The drosophila SK channel (dSK) contributes to photoreceptor performance by mediating sensitivity control at the first visual network

Journal of Neuroscience

Volumn 31, Issue 39, 2011, Pages 13897-13910

  Tayoun, Ahmad N Abou ^a   Li, Xiaofeng ^b,c   Chu, Brian ^d   Hardie, Roger C ^d   Juusola, Mikko ^b,c   Dolph, Patrick J ^a  

^a Lamont Doherty Earth Observatory   (United States)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c BEIJING NORMAL UNIVERSITY   (China)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

ADAPTIVE BEHAVIOR; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE; GENE FUNCTION; GENETIC CODE; INSECT GENOME; INTERNEURON; LIGHT DARK CYCLE; MALE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NERVE FIBER; NONHUMAN; OSCILLATORY POTENTIAL; PHOTORECEPTOR POTENTIAL; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN FUNCTION; SK GENE; SYNAPSE; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; MOLECULAR SEQUENCE DATA; NERVE NET; PHOTORECEPTOR CELLS; SMALL-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; VISUAL PATHWAYS;

EID: 80053242027     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3134-11.2011     Document Type: Article

References (68)

1. Barlow H (1961) Possible principles underlying the transformations of sensory messages. In: Sensory communication, Chap 13 (WA Rosenblith, ed), pp 217-234. Cambridge, MA: MIT.
2. Blatz AL, Magleby KL (1986) Single apamin-blocked Ca-activated K_ channels of small conductance in cultured rat skeletal muscle. Nature 323:718-720.
3. Chinchore Y, Mitra A, Dolph PJ (2009) Accumulation of rhodopsin in late endosomes triggers photoreceptor cell degeneration. PLoS Genet 5: e1000377.
4. + channel activation. J Neurosci 29:11237-11245.
5. de Polavieja GG (2002) Errors drive the evolution of biological signalling to costly codes. J Theor Biol 214:657-664.
6. de Polavieja GG (2004) Reliable biological communication with realistic constraints. Phys Rev E Stat Nonlin Soft Matter Phys 70:061910.
7. Faber ES, Delaney AJ, Sah P (2005) SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala. Nat Neurosci 8:635-641.
8. Fischbach KF, Dittrich AP (1989) The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441-475.
9. Gengs C, Leung HT, Skingsley DR, Iovchev MI, Yin Z, Semenov EP, Burg MG, Hardie RC, Pak WL (2002) The target of Drosophila photoreceptor synaptic transmission is a histamine-gated chloride channel encoded by ort (hclA). J Biol Chem 277:42113-42120.
10. Gho M, Mallart A (1986) Two distinct calcium-activated potassium currents in larval muscle fibres of Drosophila melanogaster. Pflugers Arch 407:526-533.
11. Gonzalez-Bellido PT, Wardill TJ, Juusola M (2011) Compound eyes and retinal information processing in miniature dipteran species match their specific ecological demands. Proc Natl Acad Sci U S A 108:4224-4229.
12. Gu Y, Oberwinkler J, Postma M, Hardie RC (2005) Mechanisms of light adaptation in Drosophila photoreceptors. Curr Biol 15:1228-1234.
13. Hallworth NE, Wilson CJ, Bevan MD (2003) Apamin-sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons in vitro. J Neurosci 23:7525-7542.
14. Hardie RC (1987) Is histamine a neurotransmitter in insect photoreceptors? J Comp Physiol A 161:201-213.
15. Hardie RC (1989) A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse. Nature 339:704-706.
16. 2+chelation on the light response in Drosophila photoreceptors. J Comp Physiol A 177:707-721.
17. Hardie RC, Raghu P (2001) Visual transduction in Drosophila. Nature 413:186-193.
18. Hardie RC, Voss D, Pongs O, Laughlin SB (1991) Novel potassium channels encoded by the Shaker locus in Drosophila photoreceptors. Neuron 6:477-486.
19. Hardie RC, Martin F, Cochrane GW, Juusola M, Georgiev P, Raghu P (2002) Molecular basis of amplification in Drosophila phototransduction: roles for G protein, phospholipase C, and diacylglycerol kinase. Neuron 36:689-701.
20. Ishii TM, Maylie J, Adelman JP (1997) Determinants of apamin and d-tubocurarine block in SK potassium channels. J Biol Chem 272: 23195-23200.
21. Joesch M, Schnell B, Raghu SV, Reiff DF, Borst A (2010) ON and OFF pathways in Drosophila motion vision. Nature 468:300-304.
22. Juusola M, de Polavieja GG (2003) The rate of information transfer of naturalistic stimulation by graded potentials. J Gen Physiol 122:191-206.
23. Juusola M, Hardie RC (2001) Light adaptation in Drosophila photoreceptors: I. Response dynamics and signaling efficiency at 25 degrees C. J Gen Physiol 117:3-25.
24. Juusola M, Kouvalainen E, Järvilehto M, Weckström M (1994) Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors. J Gen Physiol 104:593-621.
25. Juusola M, Uusitalo RO, Weckström M (1995) Transfer of graded potentials at the photoreceptor-interneuron synapse. J Gen Physiol 105:117-148.
26. Katsov AY, Clandinin TR (2008) Motion processing streams in Drosophila are behaviorally specialized. Neuron 59:322-335.
27. Klöcker N, Oliver D, Ruppersberg JP, Knaus HG, Fakler B (2001) Developmental expression of the small-conductance Ca(2+)-activated potassium channel SK2 in the rat retina. Mol Cell Neurosci 17:514-520.
28. Köhler M, Hirschberg B, Bond CT, Kinzie JM, Marrion NV, Maylie J, Adelman JP (1996) Small-conductance, calcium-activated potassium channels from mammalian brain. Science 273:1709-1714.
29. Kolodziejczyk A, Sun X, Meinertzhagen IA, Nässel DR (2008) Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system. PLoS One 3:e2110
30. Komatsu A, Singh S, Rathe P, Wu CF (1990) Mutational and gene dosage analysis of calcium-activated potassium channels in Drosophila: correlation of micro-and macroscopic currents. Neuron 4:313-321.
31. Kwon Y, Montell C (2006) Dependence on the Lazaro phosphatidic acid phosphatase for the maximum light response. Curr Biol 16:723-729.
32. Laughlin SB, de Ruyter van Steveninck RR, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36-41.
33. Mahr A, Aberle H (2006) The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr Patterns 6:299-309.
34. Meinertzhagen IA, O'Neil SD (1991) Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J Comp Neurol 305:232-263.
35. Meinertzhagen IA, Sorra KE (2001) Synaptic organization in the fly's optic lamina: few cells, many synapses and divergent microcircuits. Prog Brain Res 131:53-69.
36. 2+-mediated feedback loop in dendritic spines. Nat Neurosci 8:642-649.
37. Nikolaev A, Zheng L, Wardill TJ, O'Kane CJ, de Polavieja GG, Juusola M (2009) Network adaptation improves temporal representation of naturalistic stimuli in Drosophila eye: II mechanisms. PLoS One 4:e4306.
38. Niven JE, Vähäsöyrinki M, Kauranen M, Hardie RC, Juusola M, Weckström M (2003) The contribution of Shaker K+ channels to the information capacity of Drosophila photoreceptors. Nature 421:630-634.
39. 2+-activated K+ channels. J Biol Chem 282:3478-3486.
40. Parks AL, Cook KR, Belvin M, Dompe NA, Fawcett R, Huppert K, Tan LR, Winter CG, Bogart KP, Deal JE, Deal-Herr ME, Grant D, Marcinko M, Miyazaki WY, Robertson S, Shaw KJ, Tabios M, Vysotskaia V, Zhao L, Andrade RS, et al. (2004) Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet 36:288-292.
41. 2+-activated K+ channels. J Biol Chem 276:9762-9769.
42. Raghu SV, Borst A (2011) Candidate glutamatergic neurons in the visual system of Drosophila. PLoS One 5:e19472.
43. Reinke R, Krantz DE, Yen D, Zipursky SL (1988) Chaoptin, a cell surface glycoprotein required for Drosophila photoreceptor cell morphogenesis, contains a repeat motif found in yeast and human. Cell 52:291-301.
44. Rister J, Pauls D, Schnell B, Ting CY, Lee CH, Sinakevitch I, Morante J, Strausfeld NJ, Ito K, Heisenberg M (2007) Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster. Neuron 56:155-170.
45. Salkoff L, Wei AD, Baban B, Butler A, Fawcett G, Ferreira G, Santi CM (2005) Potassium channels in C. elegans. WormBook 30:1-15.
46. Sanes JR, Zipursky SL (2010) Design principles of insect and vertebrate visual systems. Neuron 66:15-36.
47. Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379-423.
48. Shatz CJ (1990) Impulse activity and the patterning of connections during CNS development. Neuron 5:745-756.
49. Shaw SR (1984) Early visual processing in insects. J Exp Biol 112:225-251.
50. Sinakevitch I, Strausfeld NJ (2004) Chemical neuroanatomy of the fly's movement detection pathway. J Comp Neurol 468:6-23.
51. Singh S, Wu CF (1989) Complete separation of four potassium currents in Drosophila. Neuron 2:1325-1329.
52. Stocker M (2004) Ca(2+)-activated K+ channels: molecular determinants and function of the SK family. Nat Rev Neurosci 5:758-770.
53. Strausfeld NJ, Campos-Ortega JA (1977) Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition. Science 195: 894-897.
54. Uusitalo RO, Juusola M, Weckström M (1995a) Graded responses and spiking properties of identified first-order visual interneurons of the fly compound eye. J Neurophysiol 73:1782-1792.
55. Uusitalo RO, Juusola M, Kouvalainen E, Weckström M (1995b) Tonic transmitter release in a graded potential synapse. J Neurophysiol 74:470-473.
56. Vähäsöyrinki M, Niven JE, Hardie RC, Weckström M, Juusola M (2006) Robustness of neural coding in Drosophila photoreceptors in the absence of slow delayed rectifier K+ channels. J Neurosci 26:2652-2660.
57. van Hateren JH (1992) A theory of maximizing sensory information. Biol Cybern 68:23-29.
58. van Hateren JH (1997) Processing of natural time series of intensities by the visual system of the blowfly. Vision Res 37:3407-3416.
59. Van Vactor D Jr, Krantz DE, Reinke R, Zipursky SL (1988) Analysis of mutants in chaoptin, a photoreceptor cell-specific glycoprotein in Drosophila, reveals its role in cellular morphogenesis. Cell 52:281-290.
60. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Dürrbeck H, Buchner S, Dabauvalle MC, Schmidt M, Qin G, Wichmann C, Kittel R, Sigrist SJ, Buchner E (2006) Bruchpilot, a protein with homology to ELKS/ CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49:833-844.
61. + conductances on spontaneous discharge patterns of developing retinal ganglion cells. J Neurosci 19: 2609-2618.
62. 2+ exchanger CalX. Neuron 45:367-378.
63. Weckström M, Laughlin SB (1995) Visual ecology and voltage-gated ion channels in insect photoreceptors. Trends Neurosci 18:17-21.
64. Wolfart J, Neuhoff H, Franz O, Roeper J (2001) Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J Neurosci 21:3443-3456.
65. Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T, Keen JE, Ishii T, Hirschberg B, Bond CT, Lutsenko S, Maylie J, Adelman JP (1998) Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395:503-507.
66. Zheng L, de Polavieja GG, Wolfram V, Asyali MH, Hardie RC, Juusola M (2006) Feedback network controls photoreceptor output at the layer of first visual synapses in Drosophila. J Gen Physiol 127:495-510.
67. Zheng L, Nikolaev A, Wardill TJ, O'Kane CJ, de Polavieja GG, Juusola M (2009) Network adaptation improves temporal representation of naturalistic stimuli in Drosophila eye: I dynamics. PLoS One 4:e4307.
68. Zhu Y, Nern A, Zipursky SL, Frye MA (2009) Peripheral visual circuits functionally segregate motion and phototaxis behaviors in the fly. Curr Biol 19:613-619.