{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,20]],"date-time":"2026-04-20T22:52:22Z","timestamp":1776725542443,"version":"3.51.2"},"reference-count":122,"publisher":"MDPI AG","issue":"15","license":[{"start":{"date-parts":[[2020,8,4]],"date-time":"2020-08-04T00:00:00Z","timestamp":1596499200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["Grant No. 2013\/09\/B\/NZ7\/00726"],"award-info":[{"award-number":["Grant No. 2013\/09\/B\/NZ7\/00726"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Exposure to acute hypoxia causes a detrimental effect on the brain which is also manifested by a decrease in the ability to perform psychomotor tasks. Conversely, brain-derived neurotrophic factor (BDNF), whose levels are elevated in response to exercise, is a well-known factor in improving cognitive function. Therefore, the aim of our study was to investigate whether the exercise under hypoxic conditions affects psychomotor performance. For this purpose, 11 healthy young athletes performed a graded cycloergometer exercise test to volitional exhaustion under normoxia and acute mild hypoxia (FiO2 = 14.7%). Before, immediately after exercise and after a period of recovery, choice reaction time (CRT) and number of correct reactions (NCR) in relation to changes in serum BDNF were examined. Additionally, other selected factors which may modify BDNF production, i.e., cortisol (C), nitrite, catecholamines (adrenalin-A, noradrenaline-NA, dopamine-DA, serotonin-5-HT) and endothelin-1 (ET-1), were also measured. Exercise in hypoxic conditions extended CRT by 13.8% (p &lt; 0.01) and decreased NCR (by 11.5%) compared to rest (p &lt; 0.05). During maximal workload, NCR was lower by 9% in hypoxia compared to normoxia (p &lt; 0.05). BDNF increased immediately after exercise in normoxia (by 29.3%; p &lt; 0.01), as well as in hypoxia (by 50.0%; p &lt; 0.001). There were no differences in BDNF between normoxia and hypoxia. Considering the fact that similar levels of BDNF were seen in both conditions but cognitive performance was suppressed in hypoxia, acute elevation of BDNF did not compensate for hypoxia-induced cognition impairment. Moreover, neither potentially negative effects of C nor positive effects of A, DA and NO on the brain were observed in our study.<\/jats:p>","DOI":"10.3390\/ijms21155569","type":"journal-article","created":{"date-parts":[[2020,8,4]],"date-time":"2020-08-04T05:56:46Z","timestamp":1596520606000},"page":"5569","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Exercise-Induced Elevated BDNF Level Does Not Prevent Cognitive Impairment Due to Acute Exposure to Moderate Hypoxia in Well-Trained Athletes"],"prefix":"10.3390","volume":"21","author":[{"given":"Zofia","family":"Piotrowicz","sequence":"first","affiliation":[{"name":"Institute of Sport Sciences, The Jerzy Kukuczka Academy of Physical Education, 40-065 Katowice, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ma\u0142gorzata","family":"Chalimoniuk","sequence":"additional","affiliation":[{"name":"Department of Tourism and Health in Bia\u0142a Podlaska, The J\u00f3zef Pi\u0142sudski University of Physical Education, 00-968 Warsaw, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3516-9124","authenticated-orcid":false,"given":"Kamila","family":"P\u0142oszczyca","sequence":"additional","affiliation":[{"name":"Department of Kinesiology, Institute of Sport, 01-982 Warsaw, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mi\u0142osz","family":"Czuba","sequence":"additional","affiliation":[{"name":"Department of Kinesiology, Institute of Sport, 01-982 Warsaw, Poland"},{"name":"Faculty of Health Sciences, Jan Dlugosz University, 42-200 Czestochowa, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J\u00f3zef","family":"Langfort","sequence":"additional","affiliation":[{"name":"Institute of Sport Sciences, The Jerzy Kukuczka Academy of Physical Education, 40-065 Katowice, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,8,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1042\/cs0940279","article-title":"Metabolic and myoelectrical effects of acute hypoxaemia during isometric contraction of forearm muscles in humans: A combined 31P-magnetic resonance spectroscopy-surface electromyogram (MRS-SEMG) study","volume":"94","author":"Bendahan","year":"1998","journal-title":"Clin. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1152\/japplphysiol.00128.2002","article-title":"Anaerobic energy provision does not limit Wingate exercise performance in endurance-trained cyclists","volume":"94","author":"Calbet","year":"2003","journal-title":"J. Appl. Physiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1111\/j.1748-1716.2009.02007.x","article-title":"Decrease in cerebral oxygenation influences central motor output in humans","volume":"196","author":"Perrey","year":"2009","journal-title":"Acta Physiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1113\/jphysiol.2006.113936","article-title":"Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue in humans","volume":"575","author":"Amann","year":"2006","journal-title":"J. Physiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1007\/s004210050281","article-title":"Effects of oxygen fraction in inspired air on force production and electromyogram activity during ergometer rowing","volume":"76","author":"Peltonen","year":"1997","journal-title":"Eur. J. Appl. Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1997","DOI":"10.1152\/jappl.1999.87.6.1997","article-title":"Exercise-induced arterial hypoxemia","volume":"87","author":"Dempsey","year":"1999","journal-title":"J. Appl. Physiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"863","DOI":"10.1152\/jappl.1980.49.5.863","article-title":"Oxygen uptake, acid-base status, and performance with varied inspired oxygen fractions","volume":"49","author":"Adams","year":"1980","journal-title":"J. Appl. Physiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1152\/jappl.1999.86.4.1367","article-title":"Human muscle performance and PCr hydrolysis with varied inspired oxygen fraction: A 31P-MRS study","volume":"86","author":"Hogan","year":"1999","journal-title":"J. Appl. Physiol."},{"key":"ref_9","first-page":"904","article-title":"Oxygen uptake response during maximal cycling in hyperoxia, normoxia and hypoxia","volume":"72","author":"Peltonen","year":"2001","journal-title":"Aviat. Space Environ. Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1007\/s00421-003-0899-y","article-title":"Decrease in peak heart rate with acute hypoxia in relation to sea level VO(2max)","volume":"90","author":"Benoit","year":"2003","journal-title":"Eur. J. Appl. Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1042\/cs1010377","article-title":"Heart rate response to hypoxic exercise: Role of dopamine D2-receptors and effect of oxygen supplementation","volume":"101","author":"Lundby","year":"2001","journal-title":"Clin. Sci."},{"key":"ref_12","first-page":"634","article-title":"Fatigue and exhaustion in chronic hypobaric hypoxia: Influence of exercising muscle mass","volume":"76","author":"Kayser","year":"1994","journal-title":"Am. J. Physiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1785","DOI":"10.1161\/hc4001.097040","article-title":"Parasympathetic neural activity accounts for the lowering of exercise heart rate at high altitude","volume":"104","author":"Boushel","year":"2001","journal-title":"Circulation"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1113\/jphysiol.2007.129700","article-title":"Severity of arterial hypoxaemia affects the relative contributions of pripheral muscle fatigue to exercise performance in healthy humans","volume":"581","author":"Amann","year":"2007","journal-title":"J. Physiol."},{"key":"ref_15","first-page":"1379","article-title":"Muscle as an endocrine organ: Focus on muscle-derived interleukin-6","volume":"88","author":"Pedersen","year":"2008","journal-title":"Phys. Rev."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1097\/00005768-199701000-00008","article-title":"Possible mechanisms of central nervous system fatigue during exercise","volume":"29","author":"Davis","year":"1997","journal-title":"Med. Sci. Sports Exerc."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1038\/372325a0","article-title":"Cognitive defects at altitude","volume":"372","author":"Lieberman","year":"1994","journal-title":"Nature"},{"key":"ref_18","first-page":"107","article-title":"Cerebral blood flow velocity and psychomotor performance during acute hypoxia","volume":"77","author":"Blogg","year":"2006","journal-title":"Aviat. Space Environ. Med."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"654","DOI":"10.3357\/ASEM.2690.2010","article-title":"Hypoxia and flight performance of military instructor pilots in a flight simulator","volume":"81","author":"Temme","year":"2010","journal-title":"Aviat. Space Environ. Med."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.neubiorev.2017.01.019","article-title":"Effect of acute hypoxia on cognition: A systematic review and meta-regression analysis","volume":"74","author":"McMorris","year":"2017","journal-title":"Neurosci. A Biobehav. Rev."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1601","DOI":"10.1378\/chest.11-2214","article-title":"Neurocognitive impairment in obstructive sleep apnea","volume":"141","author":"Lal","year":"2012","journal-title":"Chest"},{"key":"ref_22","unstructured":"Jensen, A.R. (2006). Clocking the Mind: Mental Chronometry and Individual Differences, Elsevier Science. [1st ed.]."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1076\/jcen.24.7.858.8392","article-title":"Interpreting reaction time measures in between-group comparisons","volume":"24","author":"Salthouse","year":"2002","journal-title":"J. Clin. Exp. Neuropsychol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/j.physbeh.2018.02.035","article-title":"Severity-dependent influence of isocapnic hypoxia on reaction time is independent of neurovascular coupling","volume":"1","author":"Caldwell","year":"2018","journal-title":"Physiol. Behav."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.physbeh.2015.10.028","article-title":"Acute physical exercise under hypoxia improves sleep, mood and reaction time","volume":"154","author":"Santos","year":"2016","journal-title":"Physiol. Behav."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1007\/s12576-018-0603-y","article-title":"Hypoxia-induced lowered executive function depends on arterial oxygen desaturation","volume":"68","author":"Ochi","year":"2018","journal-title":"J. Physiol. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Pramsohler, S., Wimmer, S., Kopp, M., Gatterer, H., Faulhaber, M., Burtscher, M., and Netzer, N.C. (2017). Normobaric hypoxia overnight impairs cognitive reaction time. BMC Neurosi., 18.","DOI":"10.1186\/s12868-017-0362-3"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.brainres.2005.02.030","article-title":"Characterizing learning deficits and hippocampal neuron loss following transient global cerebral ischemia in rats","volume":"1043","author":"Hartman","year":"2005","journal-title":"Brain Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.brainres.2007.06.106","article-title":"Hypobaric hypoxia damages the hippocampal pyramidal neurons in the rat brain","volume":"1175","author":"Maiti","year":"2007","journal-title":"Brain Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.expneurol.2008.01.030","article-title":"Chronic hypobaric hypoxia induced apoptosis in CA1 region of hippocampus: A possible role of NMDAR mediated p75NTR upregulation","volume":"212","author":"Hota","year":"2008","journal-title":"Exp. Neurol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1017\/S1355617704101082","article-title":"Effects of hypoxia on the brain: Neuroimaging and neuropsychological findings following carbon monoxide poisoning and obstructive sleep apnea","volume":"10","author":"Gale","year":"2004","journal-title":"J. Int. Neuropsychol. Soc."},{"key":"ref_32","first-page":"406","article-title":"Multiple-choice reaction time and movement time during physical exertion","volume":"42","author":"Levitt","year":"1971","journal-title":"Res. Q."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1080\/0097840X.1975.9939549","article-title":"Relations between heart rate, reaction speed and subjective effort at different work loads on a bicycle ergometer","volume":"1","year":"1975","journal-title":"J. Hum. Stress"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1055\/s-2007-1021042","article-title":"Choice reaction time during graded exercise in relation to blood lactate and plasma catecholamine thresholds","volume":"15","author":"Chmura","year":"1994","journal-title":"Int. J. Sports Med."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1007\/s004210050303","article-title":"Psychomotor performance during prolonged exercise above and below lactate threshold","volume":"77","author":"Chmura","year":"1998","journal-title":"Eur. J. Appl. Physiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"15","DOI":"10.2466\/pms.1995.80.1.15","article-title":"Information processing and concentration as a function of fitness level and exercise-induced activation to exhaustion","volume":"80","author":"Travlos","year":"1995","journal-title":"Percept. Mot. Skills"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1007\/s002130100787","article-title":"Influence of caffeine, cold and exercise on multiple choice reaction time","volume":"157","author":"Kruk","year":"2001","journal-title":"Psychopharmacology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1007\/BF02333799","article-title":"The effect of various levels of strenuous to exhausting exercise on reaction time","volume":"35","author":"Bender","year":"1976","journal-title":"Eur. J. Appl. Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1111\/j.1749-6632.2012.06525.x","article-title":"Brain-derived neurotrophic factor as a regulator of systemic and brain energy metabolism and cardiovascular health","volume":"1264","author":"Rothman","year":"2012","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/sms.12069","article-title":"The effects of physical activity and exercise on brain-derived neurotrophic factor in healthy humans: A review","volume":"24","author":"Huang","year":"2014","journal-title":"Scand. J. Med. Sci. Sports"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1038\/344339a0","article-title":"Identyfication and characterization of a novel member of the nerve growth factor\/brain-derived neurotrophic factor family","volume":"344","author":"Hohn","year":"1990","journal-title":"Nature"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1080\/08977190410001723308","article-title":"Brain-derived neurotrophic factor","volume":"22","author":"Binder","year":"2004","journal-title":"Growth Factors"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2","DOI":"10.18388\/pb.2019_251","article-title":"Rola m\u00f3zgowego czynnika neurotroficznego (BDNF) w procesach neurodegeneracji oraz w mechanizmach neuroregeneracji wywo\u0142anej wzmo\u017con\u0105 aktywno\u015bci\u0105 fizyczn\u0105","volume":"65","author":"Piotrowicz","year":"2019","journal-title":"Post\u0119py Biochem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1101\/lm.51202","article-title":"From acquisition to consolidation: On the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning","volume":"9","author":"Tyler","year":"2002","journal-title":"Learn. Mem."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"765","DOI":"10.2165\/11534530-000000000-00000","article-title":"Neuroplasticity-exercise-induced response of peripheral brain-derived neurotrophic factor: A systematic review of experimental studies in human subjects","volume":"40","author":"Knaepen","year":"2010","journal-title":"Sports Med."},{"key":"ref_46","first-page":"119","article-title":"Endurance training increases plasma brain-derived neurotrophic factor concentration in young healthy men","volume":"59","author":"Zoladz","year":"2008","journal-title":"J. Physiol. Pharmacol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1007\/s12264-011-1531-5","article-title":"Increased basal plasma brain-derived neurotrophic factor levels in sprint runners","volume":"27","author":"Correia","year":"2011","journal-title":"Neurosci. Bull."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/S0012-1606(03)00120-9","article-title":"Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain","volume":"258","author":"Cheng","year":"2003","journal-title":"Dev. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.brainresbull.2005.08.013","article-title":"Nitric oxide synthesis is required for exercise-induced increases in hippocampal BDNF and phosphatidylinositol 3\u2032 kinase expression","volume":"68","author":"Chen","year":"2006","journal-title":"Brain Res. Bull."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1082","DOI":"10.1519\/JSC.0b013e3181d321ff","article-title":"Arginine and ornithine supplementation increases growth hormone and insulin-like growth factor-1 serum levels after heavy-resistance exercise in strength-trained athletes","volume":"24","author":"Zajac","year":"2010","journal-title":"J. Strength Cond. Res."},{"key":"ref_51","first-page":"151","article-title":"Marathon run: Effects on blood cortisol-ACTH, iodothyronines-TSH and vasopressin","volume":"95","author":"Dessypris","year":"1980","journal-title":"Acta Endocrinol. (Copenh.)"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/j.neuroscience.2012.07.019","article-title":"Effects of voluntary running on plasma levels of neurotrophins, hippocampal cell proliferation and learning and memory in stressed rats","volume":"222","author":"Yau","year":"2012","journal-title":"Neuroscience"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1038\/jcbfm.2009.208","article-title":"Brain-derived neurotrophic factor enhances the expression of the monocarboxylate transporter 2 through translational activation in mouse cultured cortical neurons","volume":"30","author":"Robinet","year":"2010","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Ng, T.K.S., Ho, C.S.H., Tam, W.W.S., Kua, E.H., and Ho, R.C. (2019). Decreased Serum Brain-Derived Neurotrophic Factor (BDNF) Levels in Patients with Alzheimer\u2019s Disease (AD): A Systematic Review and Meta-Analysis. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20020257"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"52","DOI":"10.3389\/fnins.2018.00052","article-title":"Exercise-Mediated Neurogenesis in the Hippocampus via BDNF","volume":"12","author":"Liu","year":"2018","journal-title":"Front. Neurosci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1553","DOI":"10.1016\/S0028-3908(98)00141-5","article-title":"Transport of brain-derived neurotrophic factor across the blood-brain barrier","volume":"37","author":"Pan","year":"1998","journal-title":"Neuropharmacology"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"S237","DOI":"10.33549\/physiolres.933837","article-title":"Endothelin-1 inhibition improves the mBDNF\/proBDNF ratio in endothelial cells and HT22 neurons under high glucose\/palmitate growth conditions","volume":"67","author":"Ward","year":"2018","journal-title":"Physiol. Res."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1038\/350230a0","article-title":"BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra","volume":"350","author":"Hyman","year":"1991","journal-title":"Nature"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1080\/14728222.2019.1572747","article-title":"Neuronal and behavioral plasticity: The role of serotonin and BDNF systems tandem","volume":"23","author":"Popova","year":"2019","journal-title":"Expert Opin. Ther. Targets"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"800","DOI":"10.1111\/gbb.12394","article-title":"A single bout of exercise increase hippocampal Bdnf: Influence of chronic exercise and noradrenaline","volume":"16","author":"Venezia","year":"2017","journal-title":"Genes Brain Behav."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1470320318782782","DOI":"10.1177\/1470320318782782","article-title":"A pilot investigation into the effects of acute normobaric hypoxia, high altitude exposure and exercise on serum angiotensin-converting enzyme, aldosterone and cortisol","volume":"19","author":"Cooke","year":"2018","journal-title":"J. Renin Angiotensin Aldosterone Syst."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1055\/s-2007-1024565","article-title":"A comparison of the blood lactate and plasma catecholamine thresholds in untrained male subjects","volume":"13","author":"Schneider","year":"1992","journal-title":"Int. J. Sports Med."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1080\/15622975.2016.1273551","article-title":"Prefrontal Cortex Dysfunction in Hypoxic-Ischaemic Encephalopathy Contributes to Executive Function Impairments in Rats: Potential Contribution for Attention-Deficit\/Hyperactivity Disorder","volume":"19","author":"Miguel","year":"2018","journal-title":"World J. Biol. Psychiatry"},{"key":"ref_64","unstructured":"Benzi, G. (1987). Amino acids, brain neurotransmitters and a functional link between muscle brain that is important in sustained exercise. Advances in Biochemistry, John Libby Eurotext."},{"key":"ref_65","first-page":"1352","article-title":"PET studies of the effects of aerobic exercise on human striatal dopamine release","volume":"41","author":"Wang","year":"2000","journal-title":"J. Nucl. Med."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1006\/exnr.1997.6437","article-title":"Long-term reciprocal changes in dopamine levels in prefrontal cortex versus nucleus accumbens in rats born by Caesarean section compared to vaginal birth","volume":"145","author":"Boksa","year":"1997","journal-title":"Exp. Neurol."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Piotrowicz, \u017c., Chalimoniuk, M., Ploszczyca, K., Czuba, M., and Langfort, J. (2019). Acute normobaric hypoxia does not affect the simultaneous exercise-induced increase in circulating BDNF and GDNF in young healthy men: A feasibility study. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0224207"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.1007\/s11011-019-00450-z","article-title":"Modulating effects of predconditioning exercise in the expression of ET-1 and BNP via HIF-1a in ischemically injured brain","volume":"34","author":"Wang","year":"2019","journal-title":"Metab. Brain Dis."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1097\/00003677-200204000-00006","article-title":"Exercise Enhances and Protects Brain Function","volume":"30","author":"Cotman","year":"2002","journal-title":"Exerc. Sport Sci. Rev."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1611","DOI":"10.1111\/psyp.12736","article-title":"Acute Effects of Moderate Aerobic Exercise on Specific Aspects of Executive Function in Different Age and Fitness Groups: A Meta-Analysis","volume":"53","author":"Ludyga","year":"2016","journal-title":"Psychophysiology"},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Czuba, M., Wilk, R., Karpi\u0144ski, J., Chalimoniuk, M., Zajac, A., and Langfort, J. (2017). Intermittent hypoxic training improves anaerobic performance in competitive swimmers when implemented into a direct competition mesocycle. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0180380"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1287506","DOI":"10.1155\/2019\/1287506","article-title":"Intermittent hypoxic training at lactate threshold intensity improves aiming performance in well-trained biathletes with little change of cardiovascular variables","volume":"2019","author":"Czuba","year":"2019","journal-title":"Biomed. Res. Int."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1","DOI":"10.2165\/11317920-000000000-00000","article-title":"Combining hypoxic methods for peak performance","volume":"40","author":"Millet","year":"2010","journal-title":"Sports Med."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1089\/ham.2016.0036","article-title":"Cognitive Function and Cerebral Oxygenation during Prolonged Exercise under Hypoxia in Healthy Young Males","volume":"17","author":"Dobashi","year":"2016","journal-title":"High Alt. Med. Biol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/j.physbeh.2012.03.002","article-title":"Training-dependent cognitive advantage is suppressed at high altitude","volume":"106","author":"Li","year":"2012","journal-title":"Physiol. Behav."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.brainres.2012.02.068","article-title":"The effects of acute exercise on cognitive performance: A meta-analysis","volume":"1453","author":"Chang","year":"2012","journal-title":"Brain Res."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1640","DOI":"10.2174\/1871527313666141130203245","article-title":"Effects of Physical Exercise on Depressive Symptoms and Biomarkers in Depression","volume":"13","author":"Archer","year":"2014","journal-title":"CNS Neurol. Disord. Drug Targets"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"638","DOI":"10.2174\/1871527315666161223142918","article-title":"Exercise Induced Neuroplasticity to Enhance Therapeutic Outcomes of Cognitive Remediation in Schizophrenia: Analyzing the Role of Brai Nderived Neurotrophic Factor","volume":"16","author":"Campos","year":"2017","journal-title":"CNS Neurol. Disord. Drug Targets"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.jad.2018.04.106","article-title":"High Altitude With Monotonous Environment Has Significant Impact on Mood and Cognitive Performance of Acclimatized Lowlanders: Possible Role of Altered Serum BDNF and Plasma Homocysteine Level","volume":"237","author":"Das","year":"2018","journal-title":"J. Affect. Disord."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"906","DOI":"10.1016\/S1995-7645(12)60169-2","article-title":"Relationship Between Brain-Derived Neurotrophic Factor and Cognitive Function of Obstructive Sleep Apnea\/Hypopnea Syndrome Patients","volume":"5","author":"Wang","year":"2012","journal-title":"Asian Pac. J. Trop. Med."},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Halievski, K., Nath, S., Katsuno, M., Adachi, H., Sobue, G., Breedlove, S., Lieberman, A., and Jordan, C. (2019). Disease Affects Bdnf Expression in Synaptic and Extrasynaptic Regions of Skeletal Muscle of Three SBMA Mouse Models. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20061314"},{"key":"ref_82","first-page":"449","article-title":"Repetitive Acute Intermittent Hypoxia Increases Growth\/Neurotrophic Factor Expression in Non-Respiratory Motor Neurons","volume":"332","author":"Satriotomo","year":"2016","journal-title":"Neuroscience"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/S0304-3940(02)00529-3","article-title":"Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets","volume":"328","author":"Karege","year":"2002","journal-title":"Neurosci. Lett."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1113\/expphysiol.2009.048512","article-title":"Evidence for a release of brain-derived neurotrophic factor from the brain during exercise","volume":"94","author":"Rasmussen","year":"2009","journal-title":"Exp. Physiol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"3017","DOI":"10.1073\/pnas.1015950108","article-title":"Exercise Training Increases Size of Hippocampus and Improves Memory","volume":"108","author":"Erickson","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1196\/annals.1403.009","article-title":"Neurotrophic factor in neuronal survival and behavior-related plasticity","volume":"1122","author":"Lipski","year":"2007","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1146\/annurev.neuro.24.1.677","article-title":"Neurotrophins: Roles in neuronal development and function","volume":"24","author":"Huang","year":"2009","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1249\/mss.0b013e31802f04c7","article-title":"The Effect of Acute Exercise on Serum Brain-Derived Neurotrophic Factor Levels and Cognitive Function","volume":"39","author":"Ferris","year":"2007","journal-title":"Med. Sci. Sports Exerc."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.psyneuen.2013.12.014","article-title":"Impact of Acute Aerobic Exercise and Cardiorespiratory Fitness on Visuospatial Attention Performance and Serum BDNF Levels","volume":"41","author":"Tsai","year":"2014","journal-title":"Psychoneuroedocrinology"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1016\/j.physbeh.2018.04.018","article-title":"Impact of high intensity exercise on execrative function and brain derived neurotrophic factor in healthy college aged males","volume":"191","author":"Slusher","year":"2018","journal-title":"Phsiol. Behav."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1007\/s00424-017-1964-4","article-title":"Neurobiology of Local and Intercellular BDNF Signaling","volume":"469","author":"Sasi","year":"2017","journal-title":"Plugers Arch. Eur. J. Physiol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1113\/jphysiol.2003.039594","article-title":"Systemic Hypoxia and the Depression of Synaptic Transmission in Rat Hippocampus after Carotid Artery Occlusion","volume":"550","author":"Fowler","year":"2003","journal-title":"J. Physiol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.brainres.2018.09.018","article-title":"Acute Hypoxic Exposure and Prolyl-Hydroxylase Inhibition Improves Synaptic Transmission Recovery Time from a Subsequent Hypoxic Insult in Rat Hippocampus","volume":"1701","author":"Lanigan","year":"2018","journal-title":"Brain Res."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"4663","DOI":"10.1523\/JNEUROSCI.4946-06.2007","article-title":"Adaptive Depression in Synaptic Transmission in the Nucleus of the Solitary Tract after In Vivo Chronic Intermittent Hypoxia: Evidence for Homeostatic Plasticity","volume":"27","author":"Kline","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"4491","DOI":"10.1074\/jbc.M410661200","article-title":"Exposure to Hypoxia Rapidly Induces Mitochondrial Channel Activity within a Living Synapse","volume":"280","author":"Jonas","year":"2005","journal-title":"J. Biol. Chem."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.bbr.2009.03.026","article-title":"Acetylcholinesterase Inhibitors Enhance Cognitive Functions in Rats Following Hypobaric Hypoxia","volume":"203","author":"Muthuraju","year":"2009","journal-title":"Behav. Brain Res."},{"key":"ref_97","first-page":"e1961","article-title":"Circulating Cortisol and Cognitive and Structural Brain Measures: The Framingham Heart Study","volume":"91","author":"Conner","year":"2018","journal-title":"Neurology"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"e16114","DOI":"10.1097\/MD.0000000000016114","article-title":"Effects of Brain Activity, Morning Salivary Cortisol, and Emotion Regulation on Cognitive Impairment in Elderly People","volume":"98","author":"Sroykham","year":"2019","journal-title":"Medicine"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1530\/EJE-16-0352","article-title":"Higher Diurnal Salivary Cortisol Levels Are Related to Smaller Prefrontal Cortex Surface Area in Elderly Men and Women","volume":"175","author":"Stomby","year":"2016","journal-title":"Eur. J. Endocrinol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"100161","DOI":"10.1016\/j.ynstr.2019.100161","article-title":"Sustained Corticosterone Rise in the Prefrontal Cortex Is a Key Factor for Chronic Stress-Induced Working Memory Deficits in Mice","volume":"10","author":"Dominguez","year":"2019","journal-title":"Neurobiol. Stress"},{"key":"ref_101","first-page":"647","article-title":"Leppaluoto. Effect of physical exercise in hypobaric conditions o atrial natriuretic peptide secretion","volume":"263","author":"Vuolteenaho","year":"1992","journal-title":"Am. J. Physiol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1080\/02701367.1991.10607519","article-title":"Effects of a three-year exercise program on motor function and cognitive processing speed I older woe","volume":"62","author":"Rikki","year":"1991","journal-title":"Res. Qart. Exerc. Sport"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1007\/BF02343801","article-title":"Metabolic and endocrine responses to graded exercise under acute hypoxia","volume":"55","author":"Bouissou","year":"1986","journal-title":"Eur. J. Appl. Physiol."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1055\/s-2007-1011814","article-title":"Fluid-electrolyte shift and renin-aldosterone responses to exercise under hypoxia","volume":"19","author":"Bouissou","year":"1987","journal-title":"Horm. Met. Res."},{"key":"ref_105","first-page":"389","article-title":"Catecholamines, hypoxia and high altitude","volume":"11","author":"Rostrup","year":"1988","journal-title":"Acta Phsiol. Scand."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1023\/B:NERV.0000028082.13778.14","article-title":"Clinical Perspectives on Neurobiological Effects of Psychological Trauma","volume":"14","author":"Weber","year":"2004","journal-title":"Neuropsychol. Rev."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1007\/BF01254910","article-title":"Distribution of Catecholamines and Serotonin in the Rat Cerebral Cortex: Absolute Levels and Relative Proportions","volume":"50","author":"Reader","year":"1981","journal-title":"J. Neural Transm."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1016\/j.biopsych.2019.03.983","article-title":"Prefrontal Cortex Dopamine Transporter Gene Network Moderates the Effect of Perinatal Hypoxic-Ischemic Conditions on Cognitive Flexibility and Brain Gray Matter Density in Children","volume":"86","author":"Miguel","year":"2019","journal-title":"Biol. Psychiatry"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"e12163","DOI":"10.14814\/phy2.12163","article-title":"The Effect of Changes in Cerebral Blood Flow on Cognitive Function during Exercise","volume":"2","author":"Ogh","year":"2014","journal-title":"Physiol. Rep."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"1265","DOI":"10.1016\/S0006-291X(05)81332-4","article-title":"Cloning and characterization of cDNA encoding human A-type endothelin receptor","volume":"180","author":"Adachi","year":"1991","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1038\/327524a0","article-title":"Nitric Oxide Release Accounts for the Biological Activity of Endothelium-Derived Relaxing Factor","volume":"327","author":"Palmer","year":"1987","journal-title":"Nature"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1111\/bph.14532","article-title":"Nitric oxide as a multimodal transmitter in the brain: Discovery and current status","volume":"176","author":"Garthwaite","year":"2019","journal-title":"Br. J. Pharmacol."},{"key":"ref_113","first-page":"333","article-title":"Dietary nitrate supplementation improves reaction time in type 2 diabetes: Development and application of a novel nitrate-depleted beetroot juice placebo","volume":"19","author":"Gilchrist","year":"2014","journal-title":"Nitric Oxide"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1139\/apnm-2015-0400","article-title":"Effect of acute nitrate supplementation on neurovascular coupling and cognitive performance in hypoxia","volume":"41","author":"Lefferts","year":"2016","journal-title":"Appl. Physiol. Nutr. Metab."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"401","DOI":"10.3389\/fphys.2017.00401","article-title":"Effects of Dietary Nitrate Supplementation on Physiological Responses, Cognitive Function, and Exercise Performance at Moderate and Very-High Simulated Altitude","volume":"8","author":"Shannon","year":"2017","journal-title":"Front. Physiol."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"127","DOI":"10.3233\/BPL-160040","article-title":"The Effects of Acute Exercise on Mood, Cognition, Neurophysiology, and Neurochemical Pathways: A Review","volume":"2","author":"Basso","year":"2017","journal-title":"Brain Plast."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.mito.2014.05.007","article-title":"Comprehensive review on Lactate Metabolism in Human Health","volume":"17","year":"2014","journal-title":"Mitochondrion"},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1159\/000017324","article-title":"Evidence supporting the existence of an activity-dependent astrocyte neuron lactate shuttle","volume":"20","author":"Pellerin","year":"1998","journal-title":"Dev. Neurosci."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1038\/mp.2016.179","article-title":"Peripheral administration of lactate produces antidepressant-like effects","volume":"23","author":"Carrard","year":"2018","journal-title":"Mol. Psychiatry"},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"2811","DOI":"10.1074\/jbc.M806409200","article-title":"Lactate inhibits lipolysis in fat cells through activation of an orphan G-protein-coupled receptor, GPR81","volume":"284","author":"Liu","year":"2009","journal-title":"J. Biol. Chem."},{"key":"ref_121","unstructured":"Urbaniak, G.C., and Plous, S. (2017, March 25). Research Randomizer (Version 4.0) [Computer Software]. Available online: http:\/\/www.randomizer.org\/."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1055\/s-2008-1025839","article-title":"Variability of aerobic performance in the laboratory and its physiological correlates","volume":"6","author":"Kuipers","year":"1985","journal-title":"Int. J. Sports Med."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/15\/5569\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:54:07Z","timestamp":1760176447000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/15\/5569"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,8,4]]},"references-count":122,"journal-issue":{"issue":"15","published-online":{"date-parts":[[2020,8]]}},"alternative-id":["ijms21155569"],"URL":"https:\/\/doi.org\/10.3390\/ijms21155569","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,8,4]]}}}