@2024 Afarand., IRAN
ISSN: 2252-0805 The Horizon of Medical Sciences 2018;24(4):316-323
ISSN: 2252-0805 The Horizon of Medical Sciences 2018;24(4):316-323
The Effect of Voluntary Training on Testosterone and Corticosterone Levels in Male Rats Following Maternal Separation
ARTICLE INFO
Article Type
Original ResearchAuthors
Yazdanshenas A. (1)Peeri M. (*)
Azarbyjani M.A. (1)
(*) Department of Exercise Physiology, Central Tehran Branch, Islamic Azad University, Tehran, Iran
(1) Department of Exercise Physiology, Central Tehran Branch, Islamic Azad University, Tehran, Iran
Correspondence
Address: Department of Exercise Physiology, Central Tehran Branch, Islamic Azad University, Tehran, IranPhone: +98 9151066146
Fax: +98 51 38790418
m.peeri@iauctb.ac.ir
Article History
Received: June 12, 2018Accepted: July 24, 2018
ePublished: October 10, 2018
ABSTRACT
Aims
The present study intends to study the effect of volunteering exercises
during adolescence on testosterone and corticosterone levels in male rats
following childhood stress.
Materials & Methods In the present study, 36 male rats were selected as subjects and separated from their mothers from 2 to 14 days for 180 minutes. Then, to determine the experimental and control groups, on the 21st day, these randomly assigned random variables were divided into 3 groups. The groups included control, with stress separated from the mother, a wheel of two rodents. The first group experienced maternal separation from 2 to 14 days, and the control group was kept from the beginning with the mother. The training groups also started volunteering on the 21st birthday. The testosterone and cortisol levels of all groups were measured and the data were statistically analyzed by T and ANOVA methods at a significant level (P< 0.05).
Findings The results showed that maternal stress severity significantly increased cortisol levels and decreased testosterone levels. On the other hand voluntary exercise, in comparison with the stress group, has increased testosterone levels and significantly reduced cortisol levels.
Conclusion The results of the study showed that exercise, especially voluntary exercise, during adolescence, reduced stress and decreased depression and anxiety behaviors in adulthood.
Materials & Methods In the present study, 36 male rats were selected as subjects and separated from their mothers from 2 to 14 days for 180 minutes. Then, to determine the experimental and control groups, on the 21st day, these randomly assigned random variables were divided into 3 groups. The groups included control, with stress separated from the mother, a wheel of two rodents. The first group experienced maternal separation from 2 to 14 days, and the control group was kept from the beginning with the mother. The training groups also started volunteering on the 21st birthday. The testosterone and cortisol levels of all groups were measured and the data were statistically analyzed by T and ANOVA methods at a significant level (P< 0.05).
Findings The results showed that maternal stress severity significantly increased cortisol levels and decreased testosterone levels. On the other hand voluntary exercise, in comparison with the stress group, has increased testosterone levels and significantly reduced cortisol levels.
Conclusion The results of the study showed that exercise, especially voluntary exercise, during adolescence, reduced stress and decreased depression and anxiety behaviors in adulthood.
CITATION LINKS
[1]Lupien SJ, Mc Ewen BS, Gunnar MR, Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci. 2009;10(6):434-45.
[2]Rao U, Chen LA, Bidesi AS, Shad MU, Thomas MA, Hammen CL. Hippocampal changes associated with early-life adversity and vulnerability to depression. Biol Psychiatry. 2010;67(4):357-64.
[3]Rice D, Barone S Jr. Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environ Health Perspect. 2000;108 Suppl 3:511-33.
[4]Marco EM, Llorente R, López-Gallardo M, Mela V, Llorente-Berzal Á, Prada C, et al. The maternal deprivation animal model revisited. Neurosci Biobehav Rev. 2015;51:151-63.
[5]Fry RW, Morton AR, Keast D. Overtraining in athletes, an update. Sports Med. 1991;12(1):32-65.
[6]Khalfa S, Bella SD, Roy M, Peretz I, Lupien SJ. Effects of relaxing music on salivary cortisol level after psychological stress. Ann N Y Acad Sci. 2003;999:374-6.
[7]Taylor SE, Burklund LJ, Eisenberger NI, Lehman BJ, Hilmert CJ, Lieberman MD. Neural bases of moderation of cortisol stress responses by psychosocial resources. J Pers Soc Psychol. 2008;95(1):197-211.
[8]Miller DB, O'Callaghan JP. Neuroendocrine aspects of the response to stress. Metabolism. 2002;51(6 Suppl 1):5-10.
[9]Diaz E, Ruiz F, Hoyos I, Zubero J, Gravina L, Gil J, et al. Cell damage, antioxidant status, and cortisol levels related to nutrition in ski mountaineering during a two-day race. J Sports Sci Med. 2010;9(2):338-46.
[10]Karlsson MK, Nordqvist A, Karlsson C. Physical activity, muscle function, falls and fractures. Food Nutr Res. 2008;52.
[11]Aakvaag A, Sand T, Opstad PK, Fonnum F. Hormonal changes in serum in young men during prolonged physical strain. Eur J Appl Physiol Occup Physiol. 1978;39(4):283-91.
[12]Chichinadze K, Chichinadze N. Stress-induced increase of testosterone: Contributions of social status and sympathetic reactivity. Physiol Behav. 2008;94(4):595-603.
[13]Rivier C, Rivest S. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: Peripheral and central mechanisms. Biol Reprod. 1991;45(4):523-32.
[14]Chrousos GP. Ultradian, circadian, and stress-related hypothalamic-pituitary-adrenal axis activity--a dynamic digital-to-analog modulation. Endocrinology. 1998;139(2):437-40.
[15]Francis DD, Diorio J, Plotsky PM, Meaney MJ. Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci. 2003; 22(18): 3-7840.
[16]Salmon P. Effects of physical exercise on anxiety, depression, and sensitivity to stress: A unifying theory. Clin Psychol Rev. 2001;21(1):33-61.
[17]Sahafi E, Peeri M, Hosseini MJ, Azarbayjani MA. Corrigendum to "Cardiac oxidative stress following maternal separation stress was mitigated following adolescent voluntary exercise in adult male rat "(Physiol Behav. 2018;183:39-45). Physiol Behav. 2018;185:121.
[18]Patki G, Li L, Allam F, Solanki N, Dao AT, Alkadhi K, et al. Moderate treadmill exercise rescues anxiety and depression-like behavior as well as memory impairment in a rat model of posttraumatic stress disorder. Physiol Behav. 2014;130:47-53.
[19]Burghardt PR, Fulk LJ, Hand GA, Wilson MA. The effects of chronic treadmill and wheel running on behavior in rats. Brain Res. 2004;1019(1-2):84-96.
[20]Fattahi Masrour F, Peeri M, Azarbayjani MA, Hosseini MJ. Voluntary exercise during adolescence mitigated negative the effects of maternal separation stress on the depressive-like behaviors of adult male rats: Role of NMDA receptors. Neurochem Res. 2018;43(5):1067-74.
[21]Gorji A, Mirdar Sh, Nazari S, Hedayati M. The effect of endurance training and curcumin supplement on lung HIF- α1 levels in rat exposed to lead acetate. Physiol Exerc Phys Act. 2012;7:523-34. [Persian]
[22]Lancaster GI, Febbraio MA. The immunomodulating role of exercise in metabolic disease. Trends Immunol. 2014;35(6):262-9.
[23]Foster JA, Mc Vey Neufeld KA. Gut-brain axis: How the microbiome influences anxiety and depression. Trends Neurosci. 2013;36(5):305-12.
[24]Cryan JF, O'Mahony SM. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil. 2011;23(3):187-92.
[25]O'Mahony SM, Hyland NP, Dinan TG, Cryan JF. Maternal separation as a model of brain-gut axis dysfunction. Psychopharmacology (Berl). 2011;214(1):71-88.
[26]O'Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, et al. Early life stress alters behavior, immunity, and microbiota in rats: Implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry. 2009;65(3):263-7.
[27]Graff LA, Walker JR, Bernstein CN. Depression and anxiety in inflammatory bowel disease: A review of comorbidity and management. Inflamm Bowel Dis. 2009;15(7):1105-18.
[28]Roozendaal B, Quirarte GL, Mc Gaugh JL. Stress-activated hormonal systems and the regulation of memory storage. Ann N Y Acad Sci. 1997;821:247-58.
[29]Beato M, Sánchez-Pacheco A. Interaction of steroid hormone receptors with the transcription initiation complex. Endocr Rev. 1996;17(6):587-609.
[30]Ströhle A. Physical activity, exercise, depression and anxiety disorders. J Neural Transm (Vienna). 2009;116(6):777-84.
[31]Romero-Martínez A, González-Bono E, Lila M, Moya-Albiol L. Testosterone/cortisol ratio in response to acute stress: A possible marker of risk for marital violence. Soc Neurosci. 2013;8(3):240-7.
[32]Tremblay MS, Chu SY. Hormonal response to exercise. In: Warren MP, Constantini NW, editors. Sports endocrinology. Totowa NJ: Humana Press; 2000. pp. 1-30.
[33]Filaire E, Bernain X, Sagnol M, Lac G. Preliminary results on mood state, salivary testosterone: Cortisol ratio and team performance in a professional soccer team. Eur J Appl Physiol. 2001;86(2):179-84.
[34]Salvador A, Suay F, González-Bono E, Serrano MA. Anticipatory cortisol, testosterone and psychological responses to judo competition in young men. Psychoneuroendocrinology. 2003;28(3):364-75.
[35]Lundberg S, Martinsson M, Nylander I, Roman E. Altered corticosterone levels and social play behavior after prolonged maternal separation in adolescent male but not female Wistar rats. Horm Behav. 2017;87:137-44.
[36]Mehta PH, Jones AC, Josephs RA. The social endocrinology of dominance: Basal testosterone predicts cortisol changes and behavior following victory and defeat. J Pers Soc Psychol. 2008;94(6):1078-93.
[37]Herbert J. Cortisol and depression: Three questions for psychiatry. Psychol Med. 2013;43(3):449-69.
[38]Kenefick RW, Maresh CM, Armstrong LE, Castellani JW, Whittlesey M, Hoffman JR, et al. Plasma testosterone and cortisol responses to training-intensity exercise in mild and hot environments. Int J Sports Med. 1998;19(3):177-81.
[39]Adlercreutz H, Härkönen M, Kuoppasalmi K, Näveri H, Huhtaniemi I, Tikkanen H, et al. Effect of training on plasma anabolic and catabolic steroid hormones and their response during physical exercise. Int J Sports Med. 1986;7 Suppl 1:27-8.
[40]Maresh CM, Whittlesey MJ, Armstrong LE, Yamamoto LM, Judelson DA, Fish KE, et al. Effect of hydration state on testosterone and cortisol responses to training-intensity exercise in collegiate runners. Int J Sports Med. 2006;27(10):765-70.
[41]Nabkasorn C, Miyai N, Sootmongkol A, Junprasert S, Yamamoto H, Arita M, et al. Effects of physical exercise on depression, neuroendocrine stress hormones and physiological fitness in adolescent females with depressive symptoms. Eur J Public Health. 2006;16(2):179-84.
[42]Daniels WM, Marais L, Stein DJ, Russell VA. Exercise normalizes altered expression of proteins in the ventral hippocampus of rats subjected to maternal separation. Exp Physiol. 2012;97(2):239-47.
[43]Bekinschtein P, Oomen CA, Saksida LM, Bussey TJ. Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable?. Semin Cell Dev Biol. 2011;22(5):536-42.
[44]Olson AK, Eadie BD, Ernst C, Christie BR. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus. 2006;16(3):250-60.
[45]Ernst M, Romeo RD, Andersen SL. Neurobiology of the development of motivated behaviors in adolescence: A window into a neural systems model. Pharmacol Biochem Behav. 2009;93(3):199-211.
[46]Morley-Fletcher S, Rea M, Maccari S, Laviola G. Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci. 2003;18(12):3367-74.
[47]Lane AR, Duke JW, Hackney AC. Influence of dietary carbohydrate intake on the free testosterone: Cortisol ratio responses to short-term intensive exercise training. Eur J Appl Physiol. 2010;108(6):1125-31.
[48]Tremblay MS, Chu SY, Mureika R. Methodological and statistical considerations for exercise-related hormone evaluations. Sports Med. 1995;20(2):90-108.
[49]Eyre H, Baune BT. Neuroimmunological effects of physical exercise in depression. Brain Behav Immun. 2012;26(2):251-66.
[50]Sigwalt AR, Budde H, Helmich I, Glaser V, Ghisoni K, Lanza S, et al. Molecular aspects involved in swimming exercise training reducing anhedonia in a rat model of depression. Neuroscience. 2011;192:661-74.
[2]Rao U, Chen LA, Bidesi AS, Shad MU, Thomas MA, Hammen CL. Hippocampal changes associated with early-life adversity and vulnerability to depression. Biol Psychiatry. 2010;67(4):357-64.
[3]Rice D, Barone S Jr. Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environ Health Perspect. 2000;108 Suppl 3:511-33.
[4]Marco EM, Llorente R, López-Gallardo M, Mela V, Llorente-Berzal Á, Prada C, et al. The maternal deprivation animal model revisited. Neurosci Biobehav Rev. 2015;51:151-63.
[5]Fry RW, Morton AR, Keast D. Overtraining in athletes, an update. Sports Med. 1991;12(1):32-65.
[6]Khalfa S, Bella SD, Roy M, Peretz I, Lupien SJ. Effects of relaxing music on salivary cortisol level after psychological stress. Ann N Y Acad Sci. 2003;999:374-6.
[7]Taylor SE, Burklund LJ, Eisenberger NI, Lehman BJ, Hilmert CJ, Lieberman MD. Neural bases of moderation of cortisol stress responses by psychosocial resources. J Pers Soc Psychol. 2008;95(1):197-211.
[8]Miller DB, O'Callaghan JP. Neuroendocrine aspects of the response to stress. Metabolism. 2002;51(6 Suppl 1):5-10.
[9]Diaz E, Ruiz F, Hoyos I, Zubero J, Gravina L, Gil J, et al. Cell damage, antioxidant status, and cortisol levels related to nutrition in ski mountaineering during a two-day race. J Sports Sci Med. 2010;9(2):338-46.
[10]Karlsson MK, Nordqvist A, Karlsson C. Physical activity, muscle function, falls and fractures. Food Nutr Res. 2008;52.
[11]Aakvaag A, Sand T, Opstad PK, Fonnum F. Hormonal changes in serum in young men during prolonged physical strain. Eur J Appl Physiol Occup Physiol. 1978;39(4):283-91.
[12]Chichinadze K, Chichinadze N. Stress-induced increase of testosterone: Contributions of social status and sympathetic reactivity. Physiol Behav. 2008;94(4):595-603.
[13]Rivier C, Rivest S. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: Peripheral and central mechanisms. Biol Reprod. 1991;45(4):523-32.
[14]Chrousos GP. Ultradian, circadian, and stress-related hypothalamic-pituitary-adrenal axis activity--a dynamic digital-to-analog modulation. Endocrinology. 1998;139(2):437-40.
[15]Francis DD, Diorio J, Plotsky PM, Meaney MJ. Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci. 2003; 22(18): 3-7840.
[16]Salmon P. Effects of physical exercise on anxiety, depression, and sensitivity to stress: A unifying theory. Clin Psychol Rev. 2001;21(1):33-61.
[17]Sahafi E, Peeri M, Hosseini MJ, Azarbayjani MA. Corrigendum to "Cardiac oxidative stress following maternal separation stress was mitigated following adolescent voluntary exercise in adult male rat "(Physiol Behav. 2018;183:39-45). Physiol Behav. 2018;185:121.
[18]Patki G, Li L, Allam F, Solanki N, Dao AT, Alkadhi K, et al. Moderate treadmill exercise rescues anxiety and depression-like behavior as well as memory impairment in a rat model of posttraumatic stress disorder. Physiol Behav. 2014;130:47-53.
[19]Burghardt PR, Fulk LJ, Hand GA, Wilson MA. The effects of chronic treadmill and wheel running on behavior in rats. Brain Res. 2004;1019(1-2):84-96.
[20]Fattahi Masrour F, Peeri M, Azarbayjani MA, Hosseini MJ. Voluntary exercise during adolescence mitigated negative the effects of maternal separation stress on the depressive-like behaviors of adult male rats: Role of NMDA receptors. Neurochem Res. 2018;43(5):1067-74.
[21]Gorji A, Mirdar Sh, Nazari S, Hedayati M. The effect of endurance training and curcumin supplement on lung HIF- α1 levels in rat exposed to lead acetate. Physiol Exerc Phys Act. 2012;7:523-34. [Persian]
[22]Lancaster GI, Febbraio MA. The immunomodulating role of exercise in metabolic disease. Trends Immunol. 2014;35(6):262-9.
[23]Foster JA, Mc Vey Neufeld KA. Gut-brain axis: How the microbiome influences anxiety and depression. Trends Neurosci. 2013;36(5):305-12.
[24]Cryan JF, O'Mahony SM. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil. 2011;23(3):187-92.
[25]O'Mahony SM, Hyland NP, Dinan TG, Cryan JF. Maternal separation as a model of brain-gut axis dysfunction. Psychopharmacology (Berl). 2011;214(1):71-88.
[26]O'Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, et al. Early life stress alters behavior, immunity, and microbiota in rats: Implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry. 2009;65(3):263-7.
[27]Graff LA, Walker JR, Bernstein CN. Depression and anxiety in inflammatory bowel disease: A review of comorbidity and management. Inflamm Bowel Dis. 2009;15(7):1105-18.
[28]Roozendaal B, Quirarte GL, Mc Gaugh JL. Stress-activated hormonal systems and the regulation of memory storage. Ann N Y Acad Sci. 1997;821:247-58.
[29]Beato M, Sánchez-Pacheco A. Interaction of steroid hormone receptors with the transcription initiation complex. Endocr Rev. 1996;17(6):587-609.
[30]Ströhle A. Physical activity, exercise, depression and anxiety disorders. J Neural Transm (Vienna). 2009;116(6):777-84.
[31]Romero-Martínez A, González-Bono E, Lila M, Moya-Albiol L. Testosterone/cortisol ratio in response to acute stress: A possible marker of risk for marital violence. Soc Neurosci. 2013;8(3):240-7.
[32]Tremblay MS, Chu SY. Hormonal response to exercise. In: Warren MP, Constantini NW, editors. Sports endocrinology. Totowa NJ: Humana Press; 2000. pp. 1-30.
[33]Filaire E, Bernain X, Sagnol M, Lac G. Preliminary results on mood state, salivary testosterone: Cortisol ratio and team performance in a professional soccer team. Eur J Appl Physiol. 2001;86(2):179-84.
[34]Salvador A, Suay F, González-Bono E, Serrano MA. Anticipatory cortisol, testosterone and psychological responses to judo competition in young men. Psychoneuroendocrinology. 2003;28(3):364-75.
[35]Lundberg S, Martinsson M, Nylander I, Roman E. Altered corticosterone levels and social play behavior after prolonged maternal separation in adolescent male but not female Wistar rats. Horm Behav. 2017;87:137-44.
[36]Mehta PH, Jones AC, Josephs RA. The social endocrinology of dominance: Basal testosterone predicts cortisol changes and behavior following victory and defeat. J Pers Soc Psychol. 2008;94(6):1078-93.
[37]Herbert J. Cortisol and depression: Three questions for psychiatry. Psychol Med. 2013;43(3):449-69.
[38]Kenefick RW, Maresh CM, Armstrong LE, Castellani JW, Whittlesey M, Hoffman JR, et al. Plasma testosterone and cortisol responses to training-intensity exercise in mild and hot environments. Int J Sports Med. 1998;19(3):177-81.
[39]Adlercreutz H, Härkönen M, Kuoppasalmi K, Näveri H, Huhtaniemi I, Tikkanen H, et al. Effect of training on plasma anabolic and catabolic steroid hormones and their response during physical exercise. Int J Sports Med. 1986;7 Suppl 1:27-8.
[40]Maresh CM, Whittlesey MJ, Armstrong LE, Yamamoto LM, Judelson DA, Fish KE, et al. Effect of hydration state on testosterone and cortisol responses to training-intensity exercise in collegiate runners. Int J Sports Med. 2006;27(10):765-70.
[41]Nabkasorn C, Miyai N, Sootmongkol A, Junprasert S, Yamamoto H, Arita M, et al. Effects of physical exercise on depression, neuroendocrine stress hormones and physiological fitness in adolescent females with depressive symptoms. Eur J Public Health. 2006;16(2):179-84.
[42]Daniels WM, Marais L, Stein DJ, Russell VA. Exercise normalizes altered expression of proteins in the ventral hippocampus of rats subjected to maternal separation. Exp Physiol. 2012;97(2):239-47.
[43]Bekinschtein P, Oomen CA, Saksida LM, Bussey TJ. Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable?. Semin Cell Dev Biol. 2011;22(5):536-42.
[44]Olson AK, Eadie BD, Ernst C, Christie BR. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus. 2006;16(3):250-60.
[45]Ernst M, Romeo RD, Andersen SL. Neurobiology of the development of motivated behaviors in adolescence: A window into a neural systems model. Pharmacol Biochem Behav. 2009;93(3):199-211.
[46]Morley-Fletcher S, Rea M, Maccari S, Laviola G. Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci. 2003;18(12):3367-74.
[47]Lane AR, Duke JW, Hackney AC. Influence of dietary carbohydrate intake on the free testosterone: Cortisol ratio responses to short-term intensive exercise training. Eur J Appl Physiol. 2010;108(6):1125-31.
[48]Tremblay MS, Chu SY, Mureika R. Methodological and statistical considerations for exercise-related hormone evaluations. Sports Med. 1995;20(2):90-108.
[49]Eyre H, Baune BT. Neuroimmunological effects of physical exercise in depression. Brain Behav Immun. 2012;26(2):251-66.
[50]Sigwalt AR, Budde H, Helmich I, Glaser V, Ghisoni K, Lanza S, et al. Molecular aspects involved in swimming exercise training reducing anhedonia in a rat model of depression. Neuroscience. 2011;192:661-74.