NeuroMolecular Medicine

, Volume 10, Issue 2, pp 67–80 | Cite as

Neuroplasticity of Dopamine Circuits After Exercise: Implications for Central Fatigue

Article

Abstract

Habitual exercise increases plasticity in a variety of neurotransmitter systems. The current review focuses on the effects of habitual physical activity on monoamine dopamine (DA) neurotransmission and the potential implication of these changes to exercise-induced fatigue. Although it is clear that peripheral adaptations in muscle and energy substrate utilization contribute to this effect, more recently it has been suggested that central nervous system pathways “upstream” of the motor cortex, which initiate activation of skeletal muscles, are also important. The contribution of the brain to exercise-induced fatigue has been termed “central fatigue.” Given the well-defined role of DA in the initiation of movement, it is likely that adaptations in DA systems influence exercise capacity. A reduction in DA neurotransmission in the substantia nigra pars compacta (SNpc), for example, could impair activation of the basal ganglia and reduce stimulation of the motor cortex leading to central fatigue. Here we present evidence that habitual wheel running produces changes in DA systems. Using in situ hybridization techniques, we report that 6 weeks of wheel running was sufficient to increase tyrosine hydroxylase mRNA expression and reduce D2 autoreceptor mRNA in the SNpc. Additionally, 6 weeks of wheel running increased D2 postsynaptic receptor mRNA in the caudate putamen, a major projection site of the SNpc. These results are consistent with prior data suggesting that habitually physically active animals may have an enhanced ability to increase DA synthesis and reduce D2 autoreceptor-mediated inhibition of DA neurons in the SNpc compared to sedentary animals. Furthermore, habitually physically active animals, compared to sedentary controls, may be better able to increase D2 receptor-mediated inhibition of the indirect pathway of the basal ganglia. Results from these studies are discussed in light of our understanding of the role of DA in the neurobiological mechanisms of central fatigue.

Keywords

Wheel running Plasticity Brain-derived neurotrophic factor Basal ganglia Physical activity 

References

  1. Abdelmalki, A., Merino, D., Bonneau, D., et al. (1997). Administration of a GABAB agonist baclofen before running to exhaustion in the rat: Effects on performance and on some indicators of fatigue. International Journal of Sports Medicine, 18, 75–78.PubMedGoogle Scholar
  2. Acworth, I., Nicholass, J., Morgan, B., et al. (1986). Effect of sustained exercise on concentrations of plasma aromatic and branched-chain amino acids and brain amines. Biochemical and Biophysical Research Communications, 137, 149–153.PubMedGoogle Scholar
  3. Adell, A., & Artigas, F. (2004). The somatodendritic release of dopamine in the ventral tegmental area and its regulation by afferent transmitter systems. Neuroscience and Biobehavioural Reviews, 28, 415–431.Google Scholar
  4. Agharanya, J. C., & Wurtman, R. J. (1982). Studies on the mechanism by which tyrosine raises urinary catecholamines. Biochemical Pharmacology, 31, 3577–3580.PubMedGoogle Scholar
  5. Ahlenius, S., & Hillegaart, V. (1986). Involvement of extrapyramidal motor mechanisms in the suppression of locomotor activity by antipsychotic drugs: A comparison between the effects produced by pre- and post-synaptic inhibition of dopaminergic neurotransmission. Pharmacology, Biochemistry and Behaviour, 24, 1409–1415.Google Scholar
  6. Ahlenius, S., Svensson, L., Hillegaart, V., et al. (1984). Antagonism by haloperidol of the suppression of exploratory locomotor activity induced by the local application of (−)3-(3-hydroxyphenyl)-N-n-propylpiperidine into the nucleus accumbens of the rat. Experientia, 40, 858–859.PubMedGoogle Scholar
  7. Altar, C. A., Boylan, C. B., Jackson, C., et al. (1992). Brain-derived neurotrophic factor augments rotational behavior and nigrostriatal dopamine turnover in vivo. Proceedings of National Academy of Sciences USA, 89, 11347–11351.Google Scholar
  8. Avraham, Y., Hao, S., Mendelson, S., et al. (2001). Tyrosine improves appetite, cognition, and exercise tolerance in activity anorexia. Medicine and Science in Sports and Exercise, 33, 2104–2110.PubMedGoogle Scholar
  9. Bailey, S. P., Davis, J. M., & Ahlborn, E. N. (1992). Effect of increased brain serotonergic activity on endurance performance in the rat. Acta Physiologica Scandinavica, 145, 75–76.PubMedGoogle Scholar
  10. Bailey, S. P., Davis, J. M., & Ahlborn, E. N. (1993a) Neuroendocrine and substrate responses to altered brain 5-HT activity during prolonged exercise to fatigue. Journal of Applied Physiology, 74, 3006–3012.PubMedGoogle Scholar
  11. Bailey, S. P., Davis, J. M., & Ahlborn, E. N. (1993b) Serotonergic agonists and antagonists affect endurance performance in the rat. International Journal of Sports and Medicne, 14, 330–333.Google Scholar
  12. Beck, K. D., Knusel, B., & Hefti, F. (1993). The nature of the trophic action of brain-derived neurotrophic factor, des(1–3)-insulin-like growth factor-1, and basic fibroblast growth factor on mesencephalic dopaminergic neurons developing in culture. Neuroscience, 52, 855–866.PubMedGoogle Scholar
  13. Belke, T. W. (1997). Running and responding reinforced by the opportunity to run: Effect of reinforcer duration. Journal of Experimental Analysis and Behaviour, 67, 337–351.Google Scholar
  14. Bhagat, B., & Wheeler, N. (1973a) Effect of amphetamine on the swimming endurance of rats. Neuropharmacology, 12, 711–713.PubMedGoogle Scholar
  15. Bhagat, B., & Wheeler, N. (1973b) Effect of nicotine on the swimming endurance of rats. Neuropharmacology, 12, 1161–1165.PubMedGoogle Scholar
  16. Bliss, E. L., & Ailion, J. (1971). Relationship of stress and activity to brain dopamine and homovanillic acid. Life Science I, 10, 1161–1169 .Google Scholar
  17. Blomstrand, E. (2006). A role for branched-chain amino acids in reducing central fatigue. Journal of Nutrition, 136, 544S–547S.PubMedGoogle Scholar
  18. Blomstrand, E., Perrett, D., Parry-Billings, M., et al. (1989). Effect of sustained exercise on plasma amino acid concentrations and on 5-hydroxytryptamine metabolism in six different brain regions in the rat. Acta Physiologica Scandinavica, 136, 473–481.PubMedGoogle Scholar
  19. Bracken, M. E., Bracken, D. R., Nelson, A. G., et al. (1988). Effect of cocaine on exercise endurance and glycogen use in rats. Journal of Applied Physiology, 64, 884–887.PubMedGoogle Scholar
  20. Bracken, M. E., Bracken, D. R., Winder, W. W., et al. (1989). Effect of various doses of cocaine on endurance capacity in rats. Journal of Applied Physiology, 66, 377–383.PubMedGoogle Scholar
  21. Burgess, M. L., Davis, J. M., Borg, T. K., et al. (1991). Intracranial self-stimulation motivates treadmill running in rats. Journal of Applied Physiology, 71, 1593–1597.PubMedGoogle Scholar
  22. Campisi, J., Leem, T. H., Greenwood, B. N., et al. (2003). Habitual physical activity facilitates stress-induced HSP72 induction in brain, peripheral, and immune tissues. American Journal of Physiology Regulatory, Integrative Comparative Physiology, 284, R520–R530.Google Scholar
  23. Chaouloff, F., Laude, D., Guezennec, Y., et al. (1986). Motor activity increases tryptophan, 5-hydroxyindoleacetic acid, and homovanillic acid in ventricular cerebrospinal fluid of the conscious rat. Journal of Neurochemistry, 46, 1313–1316.PubMedGoogle Scholar
  24. Chaouloff, F., Laude, D., Merino, D., et al. (1987). Amphetamine and alpha-methyl-p-tyrosine affect the exercise-induced imbalance between the availability of tryptophan and synthesis of serotonin in the brain of the rat. Neuropharmacology, 26, 1099–1106.PubMedGoogle Scholar
  25. Chaudhuri, A., & Behan, P. O. (2000). Fatigue and basal ganglia. Journal of Neurological Science, 179, 34–42.Google Scholar
  26. Chen, H., Zhang, S. M., Schwarzschild, M. A., et al. (2005). Physical activity and the risk of Parkinson disease. Neurology, 64, 664–669.PubMedGoogle Scholar
  27. Chinevere, T. D., Sawyer, R. D., Creer, A. R., et al. (2002). Effects of l-tyrosine and carbohydrate ingestion on endurance exercise performance. Journal of Applied Physiology, 93, 1590–1597.PubMedGoogle Scholar
  28. Cooter, G. R., & Stull, G. A. (1974). The effect of amphetamine on endurance in rats. Journal of Sports Medicine and Physical Fitness, 14, 120–126.PubMedGoogle Scholar
  29. Cotman, C. W., & Berchtold, N. C. (2002). Exercise: A behavioral intervention to enhance brain health and plasticity. Trends Neuroscience, 25, 295–301.Google Scholar
  30. Craig, A., Tran, Y., Wijesuriya, N., et al. (2005). A controlled investigation into the psychological determinants of fatigue. Biological Psychology, 72, 78–87.PubMedGoogle Scholar
  31. Crizzle, A. M., & Newhouse, I. J. (2006). Is physical exercise beneficial for persons with Parkinson’s disease? Clinical Journal of Sport Medicne, 16, 422–425.Google Scholar
  32. Davis, J. M. (1995). Central and peripheral factors in fatigue. Journal of Sports Sciences, 13(Spec No), S49–S53.Google Scholar
  33. Davis, J. M., Alderson, N. L., & Welsh, R. S. (2000). Serotonin and central nervous system fatigue: Nutritional considerations. American Journal of Clinical Nutrition, 72, 573S–578S.PubMedGoogle Scholar
  34. Davis, J. M., & Bailey, S. P. (1997). Possible mechanisms of central nervous system fatigue during exercise. Medicine and Science in Sports and Exercise, 29, 45–57.PubMedGoogle Scholar
  35. Davis, J. M., Zhao, Z., Stock, H. S., et al. (2003). Central nervous system effects of caffeine and adenosine on fatigue. American Journal of Physiology Regulatory, Integrative Comparative Physiology, 284, R399–R404.Google Scholar
  36. Derevenco, P., Sovrea, I., Stoica, N., et al. (1978). The effects of central chemical sympathectomy on the response to exercise in rats. Physiologie, 15, 215–219.PubMedGoogle Scholar
  37. Derevenco, P., Stoica, N., Sovrea, I., et al. (1986). Central and peripheral effects of 6-hydroxydopamine on exercise performance in rats. Psychoneuroendocrinology, 11, 141–153.PubMedGoogle Scholar
  38. Derevenco, P., Stoica, N., & Vaida, A. (1981). Other effects of monoaminergic inhibition with 6 hydroxydopamine and of disulfiram on the response to exercise in rats. Physiologie, 18, 181–185.PubMedGoogle Scholar
  39. Derevenco, P., Vaida, A., Stoica, N., et al. (1982). New data concerning the effects of 6-hydroxydopamine on the exercise performance in rats. Physiologie, 19, 221–228.PubMedGoogle Scholar
  40. Dishman, R. K., Berthoud, H. R., Booth, F. W., et al. (2006). Neurobiology of exercise. Scandinavian Journal of Medicine and Science in Sports, 16, 470.Google Scholar
  41. Elam, M., Svensson, T. H., & Thoren, P. (1987). Brain monoamine metabolism is altered in rats following spontaneous, long-distance running. Acta Physiologica Scandinavica, 130, 313–316.PubMedGoogle Scholar
  42. Elsworth, J. D., & Roth, R. H. (1997). Dopamine synthesis, uptake, metabolism, and receptors: Relevance to gene therapy of Parkinson’s disease. Experimental Neurology, 144, 4–9.PubMedGoogle Scholar
  43. Enoka, R. M., & Stuart, D. G. (1992). Neurobiology of muscle fatigue. Journal of Applied Physiology, 72, 1631–1648.PubMedGoogle Scholar
  44. Fernstrom, J. D., & Fernstrom, M. H. (2006). Exercise, serum free tryptophan, and central fatigue. Journal of Nutrition, 136, 553S–559S.PubMedGoogle Scholar
  45. Francois, C., Yelnik, J., Tande, D., et al. (1999). Dopaminergic cell group A8 in the monkey: Anatomical organization and projections to the striatum. Journal of Comparative Neurology, 414, 334–347.PubMedGoogle Scholar
  46. Freed, C. R., & Yamamoto, B. K. (1985). Regional brain dopamine metabolism: A marker for the speed, direction, and posture of moving animals. Science, 229, 62–65.PubMedGoogle Scholar
  47. Gandevia, S. C. (2001). Spinal and supraspinal factors in human muscle fatigue. Physiological Review, 81, 1725–1789.Google Scholar
  48. Gandevia, S. C., Allen, G. M., Butler, J. E., et al. (1996). Supraspinal factors in human muscle fatigue: Evidence for suboptimal output from the motor cortex. Journal of Physiology, 490(Pt 2), 529–536.PubMedGoogle Scholar
  49. Gandevia, S. C., Enoka, R. M., McComas, A. J., et al. (1995). Neurobiology of muscle fatigue. Advances and issues. Advances in Experimental Medicine and Biology, 384, 515–525.PubMedGoogle Scholar
  50. Gerald, M. C. (1978). Effects of (+)-amphetamine on the treadmill endurance performance of rats. Neuropharmacology, 17, 703–704.PubMedGoogle Scholar
  51. Gerin, C., Becquet, D., & Privat, A. (1995). Direct evidence for the link between monoaminergic descending pathways and motor activity. I. A study with microdialysis probes implanted in the ventral funiculus of the spinal cord. Brain Research, 704, 191–201.PubMedGoogle Scholar
  52. Gerin, C., & Privat, A. (1998). Direct evidence for the link between monoaminergic descending pathways and motor activity: II. A study with microdialysis probes implanted in the ventral horn of the spinal cord. Brain Research, 794, 169–173.PubMedGoogle Scholar
  53. Gilliam, P. E., Spirduso, W. W., Martin, T. P., et al. (1984). The effects of exercise training on [3H]-spiperone binding in rat striatum. Pharmacology, Biochemistry and Behaviour, 20, 863–867.Google Scholar
  54. Guezennec, C. Y., Abdelmalki, A., Serrurier, B., et al. (1998). Effects of prolonged exercise on brain ammonia and amino acids. International Journal of Sports and Medicine, 19, 323–327.Google Scholar
  55. Guillin, O., Diaz, J., Carroll, P., et al. (2001). BDNF controls dopamine D3 receptor expression and triggers behavioural sensitization. Nature, 411, 86–89.PubMedGoogle Scholar
  56. Hasegawa, H., Yazawa, T., Yasumatsu, M., et al. (2000). Alteration in dopamine metabolism in the thermoregulatory center of exercising rats. Neuroscience Letters, 289, 161–164.PubMedGoogle Scholar
  57. Hattori, S., Naoi, M., & Nishino, H. (1994). Striatal dopamine turnover during treadmill running in the rat: Relation to the speed of running. Brain Research Bulletin, 35, 41–49.PubMedGoogle Scholar
  58. Heyes, M. P., Garnett, E. S., & Coates, G. (1985). Central dopaminergic activity influences rats ability to exercise. Life Science, 36, 671–677.Google Scholar
  59. Heyes, M. P., Garnett, E. S., & Coates, G. (1988). Nigrostriatal dopaminergic activity is increased during exhaustive exercise stress in rats. Life Science, 42, 1537–1542.Google Scholar
  60. Hillegaart, V., & Ahlenius, S. (1987). Effects of raclopride on exploratory locomotor activity, treadmill locomotion, conditioned avoidance behaviour and catalepsy in rats: Behavioural profile comparisons between raclopride, haloperidol and preclamol. Pharmacology and Toxicology, 60, 350–354.PubMedGoogle Scholar
  61. Hillegaart, V., Ahlenius, S., Magnusson, O., et al. (1987). Repeated testing of rats markedly enhances the duration of effects induced by haloperidol on treadmill locomotion, catalepsy, and a conditioned avoidance response. Pharmacology, Biochemistry and Behaviour, 27, 159–164.Google Scholar
  62. Hoffmann, P., Elam, M., Thoren, P., et al. (1994). Effects of long-lasting voluntary running on the cerebral levels of dopamine, serotonin and their metabolites in the spontaneously hypertensive rat. Life Science, 54, 855–861.Google Scholar
  63. Horger, B. A., Iyasere, C. A., Berhow, M. T., et al. (1999). Enhancement of locomotor activity and conditioned reward to cocaine by brain-derived neurotrophic factor. Journal of Neuroscience, 19, 4110–4122.PubMedGoogle Scholar
  64. Howells, F. M., Russell, V. A., Mabandla, M. V., et al. (2005). Stress reduces the neuroprotective effect of exercise in a rat model for Parkinson’s disease. Behavourial Brain Research, 165, 210–220.Google Scholar
  65. Hyman, C., Hofer, M., Barde, Y. A., et al. (1991). BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature, 350, 230–232.PubMedGoogle Scholar
  66. Iversen, I. H. (1993). Techniques for establishing schedules with wheel running as reinforcement in rats. Journal of Experimental Analysis and Behaviour, 60, 219–238.Google Scholar
  67. Jacobs, B. L. (1991). Serotonin and behavior: Emphasis on motor control. Journal of Clinical Psychiatry, 52, 17–23.PubMedGoogle Scholar
  68. Jacobs, B. L., & Fornal, C. A. (1999). Activity of serotonergic neurons in behaving animals. Neuropsychopharmacology, 21, 9S–15S.PubMedGoogle Scholar
  69. Jacobs, I., & Bell, D. G. (2004). Effects of acute modafinil ingestion on exercise time to exhaustion. Medicine and Science in Sports and Exercise, 36, 1078–1082.PubMedGoogle Scholar
  70. Kalinski, M. I., Dluzen, D. E., & Stadulis, R. (2001). Methamphetamine produces subsequent reductions in running time to exhaustion in mice. Brain Research, 921, 160–164.PubMedGoogle Scholar
  71. Kalmar, J. M., & Cafarelli, E. (2004). Caffeine: A valuable tool to study central fatigue in humans? Exercise and Sport Sciences Reviews, 32, 143–147.PubMedGoogle Scholar
  72. Lacerda, A. C., Marubayashi, U., Balthazar, C. H., et al. (2006). Evidence that brain nitric oxide inhibition increases metabolic cost of exercise, reducing running performance in rats. Neuroscience Letters, 393, 260–263.PubMedGoogle Scholar
  73. Le Moine, C., Normand, E., & Bloch, B. (1991). Phenotypical characterization of the rat striatal neurons expressing the D1 dopamine receptor gene. Proceedings of National Academy Sciences USA, 88, 4205–4209.Google Scholar
  74. Lett, B. T., Grant, V. L., Byrne, M. J., et al. (2000). Pairings of a distinctive chamber with the aftereffect of wheel running produce conditioned place preference. Appetite, 34, 87–94.PubMedGoogle Scholar
  75. Lim, B. V., Jang, M. H., Shin, M. C., et al. (2001). Caffeine inhibits exercise-induced increase in tryptophan hydroxylase expression in dorsal and median raphe of Sprague-Dawley rats. Neuroscience Letters, 308, 25–28.PubMedGoogle Scholar
  76. Liste, I., Guerra, M. J., Caruncho, H. J., et al. (1997). Treadmill running induces striatal Fos expression via, N. M.DA glutamate and dopamine receptors. Experimental Brain Research, 115, 458–468.Google Scholar
  77. Lu, X. Y., Ghasemzadeh, M. B., & Kalivas, P. W. (1998). Expression of D1 receptor, D2 receptor, substance P and enkephalin messenger RNAs in the neurons projecting from the nucleus accumbens. Neuroscience, 82, 767–780.PubMedGoogle Scholar
  78. MacRae, P. G., Spirduso, W. W., Cartee, G. D., et al. (1987). Endurance training effects on striatal D2 dopamine receptor binding and striatal dopamine metabolite levels. Neuroscience Letters, 79, 138–144.PubMedGoogle Scholar
  79. Marshall, J. F., & Berrios, N. (1979). Movement disorders of aged rats: Reversal by dopamine receptor stimulation. Science, 206, 477–479.PubMedGoogle Scholar
  80. Martin-Iverson, M. T., Todd, K. G., & Altar, C. A. (1994). Brain-derived neurotrophic factor and neurotrophin-3 activate striatal dopamine and serotonin metabolism and related behaviors: Interactions with amphetamine. Journal of Neuroscience, 14, 1262–1270.PubMedGoogle Scholar
  81. McTavish, S. F., Cowen, P. J., & Sharp, T. (1999). Effect of a tyrosine-free amino acid mixture on regional brain catecholamine synthesis and release. Psychopharmacology (Berl), 141, 182–188.Google Scholar
  82. Meeusen, R., Piacentini, M. F., & De Meirleir, K. (2001). Brain microdialysis in exercise research. Sports Medicine, 31, 965–983.PubMedGoogle Scholar
  83. Meeusen, R., Roeykens, J., Magnus, L., et al. (1997a) Endurance performance in humans: The effect of a dopamine precursor or a specific serotonin (5-HT2A/2C) antagonist. International Journal of Sports Medicine, 18, 571–577.PubMedGoogle Scholar
  84. Meeusen, R., Smolders, I., Sarre, S., et al. (1997b) Endurance training effects on neurotransmitter release in rat striatum: An in vivo microdialysis study. Acta Physiologica Scandinavica, 159, 335–341.PubMedGoogle Scholar
  85. Meeusen, R., Watson, P., & Dvorak, J. (2006a) The brain and fatigue: New opportunities for nutritional interventions? Journal of Sports and Sciences, 24, 773–782.Google Scholar
  86. Meeusen, R., Watson, P., Hasegawa, H., et al. (2006b) Central fatigue: The serotonin hypothesis and beyond. Sports and Medicine, 36, 881–909.Google Scholar
  87. Milner, J. D., & Wurtman, R. J. (1987). Tyrosine availability: A presynaptic factor controlling catecholamine release. Advances in Experimental Medicine and Biology, 221, 211–221.PubMedGoogle Scholar
  88. Newsholme, E. A., Acworth, I. N., & Blomstrand, E. (1987). Amino acids, brain neurotransmitters and a functional link between muscle and brain that is important in sustained exercise (pp. 127–133). London, UK: John Libbey Eurotext Ltd.Google Scholar
  89. Newsholme, E. A., & Blomstrand, E. (2006). Branched-chain amino acids and central fatigue. Journal of Nutrition, 136, 274S–276S.PubMedGoogle Scholar
  90. Nielsen, B., & Nybo, L. (2003). Cerebral changes during exercise in the heat. Sports and Medicne, 33, 1–11.Google Scholar
  91. Nybo, L., Dalsgaard, M. K., Steensberg, A., et al. (2005). Cerebral ammonia uptake and accumulation during prolonged exercise in humans. Journal of Physiology, 563, 285–290.PubMedGoogle Scholar
  92. Nybo, L., & Rasmussen, P. (2007). Inadequate cerebral oxygen delivery and central fatigue during strenuous exercise. Exercise and Sport Science Review, 35, 110–118.Google Scholar
  93. Nybo, L., & Secher, N. H. (2004). Cerebral perturbations provoked by prolonged exercise. Progress in Neurobiology, 72, 223–261.PubMedGoogle Scholar
  94. Oldendorf, W. H., & Szabo, J. (1976). Amino acid assignment to one of three blood-brain barrier amino acid carriers. American Journal of Physiology, 230, 94–98.PubMedGoogle Scholar
  95. Pardridge, W. M. (1977). Kinetics of competitive inhibition of neutral amino acid transport across the blood-brain barrier. Journal of Neurochemistry, 28, 103–108.PubMedGoogle Scholar
  96. Paxinos, G., Watson, C. (1998). The rat brain in stereotaxic coordinates. CA: Academic Press.Google Scholar
  97. Petzinger, G. M., Walsh, J. P., Akopian, G., et al. (2007). Effects of treadmill exercise on dopaminergic transmission in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse model of basal ganglia injury. Journal of Neuroscience, 27, 5291–5300.PubMedGoogle Scholar
  98. Rietjens, G. J., Kuipers, H., Adam, J. J., et al. (2005). Physiological biochemical and psychological markers of strenuous training-induced fatigue. International Journal of Sports and Medicine, 26, 16–26.Google Scholar
  99. Robinson, T. E., & Berridge, K. C. (1993). The neural basis of drug craving: An incentive-sensitization theory of addiction. Brain Research Brain Research Reviews, 18, 247–291.PubMedGoogle Scholar
  100. Robinson, T. E., & Berridge, K. C. (2000). The psychology and neurobiology of addiction: An incentive-sensitization view. Addiction, 95(Suppl 2), S91–S117.PubMedGoogle Scholar
  101. Rojas Vega, S., Struder, H. K., Vera Wahrmann, B., et al. (2006). Acute BDNF and cortisol response to low intensity exercise and following ramp incremental exercise to exhaustion in humans. Brain Research, 1121, 59–65.PubMedGoogle Scholar
  102. Russo-Neustadt, A. A., & Chen, M. J. (2005). Brain-derived neurotrophic factor and antidepressant activity. Current Pharmaceutical Design, 11, 1495–1510.PubMedGoogle Scholar
  103. Sabol, K. E., Richards, J. B., & Freed, C. R. (1990). In vivo dialysis measurements of dopamine and DOPAC in rats trained to turn on a circular treadmill. Pharmacology, Biochemistry and Behaviour, 36, 21–28.Google Scholar
  104. Snider, R. M., Ordway, G. A., & Gerald, M. C. (1983). Effects of methylphenidate on rat endurance performance and neuromuscular transmission in vitro. Neuropharmacology, 22, 83–88.PubMedGoogle Scholar
  105. Speciale, S. G., Miller, J. D., McMillen, B. A., et al. (1986). Activation of specific central dopamine pathways: Locomotion and footshock. Brain Research Bulletin, 16, 33–38.PubMedGoogle Scholar
  106. Spina, M. B., Squinto, S. P., Miller, J., et al. (1992). Brain-derived neurotrophic factor protects dopamine neurons against 6-hydroxydopamine and N-methyl-4-phenylpyridinium ion toxicity: Involvement of the glutathione system. Journal of Neurochemistry, 59, 99–106.PubMedGoogle Scholar
  107. Stokes, M. J., Cooper, R. G., & Edwards, R. H. (1988). Normal muscle strength and fatigability in patients with effort syndromes. BMJ, 297, 1014–1017.PubMedCrossRefGoogle Scholar
  108. Struder, H. K., Hollmann, W., Platen, P., et al. (1998). Influence of paroxetine, branched-chain amino acids and tyrosine on neuroendocrine system responses and fatigue in humans. Hormone and Metabolic Research, 30, 188–194.PubMedGoogle Scholar
  109. Struder, H. K., & Weicker, H. (2001a) Physiology and pathophysiology of the serotonergic system and its implications on mental and physical performance. Part I. International Journal of Sports and Medicine, 22, 467–481.Google Scholar
  110. Struder, H. K., & Weicker, H. (2001b) Physiology and pathophysiology of the serotonergic system and its implications on mental and physical performance. Part II. International Journal of Sports and Medicine, 22, 482–497.Google Scholar
  111. Sutton, E. E., Coill, M. R., & Deuster, P. A. (2005). Ingestion of tyrosine: Effects on endurance, muscle strength, and anaerobic performance. International Journal of Sport Nutrition and Exercise Metabolism, 15, 173–185.PubMedGoogle Scholar
  112. Tillerson, J. L., Caudle, W. M., Reveron, M. E., et al. (2003). Exercise induces behavioral recovery and attenuates neurochemical deficits in rodent models of Parkinson’s disease. Neuroscience, 119, 899–911.PubMedGoogle Scholar
  113. Todd, G., Butler, J. E., Taylor, J. L., et al. (2005). Hyperthermia: A failure of the motor cortex and the muscle. Journal of Physiology, 563, 621–631.PubMedGoogle Scholar
  114. Trudeau, F., Peronnet, F., Beliveau, L., et al. (1990). 6-OHDA sympathectomy andexercise performance in the rat. Archives Internationales de Physiologie et de Biochimie, 98, 433–437.PubMedCrossRefGoogle Scholar
  115. Tumer, N., Demirel, H. A., Serova, L., et al. (2001). Geneexpression of catecholamine biosynthetic enzymes following exercise: Modulation by age. Neuroscience, 103, 703–711.PubMedGoogle Scholar
  116. Van Hoomissen, J. D., Chambliss, H. O., Holmes, P. V., et al. (2003). Effects of chronic exercise and imipramine on mRNA for BDNF after olfactory bulbectomy in rat. Brain Research, 974, 228–235.PubMedGoogle Scholar
  117. Vaynman, S., & Gomez-Pinilla, F. (2005). License to run: Exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabilitation and Neural Repair, 19, 283–295.PubMedGoogle Scholar
  118. Wang, G. J., Volkow, N. D., Fowler, J. S., et al. (2000). PET studies of the effects of aerobic exercise on human striatal dopamine release. Journal of Nuclear Medicine, 41, 1352–1356.PubMedGoogle Scholar
  119. Werme, M., Messer, C., Olson, L., et al. (2002). Delta FosB regulates wheel running. Journal of Neuroscience, 22, 8133–8138.PubMedGoogle Scholar
  120. Williams, M. H., & Thompson, J. (1973). Effect of variant dosages of amphetamine upon endurance. Research Quarterly, 44, 417–422.PubMedGoogle Scholar
  121. Wilson, W. M., & Marsden, C. A. (1995). Extracellular dopamine in the nucleus accumbens of the rat during treadmill running. Acta Physiologica Scandinavica, 155, 465–466.PubMedGoogle Scholar
  122. Yee, R. E., Cheng, D. W., Huang, S. C., et al. (2001). Blood-brain barrier and neuronal membrane transport of 6-[18F]fluoro-l-DOPA. Biochemical Pharmacology, 62, 1409–1415.PubMedGoogle Scholar

Copyright information

© Humana Press 2008

Authors and Affiliations

  1. 1.Department Integrative Physiology, Center for Neuroscience, Clare Small BuildingUniversity of Colorado-BoulderBoulderUSA

Personalised recommendations