Promoting motor function by exercising the brain

Brain Sciences

Volumn 3, Issue 1, 2013, Pages 101-122

  Perrey, Stephane ^a  

^a UNIVERSITY OF MONTPELLIER   (France)

Author keywords

Cerebral blood flow; Cerebral oxygenation; Endurance exercise; Hemodynamics; Neuroplasticity

Indexed keywords

DEOXYHEMOGLOBIN; OXYHEMOGLOBIN;

BLOOD VOLUME; BRAIN BLOOD FLOW; BRAIN FUNCTION; CEREBROVASCULAR ACCIDENT; DOPPLER FLOWMETRY; ENDURANCE TRAINING; EVOKED CORTICAL RESPONSE; EXERCISE; FLUORESCENCE IMAGING; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; HUMAN; MAGNETOENCEPHALOGRAPHY; MOTOR PERFORMANCE; MUSCLE FATIGUE; NEAR INFRARED SPECTROSCOPY; NERVE CELL PLASTICITY; NEUROIMAGING; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PHYSICAL ACTIVITY; RESISTANCE TRAINING; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; VOLUNTARY MOVEMENT;

EID: 84904569019     PISSN: None     EISSN: 20763425     Source Type: Journal    
DOI: 10.3390/brainsci3010101     Document Type: Review

References (107)

1. Cotman, C.W.; Berchtold, N.C. Exercise: A behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 2002, 25, 295-301.
2. Caspersen, C.J.; Powell, K.E.; Christenson, G.M. Physical activity, exercise, and physical fitness: Definitions and distinctions for health-related research. Public Health Rep. 1985, 100, 126-131.
3. Dishman, R.K.; Berthoud, H.R.; Booth, F.W.; Cotman, C.W.; Edgerton, V.R.; Fleshner, M.R.; Gandevia, S.C.; Gomez-Pinilla, F.; Greenwood, B.N.; Hillman, C.H.; et al. Neurobiology of exercise. Obesity (Silver Spring) 2006, 14, 345-356.
4. Mattson, M.P.; Maudsley, S.; Martin, B. BDNF and 5-HT: A dynamic duo in age-related neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 2004, 27, 589-594.
5. Schinder, A.F.; Poo, M. The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci. 2000, 23, 639-645.
6. Churchill, J.D.; Galvez, R.; Colcombe, S.; Swain, R.A.; Kramer, A.F.; Greenough, W.T. Exercise, experience and the aging brain. Neurobiol. Aging 2002, 23, 941-955.
7. Orlandi, G.; Murri, L. Transcranial Doppler assessment of cerebral flow velocity at rest and during voluntary movements in young and elderly healthy subjects. Int. J. Neurosci. 1996, 84, 45-53.
8. Mosso, A. Ueber den Kreislauf des Blutes im Menschlichen Gehirn; Verlag von Veit: Leipzig, Germany, 1881.
9. Roy, C.S.; Sherrington, C.S. On the regulation of the blood-supply of the brain. J. Physiol. (Lond.) 1890, 11, 85-108.
10. Seifert, T.; Secher, N.H. Sympathetic influence of cerebral blood flow and metabolism during exercise in humans. Prog. Neurobiol. 2011, 95, 406-426.
11. Dustman, R.E.; Emmerson, R.Y.; Shearer, D.E. Physical activity, age, and cognitive neurophysiological function. J. Aging Phys. Act. 1994, 2, 143-181.
12. Cui, X.; Bray, S.; Bryant, D.M.; Glover, G.H.; Reiss, A.L. A quantitative comparison of NIRS and fMRI across multiple cognitive tasks. Neuroimage 2011, 54, 2808-2821.
13. Obrig, H.; Hirth, C.; Junge-Hülsing, J.G.; Döge, C.; Wolf, T.; Dirnagl, U.; Villringer, A. Cerebral oxygenation changes in response to motor stimulation. J. Appl. Physiol. 1996, 81, 1174-1183.
14. Perrey, S. Non-invasive NIR spectroscopy of human brain function during exercise. Methods 2008, 45, 289-299.
15. Perrey, S. NIRS for measuring cerebral hemodynamic responses during exercise. In Functional Neuroimaging in Exercise and Sport Sciences, 1st ed.; Boecker, H., Hillman, C.H., Scheef, L., Strüder, H.K., Eds.; Springer: New York, NY, USA, 2012; pp. 335-349.
16. Dudley, G.A.; Fleck, S.J. Strength and endurance training. Are they mutually exclusive? Sports Med. 1987, 4, 79-85.
17. Fleck, S.J.; Kraemer, W.J. Designing Resistance Training Programs, 1st ed.; Human Kinetics Books: Champaign, IL, USA, 1987.
18. Burns, J.M.; Cronk, B.B.; Anderson, H.S.; Donnely, J.E.; Thomas, G.P.; Harsha, A.; Brooks, W.M.; Swerdlow, R.H. Cardiorespiratory fitness and brain atrophy in early Alzheimer disease. Neurology 2008, 71, 210-216.
19. Brisswalter, J.; Arcelin, R.; Audiffren, M.; Delignieres, D. Influence of physical exercise on simple reaction time: Effects of physical fitness. Percept. Mot. Skills 1997, 85, 1019-1027.
20. Tomporowski, P.D.; Cureton, K.; Armstrong, L.E.; Kane, G.M.; Sparling, P.B.; Millard-Stafford, M. Short-term effects of aerobic exercise on executive processes and emotional reactivity. Int. J. Sport Exerc. Psychol. 2005, 3, 131-146.
21. Davranche, K.; Burle, B.; Audiffren, M.; Hasbroucq, T. Information processing during physical exercise: A chronometric and electromyographic study. Exp. Brain Res. 2005, 165, 532-540.
22. Dietrich, A. Functional neuroanatomy of altered states of consciousness: The transient hypofrontality hypothesis. Conscious. Cogn. 2003, 12, 231-256.
23. Tenenbaum, G.; Yuval, R.; Elbaz, G.; Gar-Eli, M.; Weinberg, R. The relationship between cognitive characteristics and decision making. Can. J. Appl. Physiol. 1993, 18, 48-62.
24. Arent, S.M.; Landers, D.M. Arousal, anxiety, and performance: A reexamination of the Inverted-U hypothesis. Res. Q. Exerc. Sport 2003, 74, 436-444.
25. Brisswalter, J.; Collardeau, M.; Arcelin, R. Effects of acute physical exercise characteristics on cognitive performance. Sports Med. 2002, 32, 555-566.
26. Enoka, R. Neuromechanics of Human Movement, 4th ed.; Human Kinetics Books: Champaign, IL, USA, 2008.
27. Winges, S.A.; Santello, M. Common input to motor units of digit flexors during multi-digit grasping. J. Neurophysiol. 2004, 92, 3210-3220.
28. Dum, R.P.; Strick, PL. Spinal cord terminations of the medial wall motor areas in macaque monkeys. J. Neurosci. 1996, 16, 6513-6525.
29. Carroll, T.J.; Selvanayagam, V.S.; Riek, S.; Semmler, J.G. Neural adaptations to strength training: Moving beyond transcranial magnetic stimulation and reflex studies. Acta Physiol. (Oxf.) 2011, 202, 119-140.
30. Tinazzi, M.; Farina, S.; Tamburin, S.; Facchini, S.; Fiaschi, A.; Restivo, D.; Berardelli, A. Task-dependent modulation of excitatory and inhibitory functions within the human primary motor cortex. Exp. Brain Res. 2003, 150, 222-229.
31. Perez, M.A.; Lungholt, B.K.; Nyborg, K.; Nielsen, J.B. Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp. Brain Res. 2004, 159, 197-205.
32. Pearce, A.J.; Kidgell, D.J. Corticomotor excitability during precision motor tasks. J. Sci. Med. Sport 2009, 12, 280-283.
33. Carey, J.R.; Greer, K.R.; Grunewald, T.K.; Steele, J.L.; Wiemiller, J.W.; Bhatt, E.; Nagpal, A.; Lungu, O.; Auerbach, E.J. Primary motor area activation during precision-demanding versus simple finger movement. Neurorehabil. Neural Repair. 2006, 20, 361-370.
34. Biswal, B.B.; Mennes, M.; Zuo, X-N.; Gohel, S.; Kelly, C.; Smith, S.M.; Beckmann, C.F.; Adelstein, J.S.; Buckner, R.L.; Colcombe, S.; et al. Toward discovery science of human brain function. Proc. Natl. Acad. Sci. USA 2010, 107, 4734-4739.
35. Siebner, H.R.; Bergmann, T.O.; Bestmann, S.; Massimini, M.; Johansen-Berg, H.; Mochizuki, H.; Bohning, D.E.; Boorman, E.D.; Groppa, S.; Miniussi, C.; et al. Consensus paper: Combining transcranial stimulation with neuroimaging. Brain Stimul. 2009, 2, 58-80.
36. Strangman, G.; Goldstein, R.; Rauch, S.L.; Stein, J. Near-infrared spectroscopy and imaging for investigating stroke rehabilitation: Test-retest reliability and review of the literature. Arch. Phys. Med. Rehabil. 2006, 87, S12-S19.
37. Steinbrink, J.; Villringer, A.; Kempf, F.; Haux, D.; Boden, S.; Obrig, H. Illuminating the BOLD signal: Combined fMRI-fNIRS studies. Magn. Reson. Imaging 2006, 24, 495-505.
38. Kirilina, E.; Jelzow, A.; Heine, A.; Niessing, M.; Wabnitz, H.; Brühl, R.; Ittermann, B.; Jacobs, A.M.; Tachtsidis, I. The physiological origin of task-evoked systemic artefacts in functional near infrared spectroscopy. Neuroimage 2012, 15, 70-81.
39. Villringer, A.; Dirgnal, U. Coupling of brain activity and cerebral blood flow: Basis of functional neuroimaging. Cerebrovasc. Brain Metab. Rev. 1995, 7, 240-276.
40. Iwasaki, K.; Ogawa, Y.; Shibata, S.; Aoki, K. Acute exposure to normobaric mild hypoxia alters dynamic relationships between blood pressure and cerebral blood flow at very low frequency. J. Cereb. Blood Flow Metab. 2007, 27, 776-784.
41. Atkins, E.R.; Brodie, F.G.; Rafelt, S.E.; Panerai, R.B.; Robinson, T.G. Dynamic cerebral autoregulation is compromised acutely following mild ischaemic stroke but not transient ischaemic attack. Cerebrovasc. Dis. 2010, 29, 228-235.
42. Ogoh, S.; Ainslie, P.N. Cerebral blood flow during exercise: mechanisms of regulation. J. Appl. Physiol. 2009, 107, 1370-1380.
43. Rupp, T.; Perrey, S. Prefrontal cortex oxygenation and neuromuscular responses to exhaustive exercise. Eur. J. Appl. Physiol. 2008, 102, 153-163.
44. Leff, D.R.; Orihuela-Espina, F.; Elwell, C.E.; Athanasiou, T.; Delpy, D.T.; Darzi, A.W.; Yang, G.Z. Assessment of the cerebral cortex during motor task behaviours in adults: A systematic review of functional near infrared spectroscopy (fNIRS) studies. Neuroimage 2011, 54, 2922-2936.
45. Lin, P.Y.; Chen, J.J.; Lin, S.I. The cortical control of cycling exercise in stroke patients: An fNIRS study. Hum. Brain Mapp. 2012, doi:10.1002/hbm.22072.
46. Buckworth, J.; Dishman, R.K. Exercise Psychology; Human Kinetics Books: Champaign, IL, USA, 2002.
47. Liu-Ambrose, T.; Nagamatsu, L.S.; Voss, M.W.; Khan, K.M.; Handy, T.C. Resistance training and functional plasticity of the aging brain: A 12-month randomized controlled trial. Neurobiol. Aging 2012, 33, 1690-1698.
48. Cassilhas, R.C.; Viana, V.A.; Grassmann, V.; Santos, R.T.; Santos, R.F.; Tufik, S.; Mello, M.T. The impact of resistance exercise on the cognitive function of the elderly. Med. Sci. Sports Exerc. 2007, 39, 1401-1407.
49. Yarrow, J.F.; White, L.J.; McCoy, S.C.; Borst, S.E. Training augments resistance exercise induced elevation of circulating brain derived neurotrophic factor (BDNF). Neurosci. Lett. 2010, 479, 161-165.
50. Smith, S.A.; Mitchell, J.H.; Garry, M.G. The mammalian exercise pressor reflex in health and disease. Exp. Physiol. 2006, 91, 89-102.
51. Willimason, J.W.; Fadel, P.J.; Mitchell, J.H. New insights into central cardiovascular control during exercise in humans: A central command update. Exp. Physiol. 2006, 91, 51-58.
52. 2 uptake during dynamic exercise. J. Appl. Physiol. 1993, 74, 245-250.
53. Secher, N.H.; Seifert, T.; van Lieshout, J.J. Cerebral blood flow and metabolism during exercise: Implications for fatigue. J. Appl. Physiol. 2008, 104, 306-314.
54. Querido, J.S.; Sheel, A.W. Regulation of cerebral blood flow during exercise. Sports Med. 2007, 37, 765-782.
55. Delp, M.D.; Armstrong, R.B.; Godfrey, D.A.; Laughlin, M.H.; Ross, C.D.; Wilkerson, M.K. Exercise increases blood flow to locomotor, vestibular, cardiorespiratory and visual regions of the brain in miniature swine. J. Physiol. 2001, 533, 849-859.
56. Dalsgaard, M.K.; Quistorff, B.; Danielsen, E.R.; Selmer, C.; Vogelsang, T.; Secher, N.H. A reduced cerebral metabolic ratio in exercise reflects metabolism and not accumulation of lactate within the human brain. J. Physiol. 2004, 554, 571-578.
57. Bereczki, D.; Wei, L.; Acuff, V.; Gruber, K.; Tajima, A.; Patlak, C.; Fenstermacher, J. Technique-dependent variations in cerebral microvessel blood volumes and hematocrits in the rat. J. Appl. Physiol. 1992, 73, 918-924.
58. Fox, P.T.; Raichle, M.E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl. Acad. Sci. USA 1986, 83, 1140-144.
59. Hoshi, Y.; Kobayashi, N.; Tamura, M. Interpretation of near-infrared spectroscopy signals: A study with a newly developed perfused rat brain model. J. Appl. Physiol. 2001, 90, 1657-1662.
60. Rooks, C.R.; Thom, N.J.; McCully, K.K.; Dishman, R.K. Effects of incremental exercise on cerebral oxygenation measured by near-infrared spectroscopy: A systematic review. Prog. Neurobiol. 2010, 92, 134-150.
61. Bhambhani, Y.; Malik, R.; Mookerjee, S. Cerebral oxygenation declines at exercise intensities above the respiratory compensation threshold. Respir. Physiol. Neurobiol. 2007, 156, 196-202.
62. Timinkul, A.; Kato, M.; Omori, T.; Deocaris, C.C.; Ito, A.; Kizuka, T.; Sakairi, Y.; Nishijima, T.; Asada, T.; Soya, H. Enhancing effect of cerebral blood volume by mild exercise in healthy young men: A near-infrared spectroscopy study. Neurosci. Res. 2008, 61, 242-248.
63. 2 carrying capacity. Front. Physiol. 2012, 3, 265.
64. Szubski, C.; Burtscher, M.; Loscher, W.N. The effects of short-term hypoxia on motor cortex excitability and neuromuscular activation. J. Appl. Physiol. 2006, 101, 1673-1677.
65. Roach, R.C.; Hackett, P.H. Frontiers of hypoxia research: Acute mountain sickness. J. Exp. Biol. 2001, 204, 3161-3170.
66. Nybo, L.; Rasmussen, P. Inadequate cerebral oxygen delivery and central fatigue during strenuous exercise. Exerc. Sport Sci. Rev. 2007, 35, 110-118.
67. Verges, S.; Rupp, T.; Jubeau, M.; Wuyam, B.; Esteve, F.; Levy, P.; Perrey, S.; Millet, G.Y. Cerebral perturbations during exercise in hypoxia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2012, 302, R903-R916.
68. Liu, J.Z.; Dai, T.H.; Sahgal, V.; Brown, R.W.; Yue, G.H. Nonlinear cortical modulation of muscle fatigue: A functional MRI study. Brain Res. 2002, 957, 320-329.
69. Post, M.; Steens, A.; Renken, R.; Maurits, N.M.; Zijdewind, I. Voluntary activation and cortical activity during a sustained maximal contraction: An fMRI study. Hum. Brain Mapp. 2009, 30, 1014-1027.
70. Van Duinen, H.; Renken, R.; Maurits, N.; Zijdewind, I. Effects of motor fatigue on human brain activity, an fMRI study. Neuroimage 2007, 35, 1438-1449.
71. Benwell, N.M.; Mastaglia, F.L.; Thickbroom, G.W. Changes in the functional MR signal in motor and non-motor areas during intermittent fatiguing hand exercise. Exp. Brain Res. 2007, 182, 93-97.
72. Anwar, A.R.; Muthalib, M.; Perrey, S.; Galka, A.; Granert, O.; Wolff, S.; Deuschl, G.; Raethjen, J.; Heute, U.; Muthuraman, M. Directionality Analysis on Functional Magnetic Resonance Imaging during Motor Task Using Granger Causality. In Proceedings of Engineering in Medicine and Biology Society (EMBC), 2012 Annual International Conference of the IEEE, San Diego, CA, USA, 28 August-1 September 2012; pp. 2287-2290.
73. Jiang, Z.; Wang, X.-F.; Kisiel-Sajewicz, K.; Yan, J.H.; Yue, G.H. Strengthened functional connectivity in the brain during muscle fatigue. Neuroimage 2012, 60, 728-737.
74. Rupp, T.; Perrey, S. Effect of severe hypoxia on prefrontal cortex and muscle oxygenation responses at rest and during exhaustive exercise. Adv. Exp. Med. Biol. 2009, 645, 329-334.
75. Pereira, M.I.; Gomes, P.S.; Bhambhani, Y. Acute effects of sustained isometric knee extension on cerebral and muscle oxygenation responses. Clin. Physiol. Funct. Imaging 2009, 29, 300-308.
76. Matsuura, C.; Gomes, P.S.C.; Haykowsky, M.; Bhambhani, Y. Cerebral and muscle oxygenation changes during static and dynamic knee extensions to voluntary fatigue in healthy men and women: a near infrared spectroscopy study. Clin. Physiol. Funct. Imaging 2011, 31, 114-123.
77. Gomes, P.S.; Matsuura C.; Bhambhani, Y.N. Effects of hypoxia on cerebral and muscle haemodynamics during knee extensions in healthy subjects. Eur. J. Appl. Physiol. 2012, 113, 13-23.
78. Sakatani, K.; Xie, Y.; Lichty, W.; Li, S.; Zuo, H. Language-activated cerebral blood oxygenation and hemodynamic changes of the left prefrontal cortex in poststroke aphasic patients: A near-infrared spectroscopy study. Stroke 1998, 29, 1299-1304.
79. Chen, S.; Sakatani, K.; Lichty, W.; Ning, P.; Zhao, S.; Zuo, H. Auditory-evoked cerebral oxygenation changes in hypoxic-ischemic encephalopathy of newborn infants monitored by near infrared spectroscopy. Early Hum. Dev. 2002, 67, 113-121.
80. Miyazawa, T.; Horiuchi, M.; Ichikawa, D.; Sato, K.; Tanaka, N.; Bailey, D.M.; Ogoh, S. Kinetics of exercise-induced neural activation; interpretive dilemma of altered cerebral perfusion. Exp. Physiol. 2011, 97, 219-227.
81. Lange-Assechenfeldt, C.; Kjoda, G. Alzheimer's disease, cerebrovascular dysfunction and the benefits of exercise: From vessels to neurons. Exp. Gerontol. 2008, 43, 499-504.
82. McCloskey, D.P.; Adamo, D.S.; Anderson, B.J. Exercise increases metabolic capacity in the motor cortex and striatum, but not in the hippocampus. Brain Res. 2001, 891, 168-175.
83. Johnson, R.A.; Mitchell, G.S. Exercise-induced changes in hippocampal brain-derived neurotrophic factor and neurotrophin-3: Effects of rat strain. Brain Res. 2003, 983, 108-114.
84. Pereira, A.C.; Huddleston, D.E.; Brickman, A.M.; Sosunov, A.A.; Hen, R.; McKhann, G.M.; Sloan, R.; Gage, F.H.; Brown, T.R.; Small, S.A. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. USA 2007, 104, 5638-5643.
85. Ogunshola, O.O.; Stewart, W.B.; Mihalcik, V.; Solli, T.; Madri, J.A.; Ment, L.R. Neuronal VEGF expression correlates with angiogenesis in postnatal developing rat brain. Brain Res. Dev. Brain Res. 2000, 119, 139-153.
86. Kleim, J.A.; Cooper, N.R.; vandenBerg, P.M. Exercise induces angiogenesis but dose not alter movement representations within rat motor cortex. Brain Res. 2002, 934, 1-6.
87. Swain, R.A.; Harris, A.B.; Wiener, E.C.; Dutka, M.V.; Morris, H.D.; Theien, B.E.; Konda, S.; Engberg, K.; Lauterbur, P.C.; Greenough, W.T. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 2003, 117, 1037-1046.
88. Ding, Y.; Li, J.; Luan, X.; Ding, Y.H.; Lai, Q.; Rafols, J.A.; Phillis, J.W.; Clark, J.C.; Diaz, F.G. Exercise pre-conditioning reduces brain damage in ischemic rats that may be associated with regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience 2004, 124, 583-591.
89. Li, J.; Ding, Y.H.; Rafols, J.A.; Lai, Q.; McAllister, J.P.; Ding, Y. Increased astrocyte proliferation in rats after running exercise. Neurosci. Lett. 2005, 386, 160-164.
90. Ainslie, P.N.; Cotter, J.D.; George, K.P.; Lucas, S.; Murrell, C.; Shave, R.; Thomas, K.N.; Williams, M.J.; Atkinson, G. Elevation in cerebral blood flow velocity with aerobic fitness throughout healthy human ageing. J. Physiol. 2008, 586, 4005-400.
91. Hooker, S.P.; Sui, X.; Colabianchi, N.; Vena, J.; Laditka, J.; LaMonte, M.J.; Blair, S.N. Cardiorespiratory fitness as a predictor of fatal and nonfatal stroke in asymptomatic women and men. Stroke 2008, 39, 2950-2957.
92. Larson, E.B.; Wang, L.; Bowen, J.D.; McCormick, W.C.; Teri, L.; Crane, P.; Kukull, W. Exercise is associated with reduced risk for incident dementia among persons 65 years of age and older. Ann. Intern. Med. 2006, 144, 73-81.
93. Bundo, M.; Inao, S.; Nakamura, A.; Kato, T.; Ito, K.; Tadokoro, M.; Kabeya, R.; Sugimoto, T.; Kajita, Y.; Yoshida, J. Changes of neural activity correlate with the severity of cortical ischemia in patients with unilateral major cerebral artery occlusion. Stroke 2002, 33, 61-66.
94. Frost, S.B.; Barbay, S.; Friel, K.M.; Plautz, E.J.; Nudo, R.J. Reorganization of remote cortical regions after ischemic brain injury: A potential substrate for stroke recovery. J. Neurophysiol. 2003, 89, 3205-3214.
95. Plate, K.H. Mechanism of angiogenesis in the brain. J. Neuropathol. Exp. Neurol. 1999, 58, 313-320.
96. Kolb, B.; Gibb, R. Possible anatomical basis of recovery of function after neonatal frontal lesions in rats. Behav. Neurosci. 1993, 107, 799-811.
97. Ward, N.S.; Brown, M.M.; Thompson, A.J.; Frackowiak, R.S. Neural correlates of motor recovery after stroke: A longitudinal fMRI study. Brain 2003, 126, 2476-2496.
98. Krupinski, J.; Kaluza, J.; Kumar, P.; Kumar, S.; Wang, J.M. Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 1994, 25, 1794-1798.
99. Cramer, S.C.; Nelles, G.; Benson, R.R.; Kaplan, J.D.; Parker, R.A.; Kwong, K.K.; Kennedy, D.N.; Finklestein, S.P.; Rosen, B.R. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 1997, 28, 2518-2527.
100. Isaacs, K.R.; Anderson, B.J.; Alcantara, A.A.; Black, J.E.; Greenough, W.T. Exercise and the brain: angiogenesis in the adult rat cerebellum after vigorous physical activity and motor skill learning. J. Cereb. Blood Flow Metab. 1992, 12, 10-119.
101. Hayes, K.; Sprague, S.; Guo, M.; Davis, W.; Friedman, A.; Kumar, A.; Jimenez, D.F.; Ding, Y. Forced, not voluntary, exercise effectively induces neuroprotection in stroke. Acta Neuropathol. 2008, 115, 289-296.
102. Tajiri, N.; Yasuhara, T.; Shingo, T.; Kondo, A.; Yuan, W.; Kadota, T.; Wang, F.; Baba, T.; Tayra, J.T.; Morimoto, T.; et al. Exercise exerts neuroprotective effects on Parkinson's disease model of rats. Brain Res. 2010, 1310, 200-207.
103. Petzinger, G.M.; Fisher, B.E.; van Leeuwen, J.E.; Vukovic, M.; Akopian, G.; Meshul, C.K.; Holschneider, D.P.; Nacca, A.; Walsh, J.P.; Jakowec, M.W. Enhancing neuroplasticity in the basal ganglia: The role of exercise in Parkinson's disease. Mov. Disord. 2010, 25, S141-S145.
104. Kinni, H.; Guo, M.; Ding, J.Y.; Konakondla, S.; Dornbos, D., III; Tran, R.; Guthikonda, M.; Ding, Y. Cerebral metabolism after forced or voluntary physical exercise. Brain Res. 2011, 1388, 48-55.
105. Alberts, J.L.; Linder, S.M.; Penko, A.L.; Lowe, M.J.; Philipps, M. It is not about the bike, it is about the pedaling: Forced exercise and Parkinson's disease. Exerc. Sport Sci. Rev. 2011, 39, 177-186.
106. Ding, Y.; Li, J.; Lai, Q.; Azam, S.; Rafols, J.A.; Diaz, F.G. Functional improvement after motor training is correlated with synaptic plasticity in rat thalamus. Neurol. Res. 2002, 24, 829-836.
107. Saitou, H.; Yanagi, H.; Hara, S.; Tsuchiya, S.; Tomura, S. Cerebral blood volume and oxygenationamong poststroke hemiplegic patients: Effects of 13 rehabilitation tasks measured by near-infrared spectroscopy. Arch. Phys. Med. Rehabil. 2000, 81, 1348-1356.