DOI QR코드

DOI QR Code

Lactate consumption mediates repeated high-intensity interval exercise-enhanced executive function in adult males

  • Cho, Hae-Sung (Department of Physical Education, Seoul National University) ;
  • Lee, Won Sang (Department of Physical Education, Seoul National University) ;
  • Yoon, Kyeong Jin (Department of Physical Education, Seoul National University) ;
  • Park, Soo Hong (Department of Physical Education, Seoul National University) ;
  • Shin, Hyung Eun (Health and Exercise Science Laboratory, Seoul National University) ;
  • Kim, Yeon-Soo (Department of Physical Education, Seoul National University) ;
  • Chang, Hyukki (Department of Human Movement Science, Seoul Women's University) ;
  • Moon, Hyo Youl (Department of Physical Education, Seoul National University)
  • Received : 2020.09.15
  • Accepted : 2020.12.04
  • Published : 2020.12.31

Abstract

[Purpose] Lactate is a principal energy substrate for the brain during exercise. A single bout of high-intensity interval exercise (HIIE) can increase the blood lactate level, brain lactate uptake, and executive function (EF). However, repeated HIIE can attenuate exercise-induced increases in lactate level and EF. The lactate levels in the brain and blood are reported to be correlated with exercise-enhanced EF. However, research is yet to explain the cause-and-effect relationship between lactate and EF. This study examined whether lactate consumption improves the attenuated exercise-enhanced EF caused by repeated HIIE. [Methods] Eleven healthy men performed two sets of HIIE, and after each set, 30 min were given for rest and examination. In the 2nd set, the subjects consumed experimental beverages containing (n = 6) and not containing (n = 5) lactate. Blood, cardiovascular, and psychological variables were measured, and EF was evaluated by the computerized color-word Stroop test. [Results] The lactate group had a higher EF (P < 0.05) and tended to have a higher blood lactate level (P = 0.082) than the control group in the 2nd set of HIIE. Moreover, blood lactate concentration was correlated with the interference score (i.e., reverse score of EF) (r = -0.394; P < 0.05). [Conclusion] Our results suggest that the attenuated exercise-enhanced EF after repeated HIIE can be improved through lactate consumption. However, the role of lactate needs to be elucidated in future studies, as it can be used for improving athletes' performance and also in cognitive decline-related clinical studies.

Keywords

Acknowledgement

All procedures were approved by the ethics committee of Seoul National University (IRB No. 1909/002-010). The participants provided written informed consent to participate in this study. This research was supported by the National Research Foundation (700-20190019 and NRF-2020R1C1C1006414).

References

  1. Katakam A. Data check: a historical breakdown of when teams score at the Fifa World Cup. 2018 2018.07.05 2019.04.14]; Available from: https://scroll.in/field/884136/data-check-a-historicalbreakdown-of-when-teams-score-at-the-fifa-world-cup.
  2. DE Oliveira MC, Orbetelli R, DE Barros Neto TL. Call accuracy and distance from the play: a study with Brazilian soccer referees. Int J Exerc Sci. 2011;4:30-8.
  3. Bouzat P, Sala N, Suys T, Zerlauth JB, Marques-Vidal P, Feihl F, Bloch J, Messerer M, Levivier M, Meuli R, Magistretti PJ, Oddo M. Cerebral metabolic effects of exogenous lactate supplementation on the injured human brain. Intensive Care Med. 2014;40:412-21. https://doi.org/10.1007/s00134-013-3203-6
  4. Huijgen BC, Leemhuis S, Kok NM, Verburgh L, Oosterlaan J, Elferink-Gemser MT, Visscher C. Cognitive functions in elite and sub-elite youth soccer players aged 13 to 17 years. PLoS One. 2015;10:e0144580. https://doi.org/10.1371/journal.pone.0144580
  5. Sakamoto S, Takeuchi H, Ihara N, Ligao B, Suzukawa K. Possible requirement of executive functions for high performance in soccer. PLoS One. 2018;13:e0201871. https://doi.org/10.1371/journal.pone.0201871
  6. Vestberg T, Gustafson R, Maurex L, Ingvar M, Petrovic P. Executive functions predict the success of top-soccer players. PLoS One. 2012;7:e34731. https://doi.org/10.1371/journal.pone.0034731
  7. Hashimoto T, Tsukamoto H, Takenaka S, Olesen ND, Petersen LG, Sorensen H, Nielsen HB, Secher NH, Ogoh S. Maintained exercise-enhanced brain executive function related to cerebral lactate metabolism in men. FASEB J. 2018;32:1417-27. https://doi.org/10.1096/fj.201700381rr
  8. Scarpina F, Tagini S. The stroop color and word test. Front Psychol. 2017;8:557. https://doi.org/10.3389/fpsyg.2017.00557
  9. Abd-Elfattah HM, Abdelazeim FH, Elshennawy S. Physical and cognitive consequences of fatigue: a review. J Adv Res. 2015;6:351-8. https://doi.org/10.1016/j.jare.2015.01.011
  10. Zajac A, Chalimoniuk M, Maszczyk A, Golas A, Lngfort J. Central and peripheral fatigue during resistance exercise - a critical review. J Hum Kinet. 2015;49:159-69. https://doi.org/10.1515/hukin-2015-0118
  11. Kluger BM, Krupp LB, Enoka RM. Fatigue and fatigability in neurologic illnesses: proposal for a unified taxonomy. Neurology. 2013;80:409-16. https://doi.org/10.1212/WNL.0b013e31827f07be
  12. Pattyn N, Van Cutsem J, Dessy E, Mairesse O. Bridging exercise science, cognitive psychology, and medical practice: is "cognitive fatigue" a remake of "the emperor's new clothes"? Front Psychol. 2018;9:1246. https://doi.org/10.3389/fpsyg.2018.01246
  13. Brooks GA. The science and translation of lactate shuttle theory. Cell Metab. 2018;27:757-85. https://doi.org/10.1016/j.cmet.2018.03.008
  14. Belanger M, Allaman I, Magistretti PJ. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 2011;14:724-38. https://doi.org/10.1016/j.cmet.2011.08.016
  15. Bouzier-Sore AK, Voisin P, Bouchaud V, Bezancon E, Franconi JM, Pellerin L. Competition between glucose and lactate as oxidative energy substrates in both neurons and astrocytes: a comparative NMR study. Eur J Neurosci. 2006;24:1687-94. https://doi.org/10.1111/j.1460-9568.2006.05056.x
  16. van Hall G, Stromstad M, Rasmussen P, Jans O, Zaar M, Gam C, Quistorff B, Secher NH, Nielsen HB. Blood lactate is an important energy source for the human brain. J Cereb Blood Flow Metab. 2009;29:1121-9. https://doi.org/10.1038/jcbfm.2009.35
  17. Smith KJ, Ainslie PN. Regulation of cerebral blood flow and metabolism during exercise. Exp Physiol. 2017;102:1356-71. https://doi.org/10.1113/EP086249
  18. Kemppainen J, Aalto S, Fujimoto T, Kalliokoski KK, Langsjo J, Oikonen V, Rinne J, Nuutila P, Knuuti J. High intensity exercise decreases global brain glucose uptake in humans. J Physiol. 2005;568:323-32. https://doi.org/10.1113/jphysiol.2005.091355
  19. Tsukamoto H, Suga T, Takenaka S, Tanaka D, Takeuchi T, Hamaoka T, Isaka T, Hashimoto T. Greater impact of acute high-intensity interval exercise on post-exercise executive function compared to moderate-intensity continuous exercise. Physiol Behav. 2016;155:224-30. https://doi.org/10.1016/j.physbeh.2015.12.021
  20. Tsukamoto H, Suga T, Takenaka S, Tanaka D, Takeuchi T, Hamaoka T, Isaka T, Ogoh S, Hashimoto T. Repeated high-intensity interval exercise shortens the positive effect on executive function during post-exercise recovery in healthy young males. Physiol Behav. 2016;160:26-34. https://doi.org/10.1016/j.physbeh.2016.03.029
  21. Stolen T, Chamari K, Castagna C, Wisloff U. Wisloff. Physiology of soccer: an update. Sports Med. 2005;35:501-36. https://doi.org/10.2165/00007256-200535060-00004
  22. Russell M, West DJ, Harper LD, Cook CJ, Kilduff LP. Halftime strategies to enhance second-half performance in teamsports players: a review and recommendations. Sports Med. 2015;45:353-64. https://doi.org/10.1007/s40279-014-0297-0
  23. Nybo L, Secher NH. Cerebral perturbations provoked by prolonged exercise. Prog Neurobiol. 2004;72:223-61. https://doi.org/10.1016/j.pneurobio.2004.03.005
  24. McMorris T. Developing the catecholamines hypothesis for the acute exercise-cognition interaction in humans: lessons from animal studies. Physiol Behav. 2016;165:291-9. https://doi.org/10.1016/j.physbeh.2016.08.011
  25. Grego F, Vallier JM, Collardeau M, Bermon S, Ferrari P, Candito M, Bayer P, Magnie MN, Brisswalter J. Effects of long duration exercise on cognitive function, blood glucose, and counterregulatory hormones in male cyclists. Neurosci Lett. 2004;364:76-80. https://doi.org/10.1016/j.neulet.2004.03.085
  26. Shields GS, Bonner JC, Moons WG. Does cortisol influence core executive functions? A meta-analysis of acute cortisol administration effects on working memory, inhibition, and set-shifting. Psychoneuroendocrinology. 2015;58:91-103. https://doi.org/10.1016/j.psyneuen.2015.04.017
  27. Byun K, Hyodo K, Suwabe K, Ochi G, Sakairi Y, Kato M, Dan I, Soya H. Positive effect of acute mild exercise on executive function via arousal-related prefrontal activations: an fNIRS study. NeuroImage. 2014;98:336-45. https://doi.org/10.1016/j.neuroimage.2014.04.067
  28. Holloway R, Zhou Z, Harvey HB, Levasseur JE, Rice AC, Sun D, Hamm RJ, Bullock MR. Effect of lactate therapy upon cognitive deficits after traumatic brain injury in the rat. Acta Neurochir (Wien). 2007;149:919-27. https://doi.org/10.1007/s00701-007-1241-y
  29. Warburton DE, Jamnik V, Bredin SS, Shephard RJ, Gledhill N. The 2019 physical activity readiness questionnaire for everyone (PAR-Q+) and electronic physical activity readiness medical examination (ePARmed-X+). The Health & Fitness Journal of Canada. 2018;11:80-3.
  30. Bisri T, Utomo BA, Fuadi I. Exogenous lactate infusion improved neurocognitive function of patients with mild traumatic brain injury. Asian J Neurosurg. 2016;11:151-9. https://doi.org/10.4103/1793-5482.145375
  31. Matsui T, Omuro H, Liu YF, Soya M, Shima T, McEwen BS, Soya H. Astrocytic glycogen-derived lactate fuels the brain during exhaustive exercise to maintain endurance capacity. Proc Natl Acad Sci U S A. 2017;114:6358-63. https://doi.org/10.1073/pnas.1702739114
  32. Rasmussen P, Wyss MT, Lundby C. Cerebral glucose and lactate consumption during cerebral activation by physical activity in humans. FASEB J. 2011;25:2865-73. https://doi.org/10.1096/fj.11-183822
  33. Barros, LF. Metabolic signaling by lactate in the brain. Trends Neurosci. 2013;36:396-404. https://doi.org/10.1016/j.tins.2013.04.002
  34. Smith D, Pernet A, Hallett WA, Bingham E, Marsden PK, Amiel SA. Lactate: a preferred fuel for human brain metabolism in vivo. J Cereb Blood Flow Metab. 2003;23:658-64. https://doi.org/10.1097/01.WCB.0000063991.19746.11
  35. Hu Y, Wilson GS. A temporary local energy pool coupled to neuronal activity: fluctuations of extracellular lactate levels in rat brain monitored with rapid-response enzyme-based sensor. J Neurochem. 1997;69:1484-90. https://doi.org/10.1046/j.1471-4159.1997.69041484.x
  36. Levy MJF, Boulle F, Steinbusch HW, van den Hove DLA, Kenis G, Lanfumey L. Neurotrophic factors and neuroplasticity pathways in the pathophysiology and treatment of depression. Psychopharmacology (Berl). 2018;235:2195-220. https://doi.org/10.1007/s00213-018-4950-4
  37. Bathina S, Das UN. Brain-derived neurotrophic factor and its clinical implications. Arch Med Sci. 2015;11:1164-78. https://doi.org/10.5114/aoms.2015.56342
  38. 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. 2007;39:728-34. https://doi.org/10.1249/mss.0b013e31802f04c7
  39. Schiffer T, Schulte S, Sperlich B, Achtzehn S, Fricke H, Struder HK. Lactate infusion at rest increases BDNF blood concentration in humans. Neurosci Lett. 2011;488:234-7. https://doi.org/10.1016/j.neulet.2010.11.035
  40. Maderova D, Krumpolec P, Slobodova L, Schon M, Tirpakova V, Kovanicova Z, Klepochova R, Vajda M, Sutovsky S, Cvecka J, Valkovic L, Turcani P, Krssak M, Sedliak M, Tsai CL, Ukropcova B, Ukropec J. Acute and regular exercise distinctly modulate serum, plasma and skeletal muscle BDNF in the elderly. Neuropeptides. 2019;78:101961. https://doi.org/10.1016/j.npep.2019.101961
  41. Pageaux B, Marcora SM, Rozand V, Lepers R. Mental fatigue induced by prolonged self-regulation does not exacerbate central fatigue during subsequent whole-body endurance exercise. Front Hum Neurosci. 2015;9:67. https://doi.org/10.3389/fnhum.2015.00067
  42. Shuai L, Daley D, Wang YF, Zhang JS, Kong YT, Tan X, Ji N. Ji. Executive function training for children with attention deficit hyperactivity disorder. Chin Med J. (Engl). 2017;130:549-58. https://doi.org/10.4103/0366-6999.200541