Association of Sedentary Behavior with Brain Structure and Intelligence in Children with Overweight or Obesity: The ActiveBrains Project

Juan Pablo Zavala-Crichton, Irene Esteban-Cornejo, Patricio Solis-Urra, José Mora-Gonzalez, Cristina Cadenas-Sanchez, María Rodriguez-Ayllon, Jairo H Migueles, Pablo Molina-Garcia, Juan Verdejo-Roman, Arthur F Kramer, Charles H Hillman, Kirk I Erickson, Andrés Catena, Francisco B Ortega, Juan Pablo Zavala-Crichton, Irene Esteban-Cornejo, Patricio Solis-Urra, José Mora-Gonzalez, Cristina Cadenas-Sanchez, María Rodriguez-Ayllon, Jairo H Migueles, Pablo Molina-Garcia, Juan Verdejo-Roman, Arthur F Kramer, Charles H Hillman, Kirk I Erickson, Andrés Catena, Francisco B Ortega

Abstract

We investigated the associations of different sedentary behaviors (SB) with gray matter volume and we tested whether SB related to gray matter volume is associated with intelligence.

Methods: 99 children with overweight or obesity aged 8-11 years participated in this cross-sectional study. SB was measured using the Youth Activity Profile-Spain questionnaire. T1-weighted images were acquired with a 3.0 T Magnetom Tim Trio system. Intelligence was assessed with the Kaufman Brief Test. Whole-brain voxel-wise multiple regression models were used to test the associations of each SB with gray matter volume.

Results: Watching TV was associated with lower gray matter volume in six brain regions (β ranging -0.314 to -0.489 and cluster size 106 to 323 voxels; p < 0.001), playing video games in three brain regions (β ranging -0.391 to -0.359, and cluster size 96 to 461 voxels; p < 0.001) and total sedentary time in two brain regions (β ranging -0.341 to -0.352, and cluster size 897 to 2455 voxels; p < 0.001). No brain regions showed a significant positive association (all p > 0.05). Two brain regions were related, or borderline related, to intelligence.

Conclusions: SB could have the potential to negatively influence brain structure and, in turn, intelligence in children with overweight/obesity.

Keywords: Keywords: sedentariness; TV viewing; brain; childhood; cognition; magnetic resonance imaging; obesity.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Brain regions showing negative separate associations of (A) watching TV, (B) video games and (C) total sedentary time with gray matter volume in children from the ActiveBrains projects. Analyses were adjusted for sex, peak height velocity offset (years), parent education university level (neither/one/both) and body mass index (kg/m2) in model 1, and model 2 was adjusted for model 1 plus cardiorespiratory fitness (CRF, mL/kg/min). Maps were thresholded using AlphaSim at p < 0.001with k = 77 voxels for model 1 and k = 75 for model 2 for watching TV, k = 44 voxels for model 1 and k = 45 for model 2 for video games, and k = 62 voxels for model 1 and k = 46 for model 2 for total sedentary time and surpassed the Hayasaka correction (see Table 2). The color bar represents T-values, with a lighter green color indicating a higher significant association. Images are displayed in neurological convention (i.e., the right hemisphere corresponds to the right side in coronal displays). Sagittal planes represent the left hemisphere. No brain regions showed a statistically significant positive association between any sedentary behavioral variable and gray matter volume.

References

    1. Tremblay M.S., Aubert S., Barnes J.D., Saunders T.J., Carson V., Latimer-Cheung A.E., Chastin S.F.M., Altenburg T.M., Chinapaw M.J.M. Sedentary behavior research network (SBRN)—Terminology consensus project process and outcome. Int. J. Behav. Nutr. Phys. Act. 2017;14:1–17. doi: 10.1186/s12966-017-0525-8.
    1. Tremblay M.S., LeBlanc A.G., Kho M.E., Saunders T.J., Larouche R., Colley R.C., Goldfield G., Gorber S.C. Systematic review of sedentary behaviour and health indicators in school-aged children and youth. Int. J. Behav. Nutr. Phys. Act. 2011;8:98. doi: 10.1186/1479-5868-8-98.
    1. Rideout V., Foehr U., Roberts D. Generation M2. Kaiser Family Foundation; San Francisco, CA, USA: 2010.
    1. Pate R.R., Mitchell J.A., Byun W., Dowda M. Sedentary behaviour in youth. Br. J. Sports Med. 2011;45:906–913. doi: 10.1136/bjsports-2011-090192.
    1. Hancox R.J., Milne B.J., Poulton R. Association between child and adolescent television viewing and adult health: A longitudinal birth cohort study. Lancet. 2004;364:257–262. doi: 10.1016/S0140-6736(04)16675-0.
    1. Rodriguez-Ayllon M., Cadenas-Sánchez C., Estévez-López F., Muñoz N.E., Mora-Gonzalez J., Migueles J.H., Molina-García P., Henriksson H., Mena-Molina A., Martínez-Vizcaíno V., et al. Role of physical activity and sedentary behavior in the mental health of preschoolers, children and adolescents: A systematic review and meta-analysis. Sport Med. 2019;49:1383–1410. doi: 10.1007/s40279-019-01099-5.
    1. Esteban-Cornejo I., Martinez-Gomez D., Sallis J.F., Cabanas-Sánchez V., Fernández-Santos J., Castro-Piñero J., Veiga O.L. Objectively measured and self-reported leisure-time sedentary behavior and academic performance in youth: The UP & DOWN Study. Prev. Med. 2015;77:106–111.
    1. Carson V., Hunter S., Kuzik N., Gray C.E., Poitras V.J., Chaput J.-P., Saunders T.J., Katzmarzyk P.T., Okely A.D., Gorber S.C., et al. Systematic review of sedentary behaviour and health indicators in school-aged children and youth: An update 1. Appl. Physiol. Nutr. Metab. 2016;41:240–265. doi: 10.1139/apnm-2015-0630.
    1. Haapala E.A., Väistö J., Lintu N., Westgate K., Ekelund U., Poikkeus A.M., Brage S., Lakka T.A. Physical activity and sedentary time in relation to academic achievement in children. J. Sci. Med. Sport. 2017;20:583–589. doi: 10.1016/j.jsams.2016.11.003.
    1. Fought E.L., Ekwaru J.P., Gleddie D., Storey K.E., Asbridge M., Veugelers P.J. The combined impact of diet, physical activity, sleep and screen time on academic achievement: A prospective study of elementary school students in Nova Scotia, Canada. Int. J. Behav. Nutr. Phys. Act. 2017;14:1–13. doi: 10.1186/s12966-017-0476-0.
    1. Adelantado-Renau M., Moliner-Urdiales D., Cavero-Redondo I., Valls B.M.R., Martínez-Vizcaíno V., Álvarez-Bueno C. Association between screen media use and academic performance among children and adolescents a systematic review and meta-analysis. JAMA Pediatr. 2019;173:1058–1067. doi: 10.1001/jamapediatrics.2019.3176.
    1. Paulus M.P., Squeglia L.M., Bagot K., Jacobus J., Kuplicki R., Breslin F.J., Bodurka J., Morris A.S., Thompson W.K., Bartsch H., et al. Screen media activity and brain structure in youth: Evidence for diverse structural correlation networks from the ABCD study. Neuroimage. 2019;185:140–153. doi: 10.1016/j.neuroimage.2018.10.040.
    1. Takeuchi H., Kawashima R. Neural mechanisms and children’s intellectual development: Multiple impacts of environmental factors. Neuroscientist. 2016;22:618–631. doi: 10.1177/1073858415610294.
    1. Horowitz-Kraus T., Hutton J.S. Brain connectivity in children is increased by the time they spend reading books and decreased by the length of exposure to screen-based media. Acta Paediatr. Int. J. Paediatr. 2018;107:685–693. doi: 10.1111/apa.14176.
    1. Takeuchi H., Taki Y., Hashizume H., Asano K., Asano M., Sassa Y., Yokota S., Kotozaki Y., Nouchi R., Kawashima R. The impact of television viewing on brain structures: Cross-sectional and longitudinal analyses. Cereb. Cortex. 2015;25:1188–1197. doi: 10.1093/cercor/bht315.
    1. Takeuchi H., Taki Y., Asano K., Asano M., Sassa Y., Yokota S. Impact of frequency of internet use on development of brain structures and verbal intelligence: Longitudinal analyses. Hum. Brain Mapp. 2018;39:4471–4479. doi: 10.1002/hbm.24286.
    1. Hillman C.H., Erickson K.I., Kramer A.F. Be smart, exercise your heart: Exercise effects on brain and cognition. Nat. Rev. Neurosci. 2008;9:58–65. doi: 10.1038/nrn2298.
    1. Kamijo K., Khan N.A., Pontifex M.B., Scudder M.R., Drollette E.S., Raine L.B., Evans E.M., Castelli D.M., Hillman C.H. The relation of adiposity to cognitive control and scholastic achievement in preadolescent children. Obesity. 2012;20:2406–2411. doi: 10.1038/oby.2012.112.
    1. Kamijo K., Pontifex M.B., Khan N.A., Raine L.B., Scudder M.R., Drollette E.S., Evans E.M., Castelli D.M., Hillman C.H. The negative association of childhood obesity to cognitive control of action monitoring. Cereb. Cortex. 2014;24:654–662. doi: 10.1093/cercor/bhs349.
    1. Yu Z.B., Han S.P., Cao X.G., Guo X.R. Intelligence in relation to obesity: A systematic review and meta-analysis. Obes. Rev. 2010;11:656–670. doi: 10.1111/j.1467-789X.2009.00656.x.
    1. Ronan L., Alexander-Bloch A.F., Wagstyl K., Farooqi S., Brayne C., Tyler L.K., Cam-CAN, Fletchera P.C. Obesity associated with increased brain age from midlife. Neurobiol. Aging. 2016;47:63–70. doi: 10.1016/j.neurobiolaging.2016.07.010.
    1. Maayan L., Hoogendoorn C., Sweat V., Convit A. Disinhibited eating in obese adolescents is associated with orbitofrontal volume reductions and executive dysfunction. Obesity. 2011;19:1382–1387. doi: 10.1038/oby.2011.15.
    1. Ou X., Andres A., Pivik R.T., Cleves M.A., Badger T.M. Brain gray and white matter differences in healthy normal weight and obese children. J. Magn. Reason. Imaging. 2015;42:1205–1213. doi: 10.1002/jmri.24912.
    1. Chaddock L., Erickson K.I., Prakash R.S., Kim J.S., Voss M.W., Vanpatter M., Pontifex M.B., Raine L.B., Konkel A., Hillman C.H., et al. A neuroimaging investigation of the association between aerobic fitness, hippocampal volume, and memory performance in preadolescent children. Brain Res. 2010;1358:172–183. doi: 10.1016/j.brainres.2010.08.049.
    1. Chaddock L., Erickson K.I., Prakash R.S., Van Patter M., Voss M.W., Pontifex M.B., Raine L.B., Hillman C.H., Kramer A.F. Basal ganglia volume is associated with aerobic fitness in preadolescent children. Dev. Neurosci. 2010;32:249–256. doi: 10.1159/000316648.
    1. Esteban-Cornejo I., Cadenas-Sanchez C., Contreras-Rodriguez O., Verdejo-Roman J., Mora-Gonzalez J., Migueles J.H., Henriksson P., Davis C.L., Verdejo-Garcia A., Catena A., et al. A whole brain volumetric approach in overweight/obese children: Examining the association with different physical fitness components and academic performance. Act. Proj. Neuroimage. 2017;159:346–354. doi: 10.1016/j.neuroimage.2017.08.011.
    1. Cadenas-Sánchez C., Mora-González J., Migueles J.H., Martín-Matillas M., Gómez-Vida J., Escolano-Margarit M.V., Maldonado J., Enriquez G.M., Pastor-Villaescusa B., de Teresa C., et al. An exercise-based randomized controlled trial on brain, cognition, physical health and mental health in overweight/obese children (ActiveBrains project): Rationale, design and methods. Contemp. Clin. Trials. 2016;47:315–324. doi: 10.1016/j.cct.2016.02.007.
    1. Cole T.J., Lobstein T. Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatr. Obes. 2012;7:284–294. doi: 10.1111/j.2047-6310.2012.00064.x.
    1. Saint-Maurice P.F., Welk G.J., Beyler N.K., Bartee R.T., Heelan K.A. Calibration of self-report tools for physical activity research: The physical activity questionnaire (PAQ) BMC Public Health. 2014;14:1–9. doi: 10.1186/1471-2458-14-461.
    1. Saint-Maurice P.F., Welk G.J. Validity and calibration of the youth activity profile. PLoS ONE. 2015;10:e0143949. doi: 10.1371/journal.pone.0143949.
    1. Kaufman A.S., Kaufman N.L. Kaufman Brief Intelligence Test. AGS; Circle Pines, MN, USA: 1990.
    1. Wang J., Kaufman A.S. Changes in fluid and crystallized intelligence across the 20- to 90-year age range on the K-BIT. J. Psychoeduc. Assess. 1993;11:29–37. doi: 10.1177/073428299301100104.
    1. Woolgar A., Duncan J., Manes F., Fedorenko E. Fluid intelligence is supported by the multiple-demand system not the language system. Nat. Hum. Behav. 2018;2:200–204. doi: 10.1038/s41562-017-0282-3.
    1. Esteban-Cornejo I., Mora-Gonzalez J., Cadenas-Sanchez C., Contreras-Rodriguez O., Verdejo-Román J., Henriksson P., Migueles J.H., Rodriguez-Ayllon M., Molina-García P., Suo C., et al. Fitness, cortical thickness and surface area in overweight/obese children: The mediating role of body composition and relationship with intelligence. Neuroimage. 2019;186:771–781. doi: 10.1016/j.neuroimage.2018.11.047.
    1. Kaufman A. Intelligence Test. American Guidance Service Inc.; Circle Pines, MN, USA: 2000. p. 113.
    1. Moore S.A., McKay H.A., Macdonald H., Nettlefold L., Baxter-Jones A.D.G., Cameron N., Brasher P.M.A. Enhancing a somatic maturity prediction model. Med. Sci. Sports Exerc. 2015;47:1755–1764. doi: 10.1249/MSS.0000000000000588.
    1. Léger L.A., Mercier D., Gadoury C., Lambert J. The multistage 20 metre shuttle run test for aerobic fitness. J. Sports Sci. 1988;6:93–101. doi: 10.1080/02640418808729800.
    1. Wierenga L.M., Sexton J.A., Laake P., Giedd J.N., Tamnes C.K. A key characteristic of sex differences in the developing brain: Greater variability in brain structure of boys than girls. Cereb. Cortex. 2018;28:2741–2751. doi: 10.1093/cercor/bhx154.
    1. Drollette E.S., Scudder M.R., Raine L.B., Moore D.R., Pontifex M.B., Erickson K.I., Hillman C.H. The sexual dimorphic association of cardiorespiratory fitness to working memory in children. Dev. Sci. 2016;19:90–108. doi: 10.1111/desc.12291.
    1. Hayasaka S., Phan K.L., Liberzon I., Worsley K.J., Nichols T.E. Nonstationary cluster-size inference with random field and permutation methods. Neuroimage. 2004;22:676–687. doi: 10.1016/j.neuroimage.2004.01.041.
    1. Peracchia S., Curcio G. Exposure to video games: Effects on sleep and on post-sleep cognitive abilities. A systematic review of experimental evidences. Sleep. Sci. 2018;11:302–314. doi: 10.5935/1984-0063.20180046.
    1. Ortega F.B., Campos D., Cadenas-Sanchez C., Altmäe S., Martínez-Zaldívar C., Martín-Matillas M., Catena A., Campoy C. Physical fitness and shapes of subcortical brain structures in children. Br. J. Nutr. 2019;122:S49–S58. doi: 10.1017/S0007114516001239.
    1. Cotterill R.M.J. Cooperation of the basal ganglia, cerebellum, sensory cerebrum and hippocampus: Possible implications for cognition, consciousness, intelligence and creativity. Prog. Neurobiol. 2001;64:1–33. doi: 10.1016/S0301-0082(00)00058-7.
    1. Gibson K.R. Evolution of human intelligence: The roles of brain size and mental construction. Brain Behav. Evol. 2002;59:10–20. doi: 10.1159/000063730.
    1. Yoon Y.B., Shin W.G., Lee T.Y., Hur J.W., Cho K.I.K., Sohn W.S., Kim S.-G., Lee K.-H., Kwon J.S. Brain structural networks associated with intelligence and visuomotor ability. Sci. Rep. 2017;7:1–9. doi: 10.1038/s41598-017-02304-z.
    1. Vias C., Dick A.S. Cerebellar contributions to language in typical and atypical development: A review. Dev. Neuropsychol. 2017;42:404–421. doi: 10.1080/87565641.2017.1334783.
    1. Moore D.M., D’Mello A.M., McGrath L.M., Stoodley C.J. The developmental relationship between specific cognitive domains and grey matter in the cerebellum. Dev. Cogn. Neurosci. 2017;24:1–11. doi: 10.1016/j.dcn.2016.12.001.
    1. Mariën P., Borgatti R. Language and the cerebellum. Handb. Clin. Neurol. 2018;154:181–202.
    1. Cotman C.W., Berchtold N.C., Christie L.A. Exercise builds brain health: Key roles of growth factor cascades and inflammation. Trends Neurosci. 2007;30:464–472. doi: 10.1016/j.tins.2007.06.011.
    1. Leckie R.L., Weinstein A.M., Hodzic J.C., Erickson K.I. Potential moderators of physical activity on brain health. J. Aging Res. 2012;2012 doi: 10.1155/2012/948981.
    1. Hillman C.H., Biggan J.R. A review of childhood physical activity, brain, and cognition: Perspectives on the future. Pediatr. Exerc. Sci. 2017;29:170–176. doi: 10.1123/pes.2016-0125.
    1. Pedersen B.K. Physical activity and muscle–brain crosstalk. Nat. Rev. Endocrinol. 2019;15:383–392. doi: 10.1038/s41574-019-0174-x.
    1. Stillman C.M., Cohen J., Lehman M.E., Erickson K.I. Mediators of physical activity on neurocognitive function: A review at multiple levels of analysis. Front Hum. Neurosci. 2016;10:1–17. doi: 10.3389/fnhum.2016.00626.
    1. Stillman C.M., Weinstein A.M., Marsland A.L., Gianaros P.J., Erickson K.I. Body-brain connections: The effects of obesity and behavioral interventions on neurocognitive aging. Front Aging Neurosci. 2017;9:1–18. doi: 10.3389/fnagi.2017.00115.
    1. Voss M.W., Soto C., Yoo S., Sodoma M., Vivar C., van Praag H. Exercise and hippocampal memory systems. Trends Cogn. Sci. 2019;23:318–333. doi: 10.1016/j.tics.2019.01.006.
    1. Arnardottir N.Y., Koster A., van Domelen D.R., Brychta R.J., Caserotti P., Eiriksdottir G., Sverrisdottir J.E., Sigurdsson S., Johannsson E., Chen K.Y., et al. Association of change in brain structure to objectively measured physical activity and sedentary behavior in older adults: Age, gene/environment susceptibility-reykjavik study. Behav. Brain Res. 2016;296:118–124. doi: 10.1016/j.bbr.2015.09.005.

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