Circadian clocks, rhythmic synaptic plasticity and the sleep-wake cycle in zebrafish

Frontiers in Neural Circuits

Volumn , Issue JAN, 2013, Pages

  Elbaz, Idan ^a   Foulkes, Nicholas S ^b   Gothilf, Yoav ^c   Appelbaum, Lior ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Circadian clock; Circadian rhythms; Hypocretin; Melatonin; Orexin; Sleep; Synaptic plasticity; Zebrafish

Indexed keywords

MELATONIN; OREXIN; PROTEIN C FOS;

ANIMAL BEHAVIOR; ARALKYLAMINE N ACETYLTRANSFERASE 2 GENE; BIOLOGICAL MODEL; CIRCADIAN RHYTHM; GENE; HOMEOSTASIS; HORMONE RELEASE; HORMONE SYNTHESIS; LOCOMOTION; MOLECULAR DYNAMICS; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROENDOCRINE SYSTEM; NONHUMAN; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SLEEP WAKING CYCLE; STRUCTURAL SYNAPTIC PLASTICITY; WAKEFULNESS; ZEBRA FISH;

EID: 84872845932     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2013.00009     Document Type: Review

References (81)

1. Adamantidis, A., and De Lecea, L. (2008). Sleep and metabolism: shared circuits, new connections. Trends Endocrinol Metab 19, 362-370.
2. Ahrens, M.B., Li, J.M., Orger, M.B., Robson, D.N., Schier, A.F., Engert, F., and Portugues, R. (2012). Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485, 471-477.
3. Appelbaum, L., Wang, G., Yokogawa, T., Skariah, G.M., Smith, S.J., Mourrain, P., and Mignot, E. (2010). Circadian and homeostatic regulation of structural synaptic plasticity in hypocretin neurons. Neuron 68, 87-98.
4. Appelbaum, L., Wang, G.X., Maro, G.S., Mori, R., Tovin, A., Marin, W., Yokogawa, T., Kawakami, K., Smith, S.J., Gothilf, Y., Mignot, E., and Mourrain, P. (2009). Sleep-wake regulation and hypocretin-melatonin interaction in zebrafish. Proc Natl Acad Sci U S A 106, 21942-21947.
5. Asakawa, K., and Kawakami, K. (2008). Targeted gene expression by the Gal4-UAS system in zebrafish. Dev Growth Differ 50, 391-399.
6. Bass, J., and Takahashi, J.S. (2010). Circadian integration of metabolism and energetics. Science 330, 1349-1354.
7. Cahill, G.M. (1996). Circadian regulation of melatonin production in cultured zebrafish pineal and retina. Brain Res 708, 177-181.
8. Cahill, G.M., Hurd, M.W., and Batchelor, M.M. (1998). Circadian rhythmicity in the locomotor activity of larval zebrafish. Neuroreport 9, 3445-3449.
9. Campbell, S.S., and Tobler, I. (1984). Animal sleep: a review of sleep duration across phylogeny. Neurosci Biobehav Rev 8, 269-300.
10. Carnevali, O., Gioacchini, G., Maradonna, F., Olivotto, I., and Migliarini, B. (2011). Melatonin induces follicle maturation in Danio rerio. PLoS One 6, e19978.
11. Carr, A.J., Tamai, T.K., Young, L.C., Ferrer, V., Dekens, M.P., and Whitmore, D. (2006). Light reaches the very heart of the zebrafish clock. Chronobiol Int 23, 91-100.
12. Cirelli, C. (2009). The genetic and molecular regulation of sleep: from fruit flies to humans. Nat Rev Neurosci 10, 549-560.
13. Cirelli, C., and Tononi, G. (2000). On the functional significance of c-fos induction during the sleep-waking cycle. Sleep 23, 453-469.
14. Cirelli, C., and Tononi, G. (2008). Is sleep essential? PLoS Biol 6, e216.
15. Damulewicz, M., and Pyza, E. (2011). The clock input to the first optic neuropil of Drosophila melanogaster expressing neuronal circadian plasticity. PLoS One 6, e21258.
16. Donlea, J.M., Ramanan, N., and Shaw, P.J. (2009). Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science 324, 105-108.
17. Dreosti, E., Odermatt, B., Dorostkar, M.M., and Lagnado, L. (2009). A geneticall364 y encoded reporter of synaptic activity in vivo. Nat Methods 6, 883-889.
18. Elbaz, I., Yelin-Bekerman, L., Nicenboim, J., Vatine, G., and Appelbaum, L. (2012). Genetic ablation of hypocretin neurons alters behavioral state transitions in zebrafish. J Neurosci 32, 12961-12972.
19. Emran, F., Rihel, J., Adolph, A.R., and Dowling, J.E. (2010). Zebrafish larvae lose vision at night. Proc Natl Acad Sci U S A 107, 6034-6039.
20. Faraco, J.H., Appelbaum, L., Marin, W., Gaus, S.E., Mourrain, P., and Mignot, E. (2006). Regulation of hypocretin (orexin) expression in embryonic zebrafish. J Biol Chem 281, 29753-29761.
21. Fernandes, A.M., Fero, K., Arrenberg, A.B., Bergeron, S.A., Driever, W., and Burgess, H.A. (2012). Deep brain photoreceptors control light-seeking behavior in zebrafish larvae. Curr Biol 22, 2042-2047.
22. Fernandez, M.P., Berni, J., and Ceriani, M.F. (2008). Circadian remodeling of neuronal circuits involved in rhythmic behavior. PLoS Biol 6, e69.
23. Frenkel, L., and Ceriani, M.F. (2011). Circadian plasticity: from structure to behavior. Int Rev Neurobiol 99, 107-138.
24. Gilestro, G.F., Tononi, G., and Cirelli, C. (2009). Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science 324, 109-112.
25. Goldshmid, R., Holzman, R., Weihs, D., and Genin, A. (2004). Aeration of corals by sleep-swimming fish. Limnology and oceanography, 1832-1839.
26. Gothilf, Y., Coon, S.L., Toyama, R., Chitnis, A., Namboodiri, M.A., and Klein, D.C. (1999). Zebrafish serotonin N-acetyltransferase-2: marker for development of pineal photoreceptors and circadian clock function. Endocrinology 140, 4895-4903.
27. Granados-Fuentes, D., and Herzog, E.D. (2012). The clock shop: Coupled circadian oscillators. Exp Neurol.
28. Hartse, K.M. (2011). The phylogeny of sleep. Handb Clin Neurol 98, 97-109.
29. Hendricks, J.C., Finn, S.M., Panckeri, K.A., Chavkin, J., Williams, J.A., Sehgal, A., and Pack, A.I. (2000). Rest in Drosophila is a sleep-like state. Neuron 25, 129-138.
30. Hurd, M.W., and Cahill, G.M. (2002). Entraining signals initiate behavioral circadian rhythmicity in larval zebrafish. J Biol Rhythms 17, 307-314.
31. Hurd, M.W., Debruyne, J., Straume, M., and Cahill, G.M. (1998). Circadian rhythms of locomotor activity in zebrafish. Physiol Behav 65, 465-472.
32. Karlsson, K.A., and Blumberg, M.S. (2005). Active medullary control of atonia in week400 old rats. Neuroscience 130, 275-283.
33. Karlsson, K.A., Gall, A.J., Mohns, E.J., Seelke, A.M., and Blumberg, M.S. (2005). The neural substrates of infant sleep in rats. PLoS Biol 3, e143.
34. Kaslin, J., Nystedt, J.M., Ostergard, M., Peitsaro, N., and Panula, P. (2004). The orexin/hypocretin system in zebrafish is connected to the aminergic and cholinergic systems. J Neurosci 24, 2678-2689.
35. Kazimi, N., and Cahill, G.M. (1999). Development of a circadian melatonin rhythm in embryonic zebrafish. Brain Res Dev Brain Res 117, 47-52.
36. Lin, L., Faraco, J., Li, R., Kadotani, H., Rogers, W., Lin, X., Qiu, X., de Jong, P. J., Nishino, S., and Mignot, E. (1999) The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98, 365-376.
37. Mehnert, K.I., Beramendi, A., Elghazali, F., Negro, P., Kyriacou, C.P., and Cantera, R. (2007). Circadian changes in Drosophila motor terminals. Dev Neurobiol 67, 415-421.
38. Meyer, M.P., and Smith, S.J. (2006). Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J Neurosci 26, 3604-3614.
39. Mignot, E. (2008). Why we sleep: the temporal organization of recovery. PLoS Biol 6, e106.
40. Morris, C.J., Aeschbach, D., and Scheer, F.A. (2012). Circadian system, sleep and endocrinology. Mol Cell Endocrinol 349, 91-104.
41. Naumann, E.A., Kampff, A.R., Prober, D.A., Schier, A.F., and Engert, F. (2010). Monitoring neural activity with bioluminescence during natural behavior. Nat Neurosci 13, 513-520.
42. Niell, C.M., Meyer, M.P., and Smith, S.J. (2004). In vivo imaging of synapse formation on a growing dendritic arbor. Nat Neurosci 7, 254-260.
43. Nishino, S., and Sakurai, T. (2006). The orexin/hypocretin system: physiology and pathophysiology. Towota, NJ: Humana Press.
44. Noche, R.R., Lu, P.N., Goldstein-Kral, L., Glasgow, E., and Liang, J.O. (2011). Circadian rhythms in the pineal organ persist in zebrafish larvae that lack ventral brain. BMC Neurosci 12, 7.
45. Pando, M.P., Pinchak, A.B., Cermakian, N., and Sassone-Corsi, P. (2001). A cell-based system that recapitulates the dynamic light-dependent regulation of the vertebrate clock. Proc Natl Acad Sci U S A 98, 10178-10183.
46. Panula, P. (2010). Hypocretin/orexin in fish physiology with emphasis on zebrafish. Acta Physiol (Oxf) 198, 381-386.
47. Panula, P., Chen, Y.C., Priyadarshini, M., Kudo, H., Semenova, S., Sundvik, M., and Sallinen, V. (2010). The comparative neuroanatomy and neurochemistry of zebrafish CNS systems of relevance to human neuropsychiatric diseases. Neurobiol Dis 40, 46-57.
48. Piccinetti, C.C., Migliarini, B., Olivotto, I., Coletti, G., Amici, A., and Carnevali, O. (2010). Appetite regulation: the central role of melatonin in Danio rerio. Horm Behav 58, 780-785.
49. Prober, D.A., Rihel, J., Onah, A.A., Sung, R.J., and Schier, A.F. (2006). Hypocretin/orexin overexpression induces an insomnia-like phenotype in zebrafish. J Neurosci 26, 13400-13410.
50. Pyza, E., and Gorska-Andrzejak, J. (2008). External and internal inputs affecting plasticity of dendrites and axons of the fly's neurons. Acta Neurobiol Exp (Wars) 68, 322-333.
51. Raizen, D.M., Zimmerman, J.E., Maycock, M.H., Ta, U.D., You, Y.J., Sundaram, M.V., and Pack, A.I. (2008). Lethargus is a Caenorhabditis elegans sleep-like state. Nature 451, 569-572.
52. Rawashdeh, O., De Borsetti, N.H., Roman, G., and Cahill, G.M. (2007). Melatonin suppresses nighttime memory formation in zebrafish. Science 318, 1144-1146.
53. Reppert, S.M., Perlow, M.J., Ungerleider, L.G., Mishkin, M., Tamarkin, L., Orloff, D.G., Hoffman, H.J., and Klein, D.C. (1981). Effects of damage to the suprachiasmatic area of the anterior hypothalamus on the daily melatonin and cortisol rhythms in the rhesus monkey. J Neurosci 1, 1414-1425.
54. Rihel, J., Prober, D.A., Arvanites, A., Lam, K., Zimmerman, S., Jang, S., Haggarty, S.J., Kokel, D., Rubin, L.L., Peterson, R.T., and Schier, A.F. (2010). Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 327, 348-351.
55. Saper, C.B., Scammell, T.E., and Lu, J. (2005). Hypothalamic regulation of sleep and circadian rhythms. Nature 437, 1257-1263.
56. Scott, E.K., Mason, L., Arrenberg, A.B., Ziv, L., Gosse, N.J., Xiao, T., Chi, N.C., Asakawa, K., Kawakami, K., and Baier, H. (2007). Targeting neural circuitry in zebrafish using GAL4 enhancer trapping. Nat Methods 4, 323-326.
57. Sehgal, A., and Mignot, E. (2011). Genetics of sleep and sleep disorders. Cell 146, 194-207.
58. Shapiro, C.M., and Hepburn, H.R. (1976). Sleep in a schooling fish, Tilapia mossambica. Physiol Behav 16, 613-615.
59. Siegel, J.M. (2005). Clues to the functions of mammalian sleep. Nature 437, 1264-1271.
60. Sigurgeirsson, B., Thornorsteinsson, H., Arnardottir, H., Johannesdottir, I.T., and Karlsson, K.A. (2011). Effects of modafinil on sleep-wake cycles in larval zebrafish. Zebrafish 8, 133-140.
61. Tamai, T.K., Carr, A.J., and Whitmore, D. (2005). Zebrafish circadian clocks: cells that see light. Biochem Soc Trans 33, 962-966.
62. Tamai, T.K., Young, L.C., and Whitmore, D. (2007). Light signaling to the zebrafish circadian clock by Cryptochrome 1a. Proc Natl Acad Sci U S A 104, 14712-14717.
63. Tauber, E., Weitzman, E., and Korey, S. (1969). Eye movements during behavioral inactivity in certain Bermuda reef fish. Commun Behav Biol 3, 131-135.
64. Thannickal, T.C., Moore, R.Y., Nienhuis, R., Ramanathan, L., Gulyani, S., Aldrich, M., Cornford, M., and Siegel, J.M. (2000). Reduced number of hypocretin neurons in human narcolepsy. Neuron 27, 469-474.
65. Tobler, I., and Borbely, A.A. (1985). Effect of rest deprivation on motor activity of fish. J Comp Physiol A 157, 817-822.
66. Tononi, G., and Cirelli, C. (2006). Sleep function and synaptic homeostasis. Sleep Med Rev 10, 49-62.
67. Tovin, A., Alon, S., Ben-Moshe, Z., Mracek, P., Vatine, G., Foulkes, N.S., Jacob-Hirsch, J., Rechavi, G., Toyama, R., Coon, S.L., Klein, D.C., Eisenberg, E., and Gothilf, Y. (2012). Systematic Identification of Rhythmic Genes Reveals camk1gb as a New Element in the Circadian Clockwork. PLoS Genet 8, e1003116.
68. Vallone, D., Gondi, S.B., Whitmore, D., and Foulkes, N.S. (2004). E-box function in a period gene repressed by light. Proc Natl Acad Sci U S A 101, 4106-4111.
69. Vallone, D., Lahiri, K., Dickmeis, T., and Foulkes, N.S. (2005). Zebrafish cell clocks feel the heat and see the light! Zebrafish 2, 171-187.
70. Vatine, G., Vallone, D., Appelbaum, L., Mracek, P., Ben-Moshe, Z., Lahiri, K., Gothilf, Y., and Foulkes, N.S. (2009). Light directs zebrafish period2 expression via conserved D and E boxes. PLoS Biol 7, e1000223.
71. Vatine, G., Vallone, D., Gothilf, Y., and Foulkes, N.S. (2011). It's time to swim500! Zebrafish and the circadian clock. FEBS Lett 585, 1485-1494.
72. Vatine, G.D., Zada, D., Lerer-Goldshtein, T., Tovin, A., Malkinson, G., Yaniv, K., and Appelbaum, L. (2013). Zebrafish as a model for monocarboxyl transporter 8-deficiency. J Biol Chem. 288, 169-180
73. Vuilleumier, R., Besseau, L., Boeuf, G., Piparelli, A., Gothilf, Y., Gehring, W.G., Klein, D.C., and Falcon, J. (2006). Starting the zebrafish pineal circadian clock with a single photic transition. Endocrinology 147, 2273-2279.
74. Wang, G., Grone, B., Colas, D., Appelbaum, L., and Mourrain, P. (2011). Synaptic plasticity in sleep: learning, homeostasis and disease. Trends Neurosci 34, 452-463.
75. Whitmore, D., Foulkes, N.S., and Sassone-Corsi, P. (2000). Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 404, 87-91.
76. Yokogawa, T., Marin, W., Faraco, J., Pezeron, G., Appelbaum, L., Zhang, J., Rosa, F., Mourrain, P., and Mignot, E. (2007). Characterization of sleep in zebrafish and insomnia in hypocretin receptor mutants. PLoS Biol 5, e277.
77. Zhdanova, I.V. (2005). Melatonin as a hypnotic: pro. Sleep Med Rev 9, 51-65.
78. Zhdanova, I.V. (2011). Sleep and its regulation in zebrafish. Rev Neurosci 22, 27-36.
79. Zhdanova, I.V., Wang, S.Y., Leclair, O.U., and Danilova, N.P. (2001). Melatonin promotes sleep-like state in zebrafish. Brain Res 903, 263-268.
80. Zimmerman, J.E., Naidoo, N., Raizen, D.M., and Pack, A.I. (2008). Conservation of sleep: insights from non-mammalian model systems. Trends Neurosci 31, 371-376.
81. Ziv, L., Levkovitz, S., Toyama, R., Falcon, J., and Gothilf, Y. (2005). Functional development of the zebrafish pineal gland: light-induced expression of period2 is required for onset of the circadian clock. J Neuroendocrinol 17, 314-320.