Delayed-Rectifier K Channels Contribute to Contrast Adaptation in Mammalian Retinal Ganglion Cells

Neuron

Volumn 71, Issue 1, 2011, Pages 166-179

  Weick, Michael ^a   Demb, Jonathan B ^a,b,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DELAYED RECTIFIER POTASSIUM CHANNEL; SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; CHANNEL GATING; CONTRAST ADAPTATION; CONTROLLED STUDY; GUINEA PIG; HYPERPOLARIZATION; IN VITRO STUDY; MEMBRANE DEPOLARIZATION; NERVE CELL EXCITABILITY; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; RETINA GANGLION CELL; VISUAL ADAPTATION; VISUAL STIMULATION;

ACTION POTENTIALS; ADAPTATION, OCULAR; ANIMALS; CALCIUM CHANNEL BLOCKERS; DELAYED RECTIFIER POTASSIUM CHANNELS; ELECTRIC STIMULATION; GUINEA PIGS; MEMBRANE POTENTIALS; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; POTASSIUM CHANNEL BLOCKERS; RETINAL GANGLION CELLS; SODIUM CHANNEL BLOCKERS; TETRAETHYLAMMONIUM;

EID: 79960191251     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.04.033     Document Type: Article

References (59)

1. Baccus S.A., Meister M. Fast and slow contrast adaptation in retinal circuitry. Neuron 2002, 36:909-919.
2. Baranauskas G. Ionic channel function in action potential generation: current perspective. Mol. Neurobiol. 2007, 35:129-150.
3. Beaudoin D.L., Borghuis B.G., Demb J.B. Cellular basis for contrast gain control over the receptive field center of mammalian retinal ganglion cells. J. Neurosci. 2007, 27:2636-2645.
4. Beaudoin D.L., Manookin M.B., Demb J.B. Distinct expressions of contrast gain control in parallel synaptic pathways converging on a retinal ganglion cell. J. Physiol. 2008, 586:5487-5502.
5. Benardete E.A., Kaplan E., Knight B.W. Contrast gain control in the primate retina: P cells are not X-like, some M cells are. Vis. Neurosci. 1992, 8:483-486.
6. Berry M.J., Warland D.K., Meister M. The structure and precision of retinal spike trains. Proc. Natl. Acad. Sci. USA 1997, 94:5411-5416.
7. Cardin J.A., Palmer L.A., Contreras D. Cellular mechanisms underlying stimulus-dependent gain modulation in primary visual cortex neurons in vivo. Neuron 2008, 59:150-160.
8. Chance F.S., Abbott L.F., Reyes A.D. Gain modulation from background synaptic input. Neuron 2002, 35:773-782.
9. Chander D., Chichilnisky E.J. Adaptation to temporal contrast in primate and salamander retina. J. Neurosci. 2001, 21:9904-9916.
10. Chouabe C., Drici M.D., Romey G., Barhanin J., Lazdunski M. HERG and KvLQT1/IsK, the cardiac K+ channels involved in long QT syndromes, are targets for calcium channel blockers. Mol. Pharmacol. 1998, 54:695-703.
11. Colbert C.M., Magee J.C., Hoffman D.A., Johnston D. Slow recovery from inactivation of Na+ channels underlies the activity-dependent attenuation of dendritic action potentials in hippocampal CA1 pyramidal neurons. J. Neurosci. 1997, 17:6512-6521.
12. Demb J.B. Functional circuitry of visual adaptation in the retina. J. Physiol. 2008, 586:4377-4384.
13. Demb J.B., Zaghloul K., Haarsma L., Sterling P. Bipolar cells contribute to nonlinear spatial summation in the brisk-transient (Y) ganglion cell in mammalian retina. J. Neurosci. 2001, 21:7447-7454.
14. Eller P., Berjukov S., Wanner S., Huber I., Hering S., Knaus H.G., Toth G., Kimball S.D., Striessnig J. High affinity interaction of mibefradil with voltage-gated calcium and sodium channels. Br. J. Pharmacol. 2000, 130:669-677.
15. Escoubas P., Diochot S., Célérier M.L., Nakajima T., Lazdunski M. Novel tarantula toxins for subtypes of voltage-dependent potassium channels in the Kv2 and Kv4 subfamilies. Mol. Pharmacol. 2002, 62:48-57.
16. Fukami H., Bradley R.M. Biophysical and morphological properties of parasympathetic neurons controlling the parotid and von Ebner salivary glands in rats. J. Neurophysiol. 2005, 93:678-686.
17. Gasparini S., DiFrancesco D. Action of the hyperpolarization-activated current (Ih) blocker ZD 7288 in hippocampal CA1 neurons. Pflugers Arch. 1997, 435:99-106.
18. Gaudry K.S., Reinagel P. Benefits of contrast normalization demonstrated in neurons and model cells. J. Neurosci. 2007, 27:8071-8079.
19. Gaudry K.S., Reinagel P. Contrast adaptation in a nonadapting LGN model. J. Neurophysiol. 2007, 98:1287-1296.
20. Gollisch T., Meister M. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 2010, 65:150-164.
21. Grissmer S., Nguyen A.N., Aiyar J., Hanson D.C., Mather R.J., Gutman G.A., Karmilowicz M.J., Auperin D.D., Chandy K.G. Pharmacological characterization of five cloned voltage-gated K+ channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol. Pharmacol. 1994, 45:1227-1234.
22. Guan D., Lee J.C., Higgs M.H., Spain W.J., Foehring R.C. Functional roles of Kv1 channels in neocortical pyramidal neurons. J. Neurophysiol. 2007, 97:1931-1940.
23. Harvey A.L. Twenty years of dendrotoxins. Toxicon 2001, 39:15-26.
24. Hochstein S., Shapley R.M. Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. J. Physiol. 1976, 262:265-284.
25. Höltje M., Brunk I., Grosse J., Beyer E., Veh R.W., Bergmann M., Grosse G., Ahnert-Hilger G. Differential distribution of voltage-gated potassium channels Kv 1.1-Kv1.6 in the rat retina during development. J. Neurosci. Res. 2007, 85:19-33.
26. Ishida A.T. Ion channel mutations in retinal neurons. Arch. Soc. Esp. Oftalmol. 2000, 75:69-70.
27. Kaneda M., Kaneko A. Voltage-gated sodium currents in isolated retinal ganglion cells of the cat: relation between the inactivation kinetics and the cell type. Neurosci. Res. 1991, 11:261-275.
28. Kim K.J., Rieke F. Temporal contrast adaptation in the input and output signals of salamander retinal ganglion cells. J. Neurosci. 2001, 21:287-299.
29. Kim K.J., Rieke F. Slow Na+ inactivation and variance adaptation in salamander retinal ganglion cells. J. Neurosci. 2003, 23:1506-1516.
30. Lee S.C., Ishida A.T. Ih without Kir in adult rat retinal ganglion cells. J. Neurophysiol. 2007, 97:3790-3799.
31. Lesica N.A., Jin J., Weng C., Yeh C.I., Butts D.A., Stanley G.B., Alonso J.M. Adaptation to stimulus contrast and correlations during natural visual stimulation. Neuron 2007, 55:479-491.
32. Liang Z., Freed M.A. The ON pathway rectifies the OFF pathway of the mammalian retina. J. Neurosci. 2010, 30:5533-5543.
33. Mahon S., Delord B., Deniau J.M., Charpier S. Intrinsic properties of rat striatal output neurones and time-dependent facilitation of cortical inputs in vivo. J. Physiol. 2000, 527:345-354.
34. Manookin M.B., Demb J.B. Presynaptic mechanism for slow contrast adaptation in mammalian retinal ganglion cells. Neuron 2006, 50:453-464.
35. Manookin M.B., Beaudoin D.L., Ernst Z.R., Flagel L.J., Demb J.B. Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. J. Neurosci. 2008, 28:4136-4150.
36. Mante V., Bonin V., Carandini M. Functional mechanisms shaping lateral geniculate responses to artificial and natural stimuli. Neuron 2008, 58:625-638.
37. Mao B.-Q., MacLeish P.R., Victor J.D. The intrinsic dynamics of retinal bipolar cells isolated from tiger salamander. Vis. Neurosci. 1998, 15:425-438.
38. Mao B.-Q., MacLeish P.R., Victor J.D. Relation between potassium-channel kinetics and the intrinsic dynamics in isolated retinal bipolar cells. J. Comput. Neurosci. 2002, 12:147-163.
39. Margolis D.J., Detwiler P.B. Different mechanisms generate maintained activity in ON and OFF retinal ganglion cells. J. Neurosci. 2007, 27:5994-6005.
40. Mayer M.L., Sugiyama K. A modulatory action of divalent cations on transient outward current in cultured rat sensory neurones. J. Physiol. 1988, 396:417-433.
41. Münch T.A., da Silveira R.A., Siegert S., Viney T.J., Awatramani G.B., Roska B. Approach sensitivity in the retina processed by a multifunctional neural circuit. Nat. Neurosci. 2009, 12:1308-1316.
42. Murphy G.J., Rieke F. Network variability limits stimulus-evoked spike timing precision in retinal ganglion cells. Neuron 2006, 52:511-524.
43. Nisenbaum E.S., Xu Z.C., Wilson C.J. Contribution of a slowly inactivating potassium current to the transition to firing of neostriatal spiny projection neurons. J. Neurophysiol. 1994, 71:1174-1189.
44. Nistri A., Cherubini E. Inactivation characteristics of a sustained, Ca(2+)-independent K+ current of rat hippocampal neurones in vitro. J. Physiol. 1992, 457:575-590.
45. O'Brien B.J., Isayama T., Richardson R., Berson D.M. Intrinsic physiological properties of cat retinal ganglion cells. J. Physiol. 2002, 538:787-802.
46. Perchenet L., Clément-Chomienne O. Characterization of mibefradil block of the human heart delayed rectifier hKv1.5. J. Pharmacol. Exp. Ther. 2000, 295:771-778.
47. Pinto L.H., Klumpp D.J. Localization of potassium channels in the retina. Prog. Retin. Eye Res. 1998, 17:207-230.
48. Rauer H., Lanigan M.D., Pennington M.W., Aiyar J., Ghanshani S., Cahalan M.D., Norton R.S., Chandy K.G. Structure-guided transformation of charybdotoxin yields an analog that selectively targets Ca(2+)-activated over voltage-gated K(+) channels. J. Biol. Chem. 2000, 275:1201-1208.
49. Rieke F. Temporal contrast adaptation in salamander bipolar cells. J. Neurosci. 2001, 21:9445-9454.
50. Rieke F., Rudd M.E. The challenges natural images pose for visual adaptation. Neuron 2009, 64:605-616.
51. Scott V.E., Muniz Z.M., Sewing S., Lichtinghagen R., Parcej D.N., Pongs O., Dolly J.O. Antibodies specific for distinct Kv subunits unveil a heterooligomeric basis for subtypes of alpha-dendrotoxin-sensitive K+ channels in bovine brain. Biochemistry 1994, 33:1617-1623.
52. Shapley R.M., Victor J.D. The effect of contrast on the transfer properties of cat retinal ganglion cells. J. Physiol. 1978, 285:275-298.
53. Spain W.J., Schwindt P.C., Crill W.E. Post-inhibitory excitation and inhibition in layer V pyramidal neurones from cat sensorimotor cortex. J. Physiol. 1991, 434:609-626.
54. Storm J.F. Functional diversity of K+ currents in hippocampal pyramidal neurons. Semin. Neurosci. 1993, 5:79-92.
55. van Wyk M., Wässle H., Taylor W.R. Receptive field properties of ON- and OFF-ganglion cells in the mouse retina. Vis. Neurosci. 2009, 26:297-308.
56. Victor J.D. The dynamics of the cat retinal X cell centre. J. Physiol. 1987, 386:219-246.
57. Werblin F.S. Six different roles for crossover inhibition in the retina: correcting the nonlinearities of synaptic transmission. Vis. Neurosci. 2010, 27:1-8.
58. Yoo H.Y., Zheng H., Nam J.H., Nguyen Y.H., Kang T.M., Earm Y.E., Kim S.J. Facilitation of Ca2+-activated K+ channels (IKCa1) by mibefradil in B lymphocytes. Pflugers Arch. 2008, 456:549-560.
59. Zaghloul K.A., Boahen K., Demb J.B. Contrast adaptation in subthreshold and spiking responses of mammalian Y-type retinal ganglion cells. J. Neurosci. 2005, 25:860-868.