Physikalische Medizin, Rehabilitationsmedizin, Kurortmedizin 2021; 31(06): 377-385
DOI: 10.1055/a-1493-4911
Original Article

Positive Effects of Probiotics on Motor Coordination and Brain during Moderate and High-Intensity Exercise in Adolescent Female Mice

Positive Effekte von Probiotika auf die motorische Fähigkeit und das Gehirn während moderatem und hochintensivem Training bei heranwachsenden weiblichen Mäusen
1   Department of Physical Therapy, Sang Ji University, Wonju, Korea (the Republic of)
,
Junechul Kim
2   Department of Counseling, Health and Kinesiology, Texas A&M University - San Antonio, San Antonio, United States
› Author Affiliations

Abstract

Objectives This study aimed to investigate the effects of probiotics on inflammatory cytokines, neurotransmitters, and motor functions during different levels of exercise.

Methods Female adolescent mice (n=140) were divided into two groups, of which one group was fed probiotics and the other group was not. For both groups, three levels of exercise were conducted: non-exercise, moderate-intensity exercise, and high-intensity exercise. Probiotics acquisition and aerobic treadmill exercise were the main variables during the growth period. We evaluated motor function with a rotarod test and analyzed cytokines and neurotransmitters in the cerebellum.

Results In acceleration mode, the moderate and high-intensity exercise groups showed longer running times than the non-exercise groups (P<0.001). Also, the probiotic-ingestion group had longer latency before falling than those who did not take probiotics in both the high-intensity and the non-exercise groups (P=0.002, P=0.002, respectively). In steady-state mode, the non-exercise group showed lower records compared with the moderate and high-intensity exercise groups (P=0.017, P=0.004, respectively). The inflammatory cytokine levels were high in the groups that performed moderate and high-intensity exercises, but the high levels were relieved in those taking probiotics. The GABA concentration was high for the exercise group and the probiotic-ingestion group.

Conclusion Taken together, probiotics help improve motor skills during moderate and high-intensity exercise and help relieve inflammatory responses in the brain. Thus, we suggest that probiotics can be a useful supplement for brain and body development during exercise in adolescence.

Zusammenfassung

Ziele Ziel dieser Studie war es, die Wirkung von Probiotika auf die Konzentration inflammatorischer Zytokine und Neurotransmitter sowie auf die motorische Fähigkeit während verschiedener Belastungsstufen zu untersuchen.

Methoden Weibliche adoleszente Mäuse (n=140) wurden in 2 Gruppen aufgeteilt: eine Gruppe wurde mit Probiotika gefüttert, die andere Gruppe nicht. Mit beiden Gruppen wurden Trainings in 3 Stufen durchgeführt: kein Training (Nicht-Trainingsgruppe), mäßig intensive Belastung und hohe Belastung. Die Gabe von Probiotika und aerobes Laufbandtraining waren die Hauptvariablen in der Wachstumsperiode. Die motorische Fähigkeit wurde mit einem Rotarod-Test bestimmt. Außerdem wurde die Konzentration von Zytokinen und Neurotransmittern im Kleinhirn gemessen.

Ergebnisse Im Beschleunigungsmodus zeigten die moderaten und hochintensiven Trainingsgruppen längere Laufzeiten als die Nicht-Trainingsgruppen (P<0,001). Außerdem zeigte die Probiotika-Gruppe eine längere Dauer bis zum Herabfallen als die Gruppe ohne Probiotika, und zwar sowohl in der hochintensiven als auch in der Nicht-Trainingsgruppe (jeweils P=0,002, P=0,002). Im Steady-State-Modus zeigte die Nicht-Trainingsgruppe niedrigere Werte im Vergleich zu den Gruppen mit mäßiger und hoher Belastung (P=0,017 bzw. P=0,004). Die Werte der inflammatorischen Zytokine waren in den Gruppen mit mäßiger und hoher Belastung erhöht, in den Probiotika-Gruppen wurden jedoch die hohen Werte gemildert. Die GABA-Konzentration war in der Trainingsgruppe und in der Probiotika-Gruppe hoch.

Schlussfolgerung Insgesamt tragen Probiotika dazu bei, die motorischen Fähigkeiten während moderatem und hochintensivem Training zu verbessern und können dazu beitragen, Entzündungsreaktionen im Gehirn zu mildern. Probiotika könnten daher beim Training von Jugendlichen ein nützliches Ergänzungsmittel sein, das die Entwicklung von Gehirn und Körper positiv beeinflusst.



Publication History

Received: 30 January 2021

Accepted after revision: 27 April 2021

Article published online:
22 June 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Lawrence SN. Adolescent Health Care 2nd edition. Baltimore: Williams & Wilkins publishers; 1991: 3-36
  • 2 Herting MM, Chu X. Exercise, cognition, and the adolescent brain. Birth Defects Res 2017; 109: 1672-1679
  • 3 Ardoy DN, Fernández-Rodríguez JM, Jiménez-Pavón D. et al. A physical education trial improves adolescents’ cognitive performance and academic achievement: the EDUFIT study. Scand J Med Sci Sports 2014; 24: e52-e61
  • 4 Bounous G, Molson JH. The antioxidant system. Anticancer Research 2003; 23: 1411-1415
  • 5 Li CY, Hsu GS, Suzuki K. et al. Salivary immuno factors, cortisol and testosterone responses in athletes of a competitive 5,000 m race. Chin J Physiol 2015; 58: 263-269
  • 6 Gremion G, Kuntzer T. Fatigue and reduction in motor performance in sports people or overtraining syndrome. Revue Medicale Suisse 2014; 10: 964-965
  • 7 Jin CH, Paik IY, Kwak YS. et al. Exhaustive submaximal endurance and resistance exercises induce temporary immunosuppression via physical and oxidative stress. J Exerc Rehabil 2015; 11: 198-203
  • 8 Luke A, Lazaro RM, Bergeron MF. et al. Sports-related injuries in youth athletes: is overscheduling a risk factor?. Clin J Sport Med 2011; 21: 307-314
  • 9 Bruunsgaard H, Galbo H, Halkjaer-Kristensen J. et al. Exercise-induced increase in serum interleukin-6 in humans is related to muscle damage. J Physiol 1997; 499: 833-841
  • 10 Campbell JP, Turner JE. Debunking the myth of exercise-induced immune suppression: redefining the impact of exercise on immunological health across the lifespan. Front Immunol 2018; 9: 648
  • 11 Naughton G, Farpour-Lambert NJ, Carlson J. et al. Physiological issues surrounding the performance of adolescent athletes. Sports Med 2000; 30: 309-325
  • 12 Yizhar O, Fenno LE, Prigge M. et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 2011; 477: 171-178
  • 13 Woo J, Min JO, Kang DS. et al. Control of motor coordination by astrocytic tonic GABA release through modulation of excitation/inhibition balance in cerebellum. Proc Natl Acad Sci U S A 2018; 115: 5004-5009
  • 14 Maddock RJ, Casazza GA, Fernandez DH. et al. Acute modulation of cortical glutamate and GABA content by physical activity. J Neurosci 2016; 36: 2449-2457
  • 15 Coxon JP, Cash RFH, Hendrikse JJ. et al. GABA concentration in sensorimotor cortex following high-intensity exercise and relationship to lactate levels. J Physiol 2018; 596: 691-702 DOI: 10.1113/JP274660.
  • 16 Silveri MM, Sneider JT, Crowley DJ. et al. Frontal lobe γ-aminobutyric acid levels during adolescence: associations with impulsivity and response inhibition. Biol Psychiatry 2013; 74: 296-304
  • 17 Bravo JA, Forsythe P, Chew MV. et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A 2011; 108: 16050-16055
  • 18 Michalickova DM, Kostic-Vucicevic MM, Vukasinovic-Vesic MD. et al. Lactobacillus helveticus Lafti L10 supplementation modulates mucosal and humoral immunity in elite athletes: a randomized, double-blind, placebo-controlled trial. J Strength Cond Res 2017; 31: 62-70
  • 19 Rather IA, Bajpai VK, Kumar S. et al. Probiotics and atopic dermatitis: an overview. Front Microbiol 2016; 7: 507
  • 20 Komano Y, Shimada K, Naito H. et al. Efficacy of heat-killed Lactococcus lactis JCM 5805 on immunity and fatigue during consecutive high intensity exercise in male athletes: a randomized, placebo-controlled, double-blinded trial. J Int Soc Sports Nutr 2018; 15: 39
  • 21 Huang WC, Wei CC, Huang CC. et al. The beneficial effects of Lactobacillus plantarum PS128 on high-intensity, exercise-induced oxidative stress, inflammation, and performance in triathletes. Nutrients 2019; 11: 353
  • 22 Scheiman J, Luber JM, Chavkin TA. et al. Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism. Nat Med 2019; 25: 1104-1109
  • 23 McCabe LR, Irwin R, Schaefer L. et al. Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J Cell Physiol 2013; 228: 1793-1798
  • 24 Chen YM, Wei L, Chiu YS. et al. Lactobacillus plantarum TWK10 supplementation improves exercise performance and increases muscle mass in mice. Nutrients 2016; 8: 205
  • 25 Huang WC, Hsu YJ, Li H. et al. Effect of lactobacillus plantarum TWK10 on improving endurance performance in humans. Chin J Physiol 2018; 61: 163-170
  • 26 Verkhratsky A, Butt AM. “Numbers: how many glial cells are in the brain?”. Glial Physiology and Pathophysiology. John Wiley and Sons publishers; 2013: 93-96
  • 27 Filiano AJ, Gadani SP, Kipnis J. Interactions of innate and adaptive immunity in brain development and function. Brain Res 2015; 1617: 18-27
  • 28 Roshchina VV. Evolutionary considerations of neurotransmitters in microbial, plant and animal cells. Microbial Endocrinology: Interkingdom signaling in infectious disease and health. Springer; 2010: 17-52
  • 29 Hoydal MA, Wisloff U, Kemi OJ. et al. Running speed and maximal oxygen uptake in rats and mice: practical implications for exercise training. Eur J Cardiovasc Prev Rehabil 2007; 14: 753-760
  • 30 Arida RM, Scorza FA, Gomes da SS. et al. Exercise Paradigms to Study Brain Injury Recovery in Rodents. Am J Phys Med Rehabil 2011; 90: 452-465
  • 31 Brooks SP, Dunnett SB. Tests to assess motor phenotype in mice: a user’s guide. Nat Rev Neurosci 2009; 10: 519-529
  • 32 Behringer M, Vom Heede A, Matthews M. et al. Effects of strength training on motor performance skills in children and adolescents: a meta-analysis. Pediatr Exerc Sci 2011; 23: 186-206
  • 33 McMorris T, Sproule J, Turner A. et al. Acute, intermediate intensity exercise, and speed and accuracy in working memory tasks: a meta-analytical comparison of effects. Physiol Behav 2011; 102: 421-428
  • 34 Hyer MM, Phillips LL, Neigh GN. Sex differences in synaptic plasticity: hormones and beyond. Front Mol Neurosci 2018; 11: 266
  • 35 Statton MA, Encarnacion M, Celnik P. et al. A single bout of moderate aerobic exercise improves motor skill acquisition. PLoS One 2015; 10: e0141393
  • 36 Hadiono BM, Wara K. High Intensity Interval Training (HIIT) and Moderate Intensity Training (MIT) Against TNF-α and IL-6 levels In Rats. AHSR 2018; 7: 87-90
  • 37 Imai T, Seki S, Dobashi H. et al. Effect of weight loss on T-cell receptor-mediated T-cell function in elite athletes. Med Sci Sports Exerc 2002; 34: 245-250
  • 38 Richter-Levin G, Canevari L, Bliss TV. Long-term potentiation and glutamate release in the dentate gyrus: links to spatial learning. Behav Brain Res 1995; 66: 37-40
  • 39 Fan LW, Pang Y. Dysregulation of neurogenesis by neuroinflammation: key differences in neurodevelopmental and neurological disorders. Neural Regen Res 2017; 12: 366-371
  • 40 Desbonnet L, Garrett L, Clarke G. et al. The probiotic Bifidobacteria infantis: An assessment of potential antidepressant properties in the rat. J Psychiatr Res 2008; 43: 164-174
  • 41 D’Mello C, Ronaghan N, Zaheer R. et al. Probiotics improve inflammation-associated sickness behavior by altering communication between the peripheral immune system and the brain. J Neurosci 2015; 35: 10821-10830
  • 42 Madden JA, Plummer SF, Tang J. et al. Effect of probiotics on preventing disruption of the intestinal microflora following antibiotic therapy: a double-blind, placebo-controlled pilot study. Int Immunopharmacol 2005; 5: 1091-1097
  • 43 McEntee WJ, Crook TH. Glutamate: its role in learning, memory, and the aging brain. Psychopharmacology (Berl) 1996; 111: 391-401