Journal of Exercise Physiologyonline

April 2017Volume 20 Number 2

Editor-in-ChiefTommy Boone, PhD, MBAReview BoardTodd Astorino, PhDJulien Baker, PhDSteve Brock, PhDLance Dalleck, PhDEric Goulet, PhDRobert Gotshall, PhDAlexander Hutchison, PhDM. Knight-Maloney, PhDLen Kravitz, PhDJames Laskin, PhDYit Aun Lim, PhDLonnie Lowery, PhDDerek Marks, PhDCristine Mermier, PhDRobert Robergs, PhDChantal Vella, PhDDale Wagner, PhDFrank Wyatt, PhDBen Zhou, PhD

Official Research Journal of the American Society of

Exercise Physiologists

ISSN 1097-9751

Official Research Journal of the American Society of

Exercise Physiologists

ISSN 1097-9751

JEPonline

Ten Minutes of Exercise Performed Above Lactate Threshold Improves Executive Control in Children

Isabela Almeida Ramos1, Rodrigo Alberto Vieira Browne2, Daniel Gomes da Silva Machado2,3, Marcelo Magalhães Sales4, Raiane Maiara dos Santos Pereira1, Carmen Silvia Grubert Campbell1

1Graduate Program in Physical Education, Catholic University of Brasília, Brasília, Brazil, 2Department of Physical Education, Federal University of Rio Grande do Norte, Natal, Brazil, 3Graduate Program in Physical Education, State University of Londrina, Londrina, Brazil, 4Department of Physical Education, State University of Goiás, Quirinópolis, Brazil

ABSTRACT

Ramos IA, Browne RAV, Machado DGS, Sales MM, Pereira RMS, Campbell CSG. Ten Minutes of Exercise Performed Above Lactate Threshold Improves Executive Control in Children. JEPonline 2017;20(2):73-83. The purpose of this study was to verify and compare the effect of 10 min of aerobic exercise performed above and below lactate threshold (LT) on executive control in children. Nine children (10.3 ± 0.5 yrs) underwent three sessions in randomized order: (a) 110%LT: 10 min of aerobic exercise at 110%LT; (b) 90%LT:10 min of aerobic exercise at 90%LT; and (c) control (CON): seated resting. The inhibitory control, declarative memory, cognitive flexibility, and logical reasoning were accessed over the post- session recovery by the Flanker task, free recall memory, trail making test, and tangram puzzle, respectively. Flanker task performance [performance = reaction time (ms) / correct responses (%)] was significantly better after 110%LT when compared with CON (1950.6 ± 1099.6 vs. 2827.4 ± 1385.1 ms; P=0.028). There was no significant difference among conditions in free recall memory, trail making test, and tangram puzzle (P>0.05). The findings indicate that 10 min of aerobic exercise above LT can acutely improve the inhibitory control in children.

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Key Words: Aerobic Exercise, Children, Cognition, Executive Function

INTRODUCTION

In recent years, children have become increasingly sedentary, which contributes to increase the prevalence of overweight and low physical fitness (20). Such inactivity detrimentally affects brain health and some aspects of cognition, especially the executive control (15). This is concerning because during childhood there are extensive changes in the brain structure, function, and connectivity. Thus, an active lifestyle during childhood may have protective effects on brain health across the lifespan (14).

Notwithstanding, the cognitive performance is vital to success in school, vocation, and life (9,11), can also be improved by exercise, especially the executive control (10), which consists of inhibition (resisting distractions or habits to maintain focus), working memory (mentally holding and manipulating information), and cognitive flexibility (multitasking). In particular, recent reviews (9,11) suggest a positive association between physical activity and executive control with respect to academics, but more experimental trials are necessary.

Cognitive improvements after a single session of aerobic exercise seem to be dependent on the level of physical fitness of participants, the nature of the cognitive task and timing of administration, exercise duration, and intensity (7). In the meta-analysis by Chang et al. (7), higher exercise intensities showed better results on cognitive function in many populations investigated. In fact, Hotting et al. (16) compared the effects of both low (<57% maximum heart rate; HR max) and high intensity (~80% HR max) exercise on memory consolidation of words in young adults, which were assessed 20 min and 24 hrs after exercise. Although the number of reminded words was not increased, the subjects in the high-intensity group forgot fewer words 24 hrs after exercise. Using a sample of children/adolescents (10 to 16 yrs of age), Browne et al. (5) showed that 20 min of moderate aerobic exercise (65 to 75% of HR reserve) improved inhibitory control in the Stroop color interference test.

A physiological hypothesis that may explain the acute effect of exercise intensity on the cognitive response is the increased cerebral blood flow, nutrient availability, and/or the increased neurotransmitter activity (21). Peripheral biomarkers are one strategy to further explore the associations between exercise and cognitive performance. In fact, one of the most rigorously investigated molecular mediators is the brain-derived neurotrophic factor (BDNF) (26). Animal studies have consistently shown that this neurotrophin and its receptor, tyrosine kinase (TrkB), play an important role in many functional and structural processes of neuroplasticity that support the long-term memory process (1). Moreover, Hötting et al. (16) and Knaepen et al. (19) have confirmed that circulating levels of BDNF are transiently increased with intense exercise.

Interestingly, Wyss et al. (32) recently showed in vivo that lactate is also used by the brain as a primary energy source, and it appears that the brain prefers lactate over glucose as an energy substrate. Hence, it can be suggested that exercise intensities that increase lactate production (e.g., above the lactate threshold [LT]) might be more effective in improving cognition. Despite the likelihood that exercise-induced improvement in executive control is related to the exercise intensity, to the best of our knowledge no studies have investigated

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the acute effects of exercise performed above and below lactate threshold on the executive control in children. Therefore, the purpose of this present study was to analyze and compare the acute effects of exercise performed above and below LT on the executive control in children. We hypothesized that the improvements in executive control after exercise in children is intensity-dependent.

METHODS

SubjectsTo test the hypothesis, 9 children (4 boys) from the 4th grade of Brazilian public elementary school participated in a randomized trial with a crossover design. The exclusion criteria included special educational services related to cognitive or attentional disorders, neurologic diseases, and physical disabilities. The present study was conducted in accordance with the Declaration of Helsinki and the Resolution 466/2012 of the Brazilian National Health Council and subsequently approved by the local Research Ethics Committee (protocol number: 139/2010). A written informed consent was provided by the parents of all children. No monetary or other incentive was offered to the pupils or school to participate in the study.

ProceduresThe subjects were assessed during 5 sessions, with an interval of 24 to 72 hrs. The first 2 sessions consisted of: (a) the anthropometric and maturation assessments; familiarization with cognitive tasks and Cooper’s 12-min running track test; and (b) the determination of LT through an incremental test. The last 3 sessions were performed in a randomized order: (a) 110%LT session; (b) 90%LT session; and (c) control session (CON). Cognitive performance was measured after a 20-min recovery of the experimental and control sessions.

Anthropometric MeasuresThe subjects’ weight and height were measured by an electronic scale (Tech 05®, China) and a portable stadiometer (Sanny® ES 2040, Brazil), respectivelly. Fat percentage was determined by an adipometer (Lange®, USA) through triceps and subscapular skinfolds measurements, as previously described by Slaughter et al. (27). In addition, information on sexual maturity was determined according to the model proposed by Tanner (29). Within the same session, cardiac function was accessed by resting electrocardiogram (GE Medical Systems, MAC 500). Resting heart rate was measured by an automatic cardiac monitor (Polar® FT1).

Lactate Threshold The subjects’ LT was obtained through an incremental test adapted from the protocol developed by Simões et al. (24), which consisted of running 6 times 500 m at 80%, 83%, 86%, 89%, 92%, and 95% of average running speed obtained with the Cooper’s 12-min track test. During the last 10 sec of each 500 m run, a 25 µl blood sample was taken from the earlobe and was transferred to Eppendorf tubes containing 50 µl of sodium fluoride (NaF) 1%. The concentrations (mM) were determined from each sample by using a blood lactate analyzer (Yellow Spring Instruments 2700, Ohio USA). The lactate threshold was determined as the intensity at which the breakpoint in the blood lactate concentration curve occurred (25).

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Cognitive Tests The subjects completed a computerized modified flanker task (12) to assess inhibitory control. Congruent and incongruent trials required the subjects to press a button corresponding to the direction of the centrally presented target arrow. Congruent trials consisted of arrows facing the same direction (e.g., <<<<< or >>>>>) and incongruent trials consisted of the middle arrow facing the opposite direction of the others (e.g., <<><< or >><>>). A total of 20 trials with black arrows on a white background were shown. The reaction time and responses accuracy were registered, the result was presented by the inverse efficiency score which was calculated by the formula: performance (ms) = reaction time (ms)/correct responses (%) (6).

The Free recall memory test (23) was used to access the subjects’ declarative short memory. Each 20-item word list was presented 1 word at a time, 5 sec each for a 100 sec total presentation time. After this period, a verbal cue signaled that subjects were requested to write down within a 2-min period as many words as possible regardless of their presentation order. The number of correct words recalled was registered.

Cognitive flexibility was assessed by the trail making test (2). In Part A, it was necessary to draw lines connecting in ascending order consecutive circles numbered from 1 to 25, distributed randomly on a sheet of paper. In Part B, the circles included numbers (1 to 13) and letters (A to L), and the child should connect them as alternating numbers and letters (e.g., 1-A-2-B-3-C…). The time to complete each part of the task was registered.

To access logical reasoning, the subjects performed a tangram puzzle test (22) composed of 7 pieces of polygons (5 triangles, 1 square, and 1 parallelogram). In each experimental session, 2 figures with the same complexity were presented; the subject was instructed to set them as quickly as possible. The time spent to set each tangram was recorded (sec).

Intervention The experimental and control sessions were performed in randomized order with a 24- to 72-hr interval. A brief warm-up was performed before starting with the intervention sessions. Thereafter, the subjects performed 10 min of running at a speed equivalent to 90% or 110%LT. The heart rate (HR) was recorded (Polar® FT1) during the interventions. The sessions were performed between 5 and 6 p.m. at the standard 400-m athletic track at Catholic University of Brasilia (UCB). The appraiser blew a whistle so that the children could run at the right pace. During the control session, the subjects remained seated at rest for 10 min in an acclimatized room coloring and drawing while HR was registered.

Statistical Analyses

The normal distribution of the data was assessed by Shapiro-Wilk’s test. The data are presented as a mean and standard deviation or median and 25th to 75th percentiles. A repeated measures ANOVA followed by contrasts analysis was used to compare the effects of exercise intensity on the cognitive performance. The sphericity assumption was tested by Mauchly’s test and the Greenhouse-Geisser correction was used when necessary. The partial eta squared (η2

p) was used as a measure of the effect size of the variances. Additionally, the Hedges’ g was calculated as a measure of the effect size of the means.

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Statistical significance was set at P<0.05. The software SPSS 22.0 for windows was used to perform all analyses (SPSS, Chicago, IL, USA).

RESULTS

Table 1 presents the general characteristics of the sample. On the Flanker test, there was an effect of session (F(2,10)=5.79; P=0.021; η2

p=0.537) (Figure 1). The post hoc analysis indicates that the children showed better performance at Flanker test after the race at 110%LT when compared to the control session (P=0.028, g=0.65) (Figure 1). On the other hand, as shown in Table 2, there was no effect of exercise on the free recall memory, trail making, and tangram puzzle tests.

DISCUSSION

This study investigated the effects of 10 min of aerobic exercise performed at intensities above and below LT on executive control in children. The main finding of this study indicates that exercise performed at the highest intensity (110%LT vs. 90%LT) improved inhibitory control compared to the control session (Figure 1). This finding is consistent with the lower reaction time adjusted by the proportion of correct answers in the Flanker test. To the best of our knowledge, this is the first study to demonstrate the impact of the running exercise at intensity around the LT on executive control in children.

Table 1. General Characteristics of the Sample (N = 9).Data of Position and

Dispersion or ProportionAge (yrs) 10.3 ± 0.5Height (m) 1.43 ± 0.03Weight (kg) 33.1 ± 4.0Body Mass Index (kg·m-2) 16.2 ± 1.5Triceps Skinfold (mm) 9.0 (8.0 – 14.0)Subscapular Skinfold (mm) 7.0 (6.0 – 11.0)Body Fat (%) 13.7 (11.1 – 19.0)Sex (boy/girl) 4/5Pubic Hair Maturation (2/3) 7/2Genital/breast Maturation (2/3) 5/412 min Run Track Test (m) 1783.3 ± 169.612 min Run Track Test (km·h-1) 8.9 ± 0.8LT (km·h-1) 7.9 ± 0.910-min Run at 90%LT (km·h-1) 7.1 ± 0.810-min Run at 110%LT (km·h-1) 8.7 ± 1.0

The data are displayed as mean ± standard deviation or median (25th and 75th percentiles). 110%LT = intensity relative to 110% of the lactate threshold; 90%LT = intensity relative to 90% of the lactate threshold.

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Table 2. Effect of Aerobic Exercise Intensity on Executive Control in Children (N = 9).Control 90%LT 110%LT F P η2

p

Memory (words) 6.7 ± 1.9 6.0 ± 1.9 7.2 ± 2.9 0.70 0.451 0.081

Trail A (s) 61.6 ± 11.1 64.9 ± 22.2 65.0 ± 25.5 0.10 0.905 0.012

Trail B (s) 114.6 ± 40.2 122.9 ± 38.4 123.9 ± 59.8 0.14 0.867 0.018

Tangram 1 (s) 109.9 ± 67.4 75.2 ± 39.5 77.4 ± 52.7 1.73 0.208 0.178

Tangram 2 (s) 96.0 ± 57.1 87.7 ± 38.6 81.8 ± 47.8 0.57 0.576 0.067

Data are displayed as mean ± standard deviation. Memory (words) – words reminded; 110%LT = intensity relative to 110% of the lactate threshold; 90%LT = intensity relative to 90% of the lactate threshold; η2

p = partial eta squared.

The fact that only the exercise intensity above LT improved the subjects’ cognitive performance confirms our hypothesis. A higher concentration of blood lactate may be involved in this positive result (32), but this parameter was not the object of the present study. In agreement, the findings of Wyss et al. (32) showed for the first time in vivo the maintenance of neuronal activity in the presence of lactate as the primary energy source, preventing severe insulin-induced hypoglycemia. Importantly, the authors showed that the brain prefers lactate over glucose as an energy substrate, given that when the plasma lactate is increased experimentally the utilization of cerebral glucose was reduced (32). The LT represents a transition point during exercise in which the blood levels of lactate increases exponentially, while in intensities below the LT the muscle itself metabolizes the lactate produced (25). Therefore, considering that higher levels of plasma lactate are found during exercise above LT and that lactate is the energy substrate of choice of the brain, it is possible that the cognitive improvement found in the present study is the result of the increases in lactate production during exercise at 110%LT.

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Figure 1. Effect of the Aerobic Exercise Intensity on the Inhibitory Control in Children (N = 9). Data displayed as mean ± standard deviation. CON = control session; 110%LT = intensity relative to 110% of the lactate threshold; 90%LT = intensity relative to 90% of the lactate threshold.

This finding is in line with previous studies (5,7,16). In particular, Chang et al. (7) in a meta-analysis showed that exercise intensity is a primary factor in the improvement of cognitive function after a delay following exercise. Recently, Hotting et al. (16) assessed the effects of a 30-min exercise session at low- (<57% HR max) and high-intensity exercise (~80% HR max) on memory consolidation 20 min and 24 hrs after exercise in a sample of 81 young adults (22 ± 2.36 yrs). Interestingly, only the high-intensity group showed an increase in BDNF after exercise concomitant with fewer words forgotten. Similarly, Etnier et al. (13) showed that BDNF and long-term memory (24 hrs) only at an intensity of 120% but not at 80% of the ventilatory threshold in 16 young men and women (23.1±2.2 yrs). Surprisingly, in both studies (13,16) the increase in BDNF levels was not related to the improvements in cognitive performance, which suggest that other mediators may play an important role in the improvement. Contrary studies suggest that middle-aged and older adults who engage in moderate intensity (but not vigorous intensity) benefit with improvement in cognition (3,18). Thus, this means that while a higher intensity is needed to elicit cognitive improvements in children and young adults, lower exercise intensity may be enough to improve the cognitive function in older adults.

The mechanisms underlying the cognitive improvements of moderate-to-vigorous intensity exercise may be attributed to a series of factors, including increases in blood flow to the brain, changes in the levels of neurotransmitters such as acetylcholine, serotonin, adrenalin, and noradrenalin, which are related to cognitive function, energy supply, and brain catecholamines. Additionally, there is evidence of increased BDNF (30), which is related to the development of neuronal activity during learning, memory, and synaptic plasticity. In a study with rodents, Vaynman, Ying, and Gomez-Pinilla (31) showed that after the blocking BDNF receptors the exercise-induced cognitive improvement in learning and memory vanished. Therefore, it is very likely that BDNF plays a role in the results of the present study, however this was not investigated.

From an educational perspective, the result of the present study may have important implications with respect to the prescription of exercise in physical education classes. In line with the present results, Howie, Schatz, and Pate (17) showed that 10 and 20 min of moderate-to-vigorous exercise improved math performance compared to the sedentary condition in 92 school children (9 to 12 yrs). Additionally, we recently showed that active playing (~70% HR max) during classes resulted in cognitive improvements and neuroelectrical changes in event-related potential N450 that was related to conflict identification on the prefrontal cortex. During a go/no-go Stroop color test, 13 children showed lower N450 amplitude during the incongruent trials and faster reaction time (RT) (4) compared to a control sedentary condition. In fact, studies have shown that both acute exercise and physical fitness is related to faster RT, improved event-related potentials, and prefrontal cortex activation (4,8,15). Therefore, a practical application of the results of the present study can be made by requiring the children to engage in exercise intensity above the LT (i.e., 110%LT) for as little as 10 min, which is likely to improve their cognitive performance. Additionally, this intensity is also associated with improvements in health and physical fitness (28). For the subjects of the present study, 110%LT corresponded to a

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running speed of 8.7 ± 1.0 km·h-1. Therefore, this active break can be used to improve not only the pupils’ health but also their cognitive performance.

Limitations of This Study

The limitations of the present study include the small sample size, which may have influenced the statistical power. However, even with the small sample size, the findings indicate positive effects of exercise performed above LT. Also, we measured neither biomarkers nor the neuroelectrical responses, which could have helped to explain the mechanisms underlying the cognitive improvements. However, it is reasonably clear that the previous studies support the mechanistic explanation presented in the present study (4,15). Future studies should consider these limitations.

CONCLUSIONS

The findings indicate that a single 10-min running bout performed above LT improves the cognitive performance of children, namely the inhibitory control. This finding confirms the initial hypothesis that high-intensity aerobic exercise exerts a better effect on executive control. From a practical point of view, the results indicate that a daily 10-min aerobic exercise program may improve the pupil’s concentration and learning, and can also be helpful in improving classroom behavior.

ACKNOWLEDGMENTS

The authors are grateful for the students' scholarships (Conselho Nacional de Desenvolvimento Científico e Tecnológico [CNPq] and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior [CAPES]).

Address for correspondence: Isabela A. Ramos, Programa de Pós-graduação Stricto Sensu em Educação Física, Universidade Católica de Brasília, QS 7, Lote 1, EPCT, Águas Claras, Brasília 71966-700, DF, Brasil, Email: ahbeuramos@gmail.com

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