Identification of nonvisual photomotor response cells in the vertebrate hindbrain

Journal of Neuroscience

Volumn 33, Issue 9, 2013, Pages 3834-3843

  Kokel, David ^a,b   Dunn, Timothy W ^c   Ahrens, Misha B ^c   Alshut, Rüdiger ^e   Cheung, Chung Yan J ^a,b   Saint Amant, Louis ^f   Bruni, Giancarlo ^a,b   Mateus, Rita ^a,b   van Ham, Tjakko J ^a,b   Shiraki, Tomoya ^d   Fukada, Yoshitaka ^d   Kojima, Daisuke ^d   Yeh, Jing Ruey J ^a   Mikut, Ralf ^e   von Lintig, Johannes ^g   Engert, Florian ^c   Peterson, Randall T ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c HARVARD UNIVERSITY   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

^e KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^f UNIVERSITÉ DE MONTRÉAL   (Canada)

^g CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; OPSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CALCIUM SIGNALING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; GENE SILENCING; LATENT PERIOD; MOTOR PERFORMANCE; MOVEMENT (PHYSIOLOGY); NERVE CELL NETWORK; NONHUMAN; PHOTORECEPTOR CELL; PHOTOTRANSDUCTION; PRIORITY JOURNAL; SENSORIMOTOR INTEGRATION; STEREOTYPY; VISUAL ADAPTATION; VISUAL STIMULATION; ZEBRA FISH;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; BIOMECHANICS; BIOPHYSICS; CALCIUM; EMBRYO, NONMAMMALIAN; FEMALE; MALE; MICROSCOPY, CONFOCAL; MORPHOLINOS; MOVEMENT; MUSCLE CELLS; NEURAL PATHWAYS; OPSINS; PHOTIC STIMULATION; PHOTORECEPTOR CELLS, VERTEBRATE; RHOMBENCEPHALON; STEREOTYPED BEHAVIOR; TIME FACTORS; ZEBRAFISH;

EID: 84874616928     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3689-12.2013     Document Type: Article

References (62)

1. Ahrens MB, Li JM, Orger MB, Robson DN, Schier AF, Engert F, Portugues R (2012) Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485:471-477. CrossRef Medline
2. Asaoka Y, Mano H, Kojima D, Fukada Y (2002) Pineal expressionpromoting element (PIPE), a cis-acting element, directs pineal-specific gene expression in zebrafish. Proc Natl Acad Sci U S A 99:15456-15461. CrossRef Medline
3. Becker HE, Cone RA (1966) Light-stimulated electrical responses from skin. Science 154:1051-1053. CrossRef Medline
4. Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073. CrossRef Medline
5. Best JD, Berghmans S, Hunt JJ, Clarke SC, Fleming A, Goldsmith P, Roach AG (2008) Non-associative learning in larval zebrafish. Neuropsychopharmacology 33:1206-1215. CrossRef Medline
6. Blackshaw S, Snyder SH (1997) Parapinopsin, a novel catfish opsin localized to the parapineal organ, defines a new gene family. J Neurosci 17:8083-8092. Medline
7. Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SC, Driever W, Dowling JE (1995) A behavioral screen for isolating zebrafish mutants with visual system defects. Proc Natl Acad Sci U S A 92:10545-10549. CrossRef Medline
8. Brustein E, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Drapeau P (2003) Steps during the development of the zebrafish locomotor network. J Physiol Paris 97:77-86. CrossRef Medline
9. Burgess HA, Granato M (2007a) Modulation of locomotor activity in larval zebrafish during light adaptation. J Exp Biol 210:2526-2539. CrossRef Medline
10. Burgess HA, Granato M (2007b) Sensorimotor gating in larval zebrafish. J Neurosci 27:4984-4994. CrossRef Medline
11. Burgess HA, Schoch H, Granato M (2010) Distinct retinal pathways drive spatial orientation behaviors in zebrafish navigation. Curr Biol 20:381-386. CrossRef Medline
12. Denk W, Strickler JH, Webb WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248:73-76. CrossRef Medline
13. Diez-Garcia J, Akemann W, Knöpfel T (2007) In vivo calcium imaging from genetically specified target cells in mouse cerebellum. Neuroimage 34: 859-869. CrossRef Medline
14. Downes GB, Granato M (2006) Supraspinal input is dispensable to generate glycine-mediated locomotive behaviors in the zebrafish embryo. J Neurobiol 66:437-451. CrossRef Medline
15. Drapeau P, Ali DW, Buss RR, Saint-Amant L (1999) In vivo recording from identifiable neurons of the locomotor network in the developing zebrafish. J Neurosci Methods 88:1-13. CrossRef Medline
16. Easter SS Jr, Nicola GN (1996) The development of vision in the zebrafish (Danio rerio). Dev Biol 180:646-663. CrossRef Medline
17. Easter SS Jr, Nicola GN (1997) The development of eye movements in the zebrafish (Danio rerio). Dev Psychobiol 31:267-276. CrossRef Medline
18. Edwards SL, Charlie NK, Milfort MC, Brown BS, Gravlin CN, Knecht JE, Miller KG (2008) A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biol 6:e198. CrossRef Medline
19. Emran F, Rihel J, Adolph AR, Wong KY, Kraves S, Dowling JE (2007) OFF ganglion cells cannot drive the optokinetic reflex in zebrafish. Proc Natl Acad Sci U S A 104:19126-19131. CrossRef Medline
20. Fernandes AM, Fero K, Arrenberg AB, Bergeron SA, Driever W, Burgess HA (2012) Deep brain photoreceptors control light-seeking behavior in zebrafish larvae. Curr Biol 22:2042-2047. CrossRef Medline
21. Golczak M, Kuksa V, Maeda T, Moise AR, Palczewski K (2005) Positively charged retinoids are potent and selective inhibitors of the trans-cis isomerization in the retinoid (visual) cycle. Proc Natl Acad Sci U S A 102:8162-8167. CrossRef Medline
22. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85-100. CrossRef Medline
23. Harth MS, Heaton MB (1973) Nonvisual photic responsiveness in newly hatched pigeons (Columba livia). Science 180:753-755. CrossRef Medline
24. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, Lem J, Biel M, Hofmann F, Foster RG, Yau KW (2003) Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424:76-81. CrossRef Medline
25. Heaton MB, Harth MS (1974) Non-visual light responsiveness in the pigeon: developmental and comparative considerations. J Exp Zool 188: 251-264. CrossRef Medline
26. Kojima D, Mano H, Fukada Y (2000) Vertebrate ancient-long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells. J Neurosci 20:2845-2851. Medline
27. Kojima D, Torii M, Fukada Y, Dowling JE (2008) Differential expression of duplicated VAL-opsin genes in the developing zebrafish. J Neurochem 104:1364-1371. CrossRef Medline
28. Kokel D, Bryan J, Laggner C, White R, Cheung CY, Mateus R, Healey D, Kim S, Werdich AA, Haggarty SJ, Macrae CA, Shoichet B, Peterson RT (2010) Rapid behavior-based identification of neuroactive small-molecules in the zebrafish. Nat Chem Biol 6:231-237. CrossRef Medline
29. Krøvel AV, Olsen LC (2002) Expression of a vas::EGFP transgene in primordial germ cells of the zebrafish. Mech Dev 116:141-150. CrossRef Medline
30. Liu J, Ward A, Gao J, Dong Y, Nishio N, Inada H, Kang L, Yu Y, Ma D, Xu T, Mori I, Xie Z, Xu XZ (2010) C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog. Nat Neurosci 13:715-722. CrossRef Medline
31. Lowery LA, Sive H (2005) Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie oko and snakehead/ atp1a1a. 1 gene products. Development 132:2057-2067. CrossRef Medline
32. Lucas RJ, Freedman MS, Muñoz M, Garcia-Fernández JM, Foster RG (1999) Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science 284:505-507. CrossRef Medline
33. Mano H, Kojima D, Fukada Y (1999) Exo-rhodopsin: a novel rhodopsin expressed in the zebrafish pineal gland. Brain Res Mol Brain Res 73:110-118. CrossRef Medline
34. Matos-Cruz V, Blasic J, Nickle B, Robinson PR, Hattar S, Halpern ME (2011) Unexpected diversity and photoperiod dependence of the zebrafish melanopsin system. PloS One 6:e25111. CrossRef Medline
35. Max M, McKinnon PJ, Seidenman KJ, Barrett RK, Applebury ML, Takahashi JS, Margolskee RF (1995) Pineal opsin: a nonvisual opsin expressed in chick pineal. Science 267:1502-1506. CrossRef Medline
36. Mikut OB, Braun S, Reischl M (2008) The open source Matlab toolbox Gait-CAD and its application to bioelectric signal processing. In: Proc, DGBMT-Workshop Biosignalverarbeitung, pp 109-111. Potsdam, Germany.
37. Morris AC, Fadool JM (2005) Studying rod photoreceptor development in zebrafish. Physiol Behav 86:306-313. CrossRef Medline
38. Nakane Y, Ikegami K, Ono H, Yamamoto N, Yoshida S, Hirunagi K, Ebihara S, Kubo Y, Yoshimura T (2010) A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. Proc Natl Acad Sci U S A 107:15264-15268. CrossRef Medline
39. Noseda R, Kainz V, Jakubowski M, Gooley JJ, Saper CB, Digre K, Burstein R (2010) A neural mechanism for exacerbation of headache by light. Nat Neurosci 13:239-245. CrossRef Medline
40. Okano T, Yoshizawa T, Fukada Y (1994) Pinopsin is a chicken pineal photoreceptive molecule. Nature 372:94-97. CrossRef Medline
41. Park HC, Kim CH, Bae YK, Yeo SY, Kim SH, Hong SK, Shin J, Yoo KW, Hibi M, Hirano T, Miki N, Chitnis AB, Huh TL (2000) Analysis of upstream elements in the HuC promoter leads to the establishment of transgenic zebrafish with fluorescent neurons. Dev Biol 227:279-293. CrossRef Medline
42. Peirson SN, Halford S, Foster RG (2009) The evolution of irradiance detection: melanopsin and the non-visual opsins. Philos Trans R Soc Lond Biol Sci 364:2849-2865. CrossRef Medline
43. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD (1998) Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci U S A 95:340-345. CrossRef Medline
44. Reppert SM, Weaver DR (2001) Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 63:647-676. CrossRef Medline
45. Ribera AB, Nüsslein-Volhard C (1998) Zebrafish touch-insensitive mutants reveal an essential role for the developmental regulation of sodium current. J Neurosci 18:9181-9191. Medline
46. Rick JM, Horschke I, Neuhauss SC (2000) Optokinetic behavior is reversed in achiasmatic mutant zebrafish larvae. Curr Biol 10:595-598. CrossRef Medline
47. Ridge KD, Abdulaev NG, Sousa M, Palczewski K (2003) Phototransduction: crystal clear. Trends Biochem Sci 28:479-487. CrossRef Medline
48. Saint-Amant L, Drapeau P (1998) Time course of the development of motor behaviors in the zebrafish embryo. J Neurobiol 37:622-632. CrossRef Medline
49. Saint-Amant L, Drapeau P (2000) Motoneuron activity patterns related to the earliest behavior of the zebrafish embryo. J Neurosci 20:3964-3972. Medline
50. Saint-Amant L, Drapeau P (2001) Synchronization of an embryonic network of identified spinal interneurons solely by electrical coupling. Neuron 31:1035-1046. CrossRef Medline
51. Schmitt EA, Dowling JE (1999) Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses. J Comp Neurol 404: 515-536. CrossRef Medline
52. Schonthaler HB, Lampert JM, Isken A, Rinner O, Mader A, Gesemann M, Oberhauser V, Golczak M, Biehlmaier O, Palczewski K, Neuhauss SC, von Lintig J (2007) Evidence for RPE65-independent vision in the conedominated zebrafish retina. Eur J Neurosci 26:1940-1949. CrossRef Medline
53. Sexton TJ, Golczak M, Palczewski K, Van Gelder RN (2012) Melanopsin is highly resistant to light and chemical bleaching in vivo. J Biol Chem 287:20888-20897. CrossRef Medline
54. Tu DC, Owens LA, Anderson L, Golczak M, Doyle SE, McCall M, Menaker M, Palczewski K, Van Gelder RN (2006) Inner retinal photoreception independent of the visual retinoid cycle. Proc Natl Acad Sci U S A 103:10426-10431. CrossRef Medline
55. Vigh B, Manzano MJ, Zádori A, Frank CL, Lukáts A, Röhlich P, Szel A, Dávid C (2002) Nonvisual photoreceptors of the deep brain, pineal organs and retina. Histol Histopathol 17:555-590. Medline
56. Wakamatsu Y, Kawamura S, Yoshizawa T (1980) Light-induced pigment aggregation in cultured fish melanophores: spectral sensitivity and inhibitory effects of theophylline and cyclic adenosine-3',5'-monophosphate. J Cell Sci 41:65-74. Medline
57. White RM, Sessa A, Burke C, Bowman T, LeBlanc J, Ceol C, Bourque C, Dovey M, Goessling W, Burns CE, Zon LI (2008) Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2:183-189. CrossRef Medline
58. Xiang Y, Yuan Q, Vogt N, Looger LL, Jan LY, Jan YN (2010) Lightavoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468:921-926. CrossRef Medline
59. Yoshikawa T, Okano T, Oishi T, Fukada Y (1998) A deep brain photoreceptive molecule in the toad hypothalamus. FEBS Lett 424:69-72. CrossRef Medline
60. Young JZ (1935) The photoreceptors of lampreys: I. Light-sensitive fibres in the lateral line nerves. J Exp Biol 12:229-238.
61. Zaidi FH, Hull JT, Peirson SN, Wulff K, Aeschbach D, Gooley JJ, Brainard GC, Gregory-Evans K, Rizzo JF 3rd, Czeisler CA, Foster RG, Moseley MJ, Lockley SW (2007) Short-wavelength light sensitivity of circadian, pupillary, and visual awareness in humans lacking an outer retina. Curr Biol 17:2122-2128. CrossRef Medline
62. Zimmerman K, Heatwole H (1990) Cutaneous photoreception: a new sensory mechanism for reptiles. Copeia 3:860-862.