From Neurogenetic Studies in the Fly Brain to a Concept in Circadian Biology

References

• Agrawal, T., Sadaf, S., & Hasan, G. (2013). A genetic RNAi screen for IP(3)/Ca(2)(+) coupled GPCRs in Drosophila identifies the PdfR as a regulator of insect flight. PLoS Genet, 9, e1003849.
   PubMed Web of Science ®Google Scholar
• Akten, B., Jauch, E., Genova, G. K., Kim, E. Y., Edery, I., Raabe, T., & Jackson, F. R. (2003). A role for CK2 in the Drosophila circadian oscillator. Nat Neurosci, 6, 251–257.
   PubMed Web of Science ®Google Scholar
• Allada, R., White, N. E., So, W. V., Hall, J. C., & Rosbash, M. (1998). A mutant Drosophila homolog of mammalian Clock disrupts circadian rhythms and transcription of period and timeless. Cell, 93, 791–804.
   PubMed Web of Science ®Google Scholar
• An, S., Harang, R., Meeker, K., Granados-Fuentes, D., Tsai, C. A., Mazuski, C., Kim, J., Doyle, F. J., 3rd, Petzold, L. R., & Herzog, E. D. (2013). A neuropeptide speeds circadian entrainment by reducing intercellular synchrony. Proc Natl Acad Sci U S A, 110, E4355–E4361.
   Web of Science ®Google Scholar
• Bachleitner, W., Kempinger, L., Wülbeck, C., Rieger, D., & Helfrich-Förster, C. (2007). Moonlight shifts the endogenous clock of Drosophila melanogaster. Proc Natl Acad Sci U S A, 104, 3538–3543.
   PubMed Web of Science ®Google Scholar
• Belvin, M. P., Zhou, H., & Yin, J. C. (1999). The Drosophila dCREB2 gene affects the circadian clock. Neuron, 22, 777–787.
   PubMed Web of Science ®Google Scholar
• Benito, J., Houl, J. H., Roman, G. W., & Hardin, P. E. (2008). The blue-light photoreceptor CRYPTOCHROME is expressed in a subset of circadian oscillator neurons in the Drosophila CNS. J Biol Rhythms, 23, 296–307.
   PubMed Web of Science ®Google Scholar
• Blanchardon, E., Grima, B., Klarsfeld, A., Chelot, E., Hardin, P. E., Preat, T., & Rouyer F. (2001). Defining the role of Drosophila lateral neurons in the control of circadian rhythms in motor activity and eclosion by targeted genetic ablation and PERIOD protein overexpression. Eur J Neurosci, 13, 871–888.
   PubMed Web of Science ®Google Scholar
• Blau, J., & Young, M. W. (1999). Cycling vrille expression is required for a functional Drosophila clock. Cell, 99, 661–671.
   PubMedGoogle Scholar
• Blest, A. (1961). Some modifications of Holmes's Silver method for insect central nervous system. Q J Microsc Sci, 102, 413–417.
   Google Scholar
• Busza, A., Emery-Le, M., Rosbash, M., & Emery, P. (2004). Roles of the two Drosophila CRYPTOCHROME structural domains in circadian photoreception. Science, 304, 1503–1506.
   PubMed Web of Science ®Google Scholar
• Ceriani, M. F., Darlington, T. K., Staknis, D., Mas, P., Petti, A. A., Weitz, C. J., & Kay, S. A. (1999). Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science, 285, 553–556.
   PubMed Web of Science ®Google Scholar
• Chiu, J. C., Ko, H. W., & Edery, I. (2011). NEMO/NLK phosphorylates PERIOD to initiate a time-delay phosphorylation circuit that sets circadian clock speed. Cell, 145, 357–370.
   PubMed Web of Science ®Google Scholar
• Choi, C., Cao, G., Tanenhaus, A. K., McCarthy, E. V., Jung, M., Schleyer, W., Shang, Y., Rosbash, M., Yin, J. C., & Nitabach, M. N. (2013). Autoreceptor control of peptide/neurotransmitter corelease from PDF neurons determines allocation of circadian activity in Drosophila. Cell Rep, 2, 332–344.
   Web of Science ®Google Scholar
• Choi, C., Fortin, J. P., McCarthy, E., Oksman, L., Kopin, A. S., & Nitabach, M. N. (2009). Cellular dissection of circadian peptide signals with genetically encoded membrane-tethered ligands. Curr Biol, 19, 1167–1175.
   PubMed Web of Science ®Google Scholar
• Chung, B. Y., Kilman, V. L., Keath, J. R., Pitman, J. L., & Allada, R. (2009). The GABA(A) receptor RDL acts in peptidergic PDF neurons to promote sleep in Drosophila. Curr Biol, 19, 386–390.
   PubMed Web of Science ®Google Scholar
• Cusumano, P., Klarsfeld, A., Chelot, E., Picot, M., Richier, B., & Rouyer, F. (2009). PDF-modulated visual inputs and cryptochrome define diurnal behavior in Drosophila. Nat Neurosci, 12, 1431–1437.
   PubMed Web of Science ®Google Scholar
• Cyran, S. A., Buchsbaum, A. M., Reddy, K. L., Lin, M. C., Glossop, N. R., Hardin, P. E., Young, M. W., Storti, R. V., & Blau, J. (2003). vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell, 112, 329–341.
   PubMed Web of Science ®Google Scholar
• Diez-Noguera, A. (1994). A functional model of the circadian system based on the degree of intercommunication in a complex system. Am J Physiol, 267, R1118–R1135.
   PubMed Web of Science ®Google Scholar
• Dolezelova, E., Dolezel, D., & Hall, J. C. (2007). Rhythm defects caused by newly engineered null mutations in Drosophila's cryptochrome gene. Genetics, 177, 329–345.
   PubMed Web of Science ®Google Scholar
• Dushay, M. S., Rosbash, M., & Hall, J. C. (1989). The disconnected visual system mutations in Drosophila melanogaster drastically disrupt circadian rhythms. J Biol Rhythms, 4, 1–27.
   PubMed Web of Science ®Google Scholar
• Duvall, L. B., & Taghert, P. H. (2012). The circadian neuropeptide PDF signals preferentially through a specific adenylate cyclase isoform AC3 in M pacemakers of Drosophila. PLoS Biol, 10, e1001337.
   PubMed Web of Science ®Google Scholar
• Duvall, L. B., & Taghert, P. H. (2013). E and M circadian pacemaker neurons use different PDF receptor signalosome components in Drosophila. J Biol Rhythms, 28, 239–248.
   PubMed Web of Science ®Google Scholar
• el Jundi, B., Pfeiffer, K., & Homberg, U. (2011). A distinct layer of the medulla integrates sky compass signals in the brain of an insect. PloS ONE, 6, e27855.
   Web of Science ®Google Scholar
• Emery, P., So, W. V., Kaneko, M., Hall, J. C., & Rosbash, M. (1998). CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell, 95, 669–679.
   PubMed Web of Science ®Google Scholar
• Emery, P., Stanewsky, R., Hall, J. C., & Rosbash, M. (2000). A unique circadian-rhythm photoreceptor. Nature, 404, 456–457.
   PubMed Web of Science ®Google Scholar
• Ewer, J., Frisch, B., Hamblen-Coyle, M. J., Rosbash, M., & Hall, J. C. (1992). Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells’ influence on circadian behavioral rhythms. J Neurosci, 12, 3321–3349.
   PubMed Web of Science ®Google Scholar
• Fischbach, K. F. (1983). Neural cell types surviving congenital sensory deprivation in the optic lobes of Drosophila melanogaster. Dev Biol, 95, 1–18.
   PubMed Web of Science ®Google Scholar
• Fischbach, K. F., & Technau, G. (1984). Cell degeneration in the developing optic lobes of the sine oculis and small-optic-lobes mutants of Drosophila melanogaster. Dev Biol, 104, 219–239.
   PubMed Web of Science ®Google Scholar
• Fogle, K. J., Parson, K. G., Dahm, N. A., & Holmes, T. C. (2011). CRYPTOCHROME is a blue-light sensor that regulates neuronal firing rate. Science, 331, 1409–1413.
   PubMed Web of Science ®Google Scholar
• Frisch, B., Fleissner, G., Brandes, C., & Hall, J. C. (1996). Staining in the brain of Pachymorpha sexguttata mediated by an antibody against a Drosophila clock-gene product: Labeling of cells with possible importance for the beetle's circadian rhythms. Cell Tissue Res, 286, 411–429.
   PubMed Web of Science ®Google Scholar
• Ginty, D. D., Kornhauser, J. M., Thompson, M. A., Bading, H., Mayo, K. E., Takahashi, J. S., & Greenberg, M. E. (1993). Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science, 260, 238–241.
   PubMedGoogle Scholar
• Gmeiner, F., Kolodziejczyk, A., Yoshii, T., Rieger, D., Nässel, D. R., & Helfrich-Förster, C. (2013). GABA(B) receptors play an essential role in maintaining sleep during the second half of the night in Drosophila melanogaster. J Exp Biol, 216, 3837–3843.
   PubMed Web of Science ®Google Scholar
• Grima, B., Chelot, E., Xia, R., & Rouyer, F. (2004). Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature, 431, 869–873.
   PubMed Web of Science ®Google Scholar
• Grima, B., Lamouroux, A., Chelot, E., Papin, C., Limbourg-Bouchon, B., & Rouyer, F. (2002). The F-box protein slimb controls the levels of clock proteins period and timeless. Nature, 420, 178–182.
   PubMed Web of Science ®Google Scholar
• Hagberg, M. (1986). Ultrastructure and central projections of extraocular photoreceptors in caddiesflies (Insecta: Trichtoptera). Cell Tissue Res, 245, 643–648.
   Web of Science ®Google Scholar
• Handler, A. M., & Konopka, R. J. (1979). Transplantation of a circadian pacemaker in Drosophila. Nature, 279, 236–238.
   PubMed Web of Science ®Google Scholar
• Hardin, P. E. (2011). Molecular genetic analysis of circadian timekeeping in Drosophila. Adv Genet, 74, 141–173.
   PubMed Web of Science ®Google Scholar
• Hardin, P. E., Hall, J. C., & Rosbash, M. (1990). Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature, 343, 536–540.
   PubMed Web of Science ®Google Scholar
• Heisenberg, M., & Böhl, K. (1979). Isolation of anatomical brain mutants of Drosophila by histological means. Z Naturforsch, 34, 143–147.
   Google Scholar
• Helfrich, C. (1986). Role of the optic lobes in the regulation of the locomotor activity rhythm of Drosophila melanogaster: Behavioral analysis of neural mutants. J Neurogenet, 3, 321–343.
   PubMed Web of Science ®Google Scholar
• Helfrich, C., & Engelmann, W. (1983). Circadian rhythm of the locomotor activity in Drosophila melanogaster and its mutants “sine oculis” and “small optic lobes”. Physiol Entomol, 8, 257–272.
   Web of Science ®Google Scholar
• Helfrich, C., & Engelmann, W. (1987). Evidences for circadian rhythmicty in the per0 mutant of Drosophila melanogaster. Z Naturforsch, 42c, 1335–1338.
   Google Scholar
• Helfrich-Förster, C. (1995). The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster. Proc Natl Acad Sci U S A, 92, 612–616.
   PubMed Web of Science ®Google Scholar
• Helfrich-Förster, C. (1997). Development of pigment-dispersing hormone-immunoreactive neurons in the nervous system of Drosophila melanogaster. J Comp Neurol, 380, 335–354.
   PubMed Web of Science ®Google Scholar
• Helfrich-Förster, C. (1998). Robust circadian rhythmicity of Drosophila melanogaster requires the presence of Lateral Neurons: A brain-behavioral study of disconnected mutants. J Comp Physiol A, 182, 435–453.
   PubMed Web of Science ®Google Scholar
• Helfrich-Förster, C. (2000). 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.
   PubMed Web of Science ®Google Scholar
• Helfrich-Förster, C. (2001). The activity rhythm of Drosophila melanogaster is controlled by a dual oscillator system. J Insect Physiol, 47, 877–887.
   Web of Science ®Google Scholar
• Helfrich-Förster, C. (2005). Organization of endogenous clocks in insects. Biochem Soc Trans, 33, 957–961.
   PubMed Web of Science ®Google Scholar
• Helfrich-Förster, C. (2009a). Does the morning and evening oscillator model fit better for flies or mice?J Biol Rhythms, 24, 259–270.
   PubMed Web of Science ®Google Scholar
• Helfrich-Förster, C. (2009b). The role of PDF in the circadian clock of Drosophila melanogaster. Sleep Biol Rhythms, 7, 130–143.
   Web of Science ®Google Scholar
• Helfrich-Förster, C., & Diez Noguera, A. (1993). Use of a multioscillatory system to simulate experimental results obtained for the period-mutants of Drosophila melanogaster. J Interdiscipl Cycle Res, 24, 225–231.
   Web of Science ®Google Scholar
• Helfrich-Förster, C., Edwards, T., Yasuyama, K., Wisotzki, B., Schneuwly, S., Stanewsky, R., Meinertzhagen, I. A., & Hofbauer, A. (2002). The extraretinal eyelet of Drosophila: Development, ultrastructure, and putative circadian function. J Neurosci, 22, 9255–9266.
   PubMed Web of Science ®Google Scholar
• Helfrich-Förster, C., & Homberg, U. (1993). Pigment-dispersing hormone-immunoreactive neurons in the nervous system of wild-type Drosophila melanogaster and of several mutants with altered circadian rhythmicity. J Comp Neurol, 337, 177–190.
   PubMed Web of Science ®Google Scholar
• Helfrich-Förster, C., Shafer, O. T., Wülbeck, C., Grieshaber, E., Rieger, D., & Taghert, P. (2007). Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J Comp Neurol, 500, 47–70.
   PubMed Web of Science ®Google Scholar
• Helfrich-Förster, C., Stengl, M., & Homberg, U. (1998). Organization of the circadian system in insects. Chronobiol Int, 15, 567–594.
   PubMed Web of Science ®Google Scholar
• Hofbauer, A., & Buchner, E. (1989). Does Drosophila have seven eyes?Naturwissenschaften, 76, 335–336.
   Web of Science ®Google Scholar
• Homberg, U., Würden, S., Dircksen, H., & Rao, K. R. (1991). Comparative anatomy of pigment-dispersing hormone-immunoreactive neurons in the brain of orthopteriod insects. Cell Tissue Res, 266, 342–357.
   Web of Science ®Google Scholar
• Homberg, U., & Würden, S. (1997). Movement-sensitive polarization-sensitive,and light-sensitive neurons of the medulla and accessory medulla of the locust, Schistocerca gregaria. J Comp Neurol, 386, 329–346.
   PubMed Web of Science ®Google Scholar
• Hyun, S., Lee, Y., Hong, S. T., Bang, S., Paik, D., Kang, J., Shin, J., Lee, J., Jeon, K., Hwang, S., et al. (2005). Drosophila GPCR Han is a receptor for the circadian clock neuropeptide PDF. Neuron, 48, 267–278.
   PubMed Web of Science ®Google Scholar
• Im, S. H., Li, W., & Taghert, P. H. (2011). PDFR and CRY signaling converge in a subset of clock neurons to modulate the amplitude and phase of circadian behavior in Drosophila. PLoS ONE, 6, e18974.
   PubMed Web of Science ®Google Scholar
• Im, S. H., & Taghert, P. H. (2010). PDF receptor expression reveals direct interactions between circadian oscillators in Drosophila. J Comp Neurol, 518, 1925–1945.
   PubMed Web of Science ®Google Scholar
• Inagaki, N., Honma, S., Ono, D., Tanahashi, Y., & Honma, K. (2007). Separate oscillating cell groups in mouse suprachismatic nucleus couple photoperiodically to the onset and end of daily activity. Proc Natl Acad Sci U S A, 104, 7664–7669.
   PubMed Web of Science ®Google Scholar
• Jackson, F. R., Bargiello, T. A., Yun, S. H., & Young, M. W. (1986). Product of per locus of Drosophila shares homology with proteoglycans. Nature, 320, 185–188.
   PubMed Web of Science ®Google Scholar
• Kadener, S., Stoleru, D., McDonald, M., Nawathean, P., & Rosbash, M. (2007). Clockwork Orange is a transcriptional repressor and a new Drosophila circadian pacemaker component. Genes Dev, 21, 1675–1686.
   PubMed Web of Science ®Google Scholar
• Kaneko, M., Helfrich-Förster, C., & Hall, J. C. (1997). Spatial and temporal expression of the period and timeless genes in the developing nervous system of Drosophila: Newly identified pacemaker candidates and novel features of clock gene product cycling. J Neurosci, 17, 6745–6760.
   PubMed Web of Science ®Google Scholar
• Kaneko, M., Park, J. H., Cheng, Y., Hardin, P. E., & Hall, J. C. (2000). Disruption of synaptic transmission or clock-gene-product oscillations in circadian pacemaker cells of Drosophila cause abnormal behavioural rhythms. J Neurobiol, 43, 207–233.
   PubMedGoogle Scholar
• Ko, H. W., Jiang, J., & Edery, I. (2002). Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime. Nature, 420, 673–678.
   PubMed Web of Science ®Google Scholar
• Ko, H. W., Kim, E. Y., Chiu, J., Vanselow, J. T., Kramer, A., & Edery, I. (2010). A hierarchical phosphorylation cascade that regulates the timing of PERIOD nuclear entry reveals novel roles for proline-directed kinases and GSK-3beta/SGG in circadian clocks. J Neurosci, 30, 12664–12675.
   PubMed Web of Science ®Google Scholar
• Koehler, W. K., & Fleissner, G. (1978). Internal desynchronisation of bilaterally organised circadian oscillators in the visual system of insects. Nature, 274, 708–710.
   PubMed Web of Science ®Google Scholar
• Konopka, R. J., & Benzer, S. (1971). Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A, 68, 2112–2116.
   PubMed Web of Science ®Google Scholar
• Konopka, R. J., Pittendrigh, C., & Orr, D. (1989). Reciprocal behaviour associated with altered homeostasis and photosensitivity of Drosophila clock mutants. J Neurogenet, 6, 1–10.
   PubMed Web of Science ®Google Scholar
• Lear, B. C., Merrill, C. E., Lin, J. M., Schroeder, A., Zhang, L., & Allada, R. (2005). A G protein-coupled receptor, groom-of-PDF, is required for PDF neuron action in circadian behavior. Neuron, 48, 221–227.
   PubMed Web of Science ®Google Scholar
• Lim, C., Chung, B. Y., Pitman, J. L., McGill, J. J., Pradhan, S., Lee, J., Keegan, K. P., Choe, J., & Allada, R. (2007). Clockwork orange encodes a transcriptional repressor important for circadian-clock amplitude in Drosophila. Curr Biol, 17, 1082–1089.
   PubMed Web of Science ®Google Scholar
• Lin, J. M., Kilman, V. L., Keegan, K., Paddock, B., Emery-Le, M., Rosbash, M., & Allada, R. (2002). A role for casein kinase 2alpha in the Drosophila circadian clock. Nature, 420, 816–820.
   PubMed Web of Science ®Google Scholar
• Lin, Y., Stormo, G. D., & Taghert, P. H. (2004). The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J Neurosci, 24, 7951–7957.
   PubMedGoogle Scholar
• Loesel, R., & Homberg, U. (2001). Anatomy and physiology of neurons with processes in the accessory medulla of the cockroach Leucophaea maderae. J Comp Neurol, 439, 193–207.
   PubMed Web of Science ®Google Scholar
• Mack, J., & Engelmann, W. (1981). Circadian control of the locomotor activity in eye mutants of Drosophila melanogaster. J Interdiscipl Cycle Res,12, 313–323.
   Google Scholar
• Malpel, S., Klarsfeld, A., & Rouyer, F. (2002). Larval optic nerve and adult extra-retinal photoreceptors sequentially associate with clock neurons during Drosophila brain development. Development, 129, 1443–1453.
   PubMed Web of Science ®Google Scholar
• Martinek, S., Inonog, S., Manoukian, A. S., & Young, M. W. (2001). A role for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell, 105, 769–779.
   PubMed Web of Science ®Google Scholar
• Mazzotta, G., Rossi, A., Leonardi, E., Mason, M., Bertolucci, C., Caccin, L., Spolaore, B., Martin, A. J., Schlichting, M., Grebler, R., et al. (2013). Fly cryptochrome and the visual system. Proc Natl Acad Sci U S A, 110, 6163–6168.
   PubMed Web of Science ®Google Scholar
• Mertens, I., Vandingenen, A., Johnson, E. C., Shafer, O. T., Li, W., Trigg, J. S., De Loof, A., Schoofs, L., & Taghert, P. H. (2005). PDF receptor signaling in Drosophila contributes to both circadian and geotactic behaviors. Neuron, 48, 213–219.
   PubMed Web of Science ®Google Scholar
• Meyer, P., Saez, L., & Young, M. W. (2006). PER-TIM interactions in living Drosophila cells: An interval timer for the circadian clock. Science, 311, 226–229.
   PubMed Web of Science ®Google Scholar
• Nishiitsutsjii-Uwo, J., & Pittendrigh, C. (1968). Central nervous system control of circadian rhythmicity in the cockroach. III. The optic lobes, locus of the driving oscillation. Z Vergl Physiol, 58, 14–46.
   Google Scholar
• Nitabach, M. N., Wu, Y., Sheeba, V., Lemon, W. C., Strumbos, J., Zelensky, P. K., White, B. H., & Holmes, T. C. (2006). Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods. J Neurosci, 26, 479–489.
   PubMed Web of Science ®Google Scholar
• Page, T. L. (1982). Transplantation of the cockroach circadian pacemaker. Science, 216, 73–75.
   PubMed Web of Science ®Google Scholar
• Parisky, K. M., Agosto, J., Pulver, S. R., Shang, Y., Kuklin, E., Hodge, J. J., Kang, K., Liu, X., Garrity, P. A., Rosbash, M., & Griffith, L. C. (2008). PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron, 60, 672–682.
   PubMed Web of Science ®Google Scholar
• Park, D., & Griffith, L. C. (2006). Electrophysiological and anatomical characterization of PDF-positive clock neurons in the intact adult Drosophila brain. J Neurophysiol, 95, 3955–3960.
   PubMed Web of Science ®Google Scholar
• Park, D., Shafer, O. T., Shepherd S. P., Suh, H., Trigg, J. S., & Taghert, P. H. (2008). The Drosophila basic helix- loop-helix protein DIMMED directly activates PHM, a gene encoding a neuropeptide-amidating enzyme. Mol Cell Biol, 28, 410–421.
   PubMed Web of Science ®Google Scholar
• Park, J. H., Helfrich-Förster, C., Lee, G., Liu, L., Rosbash, M., & Hall, J. C. (2000). Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Natl Acad Sci U S A, 97, 3608–3613.
   PubMed Web of Science ®Google Scholar
• Petri, B., Homberg, U., Loesel, R., & Stengl, M. (2002). Evidence of a role of GABA and Mas-allatotropin in photic entrainment of the circadian clock of the cockroach Leucophaea maderae. J Exp Biol, 205, 1459–1469.
   PubMed Web of Science ®Google Scholar
• Petri, B., Stengl, M., Würden, S., & Homberg, U. (1995). Immunocytochemical characterization of the accessory medulla in the cockroach Leucophaea maderae. Cell Tissue Res, 282, 3–19.
   PubMed Web of Science ®Google Scholar
• Pittendrigh, C., & Daan, S. (1976). A functional analysis of circadian pademakers in nocturnal rodents. V. Pacemaker structure: A clock for all seasons. J Comp Physiol A, 106, 333–355.
   Web of Science ®Google Scholar
• Price, J. L., Blau, J., Rothenfluh, A., Abodeely, M., Kloss, B., & Young, M. W. (1998). double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell, 94, 83–95.
   PubMed Web of Science ®Google Scholar
• Rao, K. R., & Riehm, J. P. (1993). Pigment-dispersing hormones. Ann N Y Acad Sci, 638, 78–88.
   Google Scholar
• Reddy, P., Jacquier, A. C., Abovich, N., Petersen, G., & Rosbash, M. (1986). The period clock locus of D. melanogaster codes for a proteoglycan. Cell, 46, 53–61.
   PubMed Web of Science ®Google Scholar
• Reischig, T., & Stengl, M. (2002). Optic lobe commissures in a three-dimensional brain model of the cockroach Leucophaea maderae: A search for the circadian coupling pathways. J Comp Neurol, 443, 388–400.
   PubMed Web of Science ®Google Scholar
• Reischig, T., & Stengl, M. (2003). Ectopic transplantation of the accessory medulla restores circadian locomotor rhythms in arrhythmic cockroaches (Leucophaea maderae). J Exp Biol, 206, 1877–1886.
   PubMed Web of Science ®Google Scholar
• Renn, S. C., Park, J. H., Rosbash, M., Hall, J. C., & Taghert, P. H. (1999). A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell, 99, 791–802.
   PubMed Web of Science ®Google Scholar
• Reppert, S. M. (1998). A clockwork explosion!Neuron, 21, 1–4.
   PubMed Web of Science ®Google Scholar
• Richier, B., Michard-Vanhee, C., Lamouroux, A., Papin, C., & Rouyer, F. (2008). The clockwork orange Drosophila protein functions as both an activator and a repressor of clock gene expression. J Biol Rhythms, 23, 103–116.
   PubMed Web of Science ®Google Scholar
• Rieger, D., Shafer, O. T., Tomioka, K., & Helfrich-Förster, C. (2006). Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci, 26, 2531–2543.
   PubMed Web of Science ®Google Scholar
• Rieger, D., Stanewsky, R., & Helfrich-Förster, C. (2003). Cryptochrome, compound eyes, Hofbauer-Buchner eyelets, and ocelli play different roles in the entrainment and masking pathway of the locomotor activity rhythm in the fruit fly Drosophila melanogaster. J Biol Rhythms, 18, 377–391.
   PubMed Web of Science ®Google Scholar
• Rieger, D., Wülbeck, C., Rouyer, F., & Helfrich-Förster, C. (2009). Period gene expression in four neurons is sufficient for rhythmic activity of Drosophila melanogaster under dim light conditions. J Biol Rhythms, 24, 271–282.
   PubMed Web of Science ®Google Scholar
• Roberts, S. K. (1974). Circadian rhythms in cockroaches. Effects of optic lobe lesions. J Comp Physiol, 88, 21–30.
   Web of Science ®Google Scholar
• Rutila, J. E., Suri, V., Le, M., So, W. V., Rosbash, M., & Hall, J. C. (1998). CYCLE is a second bHLH-PAS clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell, 93, 805–814.
   PubMed Web of Science ®Google Scholar
• Sancar, A. (2004). Regulation of the mammalian circadian clock by cryptochrome. J Biol Chem, 279, 34079–34082.
   PubMed Web of Science ®Google Scholar
• Sathyanarayanan, S., Zheng, X., Xiao, R., & Sehgal, A. (2004). Posttranslational regulation of Drosophila PERIOD protein by protein phosphatase 2A. Cell, 116, 603–615.
   PubMed Web of Science ®Google Scholar
• Schlichting, M., Grebler, R., Peschel, N., Yoshii, T., & Helfrich-Förster, C. (2014). Moonlight detection by Drosophila's endogenous clock depends on multiple photopigments in the compound eyes. J Biol Rhythms, 29, 75–86.
   PubMed Web of Science ®Google Scholar
• Schneider, N. L., & Stengl, M. (2005). Pigment-dispersing factor and GABA synchronize cells of the isolated circadian clock of the cockroach Leucophaea maderae. J Neurosci, 25, 5138–5147.
   PubMed Web of Science ®Google Scholar
• Schulze, J., Schendzielorz, T., Neupert, S., Predel, R., & Stengl, M. (2013). Neuropeptidergic input pathways to the circadian pacemaker center of the Madeira cockroach analysed with an improved injection technique. Eur J Neurosci, 38, 2842–2852.
   PubMed Web of Science ®Google Scholar
• Schendzielorz, J., & Stengl, M. (2014). Candidates for the light entrainment pathway to the circadian clock of the Madeira cockroach Rhyparobia maderae. Cell Tissue Res,355, 447–462.
   PubMed Web of Science ®Google Scholar
• Sehgal, A., Price, J. L., Man, B., & Young, M. W. (1994). Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science, 263, 1603–1606.
   PubMed Web of Science ®Google Scholar
• Shafer, O. T., Kim, D. J., Dunbar-Yaffe, R., Nikolaev, V. O., Lohse, M. J., & Taghert, P. H. (2008). Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron, 58, 223–237.
   PubMed Web of Science ®Google Scholar
• Shafer, O. T., Rosbash, M., & Truman, J.W. (2002). Sequential nuclear accumulation of the clock proteins period and timeless in the pacemaker neurons of Drosophila melanogaster. J Neurosci, 22, 5946 –5954.
   PubMed Web of Science ®Google Scholar
• Shafer, O. T., & Taghert, P. H. (2009). RNA-interference knockdown of Drosophila pigment dispersing factor in neuronal subsets: The anatomical basis of a neuropeptide's circadian functions. PLoS ONE, 4, e8298.
   PubMed Web of Science ®Google Scholar
• Shang, Y., Griffith, L. C., & Rosbash, M. (2008). Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc Natl Acad Sci U S A, 105, 19587–19594.
   PubMed Web of Science ®Google Scholar
• Sheeba, V., Fogle, K. J., Kaneko, M., Rashid, S., Chou, Y. T., Sharma, V. K., & Holmes, T. C. (2008). Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr Biol, 18, 1537–1545.
   Google Scholar
• Siwicki, K. K., Eastman, C., Petersen, G., Rosbash, M., & Hall, J. C. (1988). Antibodies to the period gene product of Drosophila reveal diverse tissue distribution and rhythmic changes in the visual system. Neuron, 1, 141–150.
   PubMed Web of Science ®Google Scholar
• Sokolove, P. G. (1975). Localization of the cockroach optic lobe circadian pacemaker with microlesions. Brain Res, 87, 13–21.
   PubMed Web of Science ®Google Scholar
• Stanewsky, R., Kaneko, M., Emery, P., Beretta, B., Wager-Smith, K., Kay, S. A., Rosbash, M., & Hall, J. C. (1998). The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell, 95, 681–692.
   PubMed Web of Science ®Google Scholar
• Steller, H., Fischbach, K. F., & Rubin, G. M. (1987). Disconnected: A locus required for neuronal pathway formation in the visual system of Drosophila. Cell, 50, 1139–1153.
   PubMed Web of Science ®Google Scholar
• Stengl, M., & Homberg, U. (1994). Pigment-dispersing hormone-immunoreactive neurons in the cockroach Leucophaea maderae share properties with circadian pacemaker neurons. J Comp Physiol A, 175, 203–213.
   PubMed Web of Science ®Google Scholar
• Stoleru, D., Peng, Y., Agosto, J., & Rosbash, M. (2004). Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature, 431, 862–868.
   PubMed Web of Science ®Google Scholar
• Tischkau, S. A., Mitchell, J. W., Tyan, S. H., Buchanan, G. F., & Gillette, M. U. (2003). Ca2+/cAMP response element-binding protein (CREB)-dependent activation of Per1 is required for light-induced signaling in the suprachiasmatic nucleus circadian clock. J Biol Chem, 278, 718–723.
   PubMed Web of Science ®Google Scholar
• Tix, S., Minden, J. S., & Technau, G. M. (1989). Pre-existing neuronal pathways in the developing optic lobes of Drosophila. Development, 105, 739–746.
   PubMed Web of Science ®Google Scholar
• Veleri, S., Brandes, C., Helfrich-Förster, C., Hall, J. C., & Stanewsky, R. (2003). A selfsustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr Biol. 13, 1758 –1767.
   PubMed Web of Science ®Google Scholar
• Wiedenmann, G. (1983). Splitting in a circadian activity rhythm: The expression of bilaterally paired oscillators. J Comp Physiol A, 150, 51–60.
   Web of Science ®Google Scholar
• Wu, Y., Cao, G., Pavlicek, B., Luo, X., & Nitabach, M. N. (2008). Phase coupling of a circadian neuropeptide with rest/activity rhythms detected using a membrane-tethered spider toxin. PLoS Biol, 6, e273.
   Web of Science ®Google Scholar
• Wülbeck, C., Grieshaber, E., & Helfrich-Förster, C. (2008). Pigment-dispersing factor (PDF) has different effects on Drosophila's circadian clocks in the accessory medulla and in the dorsal brain. J Biol Rhythms, 23, 409–424.
   PubMed Web of Science ®Google Scholar
• Yasuyama, K., & Meinertzhagen, I. A. (1999). Extraretinal photoreceptors at the compound eye's posterior margin in Drosophila melanogaster. J Comp Neurol, 412, 193–202.
   PubMed Web of Science ®Google Scholar
• Yang, Z., & Sehgal, A. (2001). Role of molecular oscillations in generating behavioural rhythms in Drosophila. Neuron, 29, 453– 467.
   PubMed Web of Science ®Google Scholar
• Yoshii, T., Funada, Y., Ibuki-Ishibashi, T., Matsumoto, A., Tanimura, T., & Tomioka, K. (2004). Drosophila cryb mutation reveals two circadian clocks that drive locomotor rhythm and have different responsiveness to light. J Insect Physiol, 50, 479–488.
   PubMed Web of Science ®Google Scholar
• Yoshii, T., Rieger, D., & Helfrich-Förster, C. (2012). Two clocks in the brain: An update of the morning and evening oscillator model in Drosophila. Prog Brain Res, 199, 59–82.
   PubMed Web of Science ®Google Scholar
• Yoshii, T., Todo, T., Wulbeck, C., Stanewsky, R., & Helfrich-Forster, C. (2008). Cryptochrome is present in the compound eyes and a subset of Drosophila's clock neurons. J Comp Neurol, 508, 952–966.
   PubMed Web of Science ®Google Scholar
• Yoshii, T., Wülbeck, C., Sehadova, H., Veleri, S., Bichler, D., Stanewsky, R., & Helfrich-Förster, C. (2009). The neuropeptide pigment-dispersing factor adjusts period and phase of Drosophila's clock. J Neurosci, 29, 2597–2610.
   PubMed Web of Science ®Google Scholar
• Zerr, D. M., Hall, J. C., Rosbash, M., & Siwicki, K. K. (1990). Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J Neurosci, 10, 2749–2762.
   PubMed Web of Science ®Google Scholar
• Zhang, L., Lear, B. C., Seluzicki, A., & Allada, R. (2009). The CRYPTOCHROME photoreceptor gates PDF neuropeptide signaling to set circadian network hierarchy in Drosophila. Curr Biol, 19, 2050–2055.
   PubMed Web of Science ®Google Scholar