Circadian neuron feedback controls the Drosophila sleep-activity profile

Nature

Volumn 536, Issue 7616, 2016, Pages 292-297

  Guo, Fang ^a   Yu, Junwei ^a   Jung, Hyung Jae ^a   Abruzzi, Katharine C ^a   Luo, Weifei ^a   Griffith, Leslie C ^a   Rosbash, Michael ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; GLUTAMIC ACID;

ACTIVITY PATTERN; BIOASSAY; BRAIN; CELLS AND CELL COMPONENTS; CIRCADIAN RHYTHM; EXPERIMENTAL STUDY; FLY; SLEEP;

ANIMAL CELL; ANIMAL EXPERIMENT; AROUSAL; ARTICLE; CIRCADIAN RHYTHM; DROSOPHILA; FEEDBACK SYSTEM; FEMALE; HIGH TEMPERATURE; MALE; NEGATIVE FEEDBACK; NERVE CELL; NONHUMAN; OPTOGENETICS; PACEMAKER NERVE CELL; PRIORITY JOURNAL; SEX DIFFERENCE; SLEEP; SLEEP TIME; VIDEORECORDING; ANIMAL; BIOLOGICAL RHYTHM; CYTOLOGY; DROSOPHILA MELANOGASTER; METABOLISM; MOTOR ACTIVITY; PHYSIOLOGY; SEXUAL DEVELOPMENT; TEMPERATURE; WAKEFULNESS;

ANIMALS; BIOLOGICAL CLOCKS; CALCIUM; CIRCADIAN RHYTHM; DROSOPHILA MELANOGASTER; FEEDBACK, PHYSIOLOGICAL; FEMALE; GLUTAMIC ACID; MALE; MOTOR ACTIVITY; NEURONS; OPTOGENETICS; SEX CHARACTERISTICS; SLEEP; TEMPERATURE; VIDEO RECORDING; WAKEFULNESS;

EID: 84983418807     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature19097     Document Type: Article

References (52)

1. Reppert, S. M., Weaver, D. R. Coordination of circadian timing in mammals. Nature 418, 935-941 (2002).
2. Moore, R. Y. Organization and function of a central nervous system circadian oscillator: the suprachiasmatic hypothalamic nucleus. Fed. Proc. 42, 2783-2789 (1983).
3. Rieger, D., Shafer, O. T., Tomioka, K., Helfrich-Förster, C. Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J. Neurosci. 26, 2531-2543 (2006).
4. Shang, Y., Griffith, L. C., Rosbash, M. Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc. Natl Acad. Sci. USA 105, 19587-19594 (2008).
5. Cavanaugh, D. J. et al. Identification of a circadian output circuit for rest:activity rhythms in Drosophila. Cell 157, 689-701 (2014).
6. Agosto, J. et al. Modulation of GABAA receptor desensitization uncouples sleep onset and maintenance in Drosophila. Nat. Neurosci. 11, 354-359 (2008).
7. Tataroglu, O., Emery, P. Studying circadian rhythms in Drosophila melanogaster. Methods 68, 140-150 (2014).
8. 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 99, 791-802 (1999).
9. Grima, B., Chélot, E., Xia, R., Rouyer, F. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431, 869-873 (2004).
10. Guo, F., Cerullo, I., Chen, X., Rosbash, M. PDF neuron firing phase-shifts key circadian activity neurons in Drosophila. eLife 3, e02780 (2014).
11. Yao, Z., Shafer, O. T. The Drosophila circadian clock is a variably coupled network of multiple peptidergic units. Science 343, 1516-1520 (2014).
12. Stoleru, D., Peng, Y., Agosto, J., Rosbash, M. Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431, 862-868 (2004).
13. Kunst, M. et al. Calcitonin gene-related peptide neurons mediate sleep-specific circadian output in Drosophila. Curr. Biol. 24, 2652-2664 (2014).
14. Gilestro, G. F., Cirelli, C. pySolo: a complete suite for sleep analysis in Drosophila. Bioinformatics 25, 1466-1467 (2009).
15. Donelson, N. C. et al. High-resolution positional tracking for long-term analysis of Drosophila sleep and locomotion using the "tracker" program. PLoS One 7, e37250 (2012).
16. Garbe, D. S. et al. Context-specific comparison of sleep acquisition systems in Drosophila. Biol. Open 4, 1558-1568 (2015).
17. Pfeiffer, B. D. et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl Acad. Sci. USA 105, 9715-9720 (2008).
18. Zhang, L. et al. DN1(p) circadian neurons coordinate acute light and PDF inputs to produce robust daily behavior in Drosophila. Curr. Biol. 20, 591-599 (2010).
19. Zhang, Y., Liu, Y., Bilodeau-Wentworth, D., Hardin, P. E., Emery, P. Light and temperature control the contribution of specific DN1 neurons to Drosophila circadian behavior. Curr. Biol. 20, 600-605 (2010).
20. Jenett, A. et al. A GAL4-driver line resource for Drosophila neurobiology. Cell Reports 2, 991-1001 (2012).
21. Flourakis, M. et al. A conserved bicycle model for circadian clock control of membrane excitability. Cell 162, 836-848 (2015).
22. Seluzicki, A. et al. Dual PDF signaling pathways reset clocks via TIMELESS and acutely excite target neurons to control circadian behavior. PLoS Biol. 12, e1001810 (2014).
23. Klapoetke, N. C. et al. Independent optical excitation of distinct neural populations. Nat. Methods 11, 338-346 (2014).
24. Aso, Y. et al. Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila. eLife 3, e04580 (2014).
25. Inagaki, H. K. et al. Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship. Nat. Methods 11, 325-332 (2014).
26. Gradinaru, V. et al. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141, 154-165 (2010).
27. Rieger, D. et al. The fruit fly Drosophila melanogaster favors dim light and times its activity peaks to early dawn and late dusk. J. Biol. Rhythms 22, 387-399 (2007).
28. Feinberg, E. H. et al. GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57, 353-363 (2008).
29. Yao, Z., Macara, A. M., Lelito, K. R., Minosyan, T. Y., Shafer, O. T. Analysis of functional neuronal connectivity in the Drosophila brain. J. Neurophysiol. 108, 684-696 (2012).
30. Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
31. Hamasaka, Y. et al. Glutamate and its metabotropic receptor in Drosophila clock neuron circuits. J. Comp. Neurol. 505, 32-45 (2007).
32. Diao, F. et al. Plug-and-play genetic access to Drosophila cell types using exchangeable exon cassettes. Cell Reports 10, 1410-1421 (2015).
33. Liu, W. W., Wilson, R. I. Glutamate is an inhibitory neurotransmitter in the Drosophila olfactory system. Proc. Natl Acad. Sci. USA 110, 10294-10299 (2013).
34. Abruzzi, K., Chen, X., Nagoshi, E., Zadina, A., Rosbash, M. RNA-seq profiling of small numbers of Drosophila neurons. Methods Enzymol. 551, 369-386 (2015).
35. Collins, B. et al. Differentially timed extracellular signals synchronize pacemaker neuron clocks. PLoS Biol. 12, e1001959 (2014).
36. Collins, B., Kane, E. A., Reeves, D. C., Akabas, M. H., Blau, J. Balance of activity between LNvs and glutamatergic dorsal clock neurons promotes robust circadian rhythms in Drosophila. Neuron 74, 706-718 (2012).
37. Helfrich-Förster, C. Differential control of morning and evening components in the activity rhythm of Drosophila melanogaster-sex-specific differences suggest a different quality of activity. J. Biol. Rhythms 15, 135-154 (2000).
38. Low, K. H., Lim, C., Ko, H. W., Edery, I. Natural variation in the splice site strength of a clock gene and species-specific thermal adaptation. Neuron 60, 1054-1067 (2008).
39. Cao, W., Edery, I. A novel pathway for sensory-mediated arousal involves splicing of an intron in the period clock gene. Sleep 38, 41-51 (2015).
40. Majercak, J., Sidote, D., Hardin, P. E., Edery, I. How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 24, 219-230 (1999).
41. Masuyama, K., Zhang, Y., Rao, Y., Wang, J. W. Mapping neural circuits with activity-dependent nuclear import of a transcription factor. J. Neurogenet. 26, 89-102 (2012).
42. Stanewsky, R. et al. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95, 681-692 (1998).
43. Hardin, P. E., Hall, J. C., Rosbash, M. Circadian oscillations in period gene mRNA levels are transcriptionally regulated. Proc. Natl Acad. Sci. USA 89, 11711-11715 (1992).
44. Benito, J., Zheng, H., Ng, F. S., Hardin, P. E. Transcriptional feedback loop regulation, function, and ontogeny in Drosophila. Cold Spring Harb. Symp. Quant. Biol. 72, 437-444 (2007).
45. Picot, M., Klarsfeld, A., Chélot, E., Malpel, S., Rouyer, F. A role for blind DN2 clock neurons in temperature entrainment of the Drosophila larval brain. J. Neurosci. 29, 8312-8320 (2009).
46. Prober, D. A., Rihel, J., Onah, A. A., Sung, R. J., Schier, A. F. Hypocretin/orexin overexpression induces an insomnia-like phenotype in zebrafish. J. Neurosci. 26, 13400-13410 (2006).
47. Liang, X., Holy, T. E., Taghert, P. H. Synchronous Drosophila circadian pacemakers display nonsynchronous Ca2+ rhythms in vivo. Science 351, 976-981 (2016).
48. Gao, X. J. et al. A transcriptional reporter of intracellular Ca2+ in Drosophila. Nat. Neurosci. 18, 917-925 (2015).
49. Stanewsky, R. Analysis of rhythmic gene expression in adult Drosophila using the firefly luciferase reporter gene. Methods Mol. Biol. 362, 131-142 (2007).
50. Tang, C. H., Hinteregger, E., Shang, Y., Rosbash, M. Light-mediated TIM degradation within Drosophila pacemaker neurons (s-LNvs) is neither necessary nor sufficient for delay zone phase shifts. Neuron 66, 378-385 (2010).
51. Trapnell, C., Pachter, L., Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).
52. Haynes, P. R., Christmann, B. L., Griffith, L. C. A single pair of neurons links sleep to memory consolidation in Drosophila melanogaster. eLife 4, e03868 (2015).