@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
BRIEF TEXT
Depression is one of the most common psychiatric disorders and is the leading cause of disability in the 21st Century. The experience of the primary stress of life plays a key role in the development of mood disorders in humans and rodents [1, 2].
... [3]. Maternal deprivation has been reported as a valid model for investigating rodent depression behaviors [4]. According to studies, testosterone is an anabolic hormone that stimulates Protein synthesis, and plays an important role in the growth and maintenance of muscle tissue [5]. Cortisol is also a catabolic hormone and indeed the most important anti-anxiolytic hormone in the body [6]. ... [7, 8]. Studies have shown that increased levels of cortisol in the bloodstream have negative effects on the body, including an imbalance in blood glucose levels, bone loss and muscle atrophy, weakening of the body's defenses, and stimulant responses, etc. [9,10]. ... [11-14]. Although several studies have been conducted to find effective treatments for depressive disorders, little progress has been made. Recently, non-medical treatments (such as physical activity and environmental enrichment) have been shown to have potential therapeutic effects in the treatment of depression [15, 16]. Focusing on animal studies, it has been shown that any voluntary exercise has antidepressant effects in rodents [17, 18]. ... [19, 20].
The present study aimed at investigating the effect of volunteering exercises during adolescence on testosterone and corticosterone levels in male rats following childhood stress.
The present study is an experimental research.
This study was conducted on Wistar pregnant female rats in Tehran.
This study was conducted on 15 Wistar pregnant female rats.
After giving birth, 36 male baby rats were selected as the sample and 24 rats were separated from their mothers from 2nd to 14th days for 180 min (3 h). On day 21, the rats were randomly assigned into the experimental and control groups (each group=12 rats) and each 4rats kept in a cage until the day 28. The groups included control (no maternal deprivation), maternal deprivation, and rodent running wheel groups. During the study, the animals were kept in cages with a temperature of 22±22°C and 50±5% humidity under controlled conditions of light (12:12 h light-dark cycle) and were free to standard water and food (10 g per 100 g of body weight) as pellets (Behpour Co.). Volunteering exercises protocol On the day 2 after birth, rodent running wheel groups (12 rats) were placed on the machine for one week for adaption. Rodent running wheel protocol was used in accordance with the method used by Gorji et al. [21]. Two rats (male and female) with MS were kept in each training cage. The rats had free access to the running wheel for 24 h a day for 32 days, which lasted until the day 60 of birth, and the daily distance traveled (km) was recorded. To avoid social isolation effects, two rats were isolated in a cage by a permeable glass sheet that made them able to contact. On the 60th day after birth, blood samples were taken by direct blood sampling from the heart. After serum separation by centrifugation, blood samples were stored at -20°C until blood samples were taken. Cortisol hormone concentration was measured by ELISA and the kits (Cortisol ELISA, IBL International, Germany, 2.5 ng/ml) and testosterone was assessed by (CLIA Testosterone AccuLite TM, Monobind Inc., USA, 0.026 ng/ml) by luminescence quantitative method. The testosterone/cortisol ratio was also calculated by dividing the testosterone concentration (ng/ml) into serum cortisol concentration (ng/ml). T-test and one-way ANOVA using Graph-pad prism software were used for quantitative analysis of data between groups using.
The stress caused by maternal deprivation significantly increased cortisol levels and considerably and significantly decreased testosterone levels in male rats. The mean difference of cortisol and testosterone levels between MS and control group was 223.95±45.45 μg/dl and -2.22±0.27 nm/l, respectively, which showed a significant difference between two groups (p=0.0002; p=0.039). In addition, the mean difference of cortisol/testosterone in the MS and control groups was -0.007852±-0.001581, which showed a significant difference between two groups (P=0.002; Table 1). Figure 1-a shows the effects of MS on cortisol levels. One-way ANOVA analysis showed an increase in cortisol level (df=13, t=4, P<0.05) in MS groups compared with the control animals. Figure 1b also shows a significant reduction in testosterone levels (t=6, t=8, P<0.0005) in MS groups compared with the control group. On the other hand, in Figure 1-c indicates a significant decrease (t=6, t=4, P<0.005) in the testosterone/cortisol ratio in MS group compared with the control group. Voluntary exercise in adolescents led to moderated levels of cortisol and testosterone induced by MS in rats. We investigated the potential protective effect of voluntary exercise on altered levels of cortisol and testosterone induced by MS in rats.
According to the evidences, stressful life events in the early stages of life have profound and prolonged effects on the brain and behavior [1]. In addition, the results of the current research showed that primary stress in life can disable individuals in controlling immune disorders and expose them to bacterial infections. Earlier studies have shown that early life stresses like MS are associated with psychological manifestations as well as cerebrospinal dysfunction [22]. In this regard, brain dysfunction has been reported to play an important role in anxiety and post-MS depression [23]. It is now quite obvious that disruption of the brain-visceral axis following stressful events in the early stages of life is associated with stress and abnormal behaviors [24]. The correlation between abdominal disorders (such as IBD and IBS) and mood and anxiety disorders has been reported in extensive studies. It has also been stated that hypothalamic-pituitary axis, immunity, intestinal inflammation and microbiota help to develop brain-gut axis dysfunction [25-27]. Our results are consistent with previous studies that MS can stimulate depressive behaviors in rodents [4]. .... [28-39]. In this study, the effect of volunteering exercise with moderate intensity on testosterone/cortisol ratio was investigated. Testosterone and cortisol concentrations are very sensitive to exercise. These concentrations can be influenced by the state and duration of exercise. [40]. ... [41-50].
It is suggested that more studies be done to determine the type, frequency and duration of exercise.
There are some differences between human and rodent immune markers; therefore, these differences should be further explored.
Exercise, especially voluntary exercise, during adolescence, reduced stress and decreased depression and anxiety behaviors in adulthood.
Special thanks to Mr. Prof. Mohsenzad Peeri, as a supervisor, for his support in selecting the topic of the thesis, the establishment of the specialized laboratory as well as conducting and writing the thesis and article.
None declared.
None declared.
This study was supported by the authors.
TABLES and CHARTS
Show attach fileCITIATION LINKS
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[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.