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«Connectivity, Organization, and Network Coordination of the Drosophila Central Circadian Clock by Zepeng Yao A dissertation submitted in partial ...»

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The various classes of clock neurons are described in the text and labeled in the schematic. The projections of each clock neuron class are depicted in the same color as their soma. The LPN projections have not been described. aMe, accessory medulla. See text for details. The figure is reprinted from Helfrich-Förster, C., Shafer, O.T., Wülbeck, C., Grieshaber, E., Rieger, D., and Taghert, P. (2007). Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J. Comp. Neurol. 500, 47–70, with permission from John Wiley and Sons.

Figure 1.4.

Neurochemistry of the Drosophila clock neuron network.

(a) A schematic of the expression patterns of Cryptochrome (CRY) and PDF receptor (PDFR) within the clock neuron network. Note that CRY and PDFR are co-expressed by many clock neurons. Re, retina; La, lamina; Me, medulla; aMe, accessory medulla. (b) A schematic of the expression of neuropeptides and neurotransmitters by the various clock neurons. PDF, pigmentdispersing factor; ITP, ion transport peptide; NPF, neuropeptide F; sNPF, short neuropeptide F;

IPNa, IPNamide. The expression of choline acetyltransferase (Cha) and vesicular glutamate transporter (GluT) indicates the presence of acetylcholine and glutamate, respectively. dpr, dorsal protocerebrum. This figure is reprinted from Curr. Opin. Insect Sci. 7. Hermann-Luibl, C., and Helfrich-Förster, C. Clock network in Drosophila. 65–70. Copyright (2015), with permission from Elsevier.

1.5 Models of the Drosophila clock neuron network function Studies employing cell ablation and mosaic genetic rescue approaches have suggested a dual-oscillator model of the Drosophila clock network function: The LNvs function collectively as a “morning oscillator” that promotes activity around dawn, whereas the LNds and the 5th sLNv function collectively as an “evening oscillator” that promotes activity around dusk (Grima et al., 2004; Stoleru et al., 2004). The LNvs are essential for robust circadian timekeeping in the absence of environmental cues (Renn et al., 1999), and are thought to be the dominant pacemaker of the clock network under short-day conditions and constant darkness (Stoleru et al., 2005, 2007). In contrast, it is thought that light activates output from the LNds/5th s-LNv, and these neurons become the dominant pacemaker under long-day conditions and constant light (Picot et al., 2007; Stoleru et al., 2007). This dual-oscillator model provides a powerful and elegant model for the functional division of the clock neuron network and the adaptation of the clock neuron network to day-length changes, but it does not account for many experimental observations (discussed by Yoshii et al., 2012).

In addition to the lateral clock neurons, recent work has highlighted the importance of another group of clock neurons, the DN1ps. DN1ps are capable of driving activity rhythms in the presence of light (Murad et al., 2007), and can promote activity both around dawn and dusk depending on the specific light and temperature conditions (Fujii and Amrein, 2010; Zhang et al., 2010a, 2010b). Furthermore, the DN1ps have been implicated as key output neurons of the clock network in the control of activity and sleep rhythms (Cavanaugh et al., 2014; Kunst et al., 2014).

1.6 References Akten, B., Jauch, E., Genova, G.K., Kim, E.Y., Edery, I., Raabe, T., and Jackson, F.R. (2003). A role for CK2 in the Drosophila circadian oscillator. Nat. Neurosci. 6, 251–257.

Allada, R., White, N.E., So, W.V., Hall, J.C., and Rosbash, M. (1998). A mutant Drosophila homolog of mammalian clock disrupts circadian rhythms and transcription of period and timeless. Cell 93, 791–804.

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Cavanaugh, D.J., Geratowski, J.D., Wooltorton, J.R.A., Spaethling, J.M., Hector, C.E., Zheng, X., Johnson, E.C., Eberwine, J.H., and Sehgal, A. (2014). Identification of a circadian output circuit for rest: Activity rhythms in drosophila. Cell 157, 689–701.

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Dunlap, J.C. (1999). Molecular bases for circadian clocks. Cell 96, 271–290.

Fujii, S., and Amrein, H. (2010). Ventral lateral and DN1 clock neurons mediate distinct properties of male sex drive rhythm in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 107, 10590– 10595.

Grima, B., Chélot, E., Xia, R., and Rouyer, F. (2004). Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431, 869–873.

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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.

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Helfrich-Förster, C., Shafer, O.T., Wülbeck, C., Grieshaber, E., Rieger, D., and Taghert, P.

(2007). Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J. Comp. Neurol. 500, 47–70.

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.

Hermann-Luibl, C., and Helfrich-Förster, C. (2015). Clock network in Drosophila. Curr. Opin.

Insect Sci. 7, 65–70.

Herzog, E.D. (2007). Neurons and networks in daily rhythms. Nat. Rev. Neurosci. 8, 790–802.

Huber, R., Hill, S.L., Holladay, C., Biesiadecki, M., Tononi, G., and Cirelli, C. (2004). Sleep homeostasis in Drosophila melanogaster. Sleep 27, 628–639.

Im, S.H., and Taghert, P.H. (2010). PDF receptor expression reveals direct interactions between circadian oscillators in Drosophila. J. Comp. Neurol. 518, 1925–1945.

Im, S.H., Li, W., and 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.

Johard, H.A.D., Yoishii, T., Dircksen, H., Cusumano, P., Rouyer, F., Helfrich-Förster, C., and Nässel, D.R. (2009). Peptidergic clock neurons in Drosophila: ion transport peptide and short neuropeptide F in subsets of dorsal and ventral lateral neurons. J. Comp. Neurol. 516, 59–73.

Kaneko, M., and Hall, J.C. (2000). Neuroanatomy of cells expressing clock genes in Drosophila:

transgenic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections. J. Comp. Neurol. 422, 66–94.

Kloss, B., Price, J.L., Saez, L., Blau, J., Rothenfluh, A., Wesley, C.S., and Young, M.W. (1998).

The Drosophila clock gene double-time encodes a protein closely related to human casein kinase Iepsilon. Cell 94, 97–107.

Kloss, B., Rothenfluh, A., Young, M.W., and Saez, L. (2001). Phosphorylation of PERIOD is influenced by cycling physical associations of DOUBLE-TIME, PERIOD, and TIMELESS in the Drosophila clock. Neuron 30, 699–706.

Kunst, M., Hughes, M.E., Raccuglia, D., Felix, M., Li, M., Barnett, G., Duah, J., and Nitabach, M.N. (2014). Calcitonin gene-related peptide neurons mediate sleep-specific circadian output in Drosophila. Curr. Biol. 24, 2652–2664.

Lee, C., Bae, K., and Edery, I. (1998). The Drosophila CLOCK protein undergoes daily rhythms in abundance, phosphorylation, and interactions with the PER-TIM complex. Neuron 21, 857– 867.

Lee, C., Bae, K., and Edery, I. (1999). PER and TIM inhibit the DNA binding activity of a Drosophila CLOCK-CYC/dBMAL1 heterodimer without disrupting formation of the heterodimer: a basis for circadian transcription. Mol. Cell. Biol. 19, 5316–5325.

Lin, J.-M., Kilman, V.L., Keegan, K., Paddock, B., Emery-Le, M., Rosbash, M., and Allada, R.

(2002). A role for casein kinase 2alpha in the Drosophila circadian clock. Nature 420, 816–820.

Martinek, S., Inonog, S., Manoukian, a S., and Young, M.W. (2001). A role for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 105, 769–779.

McDonald, M.J., Rosbash, M., and Emery, P. (2001). Wild-type circadian rhythmicity is dependent on closely spaced E boxes in the Drosophila timeless promoter. Mol. Cell. Biol. 21, 1207–1217.

Meyer, P., Saez, L., and Young, M.W. (2006). PER-TIM interactions in living Drosophila cells:

an interval timer for the circadian clock. Science 311, 226–229.

Moore-Ede, M.C., Sulzman, F.M., and Fuller, C.A. (1982). The clocks that time us: physiology of the circadian timing system (Harvard University Press).

Murad, A., Emery-Le, M., and Emery, P. (2007). A subset of dorsal neurons modulates circadian behavior and light responses in Drosophila. Neuron 53, 689–701.

Picot, M., Cusumano, P., Klarsfeld, A., Ueda, R., and Rouyer, F. (2007). Light activates output from evening neurons and inhibits output from morning neurons in the Drosophila circadian clock. PLoS Biol. 5, 2513–2521.

Price, J.L., Blau, J., Rothenfluh, a, Abodeely, M., Kloss, B., and Young, M.W. (1998). doubletime is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell 94, 83– 95.

Renn, S.C., Park, J.H., Rosbash, M., Hall, J.C., and 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.

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Shafer, O.T., Rosbash, M., and Truman, J.W. (2002). Sequential nuclear accumulation of the clock proteins period and timeless in the pacemaker neurons of Drosophila melanogaster. J.

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Shafer, O.T., Helfrich-Förster, C., Renn, S.C.P., and Taghert, P.H. (2006). Reevaluation of Drosophila melanogaster’s neuronal circadian pacemakers reveals new neuronal classes. J.

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Shaw, P.J., Cirelli, C., Greenspan, R.J., and Tononi, G. (2000). Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834–1837.

Stoleru, D., Peng, Y., Agosto, J., and Rosbash, M. (2004). Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431, 862–868.

Stoleru, D., Peng, Y., Nawathean, P., and Rosbash, M. (2005). A resetting signal between Drosophila pacemakers synchronizes morning and evening activity. Nature 438, 238–242.

Stoleru, D., Nawathean, P., Fernández, M.D.L.P., Menet, J.S., Ceriani, M.F., and Rosbash, M.

(2007). The Drosophila circadian network is a seasonal timer. Cell 129, 207–219.

Vansteensel, M.J., Michel, S., and Meijer, J.H. (2008). Organization of cell and tissue circadian pacemakers: A comparison among species. Brain Res. Rev. 58, 18–47.

Vosshall, L.B., Price, J.L., Sehgal, A., Saez, L., and Young, M.W. (1994). Block in nuclear localization of period protein by a second clock mutation, timeless. Science 263, 1606–1609.

Wang, G.K., Ousley, A., Darlington, T.K., Chen, D., Chen, Y., Fu, W., Hickman, L.J., Kay, S.A., and Sehgal, A. (2001). Regulation of the cycling of timeless (tim) RNA. J. Neurobiol. 47, 161–175.

Welsh, D.K., Takahashi, J.S., and Kay, S.A. (2010). Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 72, 551–577.

Yoshii, T., Todo, T., Wülbeck, C., Stanewsky, R., and Helfrich-Förster, C. (2008).

Cryptochrome is present in the compound eyes and a subset of Drosophila’s clock neurons. J.

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Yoshii, T., Rieger, D., and 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.

Yu, W., and Hardin, P.E. (2006). Circadian oscillators of Drosophila and mammals. J. Cell Sci.

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Zhang, L., Chung, B.Y., Lear, B.C., Kilman, V.L., Liu, Y., Mahesh, G., Meissner, R.A., Hardin, P.E., and Allada, R. (2010a). DN1p Circadian Neurons Coordinate Acute Light and PDF Inputs to Produce Robust Daily Behavior in Drosophila. Curr. Biol. 20, 591–599.

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Curr. Biol. 20, 600–605.

CHAPTER 2. Analysis of functional neuronal connectivity in the Drosophila brain 1



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