Skip to main content
Log in

Dissociation between the circadian rhythm of locomotor activity and the pineal clock in the Japanese newt

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

The circadian locomotor activity rhythm of the Japanese newt has been thought to be driven by a putative brain oscillator(s) subordinate to the pineal clock. The existence of mutual coupling between the pineal clock and the brain oscillator(s) in vivo was examined. We covered the newt's skull with aluminum foil and simultaneously reversed the light-dark cycle, thereby allowing the pineal organ to be exposed to constant darkness while the rest of the animal was exposed to the reversed light-dark cycle. In control animals, whose heads were covered with transparent plastic, the rhythm of synaptic ribbon number in the pineal photoreceptor cells was entrained to the reversed light-dark cycle. Rhythms from newts whose heads were shielded, however, were similar to those observed in the unoperated newts kept under constant darkness. The locomotor activity rhythms of both head-covered animals and control animals were entrained to the reversed light-dark cycle. These data suggest that extrapineal photoreception can entrain the putative brain oscillator(s), but not the pineal clock. Thus, at least in an aspect of photic entrainment, there seems to be little or no mutual coupling between the pineal clock and the putative brain oscillator(s) in the circadian system of the Japanese newt.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.

Similar content being viewed by others

Abbreviations

LD:

light-dark

DD:

constant darkness

SCN:

suprachiasmatic nucleus

SR:

synaptic ribbon

References

  • Barret RK, Takahashi JF (1995) Temperature compensation and temperature entrainment of the chick pineal cell circadian clock. J Neurosci 15:5681–5692

    PubMed  Google Scholar 

  • Barret RK, Underwood H (1992) The superior cervical ganglia are not necessary for entrainment or persistence of the pineal melatonin rhythm in Japanese quail. Brain Res 569:249–254

    Article  PubMed  Google Scholar 

  • Bolliet V, Ali MR, Lapointe FJ, Falcon J (1996) Rhythmic melatonin secretion in different teleost species: an in vitro study. J Comp Physiol B 165:677–683

    CAS  PubMed  Google Scholar 

  • Chiba A, Kikuchi M and Aoki K (1993) The effects of pinealectomy and blinding on the circadian locomotor activity rhythm in the Japanese newt, Cynops pyrrhogaster. J Comp Physiol A 172:683–691

    Google Scholar 

  • Falcon J, Guerlotte JF, Voisin P, Collin J-P (1987) Rhythmic melatonin biosynthesis in a photoreceptive pineal organ: a study in the pike. Neuroendocrinology 45:479–486

    CAS  PubMed  Google Scholar 

  • Foster RG, Grace MS, Provencio I, Degrip WJ, Garcia-Frenandez JM (1994) Identification of vertebrate deep brain photoreceptors. Neurosci Biobehav Rev 18:541–546

    CAS  PubMed  Google Scholar 

  • Fritzsch B (1980) Retinal projections in European Salamandridae. Cell Tissue Res 213:325–341

    CAS  PubMed  Google Scholar 

  • Gwinner E, Brandstatter R (2001) Complex bird clocks. Philos Trans R Soc Lond B 356:1801–1810

    Article  CAS  Google Scholar 

  • Hasegawa M, Adachi A, Yoshimura T, Ebihara S (1994) Retinally perceived light is not essential for photic regulation of pineal melatonin rhythms in the pigeon: studies with microdialysis. J Comp Physiol A 175:581–586

    CAS  Google Scholar 

  • Kikuchi M, Aoki K (1985) Circadian changes in synaptic ribbons in the pineal organ of the Japanese common newt, Cynops pyrrhogaster. Zool Sci 2:175–181

    Google Scholar 

  • Kikuchi M, Chiba A, Aoki K (2000) Daily melatonin injections entrain the circadian change of synaptic ribbon number in the pineal organ of the Japanese newt. Neurosci Lett 285:181–184

    Article  CAS  PubMed  Google Scholar 

  • Klein DC (1985) Photoneural regulation of the mammalian pineal gland. In: Evered D, Clark S (eds) Photoperiodism, melatonin and the pineal gland. Pitman, London, pp 38–56

  • Maitra SK, Khaledpour C, Vollrath L (1989) Day-night differences in "synaptic" ribbon numbers in the pinealocytes of a subtropical wild bird Psittacula Krameri. Neuroendocrinol Lett 11:171–176

    Google Scholar 

  • Martinez Soriano F, Welker HA, Vollrath L (1984) Correlation of the number of pineal "synaptic" ribbons and spherules with the levels of serum melatonin over a 24-hour period in male rabbits. Cell Tissue Res 236:555–560

    PubMed  Google Scholar 

  • McNulty JA (1981) Synaptic ribbons in the pineal organ of the goldfish: circadian rhythmicity and the effects of constant light and constant darkness. Cell Tissue Res 215:491–497

    CAS  PubMed  Google Scholar 

  • Menaker M, Tosini G (1996) The evolution of vertebrate circadian system. In: Honma K, Honma S (eds) Circadian organization and oscillatory coupling. Hokkaido University Press, Sapporo, Japan, pp 39–52

  • Menaker M, Wisner S (1983) Temperature-compensated circadian clock in the pineal of Anolis. Proc Natl Acad Sci USA 80:6119–6121

    CAS  PubMed  Google Scholar 

  • Minutini L, Innocenti A, Bertolucci C, Foa A (1994) Electrolytic lesions to the optic chiasm affect circadian locomotor rhythms in lizards. Neuroreport 5:525–527

    CAS  PubMed  Google Scholar 

  • Moore RY, Klein DC (1974) Visual pathways and the central neural control of a circadian rhythm in pineal serotonin N-acetyltransferase activity. Brain Res 71:17–33

    CAS  PubMed  Google Scholar 

  • Norgren RB, Silver R (1989) Retinal projections in quail (Coturnix coturnix). Vis Neurosci 3:377–387

    PubMed  Google Scholar 

  • Oshima I, Yamada H, Goto M, Sato K, Ebihara S (1989) Pineal and retinal melatonin is involved in the control of circadian locomotor activity and body temperature rhythms in the pigeon. J Comp Physiol A 166:217–226

    Google Scholar 

  • Takahashi JS, Hamm H, Menaker M (1980) Circadian rhythms of melatonin release from individual superfused chicken pineal gland in vitro. Proc Natl Acad Sci USA 77:2319–2322

    CAS  PubMed  Google Scholar 

  • Tilgner S, Lehmann L, Westphal U-I (1990) Retinohypothalamic connections in vertebrates. Klin Mbl Augenheilk 197:295–301

    CAS  PubMed  Google Scholar 

  • Tosini G, Bertolucci C, Foa A (2001) The circadian system of reptiles: a multioscillatory and multiphotoreceptive system. Physiol Behav 72:461–471

    CAS  PubMed  Google Scholar 

  • Tuinhof R, Artero C, Fasolo A, Franzoni MF, Ten-Donkelaar HJ, Wismans PG, Roubos EW (1994) Involvement of retino-hypothalamic input, suprachiasmatic nucleus, magnocellular nucleus and locus coeruleus in control of melanotrope cells of Xenopus laevis: a retrograde and anterograde tracing study. Neuroscience 61:411–420

    Article  CAS  PubMed  Google Scholar 

  • Underwood H (1994) The circadian rhythm of thermoregulation in Japanese quail. I. Role of the eyes and pineal. J Comp Physiol A 175:639–653

    CAS  PubMed  Google Scholar 

  • Underwood H, Barret RK, Siopes T (1990) Melatonin does not link the eyes to the rest of the circadian system in quail: a neural pathway is involved. J Biol Rhythms 5:349–361

    CAS  PubMed  Google Scholar 

  • Vollrath L (1973) Synaptic ribbons of a mammalian pineal gland. Circadian changes. Z Zellforsch 145:171–183

    CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Prof. M. Menaker (Virginia University, USA) for kindly reading and criticizing the manuscript. This research was supported by KAKENHI (11640686) from the Ministry of Education, Science and Culture of Japan. The experiments comply with the Principles of animal care, publication No. 86-23, revised 1985 of the National Institute of Health and also with the laws of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Chiba.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chiba, A., Kikuchi, M. & Aoki, K. Dissociation between the circadian rhythm of locomotor activity and the pineal clock in the Japanese newt. J Comp Physiol A 189, 655–659 (2003). https://doi.org/10.1007/s00359-003-0439-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-003-0439-6

Keywords

Navigation