High-intensity interval training evokes larger serum BDNF levels compared with intense continuous exercise

Journal of Applied Physiology

Volumn 119, Issue 12, 2015, Pages 1363-1373

  Marquez, Cinthia Maria Saucedo ^a   Vanaudenaerde, Bart ^c   Troosters, Thierry ^c   Wenderoth, Nicole ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

Acute exercise; BDNF; Brain health; High intensity interval training; Neuroplasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN-DERIVED NEUROTROPHIC FACTOR, HUMAN;

ADULT; BLOOD; BRAIN; COMPARATIVE STUDY; ENDURANCE; EXERCISE; EXERCISE TEST; HEALTH PROMOTION; HUMAN; MALE; OXYGEN CONSUMPTION; PHYSIOLOGY; PROCEDURES; YOUNG ADULT;

ADULT; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; EXERCISE; EXERCISE TEST; HEALTH PROMOTION; HUMANS; MALE; OXYGEN CONSUMPTION; PHYSICAL CONDITIONING, HUMAN; PHYSICAL ENDURANCE; YOUNG ADULT;

EID: 84957882550     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00126.2015     Document Type: Article

References (99)

1. Afzalpour ME, Chadorneshin HT, Foadoddini M, Eivari HA. Comparing interval and continuous exercise training regimens on neurotrophic factors in rat brain. Physiol Behav 147: 78-83, 2015.
2. Babaei P, Damirchi A, Mehdipoor M, Tehrani BS. Long term habitual exercise is associated with lower resting level of serum BDNF. Neurosci Lett 566C: 304-308, 2014.
3. Begliuomini S, Lenzi E, Ninni F, Casarosa E, Merlini S, Pluchino N, Valentino V, Luisi S, Luisi M, Genazzani AR. Plasma brain-derived neurotrophic factor daily variations in men: correlation with cortisol circadian rhythm. J Endocrinol 197: 429-435, 2008.
4. Behrens MM, Strasser U, Lobner D, Dugan LL. Neurotrophin-mediated potentiation of neuronal injury. Microsc Res Tech 45: 276-284, 1999.
5. Boutcher SH. High-intensity intermittent exercise and fat loss. J Obes 2011: 868305, 2011.
6. Castellano V, White LJ. Serum brain-derived neurotrophic factor response to aerobic exercise in multiple sclerosis. J Neurol Sci 269: 85-91, 2008.
7. Chan KL, Tong KY, Yip SP. Relationship of serum brain-derived neurotrophic factor (BDNF) and health-related lifestyle in healthy human subjects. Neurosci Lett 447: 124-128, 2008.
8. Cheeran B, Talelli P, Mori F, Koch G, Suppa A, Edwards M, Houlden H, Bhatia K, Greenwood R, Rothwell JC. A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J Physiol 586: 5717-5725, 2008.
9. Cho HC, Kim J, Kim S, Son YH, Lee N, Jung SH. The concentrations of serum, plasma and platelet BDNF are all increased by treadmill VO(2)max performance in healthy college men. Neurosci Lett 519: 78-83, 2012.
10. Cornish AK, Broadbent S, Cheema BS. Interval training for patients with coronary artery disease: a systematic review. Eur J Appl Physiol 111: 579-589, 2011.
11. Correia PR, Pansani A, Machado F, Andrade M, Silva AC, Scorza FA, Cavalheiro EA, Arida RM. Acute strength exercise and the involvement of small or large muscle mass on plasma brain-derived neurotrophic factor levels. Clinics (Sao Paulo) 65: 1123-1126, 2010.
12. Cotman CW, Berchtold NC. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25: 295-301, 2002.
13. Ding Y, Li J, Luan X, Ding YH, Lai Q, Rafols JA, Phillis JW, Clark JC, Diaz FG. Exercise pre-conditioning reduces brain damage in ischemic rats that may be associated with regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience 124: 583-591, 2004.
14. Eston RG, Davies BL, Williams JG. Use of perceived effort ratings to control exercise intensity in young healthy adults. Eur J Appl Physiol Occup Physiol 56: 222-224, 1987.
15. Ferris LT, Williams JS, Shen CL. The effect of acute exercise on serum brain-derived neurotrophic factor levels and cognitive function. Med Sci Sports Exerc 39: 728-734, 2007.
16. Figiel I. Pro-inflammatory cytokine TNF-alpha as a neuroprotective agent in the brain. Acta Neurobiol Exp (Warsz) 68: 526-534, 2008.
17. Fujimura H, Altar CA, Chen R, Nakamura T, Nakahashi T, Kambayashi J, Sun B, Tandon NN. Brain-derived neurotrophic factor is stored in human platelets and released by agonist stimulation. Thromb Haemost 87: 728-734, 2002.
18. Gibala MJ, Little JP, van Essen M, Wilkin GP, Burgomaster KA, Safdar A, Raha S, Tarnopolsky MA. Short-term sprint interval versus traditional endurance training: similar initial adaptations in human skeletal muscle and exercise performance. J Physiol 575: 901-911, 2006.
19. Gibala MJ, McGee SL, Garnham AP, Howlett KF, Snow RJ, Hargreaves M. Brief intense interval exercise activates AMPK and p38 MAPK signaling and increases the expression of PGC-1alpha in human skeletal muscle. J Appl Physiol 106: 929-934, 2009.
20. Goekint M, De Pauw K, Roelands B, Njemini R, Bautmans I, Mets T, Meeusen R. Strength training does not influence serum brain-derived neurotrophic factor. Eur J Appl Physiol 110: 285-293, 2010.
21. Goekint M, Heyman E, Roelands B, Njemini R, Bautmans I, Mets T, Meeusen R. No influence of noradrenaline manipulation on acute exercise-induced increase of brain-derived neurotrophic factor. Med Sci Sports Exerc 40: 1990-1996, 2008.
22. Gold SM, Schulz KH, Hartmann S, Mladek M, Lang UE, Hellweg R, Reer R, Braumann KM, Heesen C. Basal serum levels and reactivity of nerve growth factor and brain-derived neurotrophic factor to standardized acute exercise in multiple sclerosis and controls. J Neuroimmunol 138: 99-105, 2003.
23. Griffin OW, Mulally S, Foley C, Warmington SA, O'Mara SM, Kelly AM. Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol Behav 104: 934-941, 2011.
24. Guiraud T, Nigam A, Gremeaux V, Meyer P, Juneau M, Bosquet L. High-intensity interval training in cardiac rehabilitation. Sports Med 42: 587-605, 2012.
25. Gutsaeva DR, Carraway MS, Suliman HB, Demchenko IT, Shitara H, Yonekawa H, Piantadosi CA. Transient hypoxia stimulates mitochondrial biogenesis in brain subcortex by a neuronal nitric oxide synthasedependent mechanism. J Neurosci 28: 2015-2024, 2008.
26. Huang AM, Jen CJ, Chen HF, Yu L, Kuo YM, Chen HI. Compulsive exercise acutely upregulates rat hippocampal brain-derived neurotrophic factor. J Neural Transm 113: 803-811, 2006.
27. Iellamo F, Manzi V, Caminiti G, Vitale C, Castagna C, Massaro M, Franchini A, Rosano G, Volterrani M. Matched dose interval and continuous exercise training induce similar cardiorespiratory and metabolic adaptations in patients with heart failure. Int J Cardiol 167: 2561-2565, 2013.
28. Isaksen K, Munk PS, Valborgland T, Larsen AI. Aerobic interval training in patients with heart failure and an implantable cardioverter defibrillator: a controlled study evaluating feasibility and effect. Eur J Prev Cardiol 22: 296-303, 2015.
29. Kavanagh T. Exercise and the heart. Ann Acad Med Singapore 12: 331-337, 1983.
30. Klein AB, Williamson R, Santini MA, Clemmensen C, Ettrup A, Rios M, Knudsen GM, Aznar S. Blood BDNF concentrations reflect braintissue BDNF levels across species. Int J Neuropsychopharmacol 14: 347-353, 2011.
31. Knaepen K, Goekint M, Heyman EM, Meeusen R. Neuroplasticity -exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects. Sports Med 40: 765-801, 2010.
32. Lee DC, Sui X, Ortega FB, Kim YS, Church TS, Winett RA, Ekelund U, Katzmarzyk PT, Blair SN. Comparisons of leisure-time physical activity and cardiorespiratory fitness as predictors of all-cause mortality in men and women. Br J Sports Med 45: 504-510, 2011.
33. Lipsky RH, Marini AM. Brain-derived neurotrophic factor in neuronal survival and behavior-related plasticity. Ann NY Acad Sci 1122: 130-143, 2007.
34. Little JP, Gillen JB, Percival ME, Safdar A, Tarnopolsky MA, Punthakee Z, Jung ME, Gibala MJ. Low-volume high-intensity interval training reduces hyperglycemia and increases muscle mitochondrial capacity in patients with type 2 diabetes. J Appl Physiol 111: 1554-1560, 2011.
35. Lommatzsch M, Zingler D, Schuhbaeck K, Schloetcke K, Zingler C, Schuff-Werner P, Virchow JC. The impact of age, weight and gender on BDNF levels in human platelets and plasma. Neurobiol Aging 26: 115-123, 2005.
36. Lowensteyn I, Coupal L, Zowall H, Grover SA. The cost-effectiveness of exercise training for the primary and secondary prevention of cardiovascular disease. J Cardiopulm Rehabil 20: 147-155, 2000.
37. Matthews VB, Aström MB, Chan MH, Bruce CR, Krabbe KS, Prelovsek O, Akerström T, Yfanti C, Broholm C, Mortensen OH, Penkowa M, Hojman P, Zankari A, Watt MJ, Bruunsgaard H, Pedersen BK, Febbraio MA. Brain-derived neurotrophic factor is produced by skeletal muscle cells in response to contraction and enhances fat oxidation via activation of AMP-activated protein kinase. Diabetologia 52: 1409-1418, 2009.
38. Meyer P, Guiraud T, Gayda M, Juneau M, Bosquet L, Nigam A. High-intensity aerobic interval training in a patient with stable angina pectoris. Am J Phys Med Rehabil 89: 83-86, 2010.
39. Moholdt TT, Amundsen BH, Rustad LA, Wahba A, Lovo KT, Gullikstad LR, Bye A, Skogvoll E, Wisloff U, Slordahl SA. Aerobic interval training versus continuous moderate exercise after coronary artery bypass surgery: a randomized study of cardiovascular effects and quality of life. Am Heart J 158: 1031-1037, 2009.
40. Molteni R, Wu A, Vaynman S, Ying Z, Barnard RJ, Gomez-Pinilla F. 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, 2004.
41. Monteleone P, Artini PG, Simi G, Cela V, Casarosa E, Begliuomini S, Ninni F, Pluchino N, Luisi M, Genazzani AR. Brain derived neurotrophic factor circulating levels in patients undergoing IVF. J Assist Reprod Genet 24: 477-480, 2007.
42. Nagamatsu LS, Flicker L, Kramer AF, Voss MW, Erickson KI, Hsu CL, Liu-Ambrose T. Exercise is medicine, for the body and the brain. Br J Sports Med 48: 943-944, 2014.
43. Neeper SA, Gomez-Pinilla F, Choi J, Cotman C. Exercise and brain neurotrophins. Nature 373: 109, 1995.
44. Neeper SA, Gomez-Pinilla F, Choi J, Cotman CW. Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 726: 49-56, 1996.
45. Noble BJ. Clinical applications of perceived exertion. Med Sci Sports Exerc 14: 406-411, 1982.
46. Nofuji Y, Suwa M, Moriyama Y, Nakano H, Ichimiya A, Nishichi R, Sasaki H, Radak Z, Kumagai S. Decreased serum brain-derived neurotrophic factor in trained men. Neurosci Lett 437: 29-32, 2008.
47. Nofuji Y, Suwa M, Sasaki H, Ichimiya A, Nishichi R, Kumagai S. Different circulating brain-derived neurotrophic factor responses to acute exercise between physically active and sedentary subjects. J Sports Sci Med 11: 83-88, 2012.
48. O'Callaghan RM, Ohle R, Kelly AM. The effects of forced exercise on hippocampal plasticity in the rat: a comparison of LTP, spatial- and non-spatial learning. Behav Brain Res 176: 362-366, 2007.
49. Ogborn DI, Gardiner PF. Effects of exercise and muscle type on BDNF, NT-4/5, and TrKB expression in skeletal muscle. Muscle Nerve 41: 385-391, 2010.
50. Oliff HS, Berchtold NC, Isackson P, Cotman CW. Exercise-induced regulation of brain-derived neurotrophic factor (BDNF) transcripts in the rat hippocampus. Brain Res Mol Brain Res 61: 147-153, 1998.
51. Ozan E, Okur H, Eker C, Eker OD, Gonul AS, Akarsu N. The effect of depression, BDNF gene val66met polymorphism and gender on serum BDNF levels. Brain Res Bull 81: 61-65, 2010.
52. Pan W, Banks WA, Fasold MB, Bluth J, Kastin AJ. Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology 37: 1553-1561, 1998.
53. Perry CG, Lally J, Holloway GP, Heigenhauser GJ, Bonen A, Spriet LL. Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. J Physiol 588: 4795-4810, 2010.
54. Pichot V, Roche F, Denis C, Garet M, Duverney D, Costes F, Barthelemy JC. Interval training in elderly men increases both heart rate variability and baroreflex activity. Clin Auton Res 15: 107-115, 2005.
55. Pluchino N, Cubeddu A, Begliuomini S, Merlini S, Giannini A, Bucci F, Casarosa E, Luisi M, Cela V, Genazzani AR. Daily variation of brain-derived neurotrophic factor and cortisol in women with normal menstrual cycles, undergoing oral contraception and in postmenopause. Hum Reprod 24: 2303-2309, 2009.
56. Pokan R, Von Duvillard SP, Ludwig J, Rohrer A, Hofmann P, Wonisch M, Smekal G, Schmid P, Pacher R, Bachl N. Effect of high-volume and -intensity endurance training in heart transplant recipients. Med Sci Sports Exerc 36: 2011-2016, 2004.
57. Rasmussen P, Brassard P, Adser H, Pedersen MV, Leick L, Hart E, Secher NH, Pedersen BK, Pilegaard H. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp Physiol 94: 1062-1069, 2009.
58. Reid MB, Stokic DS, Koch SM, Khawli FA, Leis AA. N-acetylcysteine inhibits muscle fatigue in humans. J Clin Invest 94: 2468-2474, 1994.
59. Rickham PP. Human experimentation code of ethics of the world medical association. Declaration of Helsinki. Br Med J 2: 177, 1964.
60. Rognmo O, Moholdt T, Bakken H, Hole T, Molstad P, Myhr NE, Grimsmo J, Wisloff U. Cardiovascular risk of high- versus moderateintensity aerobic exercise in coronary heart disease patients. Circulation 126: 1436-1440, 2012.
61. Roig M, Nordbrandt S, Geertsen SS, Nielsen JB. The effects of cardiovascular exercise on human memory: a review with meta-analysis. Neurosci Biobehav Rev 37: 1645-1666, 2013.
62. Roig M, Skriver K, Lundbye-Jensen J, Kiens B, Nielsen JB. A single bout of exercise improves motor memory. PLoS One 7: e44594, 2012.
63. Rojas VS, Struder HK, Vera WB, Schmidt A, Bloch W, Hollmann W. Acute BDNF and cortisol response to low intensity exercise and following ramp incremental exercise to exhaustion in humans. Brain Res 1121: 59-65, 2006.
64. Saha RN, Liu X, Pahan K. Up-regulation of BDNF in astrocytes by TNF-alpha: a case for the neuroprotective role of cytokine. J Neuroimmune Pharmacol 1: 212-222, 2006.
65. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21: 55-89, 2000.
66. Sartorius A, Hellweg R, Litzke J, Vogt M, Dormann C, Vollmayr B, Danker-Hopfe H, Gass P. Correlations and discrepancies between serum and brain tissue levels of neurotrophins after electroconvulsive treatment in rats. Pharmacopsychiatry 42: 270-276, 2009.
67. Schiffer T, Schulte S, Hollmann W, Bloch W, Struder HK. Effects of strength and endurance training on brain-derived neurotrophic factor and insulin-like growth factor 1 in humans. Horm Metab Res 41: 250-254, 2009.
68. Schiffer T, Schulte S, Sperlich B, Achtzehn S, Fricke H, Struder HK. Lactate infusion at rest increases BDNF blood concentration in humans. Neurosci Lett 488: 234-237, 2011.
69. Schmidt-Kassow M, Schädle S, Otterbein S, Thiel C, Doehring A, Lötsch J, Kaiser J. Kinetics of serum brain-derived neurotrophic factor following low-intensity versus high-intensity exercise in men and women. Neuroreport 23: 889-893, 2012.
70. Schmolesky MT, Webb DL, Hansen RA. The effects of aerobic exercise intensity and duration on levels of brain-derived neurotrophic factor in healthy men. J Sports Sci Med 12: 502-511, 2013.
71. Seifert T, Brassard P, Wissenberg M, Rasmussen P, Nordby P, Stallknecht B, Adser H, Jakobsen AH, Pilegaard H, Nielsen HB, Secher NH. Endurance training enhances BDNF release from the human brain. Am J Physiol Regul Integr Comp Physiol 298: R372-R377, 2010.
72. Siamilis S, Jakus J, Nyakas C, Costa A, Mihalik B, Falus A, Radak Z. The effect of exercise and oxidant-antioxidant intervention on the levels of neurotrophins and free radicals in spinal cord of rats. Spinal Cord 47: 453-457, 2009.
73. Smith MA, Makino S, Kvetnansky R, Post RM. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 15: 1768-1777, 1995.
74. Spruit MA, Singh SJ, Garvey C, ZuWallack R, Nici L, Rochester C, Hill K, Holland AE, Lareau SC, Man WD, Pitta F, Sewell L, Raskin J, Bourbeau J, Crouch R, Franssen FM, Casaburi R, Vercoulen JH, Vogiatzis I, Gosselink R, Clini EM, Effing TW, Maltais F, van der Palen J, Troosters T, Janssen DJ, Collins E, Garcia-Aymerich J, Brooks D, Fahy BF, Puhan MA, Hoogendoorn M, Garrod R, Schols AM, Carlin B, Benzo R, Meek P, Morgan M, Rutten-van Mölken MP, Ries AL, Make B, Goldstein RS, Dowson CA, Brozek JL, Donner CF, Wouters EF; ATS/ERS Task force on Pulmonary Rehabilitation. An official American Thoracic Society/European Respiratory Society statement: key concepts and advances in pulmonary rehabilitation. Am J Respir Crit Care Med 188: e13-e64, 2013.
75. Strohle A, Stoy M, Graetz B, Scheel M, Wittmann A, Gallinat J, Lang UE, Dimeo F, Hellweg R. Acute exercise ameliorates reduced brainderived neurotrophic factor in patients with panic disorder. Psychoneuroendocrinology 35: 364-368, 2010.
76. Swift DL, Johannsen NM, Myers VH, Earnest CP, Smits JA, Blair SN, Church TS. The effect of exercise training modality on serum brain derived neurotrophic factor levels in individuals with type 2 diabetes. PLoS One 7: e42785, 2012.
77. Tang A, Sibley KM, Thomas SG, Bayley MT, Richardson D, McIlroy WE, Brooks D. Effects of an aerobic exercise program on aerobic capacity, spatiotemporal gait parameters, and functional capacity in subacute stroke. Neurorehabil Neural Repair 23: 398-406, 2009.
78. Tang SW, Chu E, Hui T, Helmeste D, Law C. Influence of exercise on serum brain-derived neurotrophic factor concentrations in healthy human subjects. Neurosci Lett 431: 62-65, 2008.
79. Tauler P, Martinez S, Moreno C, Martinez P, Aguilo A. Changes in salivary hormones, immunoglobulin A, and C-reactive protein in response to ultra-endurance exercises. Appl Physiol Nutr Metab 39: 560-565, 2014.
80. Tjønna AE, Lee SJ, Rognmo O, Stølen TO, Bye A, Haram PM, Loennechen JP, Al-Share QY, Skogvoll E, Slørdahl SA, Kemi OJ, Najjar SM, Wisløff U. Aerobic interval training versus continuous moderate exercise as a treatment for the metabolic syndrome: a pilot study. Circulation 118: 346-354, 2008.
81. Tjønna AE, Stølen TO, Bye A, Volden M, Slørdahl SA, Odegird R, Skogvoll E, Wisløff U. Aerobic interval training reduces cardiovascular risk factors more than a multitreatment approach in overweight adolescents. Clin Sci (Lond) 116: 317-326, 2009.
82. Tordi N, Dugue B, Klupzinski D, Rasseneur L, Rouillon JD, Lonsdorfer J. Interval training program on a wheelchair ergometer for paraplegic subjects. Spinal Cord 39: 532-537, 2001.
83. VanBruggen MD, Hackney AC, McMurray RG, Ondrak KS. The relationship between serum and salivary cortisol levels in response to different intensities of exercise. Int J Sports Physiol Perform 6: 396-407, 2011.
84. Vaynman S, Gomez-Pinilla F. License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabil Neural Repair 19: 283-295, 2005.
85. Vaynman S, Gomez-Pinilla F. Revenge of the "sit": how lifestyle impacts neuronal and cognitive health through molecular systems that interface energy metabolism with neuronal plasticity. J Neurosci Res 84: 699-715, 2006.
86. Vaynman S, Ying Z, Gomez-Pinilla F. Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience 122: 647-657, 2003.
87. Vaynman S, Ying Z, Gomez-Pinilla F. Exercise induces BDNF and synapsin I to specific hippocampal subfields. J Neurosci Res 76: 356-362, 2004.
88. Vaynman S, Ying Z, Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20: 2580-2590, 2004.
89. Vogiatzis I. Strategies of muscle training in very severe COPD patients. Eur Respir J 38: 971-975, 2011.
90. Wahl P, Hein M, Achtzehn S, Bloch W, Mester J. Acute effects of superimposed electromyostimulation during cycling on myokines and markers of muscle damage. J Musculoskelet Neuronal Interact 15: 53-59, 2015.
91. Wang H, Ward N, Boswell M, Katz DM. Secretion of brain-derived neurotrophic factor from brain microvascular endothelial cells. Eur J Neurosci 23: 1665-1670, 2006.
92. Wang H, Yuan G, Prabhakar NR, Boswell M, Katz DM. Secretion of brain-derived neurotrophic factor from PC12 cells in response to oxidative stress requires autocrine dopamine signaling. J Neurochem 96: 694-705, 2006.
93. Weston KS, Wisloff U, Coombes JS. High-intensity interval training in patients with lifestyle-induced cardiometabolic disease: a systematic review and meta-analysis. Br J Sports Med 48: 1227-1234, 2014.
94. Widenfalk J, Olson L, Thoren P. Deprived of habitual running, rats downregulate BDNF and TrkB messages in the brain. Neurosci Res 34: 125-132, 1999.
95. Winter B, Breitenstein C, Mooren FC, Voelker K, Fobker M, Lechtermann A, Krueger K, Fromme A, Korsukewitz C, Floel A, Knecht S. High impact running improves learning. Neurobiol Learn Mem 87: 597-609, 2007.
96. Wisløff U, Støylen A, Loennechen JP, Bruvold M, Rognmo, Haram PM, Tjønna AE, Helgerud J, Slørdahl SA, Lee SJ, Videm V, Bye A, Smith GL, Najjar SM, Ellingsen O, Skjaerpe T. Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: a randomized study. Circulation 115: 3086-3094, 2007.
97. Wrann CD, White JP, Salogiannnis J, Laznik-Bogoslavski D, Wu J, Ma D, Lin JD, Greenberg ME, Spiegelman BM. Exercise induces hippocampal BDNF through a PGC-1alpha/FNDC5 pathway. Cell Metab 18: 649-659, 2013.
98. Yarrow JF, White LJ, McCoy SC, Borst SE. Training augments resistance exercise induced elevation of circulating brain derived neurotrophic factor (BDNF). Neurosci Lett 479: 161-165, 2010.
99. Zoladz JA, Pilc A, Majerczak J, Grandys M, Zapart-Bukowska J, Duda K. Endurance training increases plasma brain-derived neurotrophic factor concentration in young healthy men. J Physiol Pharmacol 59, Suppl 7: 119-132, 2008.