Elsevier

NeuroImage

Volume 159, 1 October 2017, Pages 346-354
NeuroImage

A whole brain volumetric approach in overweight/obese children: Examining the association with different physical fitness components and academic performance. The ActiveBrains project

https://doi.org/10.1016/j.neuroimage.2017.08.011Get rights and content

Highlights

  • Physical fitness components are positively associated with gray matter volumes in overweight/obese children.

  • Cardiorespiratory fitness and speed-agility affect development of distinctive brain regions.

  • Cardiorespiratory fitness and speed-agility related-changes in brain volumes are associated with better academic performance.

  • Muscular fitness is not associated with cortical and subcortical brain volumes.

  • Physical activity that involves aerobic exercise and motor-agility tasks is important for the brain and academic performance.

Abstract

Obesity, as compared to normal weight, is associated with detectable structural differences in the brain. To the best of our knowledge, no previous study has examined the association of physical fitness with gray matter volume in overweight/obese children using whole brain analyses. Thus, the aim of this study was to examine the association between the key components of physical fitness (i.e. cardiorespiratory fitness, speed-agility and muscular fitness) and brain structural volume, and to assess whether fitness-related changes in brain volumes are related to academic performance in overweight/obese children. A total of 101 overweight/obese children aged 8–11 years were recruited from Granada, Spain. The physical fitness components were assessed following the ALPHA health-related fitness test battery. T1-weighted images were acquired with a 3.0 T S Magnetom Tim Trio system. Gray matter tissue was calculated using Diffeomorphic Anatomical Registration Through Exponentiated Lie algebra (DARTEL). Academic performance was assessed by the Batería III Woodcock-Muñoz Tests of Achievement. All analyses were controlled for sex, peak high velocity offset, parent education, body mass index and total brain volume. The statistical threshold was calculated with AlphaSim and further Hayasaka adjusted to account for the non-isotropic smoothness of structural images. The main results showed that higher cardiorespiratory fitness was related to greater gray matter volumes (P < 0.001, k = 64) in 7 clusters with β ranging from 0.493 to 0.575; specifically in frontal regions (i.e. premotor cortex and supplementary motor cortex), subcortical regions (i.e. hippocampus and caudate), temporal regions (i.e. inferior temporal gyrus and parahippocampal gyrus) and calcarine cortex. Three of these regions (i.e. premotor cortex, supplementary motor cortex and hippocampus) were related to better academic performance (β ranging from 0.211 to 0.352; all P < 0.05). Higher speed-agility was associated with greater gray matter volumes (P < 0.001, k = 57) in 2 clusters (i.e. the inferior frontal gyrus and the superior temporal gyrus) with β ranging from 0.564 to 0.611. Both clusters were related to better academic performance (β ranging from 0.217 to 0.296; both P < 0.05). Muscular fitness was not independently associated with greater gray matter volume in any brain region. Furthermore, there were no statistically significant negative association between any component of physical fitness and gray matter volume in any region of the brain. In conclusion, cardiorespiratory fitness and speed-agility, but not muscular fitness, may independently be associated with greater volume of numerous cortical and subcortical brain structures; besides, some of these brain structures may be related to better academic performance. Importantly, the identified associations of fitness and gray matter volume were different for each fitness component. These findings suggest that increases in cardiorespiratory fitness and speed-agility may positively influence the development of distinctive brain regions and academic indicators, and thus counteract the harmful effect of overweight and obesity on brain structure during childhood.

Introduction

Physical fitness is a major determinant of health throughout the lifespan. The main components of physical fitness with documented benefits on health are cardiorespiratory fitness, speed-agility and muscular fitness (Ortega et al., 2008b, Ruiz et al., 2009). While the benefits of fitness on physical health are well established (Ortega et al., 2008b, Ruiz et al., 2015), there is emerging evidence on the potential impact of physical fitness on cognitive and brain health (Donnelly et al., 2016). During childhood and adolescence, high levels of cardiorespiratory fitness have been positively associated with academic performance and cognition, as well as brain functioning and structure (Hillman et al., 2008, Chaddock et al., 2011, Esteban-Cornejo et al., 2014, Ortega et al., 2017). In contrast, individuals with lower cardiorespiratory fitness are at greater risk of having cognitive deficits and developing neurodegenerative disorders later in life (Newson and Kemps, 2006, Defina et al., 2013, Nyberg et al., 2014).

Particularly, recent evidence has shown that the brain's volumetric structure of individuals with overweight and obesity is 10 years older compared to that of lean peers, and this accelerated brain aging is evident from young adulthood onwards (Ronan et al., 2016). Indeed, obesity has been associated with detectable structural differences in the brain as compared to the brains of normal-weight individuals already during childhood and adolescence (Reinert et al., 2013). For instance, body mass index (BMI) has been negatively associated with gray matter volume in a dose-dependent manner (Maayan et al., 2011, Ou et al., 2015). In addition, overweight and obese children have worse cognitive control and academic performance compared to normal-weight children (Kamijo et al., 2012, Kamijo et al., 2014). These findings highlight the importance of examining the potential benefits of physical fitness for brain health in the context of overweight and obesity during early stages of life. It is indeed plausible that physical fitness has a positive impact on brain health, resulting in better academic performance, and may thus attenuate the negative effect of overweight and obesity on brain structure during childhood.

Despite the marked relevance of fitness for brain health in overweight/obese children (Maayan et al., 2011, Reinert et al., 2013, Ou et al., 2015), no previous volumetric study has focused on populations with excess body weight, and only two studies have been performed in normal weight children (Chaddock et al., 2010a, Chaddock et al., 2010c). These studies showed that higher cardiorespiratory fitness was associated with greater volume of the hippocampus and the dorsal striatum of the basal ganglia; and in turn, hippocampal volume was related to relational memory and dorsal striatum volume with better cognitive control and response resolution. However, there is a number of research questions that still need to be addressed (Donnelly et al., 2016). Firstly, previous studies focused on the two fitness extremes, i.e. children with a very high fitness vs. a very low fitness, leaving out from the analyses the rest of children with a middle fitness level, which it has been considered in a recent position stand as a limitation of existing evidence (Donnelly et al., 2016). Secondly, different dimensions of fitness may have different effects on the brain. For example, cardiorespiratory fitness is related to angiogenesis, whereas speed-agility and muscular fitness are associated with synaptogenesis in animals (Adkins et al., 2006). Thirdly, brain changes may translate into improved academic performance. Therefore, to have a complete picture of fitness-brain-academic performance relationships, there is a need for studies that examines all different components of fitness and their associations with gray matter volume on a whole brain level, rather than at the region-of-interest level, as well as whether these gray matter volume changes are related to academic performance.

Understanding the association of different physical fitness components with brain measures and how those brain changes relate to academic performance would help develop public health and educational strategies, since exercise programs improve physical fitness levels, which in turn, may positively influence physical and cognitive health (Voelcker-Rehage and Niemann, 2013). To the best of our knowledge, no previous study has examined the association of physical fitness with gray matter volume of all known brain structures in overweight/obese children or its links to academic performance.

Therefore, the aim of this study was twofold: (i) to examine the association between the key components of physical fitness (i.e. cardiorespiratory fitness, speed-agility and muscular fitness) and brain volume, and (ii) to examine whether fitness-related changes in brain volumes are related to academic performance in relatively large sample of overweight/obese children. To achieve this aim, firstly, we used multiple regression analyses including the three components of fitness as predictors (separately and independently), while controlling for relevant confounders using a whole-brain analytical approach; and secondly, we extracted the eigenvalues from each significant brain cluster to include them as predictors of academic performance.

Section snippets

Participants

Participants in this study were enrolled in the ActiveBrains project (http://profith.ugr.es/activebrains). ActiveBrains is a randomized controlled trial designed to examine the effects of an exercise program on brain, cognitive and academic performance, as well as on selected physical and mental health outcomes in overweight/obese children (Cadenas-Sanchez et al., 2016). A total of 110 overweight/obese children aged 8–11 years were recruited from Granada (south of Spain). All participants met

Background characteristics

Table 1 shows the sociodemographic, body composition and physical fitness characteristics of the study sample. Overall, boys had similar average BMI to that of girls (27.0 vs. 26.5 kg/m2; P > 0.05) and 25% of the participants were overweight and 75% were obese (42% obesity grade I, 21% obesity grade II and 12% obesity grade III). Boys had on average higher TBV than girls (P < 0.001).

Gray matter correlates of individual physical fitness components

Table 2 presents the brain regions showing positive associations between each physical fitness component and gray

Discussion

The main finding of the present study was that physical fitness components were positively associated with gray matter volumes in cortical and subcortical brain structures among overweight/obese children. Specifically, cardiorespiratory fitness and speed-agility, both separately and independently, were related to increased volume of differentiated and numerous cortical and subcortical brain structures. In addition, some of these brain structures (i.e. hippocampus, premotor cortex, supplementary

Conclusion

Our results support that cardiorespiratory fitness and speed-agility, but not muscular fitness, might independently be associated with greater gray matter volume of numerous cortical and subcortical brain structures. In addition, some of these brain structures (i.e. hippocampus, premotor cortex, supplementary motor cortex, inferior frontal gyrus and superior temporal gyrus) were related to better academic performance. Importantly, the identified associations of fitness and gray matter volume

Funding

This study was supported by the Spanish Ministry of Economy and Competitiveness (DEP2013-47540, DEP2016-79512-R & PSI2012-3929) and for the Spanish Ministry of Science and Innovation (RYC-2011-09011 & FJCI-2014-19563). IEC received a scholarship from the Alicia Koplowitz Foundation for a brief stay in the Monash Institute of Cognitive and Clinical Neurosciences, Monash University, Australia. CC-S is supported by a grant from the Spanish Ministry of Economy and Competitiveness (BES-2014-068829).

Acknowledgments

The authors thank children and parents who participated in this study. The authors declare no competing financial interests.

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