Cellular and Molecular Life Sciences

, Volume 67, Issue 9, pp 1397–1406 | Cite as

A comparative view of insect circadian clock systems



Recent studies revealed that the neuronal network controlling overt rhythms shows striking similarity in various insect orders. The pigment-dispersing factor seems commonly involved in regulating locomotor activity. However, there are considerable variations in the molecular oscillatory mechanism, and input and output pathways among insects. In Drosophila, autoregulatory negative feedback loops that consist of clock genes, such as period and timeless are believed to create 24-h rhythmicity. Although similar clock genes have been found in some insects, the behavior of their product proteins shows considerable differences from that of Drosophila. In other insects, mammalian-type cryptochrome (cry2) seems to work as a transcriptional repressor in the feedback loop. For photic entrainment, Drosophila type cryptochrome (cry1) plays the major role in Drosophila while the compound eyes are the major photoreceptor in others. Further comparative study will be necessary to understand how this variety of clock mechanisms derived from an ancestral one.


Insect Circadian rhythm Clock genes Entrainment Molecular mechanism Neural network 



We thank Dr. Kouji Yasuyama at Kawasaki Medical School for discussion and reading the earlier version of the manuscript, and Miss Tiffanie Chan for linguistic corrections. We also thank anonymous reviewers for their critical reading of the manuscript.


  1. 1.
    Dunlap JC, Loros J, DeCoursey PJ (2004) Chronobiology: biological timekeeping. Sinauer, SunderlandGoogle Scholar
  2. 2.
    Saunders DS (2002) Insect clocks. Elsevier, AmsterdamGoogle Scholar
  3. 3.
    Page TL (1982) Transplantation of the cockroach circadian pacemaker. Science 216:73–75PubMedCrossRefGoogle Scholar
  4. 4.
    Tomioka K, Chiba Y (1992) Characterization of optic lobe circadian pacemaker by in situ and in vitro recording of neuronal activity in the cricket Gryllus bimaculatus. J Comp Physiol A 171:1–7CrossRefGoogle Scholar
  5. 5.
    Fleissner G (1982) Isolation of an insect circadian clock. J Comp Physiol 149:311–316CrossRefGoogle Scholar
  6. 6.
    Truman JW (1974) Physiology of insect rhythms, IV: role of the brain in the regulation of the flight rhythm of the giant silkmoths. J Comp Physiol A 95:281–296CrossRefGoogle Scholar
  7. 7.
    Helfrich-Förster C (2005) Neurobiology of the fruit fly’s circadian clock. Genes Brain Behav 4:65–76PubMedCrossRefGoogle Scholar
  8. 8.
    Kasai M, Chiba Y (1987) Effects of optic lobe ablation on circadian activity in the mosquito, Culex pipiens pallens. Physiol Entomol 12:59–65CrossRefGoogle Scholar
  9. 9.
    Hardin PE (2006) Essential and expendable features of the circadian timekeeping mechanism. Curr Opin Neurobiol 16:686–692PubMedCrossRefGoogle Scholar
  10. 10.
    Helfrich-Förster C (2006) The neural basis of Drosophila’s circadian clock. Sleep Biol Rhythms 4:224–234CrossRefGoogle Scholar
  11. 11.
    Sheeba V (2008) The Drosophila melanogaster circadian pacemaker circuit. J Genet 87:485–493PubMedCrossRefGoogle Scholar
  12. 12.
    Boothroyd CE, Young MW (2008) The in(put)s and out(put)s of the Drosophila circadian clock. N Y Acad Sci 1129:350–357CrossRefGoogle Scholar
  13. 13.
    Sandrelli F, Costa R, Kyriacou CP, Rosato E (2008) Comparative analysis of circadian clock genes in insects. Insect Mol Biol 17:447–463PubMedCrossRefGoogle Scholar
  14. 14.
    Tomioka K, Yoshii T (2006) Entrainment of Drosophila circadian rhythms by temperature cycles. Sleep Biol Rhythms 4:240–247CrossRefGoogle Scholar
  15. 15.
    Grima B, Chélot E, Xia R, Rouyer F (2004) Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431:869–873PubMedCrossRefGoogle Scholar
  16. 16.
    Stoleru D, Peng Y, Agosto J, Rosbash M (2004) Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431:862–868PubMedCrossRefGoogle Scholar
  17. 17.
    Rieger D, Shafer OT, Tomioka K, Helfrich-Förster C (2006) Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 26:2531–2543PubMedCrossRefGoogle Scholar
  18. 18.
    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 USA 105:19587–19594PubMedCrossRefGoogle Scholar
  19. 19.
    Dushay MS, Rosbash M, Hall JC (1989) The disconnected visual system mutations in Drosophila drastically disrupt circadian rhythms. J Biol Rhythms 4:1–27PubMedCrossRefGoogle Scholar
  20. 20.
    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 182:435–453PubMedCrossRefGoogle Scholar
  21. 21.
    Murad A, Emery-Le M, Emery P (2007) A subset of dorsal neurons modulates circadian behavior and light responses in Drosophila. Neuron 53:689–701PubMedCrossRefGoogle Scholar
  22. 22.
    Picot M, Klarsfeld A, Chélot E, Malpel S, Rouyer F (2009) A role for blind DN2 clock neurons in temperature entrainment of the Drosophila larval brain. J Neurosci 29:8312–8320PubMedCrossRefGoogle Scholar
  23. 23.
    Wen C-J, Lee H-J (2008) Mapping the cellular network of the circadian clock in two cockroach species. Arch Insect Biochem Physiol 68:215–231PubMedCrossRefGoogle Scholar
  24. 24.
    Shiga S, Numata H (2009) Roles of PER immunoreactive neurons in circadian rhythms and photoperiodism in the blow fly, Protophormia terraenovae. J Exp Biol 212:867–877PubMedCrossRefGoogle Scholar
  25. 25.
    Lupien M, Marshall S, Leser W, Pollack GS, Honegger H-W (2003) Antibodies against the PER protein of Drosophila label neurons in the optic lobe, central brain, and thoracic ganglia of the crickets Teleogryllus commodus and Teleogryllus oceanics. Cell Tissue Res 312:377–391PubMedCrossRefGoogle Scholar
  26. 26.
    Page TL (1978) Interaction between bilaterally paired components of the cockroach circadian system. J Comp Physiol 124:225–236CrossRefGoogle Scholar
  27. 27.
    Colwell CS, Page TL (1990) A circadian rhythm in neural activity can be recorded from the central nervous system of the cockroach. J Comp Physiol A 166:643–649PubMedCrossRefGoogle Scholar
  28. 28.
    Tomioka K, Chiba Y (1984) Effects of nymphal stage optic nerve severance or optic lobe removal on the circadian locomotor rhythm of the cricket, Gryllus bimaculatus. Zool Sci 1:385–394Google Scholar
  29. 29.
    Tomioka K (1985) Residual circadian rhythmicity after bilateral lamina-medulla removal or optic stalk transection in the cricket, Gryllus bimaculatus. J Insect Physiol 31:653–657CrossRefGoogle Scholar
  30. 30.
    Rence BG, Loher W (1975) Arrhythmically singing crickets: thermoperiodic reentrainment after bilobectomy. Science 190:385–387PubMedCrossRefGoogle Scholar
  31. 31.
    Page TL (1985) Circadian organization in cockroaches: effects of temperature cycles on locomotor activity. J Insect Physiol 31:235–243CrossRefGoogle Scholar
  32. 32.
    Tomioka K, Chiba Y (1989) Photoperiodic entrainment of locomotor activity in crickets (Gryllus bimaculatus) lacking the optic lobe pacemaker. J Insect Physiol 35:827–835CrossRefGoogle Scholar
  33. 33.
    Stanewsky R (2002) Clock mechanisms in Drosophila. Cell Tissue Res 309:11–26PubMedCrossRefGoogle Scholar
  34. 34.
    Cyran SA, Buchsbaum AM, Reddy KL, Lin M-C, Glossop NRJ, Hardin PE, Young MW, Storti RV, Blau J (2003) vrille, Pdp1 and dClock form a second feedback loop in the Drosophila circadian clock. Cell 112:329–341PubMedCrossRefGoogle Scholar
  35. 35.
    Glossop NR, Houl JH, Zheng H, Ng FS, Dudek SM, Hardin PE (2003) VRILLE feeds back to control circadian transcription of clock in the Drosophila circadian oscillator. Neuron 37:249–261Google Scholar
  36. 36.
    Benito J, Zheng H, Hardin PE (2007) PDP1ε functions downstream of the circadian oscillator to mediate behavioral rhythms. J Neurosci 27:2539–2547PubMedCrossRefGoogle Scholar
  37. 37.
    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 21:1675–1686PubMedCrossRefGoogle Scholar
  38. 38.
    Lim C, Chung BY, Pitman JL, McGill JJ, Pradhan S, Lee J, Keegan KP, Choe J, Allada R (2007) Clockwork orange encodes a transcriptional repressor important for circadian-clock amplitude in Drosophila. Curr Biol 17:1082–1089PubMedCrossRefGoogle Scholar
  39. 39.
    Matsumoto A, Ukai-Tadenuma M, Yamada RG, Houl J, Uno KD, Kasukawa T, Dauwalder B, Itoh TQ, Takahashi K, Ueda R, Hardin PE, Tanimura T, Ueda HR (2007) A functional genomics strategy reveals clockwork orange as a transcriptional regulator in the Drosophila circadian clock. Gene Dev 21:1687–1700PubMedCrossRefGoogle Scholar
  40. 40.
    Richier B, Michard-Vanhée 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 23:103–116PubMedCrossRefGoogle Scholar
  41. 41.
    Bae K, Edery I (2006) Regulating a circadian clock’s period, phase and amplitude by phosphorylation: insights from Drosophila. J Biochem 140:609–617PubMedCrossRefGoogle Scholar
  42. 42.
    Weber F (2009) Remodeling the clock: coactivators and signal transduction in the cricadian clockworks. Naturwissenschaften 96:321–337PubMedCrossRefGoogle Scholar
  43. 43.
    Weber F, Hung HC, Maurer C, Kay SA (2006) Second messenger and Ras/MAPK signalling pathways regulate CLOCK/CYCLE-dependent transcription. J Neurochem 98:248–257PubMedCrossRefGoogle Scholar
  44. 44.
    Akten B, Jauch E, Genova GK, Kim EY, Edery I, Raabe T, Jackson FR (2003) A role for CK2 in the Drosophila circadian oscillator. Nat Neurosci 6:251–257PubMedCrossRefGoogle Scholar
  45. 45.
    Meyer P, Saez L, Young MW (2006) PER-TIM interactions in living Drosophila cells: an interval timer for the circadian clock. Science 311:226–229PubMedCrossRefGoogle Scholar
  46. 46.
    Ashmore LJ, Sehgal A (2003) A fly’s eye view of circadian entrainment. J Biol Rhythms 18:206–216PubMedCrossRefGoogle Scholar
  47. 47.
    Nitabach MN, Blau J, Holmes TC (2002) Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109:485–495PubMedCrossRefGoogle Scholar
  48. 48.
    Nitabach MN, Sheeva V, Vera DA, Blau J, Holmes TC (2005) Membrane electrical excitability is necessary for the free-running larval Drosophila circadian clock. J Neurobiol 62:1–13PubMedCrossRefGoogle Scholar
  49. 49.
    Zavodska R, Sehadova H, Sauman I, Sehnal F (2005) Light-dependent PER-like proteins in the cephalic ganglia of an apterygote and a pterygote insect species. Histochem Cell Biol 123:407–418PubMedCrossRefGoogle Scholar
  50. 50.
    Sauman I, Reppert SM (1996) Circadian clock neurons in the silkmoth Antheraea pernyi: novel mechanisms of period protein regulation. Neuron 17:889–900PubMedCrossRefGoogle Scholar
  51. 51.
    Sauman I, Reppert SM (1996) Molecular characterization of prothoracicotropic hormone (PTTH) from the giant silkmoth Antheraea pernyi: developmental appearance of PTTH-expressing cells and relationship to circadian clock cells in central brain. Dev Biol 178:418–429PubMedCrossRefGoogle Scholar
  52. 52.
    Chang DC, McWatters HG, Williams JA, Gotter AL, Levine JD, Reppert SM (2003) Constructing a feedback loop with circadian clock molecules from the silkmoth, Antheraea pernyi. J Biol Chem 278:38149–38158PubMedCrossRefGoogle Scholar
  53. 53.
    Zhu H, Yuan Q, Briscoe AD, Froy O, Casselman A, Reppert SM (2005) The two CRYs of the butterfly. Curr Biol 15:R953–R954PubMedCrossRefGoogle Scholar
  54. 54.
    Yuan Q, Metterville D, Briscoe AD, Reppert SM (2007) Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks. Mol Biol Evol 24:948–955PubMedCrossRefGoogle Scholar
  55. 55.
    Zhu H, Sauman I, Yuan Q, Casselman A, Emery-Le M, Emery P, Reppert SM (2008) Cryptochromes define a novel circadian clock mechanism in monarch butterflies that may underlie sun compass navigation. PLoS Biol 6:138–155CrossRefGoogle Scholar
  56. 56.
    Goto SG, Denlinger DL (2002) Short-day and long-day expression patterns of genes involved in the flesh fly clock mechanism: period, timeless, cycle and cryptochrome. J Insect Physiol 48:803–816PubMedCrossRefGoogle Scholar
  57. 57.
    Miyatake T, Matsumoto A, Matsuyama T, Ueda HR, Toyosato T, Tanimura T (2002) The period gene and allochronic reproductive isolation in Bactrocera cucurbitae. Proc R Soc Lond B 269:2467–2472CrossRefGoogle Scholar
  58. 58.
    Stanewsky R, Kaneko M, Emery P, Beretta B, Wager-Smith K, Kay SA, Rosbash M, Hall JC (1998) The cry b mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95:681–692PubMedCrossRefGoogle Scholar
  59. 59.
    Ishikawa T, Matsumoto A, Kato T Jr, Togashi S, Ryo H, Ikenaga M, Todo T, Ueda R, Tanimura T (1999) DCRY is a Drosophila photoreceptor protein implicated in light entrainment of circadian rhythm. Genes Cells 4:57–65PubMedCrossRefGoogle Scholar
  60. 60.
    Rubin EB, Shemesh Y, Cohen M, Elgavish S, Robertson HM, Bloch G (2006) Molecular and phylogenetic analyses reveal mammalian-like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock. Genome Res 16:1352–1365PubMedCrossRefGoogle Scholar
  61. 61.
    Moriyama Y, Sakamoto T, Karpova SG, Matsumoto A, Noji S, Tomioka K (2008) RNA interference of the clock gene period disrupts circadian rhythms in the cricket Gryllus bimaculatus. J Biol Rhythms 23:308–318PubMedCrossRefGoogle Scholar
  62. 62.
    Moriyama Y, Sakamoto T, Matsumoto A, Noji S, Tomioka K (2009) Functional analysis of the circadian clock gene period by RNA interference in nymphal crickets Gryllus bimaculatus. J Insect Physiol 55:396–400PubMedCrossRefGoogle Scholar
  63. 63.
    Sakamoto T, Uryu O, Tomioka K (2009) The clock gene period plays an essential role in photoperiodic control of nymphal development in the cricket Modicogryllus siamensis. J Biol Rhythms 24:379–390PubMedCrossRefGoogle Scholar
  64. 64.
    Loher W (1972) Circadian control of stridulation in the cricket Teleogryllus commodus Walker. J Comp Physiol 79:173–190CrossRefGoogle Scholar
  65. 65.
    Rence BG, Lisy MT, Garves BR, Quilan BJ (1988) The role of ocelli in circadian singing rhythms of crickets. Physiol Entomol 13:201–212CrossRefGoogle Scholar
  66. 66.
    Helfrich-Förster C, Edwards T, Yasuyama K, Wisotzki B, Schneuwly S, Stanewsky R, Meinertzhagen IA, Hofbauer A (2002) The extraretinal eyelet of Drosophila: development, ultrastracture, and putative circadian function. J Neurosci 22:9255–9266PubMedGoogle Scholar
  67. 67.
    Yoshii T, Todo T, Wülbeck 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 508:952–966PubMedCrossRefGoogle Scholar
  68. 68.
    Ceriani MF, Darlington TK, Staknis D, Mas P, Petti AA, Weitz CJ, Kay SA (1999) Light-dependent sequentation of TIMELESS by CRYPTOCHROME. Science 285:553–556PubMedCrossRefGoogle Scholar
  69. 69.
    Myers MP, Wager-Smith K, Rothenfluh-Hilfiker A, Young MW (1996) Light-induced degradation of TIMELESS and entrainment of the Drosophila circadian clock. Science 271:1736–1740PubMedCrossRefGoogle Scholar
  70. 70.
    Lee C, Parikh V, Itsukaichi T, Bae K, Edery I (1996) Resetting the Drosophila clock by photic regulation of PER and a PER-TIM complex. Science 271:1740–1744PubMedCrossRefGoogle Scholar
  71. 71.
    Hanai S, Hamasaka Y, Ishida N (2008) Circadian entrainment to red light in Drosophila: requirement of Rhodopsin 1 and Rhodopsin 6. NeuroReport 19:1441–1444PubMedCrossRefGoogle Scholar
  72. 72.
    Hanai S, Ishida N (2009) Entrainment of Drosophila circadian clock to green and yellow light by Rh1, Rh5, Rh6 and CRY. NeuroReport 20:755–758PubMedCrossRefGoogle Scholar
  73. 73.
    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 18:377–391PubMedCrossRefGoogle Scholar
  74. 74.
    Zimmerman WF, Pittendrigh CS, Pavlidis T (1968) Temperature compensation of the circadian oscillation in Drosophila pseudoobscura and its entrainment by temperature cycles. J Insect Physiol 14:669–684PubMedCrossRefGoogle Scholar
  75. 75.
    Ikeda M, Tomioka K (1993) Temperature dependency of the circadian locomotor rhythm in the cricket Gryllus bimaculatus. Zool Sci 10:597–604Google Scholar
  76. 76.
    Yoshii T, Fujii K, Tomioka K (2007) Induction of Drosophila behavioral and molecular circadian rhythms by temperature steps in constant light. J Biol Rhythms 22:103–114PubMedCrossRefGoogle Scholar
  77. 77.
    Glaser FT, Stanewsky R (2005) Temperature synchronization of the Drosophila circadian clock. Curr Biol 15:1352–1363PubMedCrossRefGoogle Scholar
  78. 78.
    Collins BH, Rosato E, Kyriacou CP (2004) Seasonal behavior in Drosophila melanogaster requires the photoreceptors, the circadian clock, and phospholipase C. Proc Natl Acad Sci USA 101:1945–1950PubMedCrossRefGoogle Scholar
  79. 79.
    Majercak J, Chen W-F, Edery I (2004) Splicing of the period gene 3′-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol Cell Biol 24:3359–3372PubMedCrossRefGoogle Scholar
  80. 80.
    Majercak J, Sidote D, Hardin PE, Edery I (1999) How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 24:219–230PubMedCrossRefGoogle Scholar
  81. 81.
    Chen W-F, Majercak J, Edery I (2006) Clock-gated photic stimulation of timeless expression at cold temperatures and seasonal adaptation in Drosophila. J Biol Rhythms 21:256–271PubMedCrossRefGoogle Scholar
  82. 82.
    Chiba Y, Uki M, Kawasaki Y, Matsumoto A, Tomioka K (1993) Entrainability of circadian activity of the mosquito Culex pipiens pallens to 24-h temperature cycles, with special reference to involvement of multiple oscillators. J Biol Rhythms 8:211–220PubMedCrossRefGoogle Scholar
  83. 83.
    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 USA 92:612–616PubMedCrossRefGoogle Scholar
  84. 84.
    Rao KR, Riehm JP (1988) Pigment-dispersing hormones: a novel family of neuropeptides from arthropods. Peptides 9(Suppl.):153–159PubMedGoogle Scholar
  85. 85.
    Park JH, Helfrich-Förster C, Lee G, Liu L, Rosbash M, Hall JC (2000) Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Natl Acad Sci USA 97:3608–3613PubMedCrossRefGoogle Scholar
  86. 86.
    Fernández MP, Berni J, Ceriani MF (2008) Circadian remodeling of neuronal circuits involved in rhythmic behavior. PLoS Biol 6:e69PubMedCrossRefGoogle Scholar
  87. 87.
    Renn SCP, 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 99:791–802PubMedCrossRefGoogle Scholar
  88. 88.
    Yoshii T, Wullbeck 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 29:2579–2610CrossRefGoogle Scholar
  89. 89.
    Tomioka K, Miyasako Y, Umezaki Y (2008) PDF as a coupling mediator between the light-entrainable and temperature-entrainable clocks in Drosophila melanogaster. Acta Biol Hung 59(Suppl.):149–155PubMedCrossRefGoogle Scholar
  90. 90.
    Miyasako Y, Umezaki Y, Tomioka K (2007) Separate sets of cerebral clock neurons are responsible for light and temperature entrainment of Drosophila circadian locomotor rhythms. J Biol Rhythms 22:115–126PubMedCrossRefGoogle Scholar
  91. 91.
    Mertens I, Vandingenen A, Johnson EC, Shafer OT, Li W, Trigg JS, Loof AD, Schoofs L, Taghert PH (2005) PDF receptor signaling in Drosophila contributes to both circadian and geotactic behaviors. Neuron 48:213–219PubMedCrossRefGoogle Scholar
  92. 92.
    Hyun S, Lee Y, Hong S-T, Bang S, Paik D, Kang J, Shin J, Lee J, Jeon K, Hwang S (2005) Drosophila GPCR Han is a receptor for the circadian clock neuropeptide PDF. Neuron 48:267–278CrossRefGoogle Scholar
  93. 93.
    Lear BC, Merrill CE, 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 48:221–227PubMedCrossRefGoogle Scholar
  94. 94.
    Petri B, Stengl M (1997) Pigment-dispersing hormone shifts the phase of the circadian pacemaker of the cockroach Leucophaea maderae. J Neurosci 17:4087–4093PubMedGoogle Scholar
  95. 95.
    Lee C-M, Su M-T, Lee H-J (2009) Pigment dispersing factor: an output regulator of the circadian clock in the german cockroach. J Biol Rhythms 24:35–43PubMedCrossRefGoogle Scholar
  96. 96.
    Okamoto A, Mori H, Tomioka K (2001) The role of optic lobe in generation of circadian rhythms with special reference to the PDH immunoreactive neurons. J Insect Physiol 47:889–895CrossRefGoogle Scholar
  97. 97.
    Saifullah ASM, Tomioka K (2003) Pigment-dispersing factor sets the night state of the medulla bilateral neurons in the optic lobe of the cricket, Gryllus bimaculatus. J Insect Physiol 49:231–239PubMedCrossRefGoogle Scholar
  98. 98.
    Abdelsalam S, Uemura H, Umezaki Y, Saifullah ASM, Shimohigashi M, Tomioka K (2008) Characterization of PDF-immunoreactive neurons in the optic lobe and cerebral lobe of the cricket, Gryllus bimaculatus. J Insect Physiol 54:1205–1212PubMedCrossRefGoogle Scholar
  99. 99.
    Pyza E, Meinertzhagen IA (1996) Neurotransmitters regulate rhythmic size changes amongst cells in the fly’s optic lobe. J Comp Physiol A 178:33–45PubMedCrossRefGoogle Scholar
  100. 100.
    Sarov-Blat L, So WV, Liu L, Rosbash M (2000) The Drosophila takeout gene is a novel molecular link between circadian rhythm and feeding behavior. Cell 101:647–656PubMedCrossRefGoogle Scholar
  101. 101.
    Meunier N, Belgacem YH, Martin J-R (2007) Regulation of feeding behaviour and locomotor activity by takeout in Drosophila. J Exp Biol 210:1424–1434PubMedCrossRefGoogle Scholar
  102. 102.
    Matsumoto A (2006) Genome-wide screenings for circadian clock genes in Drosophila. Sleep Biol Rhythms 4:248–254CrossRefGoogle Scholar
  103. 103.
    Giebultowicz JM (1999) Insect circadian clocks: is it all in their heads? J Insect Physiol 45:791–800PubMedCrossRefGoogle Scholar
  104. 104.
    Plautz JD, Kaneko M, Hall JC, Kay SA (1997) Independent photoreceptive circadian clocks throughout Drosophila. Science 278:1632–1635PubMedCrossRefGoogle Scholar
  105. 105.
    Emery IF, Noveral JM, Jamison CF, Siwickii KK (1997) Rhythms of Drosophila period gene in culture. Proc Natl Acad Sci USA 94:4092–4096PubMedCrossRefGoogle Scholar
  106. 106.
    Giebultowicz JM, Hege DM (1997) Circadian clock in Malphigian tubules. Nature 386:664PubMedCrossRefGoogle Scholar
  107. 107.
    Giebultowicz JW, Stanewsky R, Hall JC, Hege DM (2000) Transplanted Drosophila excretory tubules maintain circadian clock cycling out of phase with the host. Curr Biol 10:107–110PubMedCrossRefGoogle Scholar
  108. 108.
    Tanoue S, Krishnan P, Chatterjee A, Hardin PE (2008) G protein-coupled receptor kinase 2 is required for rhythmic olfactory responses in Drosophila. Curr Biol 18:787–794PubMedCrossRefGoogle Scholar
  109. 109.
    Mehnert KI, Cantera R (2008) A peripheral pacemaker drives the circadian rhythm of synaptic boutons in Drosophila independently of synaptic activity. Cell Tiss Res 334:103–109CrossRefGoogle Scholar
  110. 110.
    Ivanchenko M, Stanewsky R, Giebultowicz JM (2001) Circadian photoreception in Drosophila: functions of cryptochrome in periopheral and central clocks. J Biol Rhythms 16:205–215PubMedGoogle Scholar
  111. 111.
    Krishnan B, Levine JD, Lynch MK, Dowse HB, Funes P, Hall JC, Hardin PE, Dryer SE (2001) A new role for cryptochrome in a Drosophila circadian oscillator. Nature 411:313–317PubMedCrossRefGoogle Scholar
  112. 112.
    Emery P, Stanewsky R, Hall JC, Rosbash M (2000) Drosophila cryptochromes: a unique circadian-rhythm photoreceptor. Nature 404:456–457PubMedCrossRefGoogle Scholar
  113. 113.
    Ito C, Goto SG, Shiga S, Tomioka K, Numata H (2008) Peripheral circadian clock for the cuticle deposition rhythm in Drosophila melanogaster. Proc Natl Acad Sci USA 105:8446–8451PubMedCrossRefGoogle Scholar
  114. 114.
    An X, Tebo M, Song S, Frommer M, Raphael KA (2004) The cryptochrome (cry) gene and a mating isolation mechanism in tephritid fruit flies. Genetics 168:2025–2036PubMedCrossRefGoogle Scholar
  115. 115.
    Merlin C, François MC, Queguiner I, Maïbèche-Coisné M, Jacquin-Joly E (2006) Evidence for a putative antennal clock in Mamestra brassicae: Molecular cloning and characterization of two clock genes—period and cryptochrome—in antennae. Insect Mol Biol 15:137–145PubMedCrossRefGoogle Scholar
  116. 116.
    Schuckel J, Siwicki KK, Stengl M (2007) Putative circadian pacemaker cells in the antenna of the hawkmoth Manuca sexta. Cell Tiss Res 330:271–278CrossRefGoogle Scholar
  117. 117.
    Merlin C, Lucas P, Rochat D, François MC, Maïbèche-Coisné M, Jacquin-Joly E (2007) An antennal circadian clock and circadian rhythms in peripheral pheromone reception in the moth Spodoptera littoralis. J Biol Rhythms 22:502–514PubMedCrossRefGoogle Scholar
  118. 118.
    Krishnan P, Dryer SE, Hardin PE (2005) Measuring circadian rhythms in olfaction using electroantennograms. Meth Enzymol 393:495–508PubMedCrossRefGoogle Scholar
  119. 119.
    Krishnan P, Chatterjee A, Tanoue S, Hardin PE (2008) Spike amplitude of single-unit responses in antennal sensillae is controlled by the Drosophila circadian clock. Curr Biol 18:803–807PubMedCrossRefGoogle Scholar
  120. 120.
    Page TL, Koelling E (2003) Circadian rhythm in olfactory response in the antennae controlled by the optic lobe in the cockroach. J Insect Physiol 49:697–707PubMedCrossRefGoogle Scholar
  121. 121.
    Rosén WQ, Han GB, Lofstedt C (2003) The circadian rhythm of the sex-pheromone-mediated behavioral response in the tunip moth, Agrotis segetum, is not controlled at the peripheral level. J Biol Rhythms 18:402–408PubMedCrossRefGoogle Scholar
  122. 122.
    Flecke C, Dolzer J, Krannich S, Stengl M (2006) Perfusion with cGMP analogue adapts the action potential response of pheromone-sensitive sensilla trichoidea of the hawkmoth Manduca sexta in a daytime-dependent manner. J Exp Biol 209:3898–3912PubMedCrossRefGoogle Scholar
  123. 123.
    Saifullah ASM, Page TL (2009) Circadian regulation of olfactory receptor neurons in the cockroach antenna. J Biol Rhythms 24:144–152PubMedCrossRefGoogle Scholar
  124. 124.
    Flecke C, Stengl M (2009) Octopamine and tyramine modulate pheromone-sensitive olfactory sensilla of the hawkmoth Manduca sexta in a time-dependent manner. J Comp Physiol A 195:529–545CrossRefGoogle Scholar
  125. 125.
    Helfrich-Förster C (2002) The circadian system of Drosophila melanogaster and its light input pathways. Zoology 105:297–312PubMedCrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2009

Authors and Affiliations

  1. 1.Graduate School of Natural Science and TechnologyOkayama UniversityOkayamaJapan
  2. 2.Department of BiologyJuntendo University School of MedicineInba-gunJapan

Personalised recommendations