Central mechanisms of HPA axis regulation by voluntary exercise

NeuroMolecular Medicine

Volumn 10, Issue 2, 2008, Pages 118-127

  Stranahan, Alexis M ^a,b   Lee, Kim ^a   Mattson, Mark P ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

Glucocorticoid; Hippocampus; Hypothalamus; Stress; Wheel running

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTEROID; CORTICOSTERONE; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID;

ADAPTATION; BRAIN; CORRELATION ANALYSIS; CORTICOSTERONE BLOOD LEVEL; EXERCISE; GENOTYPE; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; NONHUMAN; PRIORITY JOURNAL; REVIEW; RUNNING; SEX DIFFERENCE; SOCIAL STRESS; STRESS; ANIMAL; ANIMAL EXPERIMENT; COGNITION; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; KINESIOTHERAPY; MENTAL STRESS; METABOLISM; MOTOR ACTIVITY; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ANIMALS; EXERCISE THERAPY; GLUCOCORTICOIDS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MOTOR ACTIVITY; NEURONAL PLASTICITY; PHYSICAL CONDITIONING, ANIMAL; PITUITARY-ADRENAL SYSTEM; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL; VOLITION;

EID: 52049106816     PISSN: 15351084     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12017-008-8027-0     Document Type: Review

References (73)

1. P. A. Adlard C. W. Cotman 2004 Voluntary exercise protects against stress-induced decreases in brain-derived neurotrophic factor protein expression Neuroscience 124 985 992
2. J. Amat M. V. Baratta E. Paul S. T. Bland L. R. Watkins S. F. Maier 2005 Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus Nature Neuroscience 8 365 371
3. E. A. Antoniadis C. H. Ko M. R. Ralph R. J. McDonald 2000 Circadian rhythms, aging and memory Behavioural Brain Research 114 221 233
4. D. R. Baldwin Z. C. Wilcox R. C. Baylosis 1995 Impact of differential housing on humoral immunity following exposure to an acute stressor in rats Physiology and Behaviour 57 649 653
5. Bao, A. M., Meynen, G. & Swaab, D. F. (2007). The stress system in depression and neurodegeneration: Focus on the human hypothalamus. Brain Research Reviews. doi: 10.1016/j.brainresrev.2007.04.005.
6. M. S. Bauer 1990 Intensity and precision of circadian wheel running in three outbred rat strains Physiology and Behaviour 47 397 401
7. T. W. Belke J. P. Wagner 2005 The reinforcing property and the rewarding aftereffect of wheel running in rats: A combination of two paradigms Behavioural Processes 68 165 172
8. N. C. Berchtold J. P. Kesslak C. J. Pike P. A. Adlard C. W. Cotman 2001 Estrogen and exercise interact to regulate brain-derived neurotrophic factor mRNA and protein expression in the hippocampus European Journal of Neuroscience 14 1992 2002
9. C. Bielajew A. T. Konkle Z. Merali 2002 The effects of chronic mild stress on male Sprague-Dawley and Long Evans rats: I. Biochemical and physiological analyses Behavioural Brain Research 136 583 592
10. A. Bjornebekk A. A. Mathe S. Brene 2005 The antidepressant effect of running is associated with increased hippocampal cell proliferation International Journal of Neuropsychopharmacology 8 357 368
11. P. R. Burghardt R. K. Pasumarthi M. A. Wilson J. Fadel 2006 Alterations in fear conditioning and amygdalar activation following chronic wheel running in rats Pharmacology, Biochemistry, and Behaviour 84 306 312
12. S. Cabib C. Castellano F. R. Patacchioli G. Cigliana L. Angelucci S. Puglisi-Allegra 1996 Opposite strain-dependent effects of post-training corticosterone in a passive avoidance task in mice: Role of dopamine Brain Research 729 110 118
13. J. Campisi T. H. Leem B. N. Greenwood 2003 Habitual physical activity facilitates stress-induced HSP72 induction in brain, peripheral, and immune tissues American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 284 R520 30
14. G. Collier E. Hirsch D. Levitsky A. I. Leshner 1975 Effort as a dimension of spontaneous activity in rats Journal of Comparative Physiological Psychology 88 89 96
15. P. Dahlqvist A. Ronnback A. Risedal 2003 Effects of postischemic environment on transcription factor and serotonin receptor expression after permanent focal cortical ischemia in rats Neuroscience 119 643 652
16. E. R. De Kloet 2004 Hormones and the stressed brain Annals of the New York Academy of Sciences 1018 1 15
17. S. Dronjak L. Gavrilovic D. Filipovic M. B. Radojcic 2004 Immobilization and cold stress affect sympatho-adrenomedullary system and pituitary- adrenocortical axis of rats exposed to long-term isolation and crowding Physiology and Behavior 81 409 415
18. S. K. Droste Y. Chandramohan L. E. Hill A. C. Linthorst J. M. Reul 2007 Voluntary exercise impacts on the rat hypothalamic-pituitary-adrenocortical axis mainly at the adrenal level Neuroendocrinology 86 26 37
19. S. K. Droste A. Gesing S. Ulbricht M. B. Muller A. C. Linthorst J. M. Reul 2003 Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary-adrenocortical axis Endocrinology 144 3012 3023
20. S. K. Droste M. C. Schweizer S. Ulbricht J. M. Reul 2006 Long-term voluntary exercise and the mouse hypothalamic-pituitary-adrenocortical axis: Impact of concurrent treatment with the antidepressant drug tianeptine Journal of Neuroendocrinology 18 915 925
21. B. D. Eadie V. A. Redila B. R. Christie 2005 Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density Journal of Comparative Neurology 486 39 47
22. S. Fediuc J. E. Campbell M. C. Riddell 2006 Effect of voluntary wheel running on circadian corticosterone release and on HPA axis responsiveness to restraint stress in Sprague-Dawley rats Journal of Applied Physiology 100 1867 1875
23. S. A. Ferguson A. M. Cada 2003 A longitudinal study of short- and long-term activity levels in male and female spontaneously hypertensive, Wistar-Kyoto, and Sprague-Dawley rats Behavoral Neuroscience 117 271 282
24. D. A. Freeman I. Zucker 2000 Temperature-independence of circannual variations in circadian rhythms of golden-mantled ground squirrels Journal of Biological Rhythms 15 336 343
25. I. Girard T. Garland Jr. 2002 Plasma corticosterone response to acute and chronic voluntary exercise in female house mice Journal of Applied Physiology 92 1553 1561
26. J. P. Herman M. M. Ostrander N. K. Mueller H. Figueiredo 2005 Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis Progress in Neuropsychopharmacology and Biological Psychiatry 29 1201 1213
27. I. H. Iversen 1993 Techniques for establishing schedules with wheel running as reinforcement in rats Journal of Experimental Analaysis of Behavior 60 219 238
28. R. A. Johnson G. S. Mitchell 2003 Exercise-induced changes in hippocampal brain-derived neurotrophic factor and neurotrophin-3: Effects of rat strain Brain Research 983 108 114
29. B. C. Jones A. Sarrieau C. L. Reed M. R. Azar P. Mormede 1998 Contribution of sex and genetics to neuroendocrine adaptation to stress in mice Psychoneuroendocrinology 23 505 517
30. G. A. Kennedy R. Hudson S. M. Armstrong 1994 Circadian wheel running activity rhythms in two strains of domestic rabbit Physiological Behavior 55 385 389
31. Y. Kiyokawa T. Kikusui Y. Takeuchi Y. Mori 2004 Partner's stress status influences social buffering effects in rats Behavioral Neuroscience 118 798 804
32. C. Kopp V. Ressel E. Wigger I. Tobler 2006 Influence of estrus cycle and ageing on activity patterns in two inbred mouse strains Behavioural Brain Research 167 165 174
33. Y. Kozorovitskiy E. Gould 2004 Dominance hierarchy influences adult neurogenesis in the dentate gyrus Journal of Neuroscience 24 6755 6759
34. A. F. Kramer K. I. Erickson 2007 Capitalizing on cortical plasticity: Influence of physical activity on cognition and brain function Trends in Cognitive Sciences 11 342 348
35. M. Lancel S. K. Droste S. Sommer J. M. Reul 2003 Influence of regular voluntary exercise on spontaneous and social stress-affected sleep in mice European Journal of Neuroscience 17 2171 2179
36. A. I. Leshner 1971 The adrenals & the regulatory nature of running wheel activity Physiology and Behavior 6 551 558
37. B. Leuner E. Gould T. J. Shors 2006 Is there a link between adult neurogenesis and learning? Hippocampus 16 216 224
38. J. T. Lightfoot M. J. Turner M. Daves A. Vordermark S. R. Kleeberger 2004 Genetic influence on daily wheel running activity level Physiological Genomics 19 270 276
39. Z. W. Lu C. Song A. V. Ravindran Z. Merali H. Anisman 1998 Influence of a psychogenic and a neurogenic stressor on several indices of immune functioning in different strains of mice Brain Behavior and Immunity 12 7 22
40. F. Magri L. Cravello L. Barili 2006 Stress and dementia: The role of the hypothalamicpituitary-adrenal axis Aging Clinical and Experimental Research 18 167 170
41. A. Makatsori R. Duncko M. Schwendt F. Moncek B. B. Johansson D. Jezova 2003 Voluntary wheel running modulates glutamate receptor subunit gene expression and stress hormone release in Lewis rats Psychoneuroendocrinology 28 702 714
42. S. Makino Y. Tanaka H. P. Nazarloo T. Noguchi K. Nishimura K. Hashimoto 2005 Expression of type 1 corticotropin-releasing hormone (CRH) receptor mRNA in the hypothalamic paraventricular nucleus following restraint stress in CRH-deficient mice Brain Research 1048 131 137
43. J. L. Malisch W. Saltzman F. R. Gomes E. L. Rezende D. R. Jeske T. Garland Jr. 2007 Baseline and stress-induced plasma corticosterone concentrations of mice selectively bred for high voluntary wheel running Physiological and Biochemical Zoology 80 146 156
44. J. P. McMurtry B. C. Wexler 1981 Hypersensitivity of spontaneously hypertensive rats (SHR) to heat, ether, and immobilization Endocrinology 108 1730 1736
45. C. Mirescu J. D. Peters L. Noiman E. Gould 2006 Sleep deprivation inhibits adult neurogenesis in the hippocampus by elevating glucocorticoids Proceedings of the National Academy of Sciences of the United States of America 103 19170 19175
46. R. Mitra S. Jadhav B. S. McEwen A. Vyas S. Chattarji 2005 Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala Proceedings of the National Academy of Sciences of the United States of America 102 9371 9376
47. R. Molteni A. Wu S. Vaynman Z. Ying R. J. Barnard F. Gomez-Pinilla 2004 Exercise reverses the harmful effects of consumption of a high-fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor Neuroscience 123 429 440
48. A. S. Naylor A. I. Persson P. S. Eriksson I. H. Jonsdottir T. Thorlin 2005 Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat Journal of Neurophysiology 93 2406 2414
49. A. J. Nonneman J. V. Corwin 1981 Differential effects of prefrontal cortex ablation in neonatal, juvenile, and young adult rats Journal of Comparative and Physiological Psychology 95 588 602
50. S. Ogawa J. Chan J. A. Gustafsson K. S. Korach D. W. Pfaff 2003 Estrogen increases locomotor activity in mice through estrogen receptor alpha: specificity for the type of activity Endocrinology 144 230 239
51. A. I. Persson A. S. Naylor I. H. Jonsdottir F. Nyberg P. S. Eriksson T. Thorlin 2004 Differential regulation of hippocampal progenitor proliferation by opioid receptor antagonists in running and non-running spontaneously hypertensive rats European Journal of Neuroscience 19 1847 1855
52. V. A. Redila B. R. Christie 2006 Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus Neuroscience 137 1299 1307
53. S. G. Reebs D. Maillet 2003 Effect of cage enrichment on the daily use of running wheels by Syrian hamsters Chronobiology International 20 9 20
54. R. Refinetti 2007 Absence of circadian and photoperiodic conservation of energy expenditure in three rodent species Journal of Comparative Physiology [B] 177 309 318
55. J. S. Rhodes T. Garland Jr S. C. Gammie 2003 Patterns of brain activity associated with variation in voluntary wheel-running behavior Behavioral Neuroscience 117 1243 1256
56. P. A. Rittenhouse C. Lopez-Rubalcava G. D. Stanwood I. Lucki 2002 Amplified behavioral and endocrine responses to forced swim stress in the Wistar-Kyoto rat Psychoneuroendocrinology 27 303 318
57. P. L. Roubertoux P. V. Guillot S. Mortaud 2005 Attack behaviors in mice: From factorial structure to quantitative trait loci mapping European Journal of Pharmacology 526 172 185
58. M. A. Ruis J. H. te Brake B. Buwalda 1999 Housing familiar male wildtype rats together reduces the long-term adverse behavioural and physiological effects of social defeat Psychoneuroendocrinology 24 285 300
59. M. E. Seligman G. Beagley 1975 Learned helplessness in the rat Journal of Comparative and.Physiological Psychology 88 534 541
60. Seyle, H. (1976). The stress of life. NY: McGraw-Hill.
61. T. J. Shors 1998 Stress and sex effects on associative learning: For better or for worse Neuroscientist 4 353 364
62. A. M. Stranahan D. Khalil E. Gould 2006 Social isolation delays the positive effects of running on adult neurogenesis Nature Neuroscience 9 526 533
63. Stranahan, A. M., Khalil, D. & Gould, E. (2007). Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus, 17(11), 1017-1022.
64. E. Tousson H. Meissl 2004 Suprachiasmatic nuclei grafts restore the circadian rhythm in the paraventricular nucleus of the hypothalamus Journal of Neuroscience 24 2983 2988
65. V. S. Valentinuzzi K. Scarbrough J. S. Takahashi F. W. Turek 1997 Effects of aging on the circadian rhythm of wheel-running activity in C57BL/6 mice American Journal of Physiology 273 R1957 1964
66. H. van Praag B. R. Christie T. J. Sejnowski F. H. Gage 1999 Running enhances neurogenesis, learning, and long-term potentiation in mice Proceedings of the National Academy of Sciences of the United States of America 96 13427 13431
67. S. Vaynman Z. Ying F. Gomez-Pinilla 2004 Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition European Journal of Neuroscience 20 2580 2590
68. V. Viau M. J. Meaney 1991 Variations in the hypothalamic-pituitary- adrenal response to stress during the estrous cycle in the rat Endocrinology 129 2503 2511
69. F. Wollnik F. W. Turek 1988 Estrous correlated modulations of circadian and ultradian wheel-running activity rhythms in LEW/Ztm rats Physiology and Behavior 43 389 396
70. G. E. Wood T. J. Shors 1998 Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones Proceedings of the National Academy of Sciences of the United States of America 95 4066 4071
71. C. S. Woolley E. Gould B. S. McEwen 1990 Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons Brain Research 531 225 231
72. H. Zheng Y. Liu W. Li 2006 Beneficial effects of exercise and its molecular mechanisms on depression in rats Behavioural Brain Research 168 47 55
73. D. Zillmann A. H. Katcher B. Milavshky 1972 Excitation transfer from physical exercise to subsequent aggressive behavior Journal of Experimental Social Psychology 8 247 259