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Complex circadian regulation of pineal melatonin and wheel-running in Syrian hamsters

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Abstract

Circadian regulation of pineal melatonin content was studied in Syrian hamsters (Mesocricetus auratus), especially melatonin peak width and the temporal correlation to wheel-running activity. Melatonin was measured by radioimmunoassay in glands removed at different circadian times with respect to activity onset (= CT 12). Pineal melatonin peak width (h; for mean ≥125 pg/gland) and activity duration (α) were both 4–5 h longer after 12 or 27 weeks than after 5 or 6 days in continuous darkness (DD). Increased peak width was associated with a delay in the morning decline (M) of melatonin to baseline, correlated with a similar delay in wheel-running offset. In contrast, the evening rise (E) in melatonin occurred at approximately the same circadian phase regardless of the length of DD. Fifteen min light pulses produced similar phase-shifts in melatonin and activity. In a phase advance shift, M advanced at once, while E advanced only after several days of adjustment. Independent timing of shifts in the E and M components of the melatonin rhythm suggest that these events are controlled separately by at least two circadian oscillators whose mutual phase relationship determines melatonin peak width. This two-oscillator control of melatonin peak width is integral to the circadian mechanism of hamster photoperiodic time measurement.

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Abbreviations

CT:

circadian time

DD:

continuous dark

L: D:

light: dark cycle

PMEL:

pineal melatonin

PRC:

phase response curve

RIA:

radioimmunoassay; α, duration (h) of the active phase of the circadian wheel-running rhythm; τ, free-running period

References

  • Alleva JJ (1987) The biological clock and pineal gland: How they control seasonal fertility in the golden hamster. Pineal Res Rev 5:95–131

    Google Scholar 

  • Armstrong SM (1989) Melatonin and circadian control in mammals. Experientia 45:932–938

    Google Scholar 

  • Aschoff J, Figala J, Poppel E (1973) Circadian rhythms of locomotor activity in the golden hamster measured with two different techniques. J Comp Physiol Psychol 85:20–28

    Google Scholar 

  • Bartness TJ, Goldman BD (1989) Mammalian pineal melatonin: a clock for all seasons. Experientia 45:939–945

    Google Scholar 

  • Bittman EL, Dempsey RJ, Karsch FJ (1983) Pineal melatonin secretion drives the reproductive response to daylength in the ewe. Endocrinology 113:2276–2283

    Google Scholar 

  • Cagnacci A, Elliott JA, Yen SC (1992) Melatonin: a major regulator of the circadian rhythm of core body temperature in humans. J Clin Endocrinol Metab 75:447–4152

    Google Scholar 

  • Champney TH (1989) β-Adrenergic blockers prevent short photoperiod-induced gonadal regression, but not melatonin induced regression in male Syrian hamsters. J Exp Zool 249:221–228

    Google Scholar 

  • Daan S, Pittendrigh CS (1976) A functional analysis of circadian pacemakers in nocturnal rodents. II. The variability of phase response curves. J Comp Physiol 106:253–266

    Google Scholar 

  • Elliott JA (1974) Photoperiodic regulation of testis function in the golden hamster: relation to the circadian system. PhD Diss, Univ Texas, Austin, pp 167–169

    Google Scholar 

  • Elliott JA (1976) Circadian rhythms and photoperiodic time measurement in mammals. Fed Proc 35:2339–2346

    Google Scholar 

  • Elliott JA (1981) Circadian rhythms, entrainment and photoperiodism in the Syrian hamster. In: Follett BK, Follett DE (eds) Biological clocks in seasonal reproductive cycles. Wright, Bristol, pp 203–217

    Google Scholar 

  • Elliott JA, Goldman BD (1981) Seasonal reproduction: photoperiodism and biological clocks. In: Adler NT (ed) Neuroendocrinology of reproduction. Plenum Press, New York, pp 377–423

    Google Scholar 

  • Elliott JA, Tamarkin L (1982) Phase relationship of two circadian oscillators regulates pineal melatonin rhythm in Syrian hamsters. Endocrine Soc Abstr 988:326

    Google Scholar 

  • Elliott JA, Bartness TJ, Goldman BD (1989) Effect of melatonin infusion duration and frequency on gonad, lipid, and body mass in pinealectomized male Siberian hamsters. J Biol Rhythms 4:439–455

    Google Scholar 

  • Ellis GB, Turek FW (1979) Changes in locomotor activity associated with the photoperiodic response of the testes in male golden hamsters. J Comp Physiol A 132:277–284

    Google Scholar 

  • Goldman BD, Elliott JA (1988) Photoperiodism and seasonality in hamsters: role of the pineal gland. In: Stetson MH (ed) Processing of environmental information in vertebrates. Springer, New York, pp 203–218

    Google Scholar 

  • Hastings MH, Walker AP, Herbert J (1987) Effect of asymmetrical reductions of photoperiod on pineal melatonin, locomotor activity and gonadal condition of male Syrian hamsters. J Endocrinol 114:221–229

    Google Scholar 

  • Hoffmann K, Illnerová H, Vaněček J (1986) Change in duration of the nighttime melatonin peak may be a signal driving photoperiodic responses in the Djungarian hamster (Phodopus sungorus). Neurosci Lett 67:68–72

    Google Scholar 

  • Honma S, Horoshige T (1985) Response curve, free-running period, and activity time in circadian locomotor rhythm of rats. Jpn J Physiol 35:643–658

    Google Scholar 

  • Illnerová H, Vaněcek J (1982) Two-oscillator structure of the pacemaker controlling the circadian rhythm of N-acetyltransferase in the rat pineal gland. J Comp Physiol A 145:539–548

    Google Scholar 

  • Illnerová H, Vaněček J (1987) Dynamics of discrete entrainment of the circadian rhythm in the rat pineal N-acetyltransferase activity during transient cycles. J Biol Rhythms 2:95–108

    Google Scholar 

  • Illnerová H, Vaněček J (1989) Complex control of the circadian rhythm in pineal melatonin production. In: Mess B, Ruzsas Cs, Tima L, Pevet P (eds) The pineal gland: current state of pineal research. Elsevier, Amsterdam, New York, pp 137–153

    Google Scholar 

  • Illnerová H, Vaněček J, Hoffmann K (1989) Different mechanisms of phase delays and phase advances of the circadian rhythm in rat pineal N-acetyltransferase activity. J Biol Rhythms 4:187–200

    Google Scholar 

  • Laughlin GA, Loucks AB, Yen SC (1991) Marked augmentation of nocturnal melatonin secretion in amenorrheic athletes, but not in cycling athletes: unaltered by opioidergic or dopaminergic blockade. J Clin Endocrinol Metab 73:1321–1326

    Google Scholar 

  • Lewy AJ, Ahmed S, Jackson JML, Sack RL (1992) Melatonin shifts human circadian rhythms according to a phase-response curve. Chronobiol Intl 9:380–392

    Google Scholar 

  • Maywood ES, Buttery RC, Vance GH, Herbert J, Hastings MH (1990) Gonadal responses of the male Syrian hamster to programmed infusions of melatonin are sensitive to signal duration and frequency but not to signal phase nor to lesions of the suprachiasmatic nuclei. Biol Reprod 43:174–182

    Google Scholar 

  • Mrosovsky N (1991) Double-pulse experiments with nonphotic and photic phase-shifting stimuli. J Biol Rhythms 6:167–179

    Google Scholar 

  • Mrosovsky N, Reebs SG, Honrado GI, Salmon PA (1989) Behavioral entrainment of circadian rhythms. Experientia 45:696–702

    Google Scholar 

  • Pieper DR, Borer KT, Lobocki CA, Samuel D (1988) Exercise inhibits reproductive quiescence induced by exogenous melatonin in hamsters. Am J Physiol 255: R718-R723

    Google Scholar 

  • Pittendrigh CS (198la) Circadian organization and the photoperiodic phenomena. In: Follett BK, Follett DE (eds) Biological clocks in seasonal reproductive cycles. Wright, Bristol, pp 1–35

    Google Scholar 

  • Pittendrigh CS (1981b) Circadian systems: entrainment. In: Aschoff J (ed) Biological rhythms, Handbook of behavioral neurobiology, vol. 4. Plenum Press, New York, pp 95–124

    Google Scholar 

  • Pittendrigh CS (1988) The photoperiodic phenomena: seasonal modulation of the “day within”. J Biol Rhythms 3:173–188

    Google Scholar 

  • Pittendrigh CS, Daan S (1976a) A functional analysis of circadian pacemakers in nocturnal rodents: V. Pacemaker structure: a clock for all seasons. J Comp Physiol A 106:333–355

    Google Scholar 

  • Pittendrigh CS, Daan S (1976b) A functional analysis of circadian pacemakers in nocturnal rodents. IV. Entrainment: Pacemaker as clock. J Comp Physiol A 106:291–331

    Google Scholar 

  • Pittendrigh CS, Elliott JA, Takamura T (1984) The circadian component in photoperiodic induction. CIBA Foundation Symposium 104:26–47

    Google Scholar 

  • Pratt BL, Goldman BD (1986) Activity rhythms and photoperiodism of Syrian hamsters in a simulated burrow system. Physiol Behav 36:83–89

    Google Scholar 

  • Puchalski W, Lynch GR (1988) Daily melatonin injections affect the expression of circadian rhythmicity in Djungarian hamsters kept under a long-day photoperiod. Neuroendocrinology 48:280–286

    Google Scholar 

  • Ralph CL, Mull D, Lynch HJ, Hedlund L (1971) A melatonin rhythm persists in rat pineals in darkness. Endocrinology 89:1361–1366

    Google Scholar 

  • Ralph CL, Pelham RW, MacBride SE, Reilly D (1974) Persistent rhythms of pineal and serum melatonin in cockerels in continuous darkness. J Endocrinol 63:319–324

    Google Scholar 

  • Rollag MD, Panke ES, Reiter RJ (1980) Pineal melatonin content in male hamsters throughout the seasonal reproductive cycle. Proc Soc Exp Biol Med 165:330–334

    Google Scholar 

  • Rusak B, Yu GD (1993) Regulation of melatonin-sensitivity and firing-rate rhythms of hamster suprachiasmatic nucleus neurons: pinealectomy effects. Brain Res 602:200–204

    Google Scholar 

  • Rusak B, Zucker I (1979) Neural regulation of circadian rhythms. Physiol Rev 59:449–526

    Google Scholar 

  • Takahashi JS, Zatz M (1982) Regulation of circadian rhythmicity. Science 217:1104–1111

    Google Scholar 

  • Tamarkin L, Reppert SM, Klein DC (1979) Regulation of pineal melatonin in the Syrian hamster. Endocrinology 104:385–389

    Google Scholar 

  • Tamarkin L, Reppert SM, Klein DC, Pratt B, Goldman BD (1980) Studies on the daily pattern of pineal melatonin in the Syrian hamster. Endocrinology 107:1525–1529

    Google Scholar 

  • Tamarkin L, Baird CJ, Almeida OFX (1985) Melatonin: a coordinating signal for mammalian reproduction? Science 227:714–720

    Google Scholar 

  • Underwood H, Goldman BD (1987) Vertebrate circadian and photoperiodic systems: Role of the pineal gland and melatonin. J Biol Rhythms 2:279–315

    Google Scholar 

  • Wehr TA, Moul DE, Barbato G, Giesen HA, Seidel JA, Barker C, Bender C (1993) Conservation of photoperiod-responsive mechanisms in human beings. Am J Physiol 265:R846-R857

    Google Scholar 

  • Yellon SM, Bittman EL, Lehman MN, Olster DH, Robinson JE, Karsch FJ (1985) Importance of duration of nocturnal melatonin secretion in determining the reproductive response to inductive photoperiod in the ewe. Biol Reprod 32:523–529

    Google Scholar 

  • Yu GD, Rusak B, Piggins HD (1993) Regulation of melatonin-sensitivity and firing-rate rhythms of hamster suprachiasmatic nucleus neurons: constant light effects. Brain Research 602:191–199

    Google Scholar 

Download references

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Elliott, J.A., Tamarkin, L. Complex circadian regulation of pineal melatonin and wheel-running in Syrian hamsters. J Comp Physiol A 174, 469–484 (1994). https://doi.org/10.1007/BF00191713

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  • DOI: https://doi.org/10.1007/BF00191713

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