Journal of Comparative Physiology A

, Volume 176, Issue 5, pp 601–610 | Cite as

Neural pathways involved in mutual interactions between optic lobe circadian pacemakers in the cricketGryllus bimaculatus

  • M. Yukizane
  • K. Tomioka
Original Paper


The circadian locomotor rhythm of the cricketGryllus bimaculatus is primarily generated by a pair of optic lobe circadian pacemakers. The two pacemakers mutually interact to keep a stable temporal structure in the locomotor activity. The interaction has two principal effects on the activity rhythm, i.e., phase-dependent modulation of the freerunning period and phase-dependent suppression of activity driven by the partner pacemaker. Both effects were mediated by neural pathways, since they were immediately abolished after the optic stalk connecting the optic medulla to the lobula was unilaterally severed. The neural pathways were examined by recording locomotor activity, under a 13 h light to 13 h dark cycle, after the optic nerves were unilaterally severed and the contralateral optic stalk was partially destroyed near the lobula. When the dorsal half of the optic stalk was severed, locomotor rhythm mostly split into two components: one was readily entrained to the given light-dark cycle and the other freeran with a marked fluctuation in freerunning period, where the period of the freerunning component was lengthened or shortened when the onset of the entrained component occurred during its subjective night or day, respectively. The phase-dependent modulation of activity was also observed in both components. However, severance of the ventral half of the optic stalk resulted in appearance only of the freerunning component; neither the phase-dependent modulation of its freerunning period nor the change in activity level was observed. These results suggest that neurons driving the mutual interaction and the overt activity rhythm run in the ventral half of the proximal optic stalk that includes axons of large medulla neurons projecting to the cerebral lobe and the contralateral medulla.

Key words

Circadian rhythm cricket interaction between pacemakers optic lobe neural pathways 



light dark cycle


freerunning period


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  1. Bacon JP, Altman JS (1977) A silver intensification method for cobalt-filled neurons in whole mount preparations. Brain Res 73: 359–363Google Scholar
  2. Balkenohl M, Weber F (1981) Sind auch bei holometabolen Insekten circadiane Schrittmacher der Aktivitat in den optischen Ganglion lokalisiert? Mitt Dtsch Ges Allg Angew Entomol 3: 223–227Google Scholar
  3. Daan S, Berde C (1978) Two coupled oscillators: simulations of the circadian pacemaker in mammalian activity rhythms. J Theor Biol 70: 297–313Google Scholar
  4. Fleissner G (1982) Isolation of an insect circadian clock. J Comp Physiol 149: 311–316Google Scholar
  5. Honegger H-W, Schürmann FW (1975) Cobalt sulphide staining of optic fibres in the brain of the cricket,Gryllus campestris. Cell Tissue Res 159: 213–225Google Scholar
  6. Koehler WK, Fleissner G (1978) Internal desynchronization of bilaterally organized circadian oscillators in the visual system of insects. Nature 274: 708–710Google Scholar
  7. Loher W (1972) Circadian control of stridulation in the cricketTeleogryllus commodus Walker. J Comp Physiol 79: 173–190Google Scholar
  8. Meijer JH, Rietveld WJ (1989) Neurophysiology of the suprachiasmatic circadian pacemaker in rodents. Physiol Rev 69: 671–707Google Scholar
  9. Meijer JH, Daan S, Overkamp GJF, Hermann PM (1990) The two-oscillator circadian system of tree shrews (Tupaia belangeri) and its response to light and dark pulses. J Biol Rhythms 5: 1–16Google Scholar
  10. Menaker M, Vogelbaum MA (1993) Mutant circadian period as a marker of suprachiasmatic nucleus function. J Biol Rhythms 8: S93-S98Google Scholar
  11. Nishiitsutsuji-Uwo J, Pittendrigh CS (1968) Central nervous system control of circadian rhythmicity in cockroach. III. The optic lobes, locus of the driving oscillation? Z Vergl Physiol 58: 14–46Google Scholar
  12. Page TL (1978) Interaction between bilaterally paired components of the cockroach circadian system. J Comp Physiol 124: 225–236Google Scholar
  13. Page TL (1983) Effects of optic tract regeneration on internal coupling in the circadian system of the cockroach. J Comp Physiol 153: 231–240Google Scholar
  14. Page TL (1988) Circadian organization and the representation of circadian information in the nervous systems of invertebrates. Adv Biosci 73: 67–79Google Scholar
  15. Rence BD, Lisy MT, Garves BR, Quinlan BJ (1988) The role of ocelli in circadian singing rhythms of crickets. Physiol Entomol 13: 201–212Google Scholar
  16. Roberts MH, Block GD (1983) Mutual coupling between the ocular circadian pacemakers ofBulla gouldiana. Science 221: 87–89Google Scholar
  17. Roberts MH, Block GD (1985) Analysis of mutual circadian pacemaker coupling between the two eyes ofBulla. J Biol Rhythms 1: 55–75Google Scholar
  18. Roberts MH, Block GD, Lusska AE (1987) Comparative studies of circadian pacemaker coupling in opistobranch molluscs. Brain Res 423: 286–292Google Scholar
  19. Roth RL, Sokolove PG (1975) Histological evidence for monosynaptic connection between optic lobes of the cockroach,Leucophaea maderae. Brain Res 87: 23–39Google Scholar
  20. Tomioka K (1993) Analysis of coupling between optic lobe circadian pacemakers in the cricketGryllus bimaculatus. J Comp Physiol A 172: 401–408Google Scholar
  21. 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
  22. Tomioka K, Chiba Y (1986) Circadian rhythm in the neurally isolated lamina-medulla complex of the cricket,Gryllus bimaculatus. J Insect Physiol 32: 747–755Google Scholar
  23. Tomioka K, Chiba Y (1989) Photoperiodic entrainment of locomotor activity in crickets (Gryllus bimaculatus) lacking the optic lobe pacemaker. J Insect Physiol 35: 827–835Google Scholar
  24. Tomioka K, Chiba Y (1992) Characterization of optic lobe circadian pacemaker by in situ and in vitro recording of neuronal activity in the cricketGryllus bimaculatus. J Comp Physiol A 171: 1–7Google Scholar
  25. Tomioka K, Yamada K, Yokoyama S, Chiba Y (1991) Mutual interactions between optic lobe circadian pacemakers in the cricketGryllus bimaculatus. J Comp Physiol A 169: 291–298Google Scholar
  26. Tomioka K, Nakamichi Y, Yukizane M (1994) Optic lobe circadian pacemaker sends its information to the contralateral optic lobe in the cricketGryllus bimaculatus. J Comp Physiol A 175: 381–388Google Scholar
  27. Tyrer NM, Bell EM (1974) The intensification of profiles of cobalt-injected neurons in sectioned material. Brain Res 73: 151–155Google Scholar
  28. Wiedenmann G (1983) Splitting in a circadian activity rhythm: the expression of bilaterally paired oscillators. J Comp Physiol 150: 51–60Google Scholar
  29. Wiedenmann G, Krueger-Alef K, Martin W (1988) The circadian control of calling song and walking activity patterns in male crickets (Teleogryllus commodus). Exp Biol 47: 127–137Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • M. Yukizane
    • 1
  • K. Tomioka
    • 1
  1. 1.Department of Biology, Faculty of ScienceYamaguchi UniversityYamaguchiJapan

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