Persistence of morning anticipation behavior and high amplitude morning startle response following functional loss of small ventral lateral neurons in drosophila

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Sheeba, Vasu ^a,b   Fogle, Keri J ^a   Holmes, Todd C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

HUNTINGTIN; HUNTINGTIN Q128; NEUROPEPTIDE; PIGMENT DISPERSING FACTOR; UNCLASSIFIED DRUG; HD PROTEIN, HUMAN; NERVE PROTEIN; NUCLEAR PROTEIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL TISSUE; ANTICIPATION; AROUSAL; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DROSOPHILA; IMMUNOREACTIVITY; LIGHT DARK CYCLE; LOCOMOTION; NERVE CELL; NERVE POTENTIAL; NONHUMAN; OSCILLATORY POTENTIAL; PACEMAKER NERVE CELL; PROTEIN EXPRESSION; STARTLE REFLEX; VENTRAL LATERAL NEURON; ANIMAL; CONFOCAL MICROSCOPY; ELECTROPHYSIOLOGY; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; MOTOR ACTIVITY; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALIA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; DROSOPHILA; ELECTROPHYSIOLOGY; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, CONFOCAL; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS;

EID: 77955376569     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011628     Document Type: Article

References (63)

1. Pittendrigh CS, Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: A clock for all seasons. J Comp Physiol A 106: 333-355.
2. 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.
3. Yoshii T, Funada Y, Ibuki-Ishibashi T, Matsumoto A, Tanimura T, et al. (2004) Drosophila cryb mutation reveals two circadian clocks that drive locomotor rhythm and have different responsiveness to light. J Insect Physiol 50: 479-488.
4. Stoleru D, Nawathean P, Fernandez MP, Menet JS, Ceriani MF, et al. (2007) The Drosophila circadian network is a seasonal timer. Cell 129: 207-219.
5. Stoleru D, Peng Y, Agosto J, Rosbash M (2004) Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431: 862-868.
6. Stoleru D, Peng Y, Nawathean P, Rosbash M (2005) A resetting signal between Drosophila pacemakers synchronizes morning and evening activity. Nature 438: 238-242.
7. 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.
8. Cusumano P, Klarsfeld A, Chelot E, Picot M, Richier B, et al. (2009) PDFmodulated visual inputs and cryptochrome define diurnal behavior in Drosophila. Nat Neurosci 12: 1431-1437.
9. Shafer OT, Taghert PH (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.
10. Lear BC, Zhang L, Allada R (2009) The neuropeptide PDF acts directly on evening pacemaker neurons to regulate multiple features of circadian behavior. PLoS Biol 7: e1000154.
11. Blanchardon E, Grima B, Klarsfeld A, Chelot E, Hardin PE, et al. (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.
12. Renn SC, Park JH, Rosbash M, Hall JC, Taghert PH (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.
13. Nitabach MN, Blau J, Holmes TC (2002) Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109: 485-495.
14. Petri B, Stengl M (1997) Pigment-dispersing hormone shifts the phase of the circadian pacemaker of the cockroach Leucophaea maderae. J Neurosci 17: 4087-4093.
15. Helfrich-Förster C, Tauber M, Park JH, Muhlig-Versen M, Schneuwly S, et al. (2000) Ectopic expression of the neuropeptide pigment-dispersing factor alters behavioral rhythms in Drosophila melanogaster. J Neurosci 20: 3339-3353.
16. Rieger D, Wulbeck 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.
17. Sheeba V, Sharma VK, Gu H, Chou YT, O'Dowd DK, et al. (2008) Pigment dispersing factor-dependent and -independent circadian locomotor behavioral rhythms. J Neurosci 28: 217-227.
18. Wulbeck 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.
19. Rieger D, Shafer OT, Tomioka K, Helfrich-Förster C (2006) Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 26: 2531-2543.
20. Picot M, Cusumano P, Klarsfeld A, Ueda R, Rouyer F (2007) Light activates output from evening neurons and inhibits output from morning neurons in the Drosophila circadian clock. PLoS Biol 5: e315.
21. Nitabach MN, Wu Y, Sheeba V, Lemon WC, Strumbos J, et al. (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.
22. Murad A, Emery-Le M, Emery P (2007) A subset of dorsal neurons modulates circadian behavior and light responses in Drosophila. Neuron 53: 689-701.
23. Sheeba V, Kaneko M, Sharma VK, Holmes TC (2008) The Drosophila circadian pacemaker circuit: Pas De Deux or Tarantella? Crit Rev Biochem Mol Biol 43: 37-61.
24. Nitabach MN, Taghert PH (2008) Organization of the Drosophila circadian control circuit. Curr Biol 18: R84-93.
25. Helfrich-Förster C (2009) Does the morning and evening oscillator model fit better for flies or mice? J Biol Rhythms 24: 259-270.
26. Quintero JE, Kuhlman SJ, McMahon DG (2003) The biological clock nucleus: a multiphasic oscillator network regulated by light. J Neurosci 23: 8070-8076.
27. Schaap J, Albus H, VanderLeest HT, Eilers PH, Detari L, et al. (2003) Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding. Proc Natl Acad Sci U S A 100: 15994-15999.
28. Yamaguchi S, Isejima H, Matsuo T, Okura R, Yagita K, et al. (2003) Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 302: 1408-1412.
29. Cao G, Nitabach MN (2008) Circadian control of membrane excitability in Drosophila melanogaster lateral ventral clock neurons. J Neurosci 28: 6493-6501.
30. Sheeba V, Gu H, Sharma VK, O'Dowd DK, Holmes TC (2008) Circadian- and light-dependent regulation of resting membrane potential and spontaneous action potential firing of Drosophila circadian pacemaker neurons. J Neurophysiol 99: 976-988.
31. Sheeba V, Fogle KJ, Kaneko M, Rashid S, Chou YT, et al. (2008) Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr Biol 18: 1537-1545.
32. Shang Y, Griffith LC, 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.
33. Parisky KM, Agosto J, Pulver SR, Shang Y, Kuklin E, et al. (2008) PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60: 672-682.
34. Chung BY, Kilman VL, Keath JR, Pitman JL, Allada R (2009) The GABA(A) receptor RDL acts in peptidergic PDF neurons to promote sleep in Drosophila. Curr Biol 19: 386-390.
35. Holmes TC, Sheeba V, Mizrak D, Rubovszky B, Dahdal D, eds (2007) Circuitbreaking and behavioral analysis by molecular genetic manipulation of neural activity in Drosophila. Cold Spring Harbor, Cold Spring Harbor Laboratory Press. pp 19-52.
36. Gu H, O'Dowd DK (2006) Cholinergic synaptic transmission in adult Drosophila Kenyon cells in situ. J Neurosci 26: 265-272.
37. Jackson GR, Salecker I, Dong X, Yao X, Arnheim N, et al. (1998) Polyglutamine-expanded human huntingtin transgenes induce degeneration of Drosophila photoreceptor neurons. Neuron 21: 633-642.
38. Lee WC, Yoshihara M, Littleton JT (2004) Cytoplasmic aggregates trap polyglutamine-containing proteins and block axonal transport in a Drosophila model of Huntington's disease. Proc Natl Acad Sci U S A 101: 3224-3229.
39. Steffan JS, Bodai L, Pallos J, Poelman M, McCampbell A, et al. (2001) Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 413: 739-743.
40. Pallos J, Bodai L, Lukacsovich T, Purcell JM, Steffan JS, et al. (2008) Inhibition of specific HDACs and sirtuins suppresses pathogenesis in a Drosophila model of Huntington's disease. Hum Mol Genet 17: 3767-3775.
41. 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.
42. Yang Z, Sehgal A (2001) Role of molecular oscillations in generating behavioral rhythms in Drosophila. Neuron 29: 453-467.
43. Gusella JF, Macdonald ME (2006) Huntington's disease: seeing the pathogenic process through a genetic lens. Trends Biochem Sci 31: 533-540.
44. Lin Y, Stormo GD, Taghert PH (2004) The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J Neurosci 24: 7951-7957.
45. Park JH, Helfrich-Förster C, Lee G, Liu L, Rosbash M, et al. (2000) Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Natl Acad Sci U S A 97: 3608-3613.
46. Peng Y, Stoleru D, Levine JD, Hall JC, Rosbash M (2003) Drosophila freerunning rhythms require intercellular communication. PLoS Biol 1: E13.
47. Wu Y, Cao G, Pavlicek B, Luo X, Nitabach MN (2008) Phase Coupling of a Circadian Neuropeptide With Rest/Activity Rhythms Detected Using a Membrane-Tethered Spider Toxin. PLoS Biol 6: e273.
48. Choi C, Fortin JP, McCarthy E, Oksman L, Kopin AS, et al. (2009) Cellular dissection of circadian peptide signals with genetically encoded membranetethered ligands. Curr Biol 19: 1167-1175.
49. Helfrich-Förster C, Shafer OT, Wulbeck C, Grieshaber E, Rieger D, et al. (2007) Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J Comp Neurol 500: 47-70.
50. Kaneko M, Hall JC (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.
51. Harrisingh MC, Wu Y, Lnenicka GA, Nitabach MN (2007) Intracellular Ca2+ regulates free-running circadian clock oscillation in vivo. J Neurosci 27: 12489-12499.
52. Michel S, Geusz ME, Zaritsky JJ, Block GD (1993) Circadian rhythm in membrane conductance expressed in isolated neurons. Science 259: 239-241.
53. Welsh DK, Logothetis DE, Meister M, Reppert SM (1995) Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14: 697-706.
54. Taghert PH, Shafer OT (2006) Mechanisms of clock output in the Drosophila circadian pacemaker system. J Biol Rhythms 21: 445-457.
55. Wu Y, Cao G, Nitabach MN (2008) Electrical silencing of PDF neurons advances the phase of non-PDF clock neurons in Drosophila. J Biol Rhythms 23: 117-128.
56. Im SH, Taghert PH PDF receptor expression reveals direct interactions between circadian oscillators in drosophila. J Comp Neurol 518: 1925-1945.
57. Veleri S, Brandes C, Helfrich-Förster C, Hall JC, Stanewsky R (2003) A selfsustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr Biol 13: 1758-1767.
58. Steffan JS, Agrawal N, Pallos J, Rockabrand E, Trotman LC, et al. (2004) SUMO modification of Huntingtin and Huntington's disease pathology. Science 304: 100-104.
59. Cowan CM, Raymond LA (2006) Selective neuronal degeneration in Huntington's disease. Curr Top Dev Biol 75: 25-71.
60. Kadener S, Villella A, Kula E, Palm K, Pyza E, et al. (2006) Neurotoxic protein expression reveals connections between the circadian clock and mating behavior in Drosophila. Proc Natl Acad Sci U S A 103: 13537-13542.
61. Yoshii T, Todo T, Wulbeck C, Stanewsky R, Helfrich-Förster C (2008) Cryptochrome is present in the compound eyes and a subset of Drosophila's clock neurons. J Comp Neurol 508: 952-966.
62. Zhang Y, Liu Y, Bilodeau-Wentworth D, Hardin PE, Emery P () Light and temperature control the contribution of specific DN1 neurons to Drosophila circadian behavior. Curr Biol 20: 600-605.
63. Zhang L, Chung BY, Lear BC, Kilman VL, Liu Y, et al. DN1(p) circadian neurons coordinate acute light and PDF inputs to produce robust daily behavior in Drosophila. Curr Biol 20: 591-599.