlinear spatial summation in the brisk-transient (Y) ganglion cell in mammalian retina. J Neurosci 21:7447-7454.
21. DeVries SH (2001) Exocytosed protons feedback to suppress the Ca2+ current in mammalian cone photoreceptors. Neuron 32:1107-1117.
22. Enroth-Cugell C, Jakiela HG (1980) Suppression of cat retinal ganglion cell responses by moving patterns. J Physiol (Lond) 302:49-72.
23. Fairhall AL, Lewen GD, Bialek W, de Ruyter Van Steveninck RR (2001) Efficiency and ambiguity in an adaptive neural code. Nature 412:787-792.
24. Flores-Herr N, Protti DA, Wassle H (2001) Synaptic currents generating the inhibitory surround of ganglion cells in the mammalian retina. J Neurosci 21:4852-4863.
25. Freed MA, Sterling P (1988) The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. J Neurosci 8:2303-2320.
26. Hochstein S, Shapley RM (1976) Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. J Physiol (Lond) 262:265-284.
27. Jacoby R, Stafford D, Kouyama N, Marshak D (1996) Synaptic inputs to ON parasol ganglion cells in the primate retina. J Neurosci 16:8041-8056.
28. 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.
29. Kim KJ, Rieke F (2001) Temporal contrast adaptation in the input and output signals of salamander retinal ganglion cells. J Neurosci 21:287-299.
30. + inactivation and variance adaptation in salamander retinal ganglion cells. J Neurosci 23:1506-1516.
31. Kolb H, Nelson R (1993) OFF-alpha and OFF-beta ganglion cells in cat retina: II. Neural circuitry as revealed by electron microscopy of HRP stains. J Comp Neurol 329:85-110.
32. Lankheet MJ, Prickaerts JH, van de Grind WA (1992) Responses of cat horizontal cells to sinusoidal gratings. Vision Res 32:997-1008.
33. Li W, DeVries SH (2006) Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Nat Neurosci 9:669-675.
34. MacNeil MA, Masland RH (1998) Extreme diversity among amacrine cells: implications for function. Neuron 20:971-982.
35. Manookin MB, Demb JB (2006) Presynaptic mechanism for slow contrast adaptation in mammalian retinal ganglion cells. Neuron 50:453-464.
36. Mante V, Frazor RA, Bonin V, Geisler WS, Carandini M (2005) Independence of luminance and contrast in natural scenes and in the early visual system. Nat Neurosci 8:1690-1697.
37. Mao BQ, MacLeish PR, Victor JD (1998) The intrinsic dynamics of retinal bipolar cells isolated from tiger salamander. Vis Neurosci 15:425-438.
38. Palmer MJ, Taschenberger H, Hull C, Tremere L, von Gersdorff H (2003a) Synaptic activation of presynaptic glutamate transporter currents in nerve terminals. J Neurosci 23:4831-4841.
39. Palmer MJ, Hull C, Vigh J, von Gersdorff H (2003b) Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells. J Neurosci 23:11332-11341.
40. Rieke F (2001) Temporal contrast adaptation in salamander bipolar cells. J Neurosci 21:9445-9454.
41. Robertson B (1989) Characteristics of GABA-activated chloride channels in mammalian dorsal root ganglion neurones. J Physiol (Lond) 411:285-300.
42. Roska B, Werblin F (2003) Rapid global shifts in natural scenes block spiking in specific ganglion cell types. Nat Neurosci 6:600-608.
43. Shapley RM, Victor JD (1978) The effect of contrast on the transfer properties of cat retinal ganglion cells. J Physiol (Lond) 285:275-298.
44. Shapley RM, Victor JD (1979) Nonlinear spatial summation and the contrast gain control of cat retinal ganglion cells. J Physiol (Lond) 290:141-161.
45. Shapley RM, Victor JD (1981) How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. J Physiol (Lond) 318:161-179.
46. Singer JH, Diamond JS (2006) Vesicle depletion and synaptic depression at a mammalian ribbon synapse. J Neurophysiol 95:3191-3198.
47. Solomon SG, Peirce JW, Dhruv NT, Lennie P (2004) Profound contrast adaptation early in the visual pathway. Neuron 42:155-162.
48. Stafford DK, Dacey DM (1997) Physiology of the A1 amacrine: a spiking, axon-bearing interneuron of the macaque monkey retina. Vis Neurosci 14:507-522.
49. Taylor WR (1999) TTX attenuates surround inhibition in rabbit retinal ganglion cells. Vis Neurosci 16:285-290.
50. Troy JB, Enroth-Cugell C (1993) X and Y ganglion cells inform the cat's brain about contrast in the retinal image. Exp Brain Res 93:383-390.
51. Vaney DI (1990) The mosaic of amacrine cells in the mammalian retina. In: Progress in retinol research, Vol 9 (Osborne NN, Chader G, eds), pp 49-100. Oxford: Pergamon.
52. Veruki ML, Morkve SH, Hartveit E (2006) Activation of a presynaptic glutamate transporter regulates synaptic transmission through electrical signaling. Nat Neurosci 9:1388-1396.
53. Victor JD (1987) The dynamics of the cat retinal X cell centre. J Physiol (Lond) 386:219-246.
54. Volgyi 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.
55. Walraven J, Enroth-Cugell C, Hood DC, Macleod DI, Schnapf JL (1990) The control of visual sensitivity: receptoral and postreceptoral processes. In: Visual perception: the neurophysiological foundations (Spillmann L, Werner JS, eds), pp 53-101. San Diego: Academic.
56. Wassle H (2004) Parallel processing in the mammalian retina. Nat Rev Neurosci 5:747-757.
57. Weber AJ, Stanford LR (1994) Synaptology of physiologically identified ganglion cells in the cat retina: a comparison of retinal X- and Y-cells. J Comp Neurol 343:483-499.
58. Yin L, Smith RG, Sterling P, Brainard DH (2006) Chromatic properties of horizontal and ganglion cell responses follow a dual gradient in cone opsin expression. J Neurosci 26:12351-12361.
59. Zaghloul KA, Boahen K, Demb JB (2003) Different circuits for ON and OFF retinal ganglion cells cause different contrast sensitivities. J Neurosci 23:2645-2654.
60. Zaghloul KA, Boahen K, Demb JB (2005) Contrast adaptation in subthreshold and spiking responses of mammalian Y-type retinal ganglion cells. J Neurosci 25:860-868.