Journal of APPLIED BIOMEDICINE
ISSN 1214-0287 (on-line)
ISSN 1214-021X (printed)

Volume 3 (2005), No 1, p 47-57




Changes in behaviour and in the circadian rhythms of melatonin and corticosterone in rats subjected to a forced-swimming test

Sergio Damian Paredes, Soledad Sanchez, Ruben Victor Ria, Ana Beatriz Rodriguez and Carmen Barriga

Address: Sergio Damian Paredes, Department of Physiology, Faculty of Science, University of Extremadura, Avda de Elvas s/n, 06071 Badajoz, Spain
sparedes@unex.es

Received 5th November 2004.
Revised 6th December 2004.
Published online 16th March 2005.

Full text article (pdf)

SUMMARY
We studied the influence of physical activity stress on the circadian rhythms of melatonin and corticosterone in 3-month old male Wistar rats. Every two hours for 24 h around the clock, an animal from the stressed group was first made to swim for two hours, and was then subjected to a further ten minutes of forced swimming using a modification of the apparatus employed in the Porsolt test. The capacity to resume swimming after the exhausting 2-hour swim was measured by the number of swimming movements that were made by the animal in the additional 10-min swimming period. Blood was collected immediately after the trial, and the plasma melatonin and corticosterone levels determined by RIA. Control group blood was collected at 1-h intervals in the periods from 22:00 to 06:00 and from 16:00 to 18:00, and at 2-h intervals during the remaining periods. The control rats presented plasma melatonin and corticosterone circadian rhythms with nocturnal (02:00) and diurnal (17:00) maxima, respectively. The pattern of these rhythms in the stressed rats was flatter, and the animals tested during hours of the night presented greater endurance than those tested during daytime hours. This suggests that, in evaluating an animal's response to stress, it is important to take into account the co-ordination between the time of day when the physical stressing test is applied and the natural sleep/activity periods of the study species.

KEY WORDS
Melatonin; corticosterone; behaviour; physical activity; stress; rat; circadian rhythms


REFERENCES
Abel EL: Physiological correlates of the forced swim test in rats. Physiol Behav 54:309-317, 1993a.

Abel EL: Physiological effects of alarm chemosignal emitted during the forced swim test. J Chem Ecol 19:2891-2901, 1993b.

Aoyama H, Mori N, Mori W: Anti-glucocorticoid effects of melatonin on adult rats. Acta Pathol Jap 37:1143-1148, 1987.

Arendt J: Melatonin and the mammalian pineal gland. Chapman and Hall, London 1995.

Barriga C, Marchena JM, Lea RW, Harvey S, Rodriguez AB: Effect of stress and dexamethasone treatment on circadian rhythms of melatonin and corticosterone in ring dove (Streptopelia risoria). Mol Cell Biochem 232:27-31, 2002.

Barriga C, Marchena JM, Ortega E, Martin M, Rodriguez AB: Melatonin levels and exercise in adolescent boys and girls. Biogenic Amines 15:643-653, 2000.

Barriga C, Martin MI, Tabla R, Ortega E, Rodriguez AB: Circadian rhythm of melatonin, corticosterone and phagocytosis: effect of stress. J Pineal Res 30:180-187, 2001.

Bartsch C, Bartsch H, Buchberger A et al.: Serial transplants of DMBA-induced mammary tumors in Fischer rats as a model system for human breast cancer. VI. The role of different forms of tumor-associated stress for the regulation of pineal melatonin secretion. Oncology 56:169-176, 1999.

Berger J: Why do circadian biorhythms age? J Appl Biomed 1:77-84, 2003.

Borer KT, Bestervelt LL, Mannheim M et al.: Stimulation by voluntary exercise of adrenal glucocorticoid secretion in mature female hamsters. Physiol Behav 51:713-718, 1992.

Brown GM: Light, melatonin and the sleep-wake cycle. J Psychiatry Neurosci 19:345-353, 1994.

Bunning E: The Physiological Clock. Springer, New York 1967.

Buxton OM, L'Hermite-Baleriaux M, Hirschfeld U, Cauter E: Acute and delayed effects of exercise on human melatonin secretion. J Biol Rhythms 12:568-574, 1997.

Carr DB: Plasma melatonin increases during exercise in women. J Clin Endocrinol Metab 53:224-225, 1981.

Davies KJA, Quintanilha AT, Brooks GA, Packer L: Free radicals and tissue damage produced by exercise. Biochem Biophys Res Comm 107:1198-1205, 1982.

Edery I: Circadian rhythms in a nutshell. Physiol Genomics 3:59-74, 2000.

Falcon J: Cellular circadian clocks in the pineal. Prog Neurobiol 58:121-162, 1999.

Feigelson P, Greengard O: Immunochemical evidence for increased titers of liver tryptophan pyrrolase during substrate and hormonal enzyme induction. J Biol Chem 237:3714-3717, 1962.

Ferry A, Weill B, Amiridis I, Laziry F, Rieu M: Splenic immunomodulation with swimminginduced stress in rats. Immunol Lett 29:261-264, 1991.

Forner MA, Barriga C, Rodriguez AB, Ortega E: A study of the role of corticosterone as a mediator in exercise-induced stimulation of murine macrophage phagocytosis. J Physiol 488(Pt 3):789-794, 1995.

Freeman BA, Crapo JD: Biology of disease: Free radicals and tissue injury. Lab Invest 47:412-426, 1982.

Hara M, Abe M, Suzuki T, Reiter RJ: Tissue changes in glutathione metabolism and lipid peroxidation induced by swimming are partially prevented by melatonin. Pharmacol Toxicol 78:308-312, 1996.

Hara M, Iigo M, Ohtani-Kaneko R et al.: Administration of melatonin and related indoles prevents exercise-induced cellular oxidative changes in rats. Biol Signals 6:90-100, 1997.

Jenkins RR: Free radical chemistry. Relation to exercise. Sports Med 5:156-170, 1988.

Joshi BN, Troiani ME, Milin J, Nurnburger F, Reiter RJ: Adrenal-mediated depression of Nacetyltransferase activity and melatonin levels in the rat pineal gland. Life Sci 38:1573-1580, 1986.

Kelliher P, Connor TJ, Harkin A et al.: Varying responses to the rat forced-swim test under diurnal and nocturnal conditions. Physiol Behav 69:531-539, 2000.

Kjaer M, Dela F: Endocrine responses to exercise. In: Hoffman-Goetz L (ed.), Exercise and immune function. Boca Raton. CRC, 1-20, 1996.

Lavie P: Sleep-wake as a biological rhythm. Ann Rev Psychol 52:277-303, 2001.

Lopez-Calderon A: Glandulas suprarrenales. In Tresguerres JAF (ed.), Fisiologia Humana. McGraw-Hill - Interamericana, Madrid 1999, pp. 931-951.

Lowestein PR, Pereyra EN, Gonzalez Solveyra C, Cardinali DP: Effect of naloxone on the nocturnal rise of rat pineal melatonin conent. Eur J Pharmacol 98:261-264, 1984.

Luboshitzky R, Yanai D, Shen-Orr Z et al.: Daily and seasonal variations in the concentration of melatonin in the human pineal gland. Brain Res Bull 47:271-276, 1998.

Maestroni GJ: The immunoendocrine role of melatonin. J Pineal Res 14:1-10, 1993.

Mazepa RC, Cuevas MJ, Collado PS, Gonzalez-Gallego J: Melatonin increases muscle and liver glycogen content in nonexercised and exercised rats. Life Sci 66:153-160, 2000.

Miyazaki T, Hashimoto S, Masubuchi S, Honma S, Honma KI: Phase-advance shifts of human circadian pacemaker are accelerated by day-time physical exercise. Am J Physiol Regul Integr Comp Physiol 281:R197-205, 2001.

Monteleone P, Maj M, Fuschino A, Kemali D: Physical stress in the middle of the dark phase does not affect light-depressed plasma melatonin levels in humans. Neuroendocrinology 55:367-371, 1992.

Monteleone P, Maj M, Fusco M, Orazzo C, Kemali D: Physical exercise at night blunts the nocturnal increase of plasma melatonin levels in healthy humans. Life Sci 47:1989-1995, 1990.

Nomura S, Shimizu J, Kinjo M, Kametani H, Nakazawa T: A new behavioural test for antidepressant drugs. Eur J Pharmacol 83:171-175, 1982.

Norris DO: Vertebrate endocrinology. Academic Press, New York 1997.

Novelli GP, Bracciotti G, Falsini S: Spintrappers and vitamin E prolong endurance to muscle fatigue in mice. Free Radic Biol Med 8:9-13, 1990.

Ortega E, Forner MA, Barriga C: Exerciseinduced stimulation of murine macrophage chemotaxis: role of corticosterone and prolactin a mediators. J Physiol 498(Pt 3):729-734, 1997.

Persengiev S, Kanchev L, Vezenkova G: Circadian patterns of melatonin, corticosterone, and progesterone in male rats subjected to chronic stress: effect of constant illumination. 11:57-62, 1991.

Pevet P: Melatonin and biological rhythms. Biol Signals Recept 9:203-212, 2000.

Plytycz B, Seljelid R: Rhythms of immunity. Arch Imm Ther Exper (Warsz) 45:157-162, 1997.

Porsolt RD, Anton G, Blavet N, Halfre M: Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379-391, 1978.

Reiter RJ: The melatonin rhythm: both a clock and a calendar. Experientia 49:654-664, 1993.

Reiter RJ, Richardson BA: Some perturbations that disturb the circadian melatonin rhythm. Chronobiol Int 9:314-321, 1992.

Reiter RJ, Tan DX, Poeggeler B, Kavet R: Inconsistent suppression of nocturnal pineal melatonin synthesis and serum melatonin levels in rats exposed to pulsed DC magnetic fields. Bioelectromagnetics 19:318-329, 1998.

Roberts AC, Martensz ND, Hastings MH, Herbert J: Changes in photoperiod alter the daily rhythms of pineal melatonin content and hypothalamic beta-endorphin content and the luteinizing hormone response to naloxone in the male Syrian hamster. Endocrinology 117:141-148, 1985.

Simon HB: Exercise and human immune functions. In: Arder R, Cohen N, Felten DL (eds.), Psychoneuroendocrinology. Academic Press, New York 1991, pp. 869-895.

Simonneaux V, Ribelayga C: Generation of the melatonin endocrine message in mammals: a review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters. Pharmacol Rev 55:325-395, 2003.

Skotnicka E, Hynczak AJ: Melatonin and its possible role in regulation of water and electrolyte metabolism. Med Weter 57:299-303, 2001.

Skwarlo-Sonta K: Functional connections between the pineal gland and immune system. Acta Neurobiol Exp (Wars) 56:341-357, 1996.

Tannenbaum MG, Reiter RJ, Hurlbut EC et al.: Pineal sensitivity to nighttime swimming stress changes during the active season in Richardson's ground squirrels (Spermophilus richardsonii). J Exp Zool 250:298-303, 1989.

Theron JJ, Oosthuizen JMC, Rautenbach MML: Effect of physical exercise on plasma melatonin levels in normal volunteers. South Afr Med J 66:838-841, 1984.

Troiani ME, Reiter RJ, Tannenbaum MG et al.: Neither the pituitary gland nor the sympathetic nervous system is responsible for eliciting the large drop in elevated rat pineal melatonin levels due to swimming. J Neural Transm 74:149-60, 1988a.

Troiani ME, Reiter RJ, Vaughan MK, Oaknin S, Vaughan GM: Swimming depresses nighttime melatonin content without changing N-acetyltransferase activity in the rat pineal gland. Neuroendocrinology 47:55-60, 1988b.

Turek FW: Circadian rhythms. Recent Prog Horm Res 49:43-90, 1994.

Urbanski HF: Influence of light and the pineal gland on biological rhythms. In: Conn PM, Freeman ME (eds.), Neuroendocrinology in Physiology and Medicine. Humana Press, Totowa 2000, pp. 405-420.

Van de Kar LD, Blair ML: Forebrain pathways mediating stress-induced hormone secretion. Front Neuroendocrinol 20:1-48, 1999.

Vaughan GM, Pelham RW, Pang SF et al.: Nocturnal elevation of plasma melatonin and urinary 5-hydroxindole acetic acid in young men: Attempts at modification by brief changes in environmental lighting and sleep by autonomic drugs. J Clin Endocrinol Metab 42:752-764, 1976.

Venditti P, Di Meo S: Effect of training on antioxidant capacity, tissue damage, and endurance of adult male rats. Int J Sports Med 18:497-502, 1997.

Windle RJ, Wood SA, Lightman SL, Ingram CD: The pulsatile characteristics of hypothalamo-pituitary-adrenal activity in female Lewis and Fischer 344 rats and its relationship to differential stress responses. Endocrinology 139:4044-4052, 1998.

Wu WT, Chen YC, Reiter RJ: Day-night differences in the response of the pineal gland swimming stress. Proc Soc Exp Biol Med 187:315-319, 1988.

Yaga K, Tan DX, Reiter RJ, Manchester LC, Hattori A: Unusual responses of nocturnal pineal melatonin synthesis and secretion to swimming: attempts to define mechanisms. J Pineal Res 14:90-103, 1993.
CITED

Bogdanova OV, Kanekar S, D'Anci KE, Renshaw PF. Factors influencing behavior in the forced swim test. Physiol Behav. 118: 227-239, 2013.

Escames G, Ozturk G, Bano-Otalora B, Pozo MJ, Madrid JA, Reiter RJ, Serrano E, Concepcion M, Acuna-Castroviejo D. Exercise and melatonin in humans: Reciprocal benefits. J Pineal Res. 52: 1-11, 2012.

Paredes SD, Barriga C, Reiter RJ, Rodriguez AB. Assessment of the potential role of tryptophan as the precursor of serotonin and melatonin for the aged sleep-wake cycle and immune function: Streptopelia risoria as a model. Int J Tryptophan Res. 2: 23-36, 2009.

Mateos SS, Sanchez CL, Paredes SD, Barriga C, Rodriguez AB. Circadian levels of serotonin in plasma and brain after oral administration of tryptophan in rats. Basic Clin Pharm Toxicol 104: 52-59, 2009.

Habibi A, Nikbakht M, Shakerian S, Ketabi S. Investigate and Compare the Effect of One Session Wrestling Training on Elite Wrestlers Dehydration, Hematocrit and Blood Electrolytes in the Morning and Evening. Proc First Join Int Pre-Olympic Conference Sports Sci Sports Eng, Vol II - Bio-Mech Sports Eng pp. 21-24, 2008.

Sanchez S, Sanchez CL, Paredes SD, Rodriguez AB, Barriga C. The effect of tryptophan administration on the circadian rhythms of melatonin in plasma and the pineal gland of rats. J Appl Biomed. 6: 177-186, 2008.

Sanchez S, Paredes SD, Sanchez CL, Barriga C, Reiter RJ, Rodriguez AB. Tryptophan administration in rats enhances phagocytic function and reduces oxidative metabolism. Neuroindocrinol Lett. 29: 1026-1032, 2008.

Paredes SD, Terron MP, Valero V, Barriga C, Reiter RJ, Rodriguez AB. Orally administered melatonin improves nocturnal rest in young and old ringdoves (Streptopelia risoria). Basic Clin Pharm Toxicol. 100: 258-268, 2007.

Paredes SD, Sanchez S, Parvez H, Rodriguez AB, Barriga C. Altered circadian rhythms of corticosterone, melatonin, and phagocytic activity in response to stress in rats. Neuroindocrinol Lett. 28: 489-495, 2007.

Paredes SD, Sanchez S, Parvez H, Rodriguez AB, Barriga C. Altered circadian rhythms of corticosterone, melationin, and phagocytic activity in response to stress in rats. Biog Amines. 21: 101-112, 2007.

Paredes SD, Terron MP, Marchena AM, Barriga C, Pariente JA, Reiter RJ, Rodriguez AB. Effect of exogenous melatonin on viability, ingestion capacity, and free-radical scavenging in heterophils from young and old ringdoves (Streptopelia risoria). Mol Cell Biochem. 304: 305-314, 2007.

Paredes SD, Terron MP, Marchena AM, Barriga C, Pariente JA, Reiter RJ, Rodriguez AB. Tryptophan modulates cell viability, phagocytosis and oxidative metabolism in old ringdoves. Basic Clin Pharm Toxicol. 101: 56-62, 2007.

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