The Role of Brain-Derived Neurotrophic Factor (BDNF) in the Relation between Physical Activity and Executive Functioning in Children

Julie Latomme, Patrick Calders, Hilde Van Waelvelde, Tineke Mariën, Marieke De Craemer, Julie Latomme, Patrick Calders, Hilde Van Waelvelde, Tineke Mariën, Marieke De Craemer

Abstract

Physical activity (PA) can improve children's executive functioning (EF), which might be caused by increased levels of brain-derived neurotrophic factor (BDNF). This study investigated whether acute and/or chronic PA leads to increased BDNF levels and enhanced EF in children. Methods: In total, 47 children (mean age 9.69 ± 0.60; 46.8% boys) participated. Children performed a maximal exercise test to measure acute PA. Before and after, BDNF was collected and EF was measured. Chronic PA was proxy-reported. Repeated Measures ANOVAs were performed to study the effect of acute PA on BDNF and EF. Mediation analyses were performed to investigate the mediation effect of BDNF on the association between chronic PA and BDNF. Results: A borderline significant effect of acute PA on BDNF was found (F = 3.32, p = 0.075) with an increase in BDNF (+29.58 pg/mL) after acute PA. A significant effect was found for performance on inhibition tasks (Flanker (accuracy +5.67%, p = 0.034) and Go/No-Go (+0.15%, p = 0.022)). No effect of acute PA was found on the EF outcomes. No significant correlation between chronic PA and EFs nor BDNF was found. Conclusions: Acute PA might increase BDNF and improve some EFs (i.e., inhibition) in children. Chronic PA was not associated with EF nor BDNF. Trial Registration Number: NCT02503579.

Keywords: brain-derived neurotrophic factor; children; executive functioning; exercise; physical activity.

Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, nor in the decision to publish the results.

Figures

Figure 1
Figure 1
Overview of the different measurements that were conducted (FPAQ = Flemish Physical Activity Questionnaire; BDNF = Brain-Derived Neurotrophic Factor; PEBL = the Psychology Experiment Building Language test battery; D-KEFS = Delis-Kaplan Executive Function System test battery; ELISA = Enzyme-Linked Immunosorbent Assay).
Figure 2
Figure 2
The effect of acute PA on (1) BDNF levels and (2) executive functions.
Figure 3
Figure 3
The mediation effect of chronic PA on EFs through BDNF levels.

References

    1. Tomporowski P.D., McCullick B., Pendleton D.M., Pesce C. Exercise and children’s cognition: The role of exercise characteristics and a place for metacognition. J. Sport Health Sci. 2015;4:47–55. doi: 10.1016/j.jshs.2014.09.003.
    1. Donnelly J.E., Hillman C.H., Castelli D., Etnier J.L., Lee S., Tomporowski P., Lambourne K., Szabo-Reed A.N. Physical activity, fitness, cognitive function, and academic achievement in children: A systematic review. Med. Sci. Sports Exerc. 2016;48:1197. doi: 10.1249/MSS.0000000000000901.
    1. Berkey C.S., Rockett H.R., Gillman M.W., Colditz G.A. One-year changes in activity and in inactivity among 10-to 15-year-old boys and girls: Relationship to change in body mass index. Pediatrics. 2003;111:836–843. doi: 10.1542/peds.111.4.836.
    1. Hamer M., Stamatakis E., Mishra G. Psychological distress, television viewing, and physical activity in children aged 4 to 12 years. Pediatrics. 2009;123:1263–1268. doi: 10.1542/peds.2008-1523.
    1. Sibley B.A., Etnier J.L. The relationship between physical activity and cognition in children: A meta-analysis. Pediatric. Exerc. Sci. 2003;15:243–256. doi: 10.1123/pes.15.3.243.
    1. Burton L.J., VanHeest J.L. The importance of physical activity in closing the achievement gap. Quest. 2007;59:212–218. doi: 10.1080/00336297.2007.10483549.
    1. Alvarez-Bueno C., Pesce C., Cavero-Redondo I., Sanchez-Lopez M., Martínez-Hortelano J.A., Martinez-Vizcaino V. The effect of physical activity interventions on children’s cognition and metacognition: A systematic review and meta-analysis. J. Am. Acad. Child Adolesc. Psychiatry. 2017;56:729–738. doi: 10.1016/j.jaac.2017.06.012.
    1. De Greeff J.W., Bosker R.J., Oosterlaan J., Visscher C., Hartman E. Effects of physical activity on executive functions, attention and academic performance in preadolescent children: A meta-analysis. J. Sci. Med. Sport. 2018;21:501–507. doi: 10.1016/j.jsams.2017.09.595.
    1. Hillman C.H., Biggan J.R. A review of childhood physical activity, brain, and cognition: Perspectives on the future. Pediatric. Exerc. Sci. 2017;29:170–176. doi: 10.1123/pes.2016-0125.
    1. Miyake A., Friedman N.P., Emerson M.J., Witzki A.H., Howerter A., Wager T.D. The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: A latent variable analysis. Cogn. Psychol. 2000;41:49–100. doi: 10.1006/cogp.1999.0734.
    1. Diamond A. Executive functions: Insights into ways to help more children thrive. Zero Three. 2014;35:9–17.
    1. Van Waelvelde H., Vanden Wyngaert K., Mariën T., Baeyens D., Calders P. The relation between children’s aerobic fitness and executive functions: A systematic review. Infant Child Dev. 2020;29:e2163. doi: 10.1002/icd.2163.
    1. Diamond A., Lee K. Interventions shown to aid executive function development in children 4 to 12 years old. Science. 2011;333:959–964. doi: 10.1126/science.1204529.
    1. Bailey R. Physical education and sport in schools: A review of benefits and outcomes. J. Sch. Health. 2006;76:397–401. doi: 10.1111/j.1746-1561.2006.00132.x.
    1. Etnier J.L., Salazar W., Landers D.M., Petruzzello S.J., Han M., Nowell P. The influence of physical fitness and exercise upon cognitive functioning: A meta-analysis. J. Sport Exerc. Psychol. 1997;19:249–277. doi: 10.1123/jsep.19.3.249.
    1. Best J.R. Effects of physical activity on children’s executive function: Contributions of experimental research on aerobic exercise. Dev. Rev. 2010;30:331–351. doi: 10.1016/j.dr.2010.08.001.
    1. Kashihara K., Maruyama T., Murota M., Nakahara Y. Positive effects of acute and moderate physical exercise on cognitive function. J. Physiol. Anthropol. 2009;28:155–164. doi: 10.2114/jpa2.28.155.
    1. Tomporowski P.D. Effects of acute bouts of exercise on cognition. Acta Psychol. 2003;112:297–324. doi: 10.1016/S0001-6918(02)00134-8.
    1. Pesce C. Shifting the focus from quantitative to qualitative exercise characteristics in exercise and cognition research. J. Sport Exerc. Psychol. 2012;34:766–786. doi: 10.1123/jsep.34.6.766.
    1. Gray C., Gibbons R., Larouche R., Sandseter E.B.H., Bienenstock A., Brussoni M., Chabot G., Herrington S., Janssen I., Pickett W. What is the relationship between outdoor time and physical activity, sedentary behaviour, and physical fitness in children? A systematic review. Int. J. Environ. Res. Public Health. 2015;12:6455–6474. doi: 10.3390/ijerph120606455.
    1. Rowland T.W. Developmental Exercise Physiology. Human Kinetics Publishers; Champaign, IL, USA: 1996.
    1. Fedewa A.L., Ahn S. The effects of physical activity and physical fitness on children’s achievement and cognitive outcomes: A meta-analysis. Res. Q. Exerc. Sport. 2011;82:521–535. doi: 10.1080/02701367.2011.10599785.
    1. Hillman C.H., Buck S.M., Themanson J.R., Pontifex M.B., Castelli D.M. Aerobic fitness and cognitive development: Event-related brain potential and task performance indices of executive control in preadolescent children. Dev. Psychol. 2009;45:114. doi: 10.1037/a0014437.
    1. Vaynman S., Gomez-Pinilla F. License to run: Exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabilit. Neural Repair. 2005;19:283–295. doi: 10.1177/1545968305280753.
    1. Colcombe S.J., Erickson K.I., Scalf P.E., Kim J.S., Prakash R., McAuley E., Elavsky S., Marquez D.X., Hu L., Kramer A.F. Aerobic exercise training increases brain volume in aging humans. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2006;61:1166–1170. doi: 10.1093/gerona/61.11.1166.
    1. Colcombe S.J., Kramer A.F., Erickson K.I., Scalf P., McAuley E., Cohen N.J., Webb A., Jerome G.J., Marquez D.X., Elavsky S. Cardiovascular fitness, cortical plasticity, and aging. Proc. Natl. Acad. Sci. USA. 2004;101:3316–3321. doi: 10.1073/pnas.0400266101.
    1. Kramer A.F., Hahn S., Cohen N.J., Banich M.T., McAuley E., Harrison C.R., Chason J., Vakil E., Bardell L., Boileau R.A. Ageing, fitness and neurocognitive function. Nature. 1999;400:418–419. doi: 10.1038/22682.
    1. Philippaerts R., Matton L., Wijndaele K., Balduck A.-L., De Bourdeaudhuij I., Lefevre J. Validity of a physical activity computer questionnaire in 12-to 18-year-old boys and girls. Int. J. Sports Med. 2006;27:131–136. doi: 10.1055/s-2005-837619.
    1. Delis D.C., Kramer J.H., Kaplan E., Holdnack J. Reliability and validity of the Delis-Kaplan executive function system: An update. J Int Neuropsych Soc. 2004;10:301–303. doi: 10.1017/S1355617704102191.
    1. IBM Corp . IBM SPSS Statistics for Windows, Version 26.0. IBM Corp; Armonk, NY, USA: 2020. Released 2013.
    1. Erickson K.I., Voss M.W., Prakash R.S., Basak C., Szabo A., Chaddock L., Kim J.S., Heo S., Alves H., White S.M. Exercise training increases size of hippocampus and improves memory. Proc. Natl. Acad. Sci. USA. 2011;108:3017–3022. doi: 10.1073/pnas.1015950108.
    1. Mandelman S.D., Grigorenko E.L. BDNF Val66Met and cognition: All, none, or some? A meta-analysis of the genetic association. Genes Brain Behav. 2012;11:127–136. doi: 10.1111/j.1601-183X.2011.00738.x.
    1. Egan M.F., Kojima M., Callicott J.H., Goldberg T.E., Kolachana B.S., Bertolino A., Zaitsev E., Gold B., Goldman D., Dean M. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell. 2003;112:257–269. doi: 10.1016/S0092-8674(03)00035-7.
    1. Warnault V., Darcq E., Morisot N., Phamluong K., Wilbrecht L., Massa S.M., Longo F.M., Ron D. The BDNF valine 68 to methionine polymorphism increases compulsive alcohol drinking in mice that is reversed by tropomyosin receptor kinase B activation. Biol. Psychiatry. 2016;79:463–473. doi: 10.1016/j.biopsych.2015.06.007.
    1. St Clair-Thompson H.L., Gathercole S.E. Executive functions and achievements in school: Shifting, updating, inhibition, and working memory. Q. J. Exp. Psychol. 2006;59:745–759. doi: 10.1080/17470210500162854.
    1. Toplak M.E., West R.F., Stanovich K.E. Practitioner review: Do performance-based measures and ratings of executive function assess the same construct? J. Child Psychol. Psychiatry. 2013;54:131–143. doi: 10.1111/jcpp.12001.
    1. Barkley R.A. Response inhibition in attention-deficit hyperactivity disorder. Ment. Retard. Dev. Disabil. Res. Rev. 1999;5:177–184. doi: 10.1002/(SICI)1098-2779(1999)5:3<177::AID-MRDD3>;2-G.
    1. Bexkens A., van den Wildenberg W.P., Tijms J. Rapid automatized naming in children with dyslexia: Is inhibitory control involved? Dyslexia. 2015;21:212–234. doi: 10.1002/dys.1487.
    1. Hogervorst E., Riedel W., Jeukendrup A., Jolles J. Cognitive performance after strenuous physical exercise. Percept. Mot. Ski. 1996;83:479–488. doi: 10.2466/pms.1996.83.2.479.
    1. Lichtman S., Poser E.G. The effects of exercise on mood and cognitive functioning. J. Psychosom. Res. 1983;27:43–52. doi: 10.1016/0022-3999(83)90108-3.
    1. Diamond A., Barnett W.S., Thomas J., Munro S. Preschool program improves cognitive control. Science. 2007;318:1387. doi: 10.1126/science.1151148.
    1. Merkt J., Gawrilow C. Measures of Inhibition Support the Prediction of Early Academic Skills; Proceedings of the 3rd International Congress on ADHD; Berlin, Germany. 26–29 May 2011.
    1. Bledsoe J.C., Semrud-Clikeman M., Pliszka S.R. Response inhibition and academic abilities in typically developing children with attention-deficit-hyperactivity disorder-combined subtype. Arch. Clin. Neuropsychol. 2010;25:671–679. doi: 10.1093/arclin/acq048.
    1. Schmidt M., Mavilidi M.F., Singh A., Englert C. Combining physical and cognitive training to improve kindergarten children’s executive functions: A cluster randomized controlled trial. Contemp. Educ. Psychol. 2020;63:101908. doi: 10.1016/j.cedpsych.2020.101908.
    1. Van der Niet A.G., Smith J., Scherder E.J., Oosterlaan J., Hartman E., Visscher C. Associations between daily physical activity and executive functioning in primary school-aged children. J. Sci. Med. Sport. 2015;18:673–677. doi: 10.1016/j.jsams.2014.09.006.

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