Abstract
While certain circadian hormonal changes are prominent, their predictable assessment requires a standardization of conditions of sampling. The 24-hour rhythm in circulating corticosterone of rodents, known since the 1950s, was studied as a presumed proxy for stress on 108 rats divided into 9 groups of 6 male and 9 groups of 6 female animals sampled every 4 hours for 24 hours. In a first stress study, the “no-rhythm” (zero-amplitude) assumption failed to be rejected at the 5% probability level in the two control groups and in 16 out of the 18 groups considered. A circadian rhythm could be detected with statistical significance, however, in three separate follow-up studies in the same laboratory, each on 168 rats kept on two antiphasic lighting regimens, with 4-hourly sampling for 7 or 14 days. In the first stress study, pooling of certain groups helped the detection and assessment of the circadian corticosterone rhythm. Without extrapolating to hormones other than corticosterone, which may shift more slowly or adjust differently and in response to different synchronizers, the three follow-up studies yielded uncertainty measures (95% confidence intervals) for the point estimate of its circadian period, of possible use in any future study as a reference standard.
The happenstance of a magnetic disturbance at the start of two follow-up studies was associated with the detection of a circasemiseptan component, raising the question whether a geomagnetic disturbance could be considered as a “load”. Far beyond the limitations of sample size, the methodological requirements for standardization in the experimental laboratory concerning designs of studies are considered in the context of models of depression. Lessons from nature’s unforeseen geomagnetic contribution and from human studies are noted, all to support the advocacy, in the study of loads, of sampling schedules covering more than 24 hours.
Similar content being viewed by others
References
AdanA and V Natale (2002) Gender differences in morningness-eveningness preference.Chronobiol. Int. 19, 709–720.
AdanA and M Sanchez-Turet (2001) Gender differences in diurnal variations of subjective activation and mood.Chronobiol. Int. 18(3), 491–502.
Ayensu WK, O Pucilowski, GA Mason, DH Overstreet, AH Rezvani and DS Janowsky (1995) Effects of chronic mild stress on serum complement activity, saccharin preference, and corticosterone levels in Flinders lines of rats.Physiol. Behav. 57, 165–169.
AzpirozA, E Fano, L Garmendia, A Arregi, R Cacho, G Beitia and PF Brain (1999) Effects of chronic mild stress (CMS) and imipramine administration, on spleen mononuclear cell proliferation response, serum corticosterone level and brain norepinephrine content in male mice.Psychoneuroendocrinology 24, 345–361.
Bartol-MunierI, S Gourmelen, P Pevet and E Challet (2006) Combined effects of high-fat feeding and circadian desynchronization.Int. J. Obesity 30, 60–67.
BielajewC, AT Konkle and Z Merali (2002) the effects of chronic mild stress on male Sprague-Dawley and Long Evans rats: I. Biochemical and physiological analyses.Behav. Brain Res. 136(2), 583–592.
BinghamC, B Arbogast, G Cornélissen Guillaume, JK Lee and F Halberg (1982) Inferential statistical methods for estimating and comparing cosinor parameters.Chronobiologia 9, 397–439.
Bryson RW and DF Martin (1954) 17-Ketosteroid excretion in a case of manic-depressive psychosis.The Lancet 267, 365–367.
CheetaS, G Ruigt, J van Proosdij and P Willner (1997) Changes in sleep architecture following chronic mild stress.Biol. Psychiatr. 41, 419–427.
Chibisov SM, G Cornélissen and F Halberg (2004) Magnetic storm effect on the circulation of rabbits.Biomed. Pharmacother. 58 (Suppl. 1), S15-S19.
CornélissenG and F Halberg (2005) Chronomedicine, In:Encyclopedia of Biostatistics, 2nd Ed. (ArmitageP and T Colton, Eds.) (John Wiley & Sons Ltd:Chichester, UK), 796–812.
CornélissenG, D Watson, G Mitsutake, B Fiser, J Siegelova, J Dusek, L Vohlidalova, H Svacinova and F Halberg (2005) Mapping of circaseptan and circadian changes in mood.Scripta Medica 78, 89–98.
CornélissenG, F Halberg, K Otsuka, RB Singh and CH Chen (2007) Chronobiology predicts actual and proxy outcomes whendippingfails.Hypertension 49, 237–239. doi: 10.1161/01. HYP.0000250392.51418.64.
CostaG, F Lievore, G Casaletti, E Gaffuri and S Folkard (1989) Circadian characteristics influencing individual differences in tolerances and adjustment to shift work.Ergonomics 32, 373–385.
D’Aquila PS, P Brain and P Willner (1994) Effects of chronic mild stress on performance in behavioural tests relevant to anxiety and depression.Physiol. Behav. 56, 861–867.
Dallman MF, SF Akana, S Bhatnagar, ME Bell, S Choi, A Chu, C Horsley, N Levin, O Meijer, LR Soriano, AM Strack and V Viau (1999) Starvation: early signals, sensors, and sequelae.Endocrinology 140, 4015–4023.
Dallman MF, V Viau, S Bhatnagar, F Gomez, K Laugero and ME Bell (2002) Corticotropin-releasing factor, corticosteroids, and sugar: energy balance, the brain, and behavior, In:Mammalian Hormone Systems (Pfaff DW, AP Arnold, AM Etgen, SE Fahrback and RT Rubin, Eds.) (Academic Press: San Diego, CA), 571–632.
DavisS, DK Mirick and RG Stevens (2001) Night shift work, light at night, and the risk of breast cancer.J. Natl. Cancer Inst. 93, 1557–1562.
Florida-JamesG, A Wallymahmed and T Reilly (1996) Effects of nocturnal shiftwork on mood states of student nurses.Chronobiol. Int. 13(1), 59–69.
Grippo AJ, TG Beltz and AK Johnson (2003) Behavioral and cardiovascular changes in the chronic mild stress model of depression.Physiol. Behav. 78, 703–710.
HalbergF (1960) Symposium on “Some current research methods and results with special reference to the central nervous system”. Physiopathologic approach.Am. J. Ment. Defic. 65, 156–171.
HalbergF (1961) Circadian desynchronization, In:Circadian Systems (Fomon SJ, Ed.). Report of the 39th Ross Conference on Pediatric Research. Columbus, OH: Ross Laboratories; pp. 18–19.
HalbergF (1968) Physiologic considerations underlying rhythmometry, with special reference to emotional illness. Symposium on Biological Cycles and Psychiatry, In:Symposium Bel-Air III. Cycles biologiques et psychiatrie / publié sous la direction du professeur J. de Ajuriaguerra. Geneva: Georg / Paris: Masson et Cle pp. 73–126.
HalbergF (1969) Chronobiology.Annu. Rev. Physiol. 31, 675–725.
HalbergF (1980) Chronobiology: methodological problems.ActaMed. Rom. 18, 399–440.
HalbergF and MB Visscher (1950) Regular diurnal physiological variation in eosinophil levels in five stocks of mice.Proc. Soc. Exp. Biol. 75, 846–847.
HalbergF, MB Visscher and JJ Bittner (1953) Eosinophil rhythm in mice. Range of occurrence; effects of illumination, feeding and adrenalectomy.Am. J. Physiol. 174, 109–122.
HalbergF, O Hamerston and JJ Bittner (1957) Sex difference in eosinophil counts in tail blood of mature B1 mice.Science 125, 73.
HalbergF, CP Barnum, RH Silber and JJ Bittner (1958) 24-hour rhythms at several levels of integration in mice on different lighting regimens.Proc. Soc. Exp. Biol. 97, 897–900.
HalbergF, E Haus, SS Cardoso, LE Scheving, JFW Kuhl, R Shiotsuka, G Rosene, JE Pauly, W Runge, JF Spalding, JK Lee and RA Good (1973) Toward a chronotherapy of neoplasia: tolerance of treatment depends upon host rhythms.Experientia (Basel) 29, 909–934.
HalbergF, G Cornélissen, G Katinas, EV Syutkina, RB Sothern, R Zaslavskaya, F Halberg, Y Watanabe, O Schwartzkopff, K Otsuka, R Tarquini, P Perfetto and J Siegelova (2003a) Transdisciplinary unifying implications of circadian findings in the 1950s.J. Circadian Rhythms 1, 2. p.61. www.JCircadianRhythms.com/content/ pdf/1740-3391-2-3.pdf
HalbergF, G Cornélissen, NH Spector, RP Sonkowsky, K Otsuka, I Baciu, M Hriscu, O Schwartzkopffand EE Bakken (2003b) Stress/strain/life revisited. Quantification by blood pressure chronomics: benetensive, transtensive or maletensive chrono-vasculo-neuro-immuno-modulation.Biomed. Pharmacother. 57 (Suppl. 1), 136s-163s.
Hart RP, GD Coover, A Shnerson and WP Smotherman (1980) Plasma corticosterone elevations in rats in response to consumption of concentrated sugar solutions.J. Comp. Physiol. Psychol. 94, 337–345.
HennigJ, P Kieferdorf, C Moritz, S Huwe and P Netter (1998) Changes in cortisol secretion during shiftwork: implications for tolerance to shiftwork?Ergonomics 41/5, 610–621.
JozsaR, F Halberg, G Cornélissen, M Zeman, J Kazsaki, V Csernus, GS Katinas, HW Wendt, O Schwartzkopff, K Stebelova, K Dulkova, SM Chibisov, M Engebretson, W Pan, GA Bubenik, G Nagy, M Herold, R Hardeland, G Huther, B Pöggeler, R Tarquini, F Perfetto, R Salti, A Olah, N Csokas, P Delmore, K Otsuka, EE Bakken, J Allen and C Amory-Mazaudier (2005a) Chronomics, neuroendocrine feedsidewards and the recording and consulting of nowcasts forecasts of geomagnetics.Biomed. Pharmacother. 59 (Suppl. 1), S24-S30.
JozsaR, A Olah, G Cornélissen, V Csernus, K Otsuka, M Zeman, G Nagy, J Kazsaki, K Stebelova, N Csokas, W Pan, M Herold, EE Bakken and F Halberg (2005b) Circadian and extracircadian exploration during daytime hours of circulating corticosterone and other endocrine chronomes.Biomed. Pharmacother. 59 (Suppl. 1), S109-S116.
Katz RJ and M Siebel (1982) Animal model of depression: tests of three structurally and pharmacologically novel antidepressant compounds.Pharmacol. Biochem. Behav. 16, 973–977.
Krieger DT, H Hauser amd LC Krey (1977) Suprachiasmatic nuclear lesions do not abolish food-shifted circadian adrenal and temperature rhythmicity.Science 197, 398–399.
Kripke DF, SD Youngstedt, JA Elliottet al., (2005) Circadian phase in adults of contrasting ages.Chronobiol. Int. 22, 695–709.
Lowrey PL and JS Takahashi (2004) Mammalian circadian biology: elucidating genome-wide levels of temporal organization.Annu. Rev. Genomics Hum. Genet. 5, 407–441. Review.
Marquardt DW (1963) An algorithm for least-squares estimation of nonlinear parameters.J. Soc. Indust. Appl. Math. 11, 431–441.
Minors DS and JM Waterhouse (1983) Circadian rhythm amplitude — is it related to rhythm adjustment and/or worker motivation?Ergonomics 26, 229–241.
Molina VA, CJ Heyser and LP Spear (1994) Chronic variable stress or chronic morphine facilitates immobility in forced swim test: reversal by naloxone.Psychopharmacol. 114, 433–440.
MurisonR and AL Hansen (2001) Reliability of the chronic mild stress paradigm: implications for research and animal welfare.Integr. Physiol. Behav. Sci. 36, 266–274.
MuscatR and P Willner (1992) Suppression of sucrose drinking by chronic mild unpredictable stress: a methodological analysis.Neurosci. Biobehav. Rev. 16, 507–517.
OlahA, R Jozsa, G Cornélissen, V Csernus, M Zeman, G Nagy, WH Pan, WA Hoogerwerf, J Kazsaki, K Otsuka, ZR Wang, RB Sothern, SB Sothern and F Halberg (2006) Sampling for chronomics extended circadian phase map of the laboratory rat.Proc. Intl. Conf. Frontiers of Biomed. Sci.: Chronobiol., Chengdu, China, pp 46–49.
PecoraroN, F Gomez, K Laugero and MF Dallman (2002) Brief access to sucrose engages food — entrainable rhythms in food-deprived rats.Behav. Neurosci. 116, 757–776.
Penev PD, DE Kolker, PC Zee and FW Turek (1998) Chronic circadian desynchronization decreases the survival of animals with cardiomyopathic heart disease.Am. J. Physiol. 275 (6, Pt. 2): H2334-H2337.
Ralph MR, RG Foster, FC Davis and M Menaker (1990) Transplanted suprachiasmatic nucleus determines circadian period.Science 247(sn4945), 975–978.
Schweiger H-G, S Berger, H Kretschmer, H Mörler, E Halberg, RB Sothern and F Halberg (1986) Evidence for a circaseptan and a circasemiseptan growth response to light/ dark cycle shifts in nucleated and enucleatedAcetabularia cells, respectively.Proc. Natl. Acad. Sci. USA 83, 8619–8623.
Silberman DM, M Wald and AM Genaro (2002) Effects of chronic mild stress on lymphocyte proliferative response. Participation of serum thyroid hormones and corticosterone.Int. Immunopharmacol. 2, 487–497.
StebelovaK, M Zeman, G Cornélissen, G Bubenik, R Jozsa, R Hardeland, B Poeggeler, G Huether, A Olah, G Nagy, V Csernus, J Kazsaki, W Pan, K Otsuka, EE Bakken and F Halberg (2005) Chronomics reveal and quantify circadian rhythmic melatonin in duodenum of rats.Biomed. Pharmacother. 59 (Suppl. 1), S209-S212.
TarquiniB, G Cornélissen, F Perfetto, R Tarquini and F Halberg (1997) Chronome assessment of circulating melatonin in humans.In vivo 11, 473–484.
TouitouY and E Haus (2000) Alterations with aging of the endocrine and neuroendocrine circadian system in humans.Chronobiol. Int. 17, 369–390.
Tsai LL, YC Tsai, K Hwang, YW Hwang and JE Tzeng (2005) Repeated light-dark shifts speed up body weight gain in male F344 rats.Am. J. Physiol. Endocrinol. Metab. 289 (2), E212-E217.
Van ReethO (1998) Sleep and circadian disturbances in shift-work: strategies for their management.Hormone Res. 49, 158–162.
WillnerP, D Sampson, M Papp, G Phillips and R Muscat (1991) Animal models of anhedonia, anxiety, depression and mania, In:Animal Models of Psychiatric Disorders (SoubrieP, Ed.) (Karger:Basel), pp 71–99.
WillnerP (1997) Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation.Psychopharmacol. (Berl.) 134, 319–329.
YamanakaG, K Otsuka, N Hotta, S Murakami, Y Kubo, O Matsuoka, E Takasugi, T Yamanaka, M Shinagawa, S Nunoda, Y Nishimura, K Shibata, H Saitoh, M Nishinaga, M Ishine, T Wada, K Okumiya, K Matsubayashi, S Yano, S Ishizuka, K Ichihara, G Cornélissen and F Halberg (2005) Depressive mood is independently related to stroke and cardiovascular events in a community.Biomed. Pharmacother. 59 (Suppl. 1), S31-S39.
ZemanM, R Jozsa, G Cornélissen, K Stebelova, G Bubenik, A Olah, B Poeggeler, G Huether, R Hardeland, G Nagy, V Csernus, W Pan, K Otsuka and F Halberg (2005) Chronomics: circadian lead of extrapineal vs. pineal melatonin rhythms with an infradian hypothalamic exploration.Biomed. Pharmacother. 59 (Suppl. 1), S213-S219.
Zhao ZY, Y Xie, YR Fu, YY Li, A Bogdan and Y Touitou (2003) Circadian rhythm characteristics of serum cortisol and dehydroepiandrosterone sulfate in healthy Chinese men aged 30 to 60 years. A cross-sectional study.Steroids 68(2), 133–138.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Olah, A., Jozsa, R., Csernus, V. et al. Stress, geomagnetic disturbance, infradian and circadian sampling for circulating corticosterone and models of human depression?. neurotox res 13, 85–96 (2008). https://doi.org/10.1007/BF03033560
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF03033560