Balance of Activity between LNvs and Glutamatergic Dorsal Clock Neurons Promotes Robust Circadian Rhythms in Drosophila

Neuron

Volumn 74, Issue 4, 2012, Pages 706-718

  Collins, Ben ^a   Kane, Elizabeth A ^a,c   Reeves, David C ^b   Akabas, Myles H ^b   Blau, Justin ^a  

^a NEW YORK UNIVERSITY   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTRANSMITTER;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTHROPOD LARVA; ARTICLE; CELL INTERACTION; CIRCADIAN RHYTHM; CONTROLLED STUDY; DORSAL CLOCK NERVE CELL; DROSOPHILA; GENETIC MANIPULATION; IMAGO; LIGHT AVOIDANCE; LOCOMOTION; MOLECULAR CLOCK; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE FUNCTION; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PHOTOREACTIVITY; PRIORITY JOURNAL; SLEEP WAKING CYCLE; VENTRAL LATERAL NERVE CELL;

ANIMALS; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; DROSOPHILA; DROSOPHILA PROTEINS; GLUTAMIC ACID; MOTOR ACTIVITY; NEURONS; PERIOD CIRCADIAN PROTEINS; PHOTIC STIMULATION;

EID: 84861437499     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.02.034     Document Type: Article

References (46)

1. Allada R., Chung B.Y. Circadian organization of behavior and physiology in Drosophila. Annu. Rev. Physiol. 2010, 72:605-624.
2. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
3. Cao G., Nitabach M.N. Circadian control of membrane excitability in Drosophila melanogaster lateral ventral clock neurons. J. Neurosci. 2008, 28:6493-6501.
4. Cully D.F., Vassilatis D.K., Liu K.K., Paress P.S., Van der Ploeg L.H., Schaeffer J.M., Arena J.P. Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature 1994, 371:707-711.
5. Dahdal D., Reeves D.C., Ruben M., Akabas M.H., Blau J. Drosophila pacemaker neurons require G protein signaling and GABAergic inputs to generate twenty-four hour behavioral rhythms. Neuron 2010, 68:964-977.
6. Featherstone D.E., Rushton E., Broadie K. Developmental regulation of glutamate receptor field size by nonvesicular glutamate release. Nat. Neurosci. 2002, 5:141-146.
7. Glaser F.T., Stanewsky R. Synchronization of the Drosophila circadian clock by temperature cycles. Cold Spring Harb. Symp. Quant. Biol. 2007, 72:233-242.
8. Goda T., Mirowska K., Currie J., Kim M.H., Rao N.V., Bonilla G., Wijnen H. Adult circadian behavior in Drosophila requires developmental expression of cycle, but not period. PLoS Genet. 2011, 7:e1002167.
9. Gong Z. Behavioral dissection of Drosophila larval phototaxis. Biochem. Biophys. Res. Commun. 2009, 382:395-399.
10. Grima B., Chélot E., Xia R., Rouyer F. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 2004, 431:869-873.
11. Hamada F.N., Rosenzweig M., Kang K., Pulver S.R., Ghezzi A., Jegla T.J., Garrity P.A. An internal thermal sensor controlling temperature preference in Drosophila. Nature 2008, 454:217-220.
12. B receptors and decreases in calcium. J. Neurobiol. 2005, 65:225-240.
13. Hamasaka Y., Rieger D., Parmentier M.L., Grau Y., Helfrich-Förster C., Nässel D.R. Glutamate and its metabotropic receptor in Drosophila clock neuron circuits. J. Comp. Neurol. 2007, 505:32-45.
14. Hardin P.E. Molecular genetic analysis of circadian timekeeping in Drosophila. Adv. Genet. 2011, 74:141-173.
15. Hogenesch J.B., Herzog E.D. Intracellular and intercellular processes determine robustness of the circadian clock. FEBS Lett. 2011, 585:1427-1434.
16. Keene A.C., Mazzoni E.O., Zhen J., Younger M.A., Yamaguchi S., Blau J., Desplan C., Sprecher S.G. Distinct visual pathways mediate Drosophila larval light avoidance and circadian clock entrainment. J. Neurosci. 2011, 31:6527-6534.
17. Klarsfeld A., Malpel S., Michard-Vanhée C., Picot M., Chélot E., Rouyer F. Novel features of cryptochrome-mediated photoreception in the brain circadian clock of Drosophila. J. Neurosci. 2004, 24:1468-1477.
18. Klarsfeld A., Picot M., Vias C., Chélot E., Rouyer F. Identifying specific light inputs for each subgroup of brain clock neurons in Drosophila larvae. J. Neurosci. 2011, 31:17406-17415.
19. Lin Y., Stormo G.D., Taghert P.H. The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J. Neurosci. 2004, 24:7951-7957.
20. Liu A.C., Welsh D.K., Ko C.H., Tran H.G., Zhang E.E., Priest A.A., Buhr E.D., Singer O., Meeker K., Verma I.M., et al. Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 2007, 129:605-616.
21. Maywood E.S., Reddy A.B., Wong G.K., O'Neill J.S., O'Brien J.A., McMahon D.G., Harmar A.J., Okamura H., Hastings M.H. Synchronization and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling. Curr. Biol. 2006, 16:599-605.
22. Mazzoni E.O., Desplan C., Blau J. Circadian pacemaker neurons transmit and modulate visual information to control a rapid behavioral response. Neuron 2005, 45:293-300.
23. McCarthy E.V., Wu Y., Decarvalho T., Brandt C., Cao G., Nitabach M.N. Synchronized bilateral synaptic inputs to Drosophila melanogaster neuropeptidergic rest/arousal neurons. J. Neurosci. 2011, 31:8181-8193.
24. Nitabach M.N., Taghert P.H. Organization of the Drosophila circadian control circuit. Curr. Biol. 2008, 18:R84-R93.
25. Nitabach M.N., Blau J., Holmes T.C. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 2002, 109:485-495.
26. Nitabach M.N., Wu Y., Sheeba V., Lemon W.C., Strumbos J., Zelensky P.K., White B.H., Holmes T.C. Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods. J. Neurosci. 2006, 26:479-489.
27. Pittendrigh C., Daan S. A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: a clock for all seasons. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1976, 106:333-355.
28. 2+ indicators. J. Neurosci. 2004, 24:9572-9579.
29. Pulver S.R., Pashkovski S.L., Hornstein N.J., Garrity P.A., Griffith L.C. Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. J. Neurophysiol. 2009, 101:3075-3088.
30. Reiff D.F., Ihring A., Guerrero G., Isacoff E.Y., Joesch M., Nakai J., Borst A. In vivo performance of genetically encoded indicators of neural activity in flies. J. Neurosci. 2005, 25:4766-4778.
31. Renn S.C., Park J.H., Rosbash M., Hall J.C., Taghert P.H. A Pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 1999, 99:791-802.
32. 2A domain. Nature 2002, 418:336-340.
33. Shafer O.T., Helfrich-Förster C., Renn S.C., Taghert P.H. Reevaluation of Drosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes. J. Comp. Neurol. 2006, 498:180-193.
34. Sheeba V., Fogle K.J., Kaneko M., Rashid S., Chou Y.T., Sharma V.K., Holmes T.C. Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr. Biol. 2008, 18:1537-1545.
35. Sheeba V., Gu H., Sharma V.K., O'Dowd D.K., Holmes T.C. Circadian- and light-dependent regulation of resting membrane potential and spontaneous action potential firing of Drosophila circadian pacemaker neurons. J. Neurophysiol. 2008, 99:976-988.
36. Stoleru D., Peng Y., Agosto J., Rosbash M. Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 2004, 431:862-868.
37. Stoleru D., Peng Y., Nawathean P., Rosbash M. A resetting signal between Drosophila pacemakers synchronizes morning and evening activity. Nature 2005, 438:238-242.
38. Storch K.F., Lipan O., Leykin I., Viswanathan N., Davis F.C., Wong W.H., Weitz C.J. Extensive and divergent circadian gene expression in liver and heart. Nature 2002, 417:78-83.
39. Tanoue S., Krishnan P., Krishnan B., Dryer S.E., Hardin P.E. Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr. Biol. 2004, 14:638-649.
40. Wang J., Ma X.J., Yang J.S., Zheng X.Y., Zugates C.T., Lee C.H.J., Lee T. Transmembrane/juxtamembrane domain-dependent Dscam distribution and function during mushroom body neuronal morphogenesis. Neuron 2004, 43:663-672.
41. 2+ via nicotinic receptors in cultured PDF-containing clock neurons of Drosophila. J. Neurophysiol. 2004, 91:912-923.
42. Wu Y., Cao G., Nitabach M.N. Electrical silencing of PDF neurons advances the phase of non-PDF clock neurons in Drosophila. J. Biol. Rhythms 2008, 23:117-128.
43. Xiang Y., Yuan Q., Vogt N., Looger L.L., Jan L.Y., Jan Y.N. Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 2010, 468:921-926.
44. Yang Z., Sehgal A. Role of molecular oscillations in generating behavioral rhythms in Drosophila. Neuron 2001, 29:453-467.
45. Yasuyama K., Meinertzhagen I.A. Synaptic connections of PDF-immunoreactive lateral neurons projecting to the dorsal protocerebrum of Drosophila melanogaster. J. Comp. Neurol. 2010, 518:292-304.
46. Yuan Q., Xiang Y., Yan Z., Han C., Jan L.Y., Jan Y.N. Light-induced structural and functional plasticity in Drosophila larval visual system. Science 2011, 333:1458-1462.