Abstract
The study of the anatomic and physiologic organization of circadian systems of invertebrates has a long and productive history. Modern research can be traced to the work of Janet Harker in the 1950s, who initiated efforts to localize pacemakers and photoreceptors of the circadian system of the cockroach via lesion and transplantation studies. Ultimately, Harker was not successful, but the questions and approaches she pioneered set the stage for subsequent efforts to identify components of invertebrate circadian systems. These efforts have been directed toward answering several fundamental questions about the organization of the circadian system which are the focus of this review. The first of these concerns the nature of the pacemaking system that generates the timing signal. What are the anatomic loci of component oscillators, what is the significance of multioscillator organization, and how does the pacemaking system emerge in development? Second, what are the pathways and mechanisms by which inputs to the pacemaking system regulate its phase and period? Finally, what are the neural and endocrine signals by which the pacemaking system regulates the various processes under its control?
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Abran, D., Anctil, M., & Ali, M. A. (1994). Melatonin activity rhythms in the eyes and cerebral ganglia of Aplysia californica. General and Comparative E,,ndocrinology, 96, 215–222.
Arechiga, H., Cortes, J. L., Garcia, U., & Rodriguez-Sosa, L. (1985). Neuroendocrine correlates of circadian rhythmicity in crustaceans. American Zoologist, 25, 265–274.
Barlow, R. B., Jr. (1983). Circadian rhythms in the Limulus visual system., journal ofNeuroscience, 3, 856–870.
Barlow, R. B., Jr., Balanowski, S. J., Jr., & Brachman, M. L. (1977). Efferent optic nerve fibers mediate circadian rhythms in the Limulus eye. Science, 197, 86–89.
Barlow, R. B., Jr., Kaplan, E., Renninger, G. H., & Saito, T. (1985). Efferent control of circadian rhythms in Limulus lateral eye. Neuroscience Research Supplement, 2, S65—S78.
Barrera-Mera, B. (1976). The effect of cerebroid ganglion lesions on ERG circadian rhythm in the crayfish. Physiology and Behavior, 17, 59–64.
Barrett, R. K., & Page, T. L. (1989). Effects of light on circadian pacemaker development. I. The freerunning period. Journal of Comparative Physiology, 165, 41–49.
Beiswanger, C. M., Sokolove, P. G., & Prior, D. J. (1981). Extraocular photoentrainment of the circadian locomotor rhythm of the garden slug Limax. Journal of Comparative Physiology, 216, 13–23.
Block, G. D., & Davenport, P. A. (1982). Switch from nocturnal to diurnal behavior in the cloudy bubble snail Bulla gouldiana. Journal of Experimental Zoology, 244, 57–63.
Block, G. D., & Page, T. L. (1978). Effects of efferent activity on entrainment of the Aplysia eye. Comparative Biochemistry and Physiology A, 62, 635–638.
Block, G. D., & Roberts, M. H. (1981). Circadian pacemaker in the Bursatella eye: Properties of the rhythm and its effect on locomotor behavior. Journal of Comparative Physiology, 142, 403–410.
Block, G. D., & Wallace, S. (1982). Localization of a circadian pacemaker in the eye of a mollusk, Bulla. Science, 217, 155–157.
Block, G. D., McMahon, D. G., Wallace, S., & Friesen, W. (1984). Cellular analysis of the ocular circadian pacemaker system: A model for retinal organization. Journal of Comparative Physiology, 155, 365–378.
Block, G. D., Roberts, M. H., & Lusska, A. E. (1986). Cellular analysis of circadian pacemaker coupling in Bulla. Journal of Biological Rhythms, 1, 199–217.
Block, G. D., Khalsa, S, Michel, S., Geusz, M., & McMahon, D. (1993). Cellular basis of biological timekeeping. International Review of Cytology, 146, 83–144.
Brady, J. (1975). Circadian changes in central excitability the origin of behavioral rhythms in tsetse flies and other animals? Journal of Entomology, 50, 79–95.
Chiba, Y., & Tomioka, K. (1987). Insect circadian activity with special reference to the localization of the pacemaker. Zoological Science, 4, 945–954.
Christensen, N. D., & Lewis, R. D. (1982). The circadian locomotor rhythm of Hemideina thoracica (Orthoptera; Stenopelmatidae): The circadian clock as a population of interacting oscillators. Physiological Entomology, 7, 1–13.
Colwell, C. S. (1990). Light and serotonin interact in affecting the circadian system of Aplysia. Journal of Comparative Physiology A, 167, 841–845.
Colwell, C. S., & Page, T. L. (1990). A circadian rhythm in neural activity can be recorded from the central nervous system of the cockroach. Journal of Comparative Physiology, 166, 643–649.
Colwell, C. S., Khalsa, S. B. S., & Block, G. D. (1992a). Cellular mechanisms of entrainment. Chronobiology International, 3, 163–179.
Colwell, C. S., Khalsa, S. B. S., & Block, G. D. (1992b). FMRFamide modulates the action of phase shifting agents on the ocular circadian pacemakers of Aplysia and Bulla. Journal of Comparative Physiology A, 170, 211–215.
Corrent, G., & Eskin, A. (1982). Transmitter-like action of serotonin in phase shifting a rhythm from the Aplysia eye. American Journal of Physiology, 242, R333—R338.
Corrent, G., McAdoo, D. J., & Eskin, A. (1978). Serotonin phase shifts the circadian rhythm from the Aplysia eye. Science, 202, 977–979.
Cymborowski, B. (1970). Investigations on the neurohormonal factors controlling circadian rhythm of locomotor activity in the house cricket (Acheta domesticus L.). I. The role of the brain and the subesophageal ganglion. Zoologica Poloniae, 20, 103–126.
Cymborowski, B. (1973). Control of the circadian rhythm of locomotor activity in the house cricket. Journal of Insect Physiology, 19, 1423–1440.
Cymborowski, B. (1981). Transplantation of circadian pacemaker in the house cricket, Acheta domesticus L. Journal of Interdisciplinary Cycle Research, 12, 133–140.
Cymborowski, B., Muszynska-Pytel, M., Porcheron, P., & Cassier, P. (1991). Haemolymph ecdysteroid titres controlled by a circadian clock mechanism in larvae of the wax moth, Galleria mellonella. Journal of Insect Physiology, 37, 35–40.
Cymborowski, B., Lewis, R. D., Hong, S. F., & Saunders, D. S. (1994). Circadian locomotor activity rhythms and their entrainment to light—dark cycles continue in flies (Calliphora vicina) surgically deprived of their optic lobes. Journal of Insect Physiology, 40, 501–510.
Dumortier, B. (1972). Photoreception in the circadian rhythm of stridulatory activity in Ephippiger (Ins., Orthoptera): Likely existence of two photoreceptive systems. Journal of Comparative Physiology, 77, 80–112.
Dushay, M. S., Rosbash, M., & Hall, J. (1989). The disconnected visual system mutations in Drosophila melanogaster drastically disrupt circadian rhythms. Journal of Biological Rhythms, 4, 1–28.
Engelmann, W., & Honegger, H. W. (1966). Tagesperiodische Schlüpfryhthmik liner augenlosen Droso phila melanogaster-Mutante. Naturwissenschaften, 53, 588.
Eskin, A. (1971). Properties of the Aplysia visual system: In vitro entrainment of the circadian rhythm and centrifugal regulation of the eye. Zeitschrift für Vergleichende Physiologie, 74, 353–371.
Eskin, A. (1972). Phase shifting a circadian rhythm in the eye of Aplysia by high potassium pulses. Journal of Comparative Physiology, 80, 353–376.
Eskin, A. (1977). Neurophysiological mechanisms involved in photo entrainment of the circadian rhythm from the Aplysia eye. Journal of Neurobiology, 8, 273–299.
Eskin, A., & Harcombe, E. (1977). Eye of Navanax. Optic activity, circadian rhythm and morphology. Comparative Biochemistry and Physiology, 57A, 443–449.
Eskin, A., Takahashi, J., Zatz, M., & Block, G. D. (1984). Cyclic GMP mimics the effects of light on a circadian pacemaker in the eye of Aplysia. Journal of Neuroscience, 4, 2466–2471.
Ewer, J., Frisch, B., Hamblen-Coyle, M. J., Rosbash, M., & Hall, J. (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. Journal of Neuroscience, 12, 3321–3349.
Ferrell, B. R., & Reitcheck, B. G. (1993). Circadian changes in cockroach ommatidial structure. Journal of Comparative Physiology, 173, 549–556.
Fleissner, G. (1977a). Entrainment of the scorpion’s circadian rhythm via the median eyes. Journal of Comparative Physiology, 118, 93–99.
Fleissner, G. (1977b). Scorpion lateral eyes: Extremely sensitive receptors of zeitgeber stimuli. Journal of Comparative Physiology, 118, 101–108.
Fleissner, G. (1982). Isolation of an insect circadian clock. Journal of Comparative Physiology, 149, 311–316.
Fleissner, G. (1983). Efferent neurosecretory fibres as pathways for circadian clock signals in the scorpion. Naturwissenschaften, 70, S366.
Fleissner, G. (1986). Die innere Uhr and der Lichtsinn von Skorpionen and Kafern. Naturwissenschaften, 73, 78–88.
Fleissner, G., & Fleissner, G. (1985). Neurobiology of a circadian clock in the visual system of scorpions. In F. G. Barth (Ed.), Neurobiology of arachnids (pp. 251–375). Berlin: Springer-Verlag.
Fleissner, G., Fleissner, G., & Frisch, B. (1993). A new type of putative non-visual photoreceptor in the optic lobe of beetles. Cell Tissue Research, 273, 435–445.
Foster, R. G., Provencio, I., Hudson, D., Fiske, S., De Grip, W., & Menaker, M. (1991). Circadian photo reception in the retinally degenerate mouse (rd/rd). Journal of Comparative Physiology, 169, 39–50.
Frank, K. D., & Zimmerman, W. E (1969). Action spectra for phase shifts of a circadian rhythm in Drosophila. Science, 163, 688–689.
Fuentes-Pardo, B., & Inclan-Rubio, V. (1987). Caudal photoreceptors synchronize the circadian rhythms in crayfish-I. Synchronization or the ERG and locomotor circadian rhythms. Comparative Biochemistry and Physiology, 86A, 523–527.
Fujishita, M., & Ishizaki, H. (1981). Circadian clock and prothoracicotropic hormone secretion in relation to the larval-larval ecdysis rhythm of the saturnid Samia cynthia ricini. Journal of Insect Physiology, 27, 122–128.
Geusz, M. E., & Block, G. D. (1992). The retinal cells generating the circadian small spikes in the Bulla optic nerve. Journal of Biological Rhythms, 7, 255–268.
Geusz, M. E., & Page, T. L. (1990). The circadian rhythm and photosensitivity of small impulses of the Bulla eye. Journal of Comparative Physiology, 166, 795–801.
Geusz, M. E., & Page, T. L. (1991). An opsin-based photopigment mediates phase shifts of the Bulla circadian pacemaker. Journal of Comparative Physiology A, 168, 565–570.
Geusz, M. E., Foster, R. G., Lawrence, M. D., Sc Block, G. D. (1991). Opsin-like immunoreactivity in the putative pacemaker neurons in the Bulla eye. Society for Neuroscience Abstracts, 17, 1240–1241.
Giebultowicz, J. M., Bell, R. A., & Imberski, R. B. (1988). Circadian rhythm of sperm movement in the male reproductive tract of the gypsy moth Lymantria dispar. Journal of Insect Physiology, 34, 527–532.
Giebultowicz, J. M., Riemann, J. G., Raina, A. K, & Ridgway, R. L. (1989). Circadian system controlling release of sperm in the insect testes. Science, 245, 1098–1100.
Gordon, W. H., Larimer, J. L., & Page, T. L. (1977). Circumesophageal interneurons required for reflexive and circadian locomotor behaviors in the crayfish. Journal of Comparative Physiology A, 116, 227–238.
Handler, A. M., & Konopka, R. J. (1979). Transplantation of a circadian pacemaker in Drosophila. Nature, 279, 236–238.
Hanna, W. J. B., Horne, J. A., Sc Renninger, G. H. (1988). Circadian photoreceptor organs in Limulus. Journal of Comparative Physiology A, 162, 133–140.
Helfrich, C. (1986). Role of the optic lobes in the regulation of the locomotor activity rhythm of Drosophila melanogaster. Behavioral analysis of neural mutants. Journal of Neurogenetics, 3, 321–343.
Helfrich, C., & Engelmann, W. (1983). Circadian locomotor activity in Drosophila melanogaster mutants “sine oculis” and “small optic lobes.” Physiological Entomology, 8, 257–272.
Helfrich, C., Cymborowski, B., & Engelmann, W. (1985). Circadian activity rhythm of the house fly continues after optic tract severance and lobectomy. Chronobiology International, 2, 19–32.
Helfrich-Forster, 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 with the brain of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA, 92, 612–616.
Helfrich-Forster, 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. Journal of Comparative Neurology, 337, 177–190.
Homberg, U., Wurden, S., Dircksen, H., & Rao, K. R. (1991). Comparative anatomy of pigment-dispersing hormone immunoreactive neurons in the brain of orthopteroid insects. Cell Tissue Research, 266, 343–357.
Horne, J. A., & Renninger, G. H. (1988). Circadian photoreceptor organs in Limulus. Journal of Comparative Physiology A, 162, 127–132.
Huber, E (1965). Neural integration. In M. Rockstein (Ed.), The physiology ofInsecta (Vol. 2, pp. 333–406). New York: Academic Press.
Hudson, D., & Lickey, M. (1980). Internal desynchronization between two identified circadian oscillators in Aplysia. Brain Research, 183, 481–485.
Ishizaki, H., Mizoguchi, A., & Fujishita, M. (1984). Circadian clock control of hormone secretion in Sarnia Cynthia ricini. In R. Porter & G. Collins (Eds.), Photoperiodic regulation of insect and molluscan hormones (pp. 136–145). London: Pitman.
Jacklet, J. W. (1969). Circadian rhythm of optic nerve impulses recorded in darkness from isolated eye of Aplysia. Science, 164, 562–563.
Jacklet, J. W. (1971). A circadian rhythm in the optic nerve impulses from an isolated eye in darkness. In M. Menaker (Ed.), Biochronometry (pp. 351–362). Washington DC: National Academy of Sciences.
Jacklet, J. W. (1974). The effects of constant light and light pulses on the circadian rhythm in the eye of Aplysia. Journal of Comparative Physiology, 90, 33–45.
Jacklet, J. W. (1980). Light sensitivity of the rhinophores and eyes of Aplysia. Journal of Comparative Physiology A, 136, 257–262.
Jacklet, J. W., & Barnes, S. (1993). Photoresponsive pacemaker neurons from the dissociated retina of Aplysia. Neuroreport, 5, 209–212.
Jacklet, J. W., & Colquhoun, W. (1983). Ultrastructure of photoreceptors and circadian pacemaker neurons in the eye of a gastropod, Bulla. Journal of Neurocytology, 12, 373–396.
Jacklet, J. W., Klose, M., & Goldberg, M. (1987). FMRF-amide-like immunoreactive efferent fibers and FMRF-amide suppression of pacemaker neurons in eyes of Bulla. Journal of Neurobiology, 18, 433–449.
Jordon, W. P., Lickey, M., & Hiaasen, S. (1985). Circadian organization in Aplysia: Internal desynchronize tion and amplitude of locomotor rhythm. Journal of Comparative Physiology, 156, 293–303.
Kasai, M., & Chiba, Y. (1987). Effects of optic lobe ablation on circadian activity in the mosquito, Culex pipiens pollens. Physiological Entomology, 12, 59–65.
Kass, L., & Barlow, R. B., Jr. (1984). Efferent neurotransmission of circadian rhythms in Limulus lateral eye. Journal of Neuroscience, 4, 908–917.
Kass, L., & Barlow, R. B., Jr. (1992). A circadian clock in the Limulus brain transmits synchronous efferent signals to all eyes. Visual Neuroscience, 9, 493–504.
Kavaliers, M. (1981). Circadian and ultradian activity rhythms of a freshwater gastropod, Helisoma trivolvis The effects of social factors and eye removal. Behavioral and Neural Biology, 32, 350–363.
Khalsa, S. B. S., & Block, G. D. (1988). Calcium channels mediate phase shifts of the Bulla circadian pacemaker. Journal of Comparative Physiology, 164, 195–206.
Khalsa, S. B. S., & Block, G. D. (1990). Calcium in phase control of the Bulla circadian pacemaker. Brain Research, 506, 40–45.
Klemm, E., & Ninnemann, H. (1976). Detailed action spectrum for the delay shift in pupae emergence of Drosophila pseudoobscura. Photochemistry and Photobiology, 24, 369–371.
Koehler, W. K., & Fleissner, G. (1978). Internal desynchronization of bilaterally organized circadian oscillators in the visual system of insects. Nature, 274, 708–710.
Koumenis, C., & Eskin, A. (1992). The hunt for mechanisms of circadian timing in the eye of Aplysia. Chronobiology International, 9, 201–221.
Larimer, J., & Smith, J. T. F. (1980). Circadian rhythm of retinal sensitivity in crayfish: Modulation by the cerebral and optic ganglia. Journal of Comparative Physiology, 136, 313–326.
Lickey, M., & Wozniak, J. (1979). Circadian organization in Aplysia explored with red light, eye removal, and behavioral recording. Journal of Comparative Physiology, 131, 169–177.
Lickey, M. E., Block, G. D., Hudson, D. J., & Smith, J. T. (1976). Circadian oscillators and photoreceptors in the gastropod, Aplysia. Photochemistry and Photobiology, 23, 253–273.
Lickey, M., Wozniak, J., Block, G., Hudson, D., & Augter, G. (1977). The consequences of eye removal for the circadian rhythm of behavioral activity in Aplysia. Journal of Comparative Physiology, 118, 121–143.
Lickey, M., Hudson, D., & Hiaasen, S. (1983). Circadian organization in Aplysia: Relations between locomotor rhythm and eye rhythms after cutting both, one, or neither optic nerves. Journal of Comparative Physiology, 153, 133–143.
Linn, C. E., Poole, K. R., Wen-Q, W., & Roelofs, W. L. (1995). Circadian changes in melatonin in the nervous system and hemolymph of the cabbage looper moth, Tricoplusia ni. Journal of Comparative Physiology, 176, 761–771.
Loher, W. (1972). Circadian control of stridulation in the cricket, Teleogryllus commodus Walker. Journal of Comparative Physiology, 79, 173–190.
Lober, W. (1974). Circadian control of spermatophore formation in the cricket Teleogryllus commodus Walker. Journal of Insect Physiology, 20, 1155–1172.
Loher, W., & Chandrashekaran, M. K. (1970). Circadian rhythmicity in the oviposition of the grasshopper Chorthippus curtipennis. Journal of Insect Physiology, 16, 1677–1688.
Lukat, R. (1978). Circadian growth layers in the cuticle of behaviorally arrhythmic cockroaches (Blaberus fuscus, Ins., Blattoidea). Experientia, 34, 477.
Lukat, R., & Weber, F. (1979). The structure of locomotor activity in bilobectomized cockroaches (Blaberus fuscus). Experientia, 35, 38–39.
McMahon, D. G., & Block, G. D. (1987a). The Bulla ocular circadian pacemaker I: Pacemaker neuron membrane potential controls phase through a calcium dependent mechanism. Journal of Comparative Physiology, 161, 35–346.
McMahon, D. G., & Block, G. D. (1987b). The Bulla ocular circadian pacemaker II: Pacemaker membrane potential regulates the freerunning period of the oscillator. Journal of Comparative Physiology, 161, 347–354.
Michel, S., Geusz, M. E., Zaritsky, J. J., & Block, G. D. (1993). Circadian rhythm in membrane conductance expressed in isolated neurons. Science, 259, 239–241.
Minis, D. H., & Pittendrigh, C. S. (1968). Circadian oscillation egg hatching: Its ontogeny during embryogenesis of a moth. Science, 159, 534–536.
Mizoguchi, A., & Ishizaki, H. (1982). Prothoracic glands of the saturniid moth Sarnia cynthia ricini possess a circadian clock controlling gut purge timing. Proceedings of the National Academy Sciences of the USA, 79, 2726–2730.
Mizoguchi, A., & Ishizaki, H. (1984a). Circadian clock controlling gut-purge rhythm of the saturniid Sarnia cynthia ricini: Its characterization and entrainment mechanism. Journal of Comparative Physiology A, 155, 639–647.
Mizoguchi, A., & Ishizaki, H. (1984b). Further evidence for the presence of a circadian clock in the prothoracic glands of the saturnid moth Sarnia cynthia ricini: Decapitated larvae can respond to light-changes. Development, Growth and Differentiation, 26, 607–611.
Mote, M. I., & Black, K. R. (1981). Action spectrum and threshold sensitivity of entrainment of circadian running activity in the cockroach Periplaneta americana. Photochemistry and Photobiology, 34, 257–265.
Mote, M. I., & Goldsmith, T. H. (1970). Spectral sensitivities of color receptors in the compound eye of Periplaneta americana. Journal of Experimental Zoology, 173, 137–146.
Nadakavukaran, J., Lickey, M., & Jordon, W. (1986). Regulation of the circadian clock in the Aplysia eye. Journal of Neuroscience, 6, 14–21.
Nelson, D. E., & Takahashi, J. S. (1991). Sensitivity and integration in a visual pathway for circadian entrainment in the hamster (Mesocricetus auratus). Journal of Physiology, 439, 115–145.
Nishiitsutsuji-Uwo, J., Sc Pittendrigh, C. S. (1968a). Central nervous system control of circadian rhythmicity in the cockroach. II. The pathway of light signals that entrain the rhythms. Zeitschrift gür Vergleichende Physiologie, 58, 1–13.
Nishiitsutsuji-Uwo, J., & Pittendrigh, C. S. (1968b). Central nervous system control of circadian rhythmicity in the cockroach. III. The optic lobes, locus of the driving oscillation? Zeitschriftfür Vergleichende Physiologie, 58, 14–46.
Nishiitsutsuji-Uwo, J., Petropulos, S. F., & Pittendrigh, C. S. (1967). Central nervous system control of circadian rhythmicity in the cockroach. I. Role of the pars intercerebralis. Biological Bulletin, 133, 679–696.
Page, T. L. (1978). Interactions between bilaterally paired components of the cockroach circadian system. Journal of Comparative Physiology, 124, 225–236.
Page, T. L. (1981a). Effects of localized low-temperature pulses on the cockroach circadian pacemaker. American Journal of Physiology, 240, R144–R150.
Page, T. L. (1981b). Neural and endocrine control of circadian rhythmicity in invertebrates. In J. Aschoff (Ed.), Handbook of behavioral neurobiology. Vol. 4. Biological rhythms (pp. 145–172). New York: Plenum Press.
Page, T. L. (1982a). Extraretinal photoreception in entrainment and photoperiodism in invertebrates. Experientia, 38, 1007–1013.
Page, T. L. (1982b). Transplantation of the cockroach circadian pacemaker. Science, 216, 73–75.
Page, T. L. (1983a). Regeneration of the optic tracts and circadian pacemaker activity in the cockroach Leucophaea maderae. Journal of Comparative Physiology, 152, 231–240.
Page, T. L. (1983b). Effects of optic-tract regeneration on internal coupling in the circadian system of the cockroach. Journal of Comparative Physiology, 153, 231–240.
Page, T. L. (1984). Neuronal organization of a circadian clock in the cockroach Leucophaea maderae. In R. Porter & G. Collins (Eds.), Photoperiodic regulation of insect and molluscan hormones (pp. 115–135). London: Pitman.
Page, T. L. (1985a). Clocks and circadian rhythms in insects. In G. Kerkut & L. Gilbert (Eds.), Comprehensive insect biochemistry, physiology, and pharmacology VI. Sensory physiology (pp. 577–652). Oxford: Pergamon Press.
Page, T. L. (1985b). Circadian organization in the cockroach: Effects of temperature cycles on locomotor activity. Journal of Insect Physiology, 31, 235–242.
Page, T. L. (1988). Circadian organization and the representation of circadian information in the nervous systems of invertebrates. In J. M. Hekkens, G. A. Kerkhof, & W. J. Rietveld (Eds.), Trends in chronobiology (pp. 67–79). Oxford: Pergamon Press.
Page, T. L. (1989). Masking in invertebrates. Chronobiology International, 6, 3–11.
Page, T. L. (1990a). Circadian organization in the cockroach. In I. Huber (Ed.), Cockroaches as models for neurobiology: Applications in biomedical research (pp. 225–246). Boca Raton, FL: CRC Press.
Page, T. L. (1990b). Circadian rhythms of locomotor activity in cockroach nymphs: Freerunning and entrainment. Journal of Biological Rhythms, 5, 273–290.
Page, T. L. (1991). Developmental manipulation of the circadian pacemaker in the cockroach: Relation ship between pacemaker period and response to light. Physiological Entomology, 16, 243–248.
Page, T. L., & Barrett, R. K. (1989). Effects of light on circadian pacemaker development. II. The response to light. Journal of Comparative Physiology, 165, 51–59.
Page, T. L., & Larimer, J. L. (1972). Entrainment of the circadian locomotor activity rhythm in crayfish. Journal of Comparative Physiology, 78, 107–120.
Page, T. L., & Larimer, J. L. (1975a). Neural control of circadian rhythmicity in the crayfish I. The locomotor activity rhythm. Journal of Comparative Physiology, 97, 59–80.
Page, T. L., & Larimer, J. L. (1975b). Neural control of circadian rhythmicity in the crayfish II. The ERG amplitude rhythm. Journal of Comparative Physiology, 97, 81–96.
Page, T. L., & Larimer, J. L. (1976). Extraretinal photoreception in entrainment of crustacean rhythms. Photochemistry and Photobiology, 23, 245–251.
Page, T. L., & Nalovic, K. G. (1992). Properties of mutual coupling between the two circadian pacemakers in the eyes of the mollusk Bulla gouldiana. Journal of Biological Rhythms, Z 23 213–226.
Page, T. L., Caldarola, P. C., & Pittendrigh, C. S. (1977). Mutual entrainment of bilaterally distributed circadian pacemakers. Proceedings of the National Academy of Sciences of the USA, 74, 1277–1281.
Page, T. L., Wassmer, G., Fletcher, J., & Block, G. (1997). Aftereffects of entrainment on the period of the pacemaker in the eye of the mollusk Bulla gouldiana. Journal of Biological Rhythms, 12, 218–225.
Pittendrigh, C. S. (1976). Circadian clocks: What are they? In J. W. Hastings & H. Schweiger (Eds.), Molecular basis of circadian rhythms (pp. 11–48). Berlin: Dahlem Konferenzen.
Pittendrigh, C. S. (1981). Circadian organization and the photoperiodic phenomena. In B. K. Follett & D. E. Follett (Eds.), Biological clocks in seasonal reproductive cycles (pp. 1–35). Bristol, England: Wright.
Pollard, T. G., & Larimer, J. L. (1977). Circadian rhythmicity of heart rate in the crayfish, Procambarus clarkii. Journal of Comparative Physiology, 57, 221–226.
Raju, U., Yeung, S., & Eskin, A. (1990). Involvement of proteins in light resetting ocular circadian oscillators of Aplysia. American Journal of Physiology, 258, R256–R262.
Raju, U., Nunez-Regueiro, M., Cook, R., & Eskin, A. (1993). Identification of an annexin-like protein and its possible role in the Aplysia eye circadian system. Journal of Neurochemistry, 61, 1236–1245.
Rence, B., & Loher, W. (1975). Arrhythmically singing crickets: Thermoperiodic reentrainment after bilobectomy. Science, 190, 385–387.
Riemann, J. G., Thorson, B. J., & Rudd, R. L. (1974). Daily cycle of release of sperm from the testes of the Mediterranean flour moth. Journal of Insect Physiology, 20, 195–207.
Roberts, M. H., & Block, G. D. (1987). Analysis of mutual circadian pacemaker coupling between the two eyes of Bulla. Journal of Biological Rhythms, 15, 55–75.
Roberts, M. H., & Moore, R. (1987). Localization of neuropeptides in efferent terminals in the eye in the marine snail, Bulla. Cell Tissue Research, 248, 67–73.
Roberts, M. H., Block, G. D., & Lusska, A. E. (1987). Comparative studies of circadian pacemaker coupling in opisthobranch mollusks. Brain Research, 423, 286–292.
Roberts, S. K. (1962). Circadian activity in cockroaches. II. Entrainment and phase-shifting. Journal of Cellular and Comparative Physiology, 59, 175–186.
Roberts, S. K. (1965). Photoreception and entrainment of cockroach activity rhythms. Science, 148, 958–959.
Roberts, S. K. (1966). Circadian activity rhythms in cockroaches. III. The role of endocrine and neural factors. Journal of Cellular and Comparative Physiology, 67, 473–486.
Roberts, S. K. (1974). Circadian rhythms in cockroaches: Effects of optic lobe lesions. Journal of Comparative Physiology, 88, 21–30.
Roberts, S. K, Skopik, S. D., & Driskill, R. J. (1971). Circadian rhythms in cockroaches: Does brain hormone mediate the locomotor cycle? In M. Menaker (Ed.), Biochronometry (pp. 505–515). Washington, DC: National Academy of Sciences.
Sanchez, J. A., & Fuentes-Pardo, B. (1977). Circadian rhythm of the amplitude of the electroretinogram in the isolated eyestalk of the crayfish. Comparative Biochemistry and Physiology, 56, 601–605.
Sandeman, D. C., Sandeman, R. E., & de Couet, H. G. (1990). Extraretinal photoreceptors in the brain of the crayfish Cherax destructor. Journal of Neurobiology, 21, 619–629.
Sasaki, M., Yamazaki, S., & Chiba, K. (1987). Brain photoreception in the calling rhythm of a noctuid moth, Anadevidia peponiv Method of making eyeless moth and micro-irradiation of brain with fiber optics. Bulletin of the Faculty of Agriculture, 27, 81–90.
Schulz, W., Schluter, U., & Seifert, G. (1984). Extraocular photoreceptors in the brain of Epilachna varivestis (Coleoptera, Coccinellidae). Cell Tissue Research, 236, 317–320.
Sehgal, A., Price, J., & Young, M. W. (1992). Ontogeny of a biological clock in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA, 89, 1423–1427.
Shimizu, L, & Matsui, K. (1983). Photoreceptions in the eclosion of the silkworm Bombyx mori. Photochemistry and Photobiology, 37, 409–413.
Sokolove, P. G. (1975). Localization of the cockroach optic lobe circadian pacemaker with microlesions. Brain Research, 87, 13–21.
Sokolove, P. G., & Loher, W. (1975). Role of eyes, optic lobes, and pars intercerebralis in locomotory and stridulatory circadian rhythms of Teleogryllus commodus. Journal of Insect Physiology, 21, 785–799.
Steel, G. H., & Ampleford, E. J. (1984). Circadian control of haemolymph ecdysteroid titres and the ecdysis rhythm in Rhodnius prolixus. In R. Porter & G. Collins (Eds.), Photoperiodic regulation of insect and molluscan hormones (pp. 150–163). London: Pitman.
Stengl, M. (1995). Pigment-dispersing hormone-immunoreactive fibers persist in crickets which remain rhythmic after bilateral transection of the optic stalks. Journal of Comparative Physiology, 176, 217–228.
Stengl, M., & Homberg, U. (1994). Pigment-dispersing hormone immunoreactive neurons in the cockroach Leucophaea maderae share properties with circadian pacemaker neurons. Journal of Comparative Physiology, 175, 203–213.
Strumwasser, F. (1973). Neural and humoral factors in the temporal organization of behavior. Physiologist, 16, 9–42.
Takahashi, J. S., Nelson, D., & Eskin, A. (1989). Immunocytochemical localization of serotonergic fibers innervating the ocular circadian system of Aplysia. Neuroscience, 28, 139–147.
Thorson, B. J., & Riemann, J. G. (1977). Abdominally entrained periodicities of testis and vas deferens activity in the Mediterranean flour moth. Journal of Insect Physiology, 23, 1189–1197.
Tomioka, K. (1985). Residual circadian rhythmicity after bilateral lamina-medulla removal or optic stalk transection in the cricket Gryllus bimaculatus. Journal of Insect Physiology, 31, 653–657.
Tomioka, K, & Chiba, Y. (1982). Persistence of circadian ERG rhythm in the cricket with optic tract severed. Naturwissenschaften, 69, 395–396.
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. Zoological Science, 1, 375–382.
Tomioka, K, & Chiba, Y. (1986). Circadian rhythm in the neurally isolated lamina-medulla complex of the cricket Gryllus bimaculatus. Journal of Insect Physiology, 32, 747–755.
Tomioka, K., & Chiba, Y. (1992). Characterization of an optic lobe circadian pacemaker by in situ and in vitro recording of neural activity in the cricket, Gryllus bimaculatus. Journal of Comparative Physiology, 171, 1–8.
Tomioka, K, Okada, Y., & Chiba, Y. (1990). Distribution of circadian photoreceptors in the compound eye of the cricket Gryllus bimaculatus. Journal of Biological Rhythms, 5, 303–314.
Tomioka, K, Yamada, K., Yokoyama, S., & Chiba, Y. (1991). Mutual interactions between optic lobe circadian pacemakers in the cricket Gryllus bimaculatus. Journal of Comparative Physiology, 169, 291–298.
Tomioka, K., Nakamichi, Y., &Yukizane, M. (1994). Optic lobe circadian pacemaker sends its information to the contralateral optic lobe in the cricket Gryllus bimaculatus. Journal of Comparative Physiology, 175, 381–388.
Truman, J. W. (1971a). Circadian rhythms and physiology with special reference to neuroendocrine processes in insects. In Proceedings of the International Symposium on Circadian Rhythmicity (pp. 111–135). Wageningen, Netherlands: Pudoc Press.
Truman, J. W. (1971b). Physiology of insect ecdysis. I. The eclosion behavior of silkmoths and its hormonal control. Journal of Experimental Biology, 54, 805–814.
Truman, J. W. (1972a). Physiology of insect rhythms. I. Circadian organization of the endocrine events underlying the moulting cycle of larval tobacco hornworms. Journal of Experimental Biology, 57, 805–820.
Truman, J. W. (1972b). Physiology of insect rhythms. II. The silk moth brain as the location of the biological clock controlling eclosion. Journal of Comparative Physiology, 81, 99–114.
Truman, J. W. (1973). Physiology of insect ecdysis. II. The assay and occurrence of the eclosion hormone in the Chinese oak silkmoth, Antheraea pernyi. Biological Bulletin, 114, 200–211.
Truman, J. W. (1974a). Circadian release of a prepatterned neural program in silkmoths. In F. O. Schmitt & F. G. Worden (Eds.), The neurosciences: Third study program (pp. 525–529). Cambridge, MA: MIT Press.
Truman, J. W. (1974b). Physiology of insect rhythms. IV. Role of the brain in the regulation of the flight rhythm of the giant silkmoths. Journal of Comparative Physiology, 95, 281–296.
Truman, J. W. (1976). Extraretinal photoreception in insects. Photochemistry and Photobiology, 23, 215–225.
Truman, J. W. (1984a). Physiological aspects of the two oscillators that regulate timing of eclosion in moths. In R. Porter & G. Collins (Eds.), Photoperiodic regulation of insect and molluscan hormones (pp.
Truman, J. W. (1984b). The preparatory behavior rhythms of the moth Manduca sexta: An ecdysteroid triggered circadian rhythm that is independent of the brain. Journal of Comparative Physiology, 155, 521–528.
Truman, J. W., & Riddiford, L. M. (1970). Neuroendocrine control of ecdysis in silkmoths. Science, 167, 1624–1626.
Truman, J. W., & Sokolove, P. J. (1972). Silkmoth eclosion: Hormonal triggering of a centrally programmed pattern of behavior. Science, 175, 1491–1493.
Vafopoulou, X., & Steel, C. G. H. (1991). Circadian regulation of synthesis of ecdysteroids by prothoracic glands of the insect Rhodnius prolixus Evidence of a dual oscillator system. General and Comparative Endocrinology, 83, 27–34.
Vafopoulou, X., & Steel, C. G. H. (1992). In vitro photosensitivity of ecdysteroid synthesis by prothoracic glands of Rhodnius prolixus. General and Comparative Endocrinology, 86, 1–9.
Waddel, B., Lewis, R. D., & Engelmann, W. (1990). Localization of the circadian pacemakers of Hemideina thoracica (Orthoptera; Stenopelmatidae). Journal of Biological Rhythms, 5, 131–140.
Weber, E (1985). Postmolt cuticle growth in a cockroach: In vitro deposition of multilamellate and circadian-like layered endocuticle. Experientia, 41, 398–400.
Wiedenmann, G. (1983). Splitting in a circadian activity rhythm: The expression of bilaterally paired oscillators. Journal of Comparative Physiology, 150, 51–60.
Wiedenmann, G., & Loher, W. (1984). Circadian control of singing in crickets: Two different pacemakers for early-evening and before-dawn activity. Journal of Insect Physiology, 30, 145–151.
Wiedenmann, G., Lukat, R., & Weber, E (1986). Cyclic layer deposition in the cockroach endocuticle: A circadian rhythm? Journal of Insect Physiology, 32, 1019–1027.
Wills, S. A., Page, T. L., & Colwell, C. (1985). Circadian rhythms in the electroretinogram of the cockroach. Journal of Biological Rhythms, 1, 25–37.
Woolum, J., & Strumwasser, E (1980). The differential effects of ionizing radiation on the circadian oscillator and other functions in the eye of Aplysia. Proceedings of the National Academy of Sciences of the USA, 77, 5542–5546.
Yukizane, M., & Tomioka, K. (1995). Neural pathways involved in mutual interactions between optic lobe circadian pacemakers in the cricket Gryllus bimaculatus. Journal of Comparative Physiology, 176, 601–610.
Zimmerman, W. E, & Goldsmith, T. H. (1971). Photosensitivity of the circadian rhythm and of visual receptors in carotenoid depleted Drosophila. Science, 171, 1167–1168.
Zimmerman, W. E, & Ives, D. (1971). Some photophysical aspects of circadian rhythmicity in Drosophila. In M. Menaker (Ed.), Biochrcmometry (pp. 381–391). Washington, DC: National Academy of Sciences.
Zwicky, K. T. (1970). Behavioral aspects of the extraocular light sense of Urodacus
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Page, T.L. (2001). Circadian Systems of Invertebrates. In: Takahashi, J.S., Turek, F.W., Moore, R.Y. (eds) Circadian Clocks. Handbook of Behavioral Neurobiology, vol 12. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1201-1_5
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