Introduction

Cardiorespiratory fitness (CRF) is a direct measure of the combined ability of a person's cardiovascular and respiratory systems to perform physical exercise and plays a vital role in a person's physical and mental health1,2. Studies have shown that an increase in cardiopulmonary endurance level by 1 unit can reduce the risk of death by 17%, and an increase in maximal oxygen uptake by 1 MET can reduce the all-cause mortality by 31.5%3. Meanwhile, longitudinal studies suggested that low CRF in childhood and adolescence is associated with increased risk of cardiometabolic disease, BMI, body fat, metabolic syndrome, and death in early adulthood4,5. This shows the important role and significance of CRF for the healthy development of children and adolescents.

Executive function (EF) refers to the mental process by which an organism exercises conscious control over thoughts and actions. Being a process occurring in the prefrontal and parietal regions of the brain6, EF has become a hot topic in the field of psychology since the twenty-first century7. With the deepening of research, several observations shown that EF plays a fundamental role in human development8. For example, EF is considered necessary for learning and is positively correlated with the academic performance of children and adolescents aged 5–17 years9. Besides, EF is also related to school preparation and socio-emotional competence10,11. A review presents data from 26 articles suggested enhanced executive functioning in children with higher aerobic fitness levels12. This shows that EF has a significant impact on the health and academic performance of children and adolescents. However, findings on the association between CRF and EF are not consistent. Some studies have confirmed that there is no association between CRF and inhibition of EF13.

Physical activity is considered to be an important variable for promoting executive function in children and adolescents14. Always being considered as a substitute for physical activity, CRF was found to be positively related to EF in children and adolescents15. In adolescents, higher CRF is associated with improved inhibitory control, cognitive flexibility, and attentional subdomain performance16. CRF and EF, as the core and important components of physical health and brain cognitive function respectively, are particularly important for the development of physical and mental health adolescents. Previous studies on the relationship between CRF and EF were mainly conducted in samples from western countries such as United State17,18 Europe19,20,21or Japan22. However, currently no studies have been found on the association between CRF and EF in Chinese children and adolescents.

Given the importance of EF during adolescence that neuroplasticity increases and the brain becomes more susceptible to environmental influences23. In addition, CRF, as a core factor in the physical health of children and adolescents, is of great significance to the healthy physical and mental development of children and adolescents. Therefore, the present study aimed to investigate the association between CRF and EF in children and adolescents using data from a cross-sectional study in China. It provides references and lessons for improving the level of EF in Chinese children and adolescents. It also provides reference and assistance for the intervention and promotion of EF in Chinese children and adolescents.

Materials and methods

Study design and population

In this study, a three-stage stratified random whole cluster sampling method was used for the selection of research subjects. In the first stage, Anhui Province in the eastern part of China and Xinjiang Uygur Autonomous Region in the western part of China were selected as the survey and test areas. In the second stage, 2 middle and high schools were selected in two selected Chinese provinces, based on geographic area and economic level. The first to third grades of junior high school and the first to second grades of high school are the sample grades for this study. In the third stage, each grade uses the class as the sampling unit, and randomly selects 2 teaching classes as a cluster. A total of 1407 middle school students from 40 teaching classes in 2 provinces were selected for this study. After the survey assessment, 67 middle school students with missing important demographic information and 95 middle school students with an EF assessment accuracy rate of less than 80% were excluded. Finally, a total of 1245 middle school students were included in our study, and the effective data recovery rate was 88.5%. The survey period of this study is from March to May 2023. The specific sampling process is shown in Fig. 1.

Figure 1
figure 1

The sampling process of the subjects in this study.

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The inclusion criteria of the subjects in our study were: First, middle school students who are enrolled in school. Second, with the assistance of the head teacher, students with serious mental health problems and physical fitness problems in the class were excluded. Third, subjects gave voluntary informed consent and obtained written informed consent from their parents or guardians. Our research was conducted in strict compliance with human ethics requirements and was approved by the Human Ethics Committee of Chizhou University (202204057).

Cardiorespiratory fitness (CRF)

At present, countries often use Maximal oxygen intake (VO2max) to evaluate the CRF level of adolescents. VO2max assessment includes direct test method and indirect test method. Direct test methods, such as the direct test method of Bruce treadmill24, the direct test method of Astrand power bicycle25, etc. However, the test is limited by the relatively expensive equipment and complicated test methods and procedures, so large-scale tests cannot be carried out. Indirect test methods include 20 m shuttle run test (20-m SRT), step test, 12 min run, Fox method, etc. Indirect test methods have low cost and are suitable for large-scale testing. 20-m SRT is a relatively recognized method for testing CRF in various countries in the world, and has been used in many countries in the world26,27. Studies have shown that more than 50 countries use the 20mSRT to measure cardiorespiratory endurance levels in children and adolescents, and that there is a high correlation between the 20 m SRT and VO2max levels (r = 0.91)28. Our study also used 20-m SRT to indirectly test the CRF level of the subjects, and the specific test method was described in detail in previous studies27. Use Leger's calculation equation to calculate VO2max29. The test method is as follows: the participant runs back and forth between 2 lines at a distance of 20 m, each completion of 20 m is recorded as 1 lap (times), the running time is controlled by the music, the initial speed at the beginning of the initial speed of 8.0 km h−1, the speed of the second minute is 9.0 km h−1, and then accelerated by one speed level every minute, i.e., each time the increase is 0.5 km h−1. The participant tries his/her best to complete the running speed level, and the test ends when he/she cannot follow the rhythm to reach the 20 m end line for 2 times consecutively. The test ends when the participant fails to follow the tempo to the 20 m end line for 2 consecutive times, and the final number of laps (times) is recorded. The specific calculation equation is:

$$ {\text{VO}}_{{{\text{2max}}}} ({\text{mL}}\;{\text{kg}}^{{ - {1}}} \;{\text{min}}^{{ - {1}}} ) \, = { 31}.0{25 } + { 3}.{238 } \times {\text{ S }} - { 3}.{248 } \times {\text{ Age }} + \, 0.{1536 } \times {\text{ S }} \times {\text{ Age}} $$

S: the running speed at the last completed stage (km h−1).

Executive function

The EF assessment in this study uses the flanker experimental paradigm to assessment the inhibit function; the 1-back and 2-back experimental paradigms are used to assessment the refresh memory function; the more-odd shifting experimental paradigm is used to assessment the cognitive flexibility. The specific assessment methods for inhibit function, refresh memory function, and cognitive flexibility functions have been described in detail in previous studies30. The specific EF test methods are:

1. The Flanker experimental paradigm was used to test the inhibition function. At the beginning of the experiment, a computer screen was gazed at the centre of the screen for 500 ms, after which a series of five capital letters would appear on the screen for 1000 ms, with two different conditions appearing randomly, one being a congruent condition such as "F F F F F F" or "L L L L L L L L L ", and the other was an incongruent condition, such as "F F F L F F F" or "L L L F L L L", with each stimulus appearing at 2 s intervals, while the "+" sign. Participants quickly pressed the capital letter "F" or "L" that appeared at the position of the "+" sign while ensuring that it was correct, and if the capital letter "F" or "L" that appeared at the position of the "+" sign was pressed, the participant was asked to press the "F" or "L" button if the "+" sign was correct. If the capital letter appearing in the "+" position is "F", the subject quickly presses the "F" key on the keyboard, if the capital letter appearing in the "+" position is "L", the subject quickly presses the "F" key on the keyboard. If the capital letter in the "+" position is "L", then the subject quickly presses the "L" key on the keyboard. The faster the response, the better the inhibition.

2. The 1-back and 2-back experimental paradigms tested the memory refreshing function. 1-back used five capital letters of the English language, such as A, S, P, G, T, etc., and each letter was presented in the centre of the screen individually. During the task test, subjects were asked to remember the appearing letters carefully and accurately, and if the appearing capital letter was consistent with the previous one, they quickly pressed the "F" key on the keyboard; if the appearing capital letter was inconsistent with the previous one, they quickly pressed the "J key" on the keyboard if the capital letter does not match the previous one. The formal test was divided into 2 phases of 25 trials each, with 5 letters appearing randomly. The stimulus interval for each uppercase letter was 3 s, and the time for the letter to be presented on the screen was 2000 ms. Participants were required to press the "F" key or the "J" key quickly to ensure that the letter was correct, and the result was the mean value of each reaction time. The result is the mean of each reaction time, and the faster the reaction time, the better the participant's refreshing function.

The result is the mean value of each reaction time, and the faster the reaction time, the better the refreshing function of the participant. 2-back: if the capital letter appearing in the centre of the screen is the same as the one appearing one letter before it, then quickly press the "F" key on the keyboard; if the capital letter appearing is not the same as the one appearing one letter before it, then quickly press the "J" key on the keyboard. key" on the keyboard quickly if the capital letters appearing do not match the capital letters appearing one letter before. Other test requirements and methods are the same as 1-back.

3. More-odd Shifting experimental paradigm to test the conversion function. The experiment is divided into three test sections. The first part: after the task starts, a random black Arabic number will appear continuously in the centre of the test computer screen, but not "5", each number is presented for 2000 ms, with a time interval of 3 s. Subjects compare the number appearing in the centre of the screen with "5", and press "D" quickly if it is less than 5. The test subject compares the number appearing in the centre of the screen with "5" and quickly presses the "D" key if it is less than 5, or presses the "F" key if it is greater than 5. Part 2: A green random number 1 ~ 9 appears in the centre of the screen, but there is no 5. If the number is odd, press "J", if it is even, press "K". If the number is odd, press "J", if it is even, press "K". The result is the average reaction time of each reaction, i.e. the time of non-conversion reaction. The third part of the test is a combination of the first part and the second part of the test. If the number appears in black, judge the size of the number with 5, if it is less than 5, then press "D" with your left hand, and if it is greater than 5, then press "F". If the number appears in green, judge the number of odd and even numbers, and if it is odd, then press "J" with your right hand. If the number appears in green, then judge the odd–even number, if odd, press "J" with your right hand, and if even, press "K". The faster the response, the better the performance of the switching function, provided that it is correct. The result is the average reaction time, i.e., the switching reaction time. The conversion reaction time of the subject is the conversion reaction time minus the non-conversion reaction time of the subject, and the shorter the difference, the better the conversion function.

The assessment of EF is carried out by computer, and the program runs through E-prime 1.1 software system. The assessment environment for EF requires testing in a bright and spacious environment. Subjects are required to be highly focused and not stay up late, drink alcohol, or take excitatory or hypnotic drugs the day before the assessment.

Covariates

Covariates in our study included demographic information, father's education, mother's education, duration of sleep, when to take a lunch break, breakfast frequency, soy products, dairy products, body mass index (BMI), moderate and vigorous physical activity (MVPA).

The specific assessment methods and classifications for covariates are: (1) Demographic information includes school, age, gender, class, etc. (2) The educational level of parents is divided into two categories: Primary School or Below and Junior high school and above. (3) Based on the National Sleep Foundation's research recommendations of 8–11 h of recommended sleep duration per day for adolescents, this study the duration of sleep is divided into ≥ 8 h day−1 and < 8 h day−131. (4) Whether to take a lunch break is divided into two categories: yes and no. (5) Breakfast frequency is divided into two types: ≤ 2 times/week and ≥ 3 times/week. (6) Soy products are also divided into two types: ≤ 2 times/week and ≥ 3 times/week. Soy products include drinking soy milk, edible tofu, dried tofu and soy products with beans as the main raw material. (7) Dairy products are also divided into two types: ≤ 2 times/week and ≥ 3 times/week. Dairy products mainly include drinking milk, goat milk, fermented yogurt and dairy products with milk as the main raw material. (8) The calculation of BMI is based on the height and weight of the assessment subjects, BMI = weight (kg)/height (m)2. The assessment methods and requirements for height and weight are tested according to the methods required by the Chinese Student Physical Health Survey , the height is accurate to 0.1 cm, and the weight is accurate to 0.1 kg32. (9) The MVPA assessment is carried out according to the test method of the physical activity part of the Chinese Student Physical Health Questionnaire32. The time and frequency of moderate to high-intensity physical activity performed by the subjects in the past 7 days were tested, and the average daily physical activity was calculated. Moderate to high intensity is defined as performing physical activities that feel breathless to sweating, such as lifting heavy objects, cycling, running, ball games, swimming, skating, etc. This physical activity questionnaire has been used in several studies and has good reliability and validity for evaluating physical activity in Chinese children and adolescents33.

Statistical analyses

Our findings are presented as means and standard deviations (M ± SD) for continuous variables and for categorical variables as percentages. One-way ANOVA was used to compare continuous variables of different VO2max classifications, and chi-square test was used to compare categorical variables. VO2max classification is to divide VO2max according to percentiles according to different ages and genders. By referring to previous relevant studies, after stratification by age and gender, they were divided according to percentile, we divide VO2max into three categories: < P25, P25–75, and > P7534. The association analysis between CRF and EF was carried out in two aspects. One is to conduct multiple linear regression analysis of continuous variables in VO2max and EF response, which are divided into model 1, model 2 and model 3. Model 1 does not adjust variables; Model 2 adjusts sex, father's education, mother's education, duration of sleep, when to take a lunch break, BMI, MVPA; Model 3 adjusts breakfast frequency, soy products, dairy products on the basis of Model 2. Second, logistic regression analysis of VO2max (< P25, P25–75, > P75) and executive dysfunction was performed, which were divided into model 1, model 2 and model 3. Adjustment for covariates was consistent with the multiple linear regression analysis. The criteria for the classification of executive dysfunction were stratified by age and gender, and adolescents with an EF response time higher than the average + 1SD were classified as having executive dysfunction34,35.

Ethics approval and consent to participate

All methods were performed in accordance with the Declaration of Helsinki. Written informed consent was obtained from the subjects and parents prior to the investigation of this study, and the investigation was conducted on a voluntary basis. This study was approved by the Ethics Committee of Chizhou University (202204057).

Results

We assessment CRF and EF in 1245 (595 boys, 47.8%) Chinese adolescents with an average age of (15.23 ± 1.43) years. In terms of father's education, mother's education, duration of sleep, whether to take a lunch break, breakfast frequency, and soy products, the detection rate of VO2max classification was significantly different (χ2 -value was 51.160, 48.488, 111.340, 17.971, 26.356, 34.084, P < 0.001). The proportion of Chinese adolescents whose father's and mother's education is primary school or below, duration of sleep ≥ 8 h day−1, lunch break, breakfast frequency ≥ 3 times/week, and soy products ≥ 3 times/week is higher than P75 (Table 1).

Table 1 Comparison of VO2max among Chinese adolescents with different demographic characteristics.
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Our study showed that the inhibitory function, refresh memory function, cognitive flexibility and the response time of each sub-function of EF in Chinese adolescents with different CRFs (VO2max < P25, P25–75, > P75) were significantly different (F -values were 78.391, 75.795, 3.933, 56.396, 58.517, 78.075, 107.149, 21.178, P values were all < 0.05). Overall, Chinese adolescents with VO2max > P75 had shorter EF and its sub-function response times, indicating that the level of EF relatively high (Table 2).

Table 2 One-way ANOVA of EF response time of Chinese adolescents with different CRFs.
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Table 3 shows that after adjusting for relevant confounding factors (Model 3), compared with Chinese adolescents with VO2max < P25, Chinese adolescents with VO2max P25-75 decreased inhibitory function reaction time, 1back reaction time, 2back reaction time, and cognitive flexibility response time by 1.26 ms, 138.89 ms, 146.56 ms, 57.63 ms, respectively; Chinese adolescents with VO2max > P75 decreased by 1.41 ms, 238.73 ms, 273.09 ms, and 74.14 ms, respectively. The decrease of 1 back reaction time, 2 back reaction time, and cognitive flexibility response time was more significant (P < 0.001). The same trend also exists in each sub-function of EF.

Table 3 Multiple linear regression analysis of EF in Chinese adolescents with different CRF classifications (n = 1245).
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After adjusting for relevant confounding factors (Model 3), compared with Chinese adolescents with VO2max > P75, Chinese adolescents with VO2max P25–75 developed 1 back dysfunction (OR 2.47, 95% CI 1.66, 3.67), 2back dysfunction (OR 3.26, 95% CI 2.11, 5.03) risk was higher (P < 0.01). Chinese adolescents with VO2max < P25 developed inhibitory function dysfunction (OR 2.03, 95% CI 1.29, 3.20), 1 back dysfunction (OR 6.26, 95% CI 3.94, 9.97), 2 back dysfunction (OR 8.94, 95% CI 5.40, 14.82), the risk of cognitive flexibility dysfunction (OR 2.26, 95% CI 1.44, 3.57) was the highest (P < 0.01) (Table 4). As can be seen in Fig. 2, adolescents with VO2max < P25 had a significantly increased risk of executive dysfunction compared to adolescents with VO2max > P75 (P < 0.01).

Table 4 Logistic regression analysis of EF in Chinese adolescents with different VO2max classification (n = 1245).
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Figure 2
figure 2

Logistic regression analysis OR value of EF in Chinese adolescents with different VO2max classification.

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Discussion

This study is the first to analyze the association between CRF and EF in Chinese adolescents. The results showed that there was a association between CRF and EF. Children with higher CRF had shorter EF response time, that is, higher levels of executive function. Our findings are consistent with the conclusions of multiple previous studies that higher CRF is associated with better EF performance36. The World Health Organization has identified CRF as a major clinical marker of physical fitness in adolescents37, which reinforces its link to cognitive function36. However, few scholars have observed an association between CRF and adolescent EF, and the conclusions are inconsistent38,39. These differences in results may be caused by differences in different research methods, and there are certain differences in EF tested by different methods.

After adjusting for relevant confounding factors, we found that Chinese adolescents with different CRFs showed significant differences in inhibition function, refresh memory function, and cognitive flexibility. Adolescents with VO2max of P25–75 performed better than those with VO2max < P25 in all three aspects. The results of this study are consistent with previous studies on the association between CRF and EF in adolescents. A positive correlation between CRF and inhibitory control levels and task performance has been found using field-based (eg PACER) or laboratory-based VO2max assessments40. Cross-sectional studies of laboratory-based CRF assessments have also revealed positive associations between VO2max and working memory capacity41 and cognitive flexibility42. Overall, this study further expands the current outcome evidence for a positive association between CRF and EF in Chinese adolescents.

Improving EF is particularly important during adolescent development, which is influenced by many factors, including education, diet, environmental exposure, and physical activity43. Relevant studies have shown that high levels of physical activity, low levels of recreational screen time and adequate sleep are positively correlated with the development of executive function in children14. Research has shown that a higher level of cardiopulmonary endurance (CRF), to a beneficial effect of school-age children grades before puberty, play intermediary effect between EF in CRF and academic performance, although the nature of this relationship remains unclear44, may be associated with CRF related EF enhance45. CRF can reflect a person's past and present physical fitness level, and the higher the CRF, the stronger the physical fitness46. Studies have shown that children with higher levels of physical fitness perform better cognitively47. Physical fitness centered on CRF is an important factor in increasing neuroplasticity, which can induce important structural and functional changes in the brain. These changes include increased cerebral blood flow, increased gray matter volume in the frontal lobe and hippocampus, and increased blood levels of brain-derived neurotrophic factor, thereby improving EF levels48. The reason for the association between CRF and EF in adolescents may be that the cerebral blood flow and oxygen-carrying capacity of the people with high CRF are high, resulting in a higher level of EF function.

Currently, there is little literature on the reasons for the association between CRF and EF. Research has shown that higher CRF is beneficial to the structure of the brain's white matter, which is responsible for communication between different areas of the brain, thus contributing to the improvement of EF49. The association between CRF and various brain structural changes in humans has indeed been observed. The study shows that higher levels of CRF have been found to be positively correlated with enhanced attentional allocation, cognitive regulation, and increased neural efficiency50, and better relational memory51. This may be related to the effects of CRF on angiogenesis, neurogenesis and neuroplasticity by increasing brain-derived neurotrophic factor52,53,54. The association between CRF and EF may be related to the CRF-mediated association of brain regions associated with attentional control (parietal regions) and stimulus features associated with processing tasks (occipital regions)55. The above study can further better explain and support the close association relationship between CRF and the presence of EF in Chinese adolescents.

As far as we know, this study has the following advantages: For the first time, the three functions of inhibit function, refresh memory function and cognitive flexibility of CRF and EF were simultaneously evaluated in China, which provided a basis for better intervention and policy formulation in the future. Secondly, The internationally recognized CRF test method and EF test paradigm for the first time to evaluate Chinese adolescents. The results are more convincing, and it is also convenient for international horizontal comparison in the future. Of course, our findings are exciting, but there are still some limitations to the study. First, our sample size is limited. China is a vast, multi-ethnic country, and both genetic and environmental factors can increase or limit the association between CRF and EF16. In contrast, this study only sampled participants for assessment in Anhui and Xinjiang, and its limited selection of regions for study participants is a limitation of this study. In the future, the investigation area should be further expanded to include more participants to better analyse the association that exists between CRF and EF. Second, this is a cross-sectional study and cannot establish a causal relationship between CRF and EF. Future prospective cohort studies should be conducted to analyse the causal association that exists between CRF and EF in adolescents. In addition, 20mSRT, although an internationally recognized method for testing CRF, is still an indirect assessment of CRF in adolescents, rather than a direct test in a laboratory setting. Therefore, subjects may fail to achieve their maximum aerobic capacity.

Conclusions

We conducted a cross-sectional assessment of CRF and EF in Chinese adolescents. Studies have shown a positive association between CRF and EF, and that adolescents with higher CRF have shorter EF response times, that is, higher EF levels. In the future, measures such as physical fitness intervention and brain training should be adopted, focusing on improving the CRF and EF levels of Chinese adolescents, which may be a practical strategy to improve the physical and mental health of Chinese adolescents.