Aerobic fitness is associated with greater white matter integrity in children

Frontiers in Human Neuroscience

Volumn 8, Issue AUG, 2014, Pages

  Chaddock Heyman, Laura ^a   Erickson, Kirk I ^b   Holtrop, Joseph L ^a,c   Voss, Michelle W ^d   Pontifex, Matthew B ^e   Raine, Lauren B ^a   Hillman, Charles H ^a   Kramer, Arthur F ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c University of Illinois at Urbana Champaign   (United States)

^d E11 SSH   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Cardiorespiratory fitness; Development; Diffusion tensor imaging; Fiber tracts; Microstructure

Indexed keywords

ARTICLE; CARDIORESPIRATORY FITNESS; CHILD; CONTROLLED STUDY; CORONA RADIATA (BRAIN); CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; MALE; MYELINATION; NERVE TRACT; NEUROIMAGING; SCHOOL CHILD; SUPERIOR LONGITUDINAL BUNDLE; WHITE MATTER;

EID: 84932108276     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00584     Document Type: Article

References (72)

1. American College of Sports Medicine. (2006). ACSM's Guidelines for Exercise Testing and Prescription, 7th Edn. New York, NY: Lippincott Williams & Wilkins.
2. Andersson, J. R., Jenkinson, M., and Smith, S. (2007a). TR07JA1: Non-Linear Optimisation. Available at: http: //www. fmrib. ox. ac. uk/analysis/techrep (accessed March 1, 2014).
3. Andersson, J. R., Jenkinson, M., and Smith, S. (2007b). TR07JA2: Non-Linear Registration, Aka Spatial Normalisation. Available at: http: //www. fmrib. ox. ac. uk/analysis/techrep (accessed March 1, 2014).
4. Barnea-Goraly, N., Menon, V., Eckert, M., Tamm, L., Bammer, R., Karchemskiy, A., et al. (2005). White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Cereb. Cortex 15, 1848-1854. doi: 10.1093/cercor/bhi062
5. Bar-Or, O. (1983). Pediatric Sports Medicine For The Practitioner: From Physiologic Principles to Clinical Applications. New York, NY: Springer. doi: 10.1007/978-1-4612-5593-2
6. Basser, P. J. (1995). Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed. 8, 333-344. doi: 10.1002/nbm.1940080707
7. Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system: a technical review. NMR Biomed. 15, 435-455. doi: 10.1002/nbm.782
8. Bendlin, B. B., Fitzgerald, M. E., Ries, M. L., Xul, G., Kastman, E. K., Thiel, B. W., et al. (2010). White matter in aging and cognition: a cross-sectional study of microstructure in adults aged eighteen to eighty-three. Dev. Neuropsychol. 35, 257-277. doi: 10.1080/87565641003696775
9. Birnbaum, A. S., Lytle, L. A., Murray, D. M., Story, M., Perry, C. L., and Boutelle, K. N. (2002). Survey development for assessing correlates of young adolescents' eating. Am. J. Health Behav. 26, 284-295. doi: 10.5993/AJHB.26.4.5
10. Budde, M. D., Kim, J. H., Liang, H. F., Schmidt, R. E., Russell, J. H., Cross A. H., et al. (2007). Toward accurate diagnosis of white matter pathology using diffusion tensor imaging. Magn. Reson. Med. 57, 688-695. doi: 10.1002/mrm.21200
11. Bunge, S. A., and Crone, E. A. (2009). "Neural correlates of the development of cognitivecontrol, " in Neuroimaging in Developmental Clinical Neuroscience, eds J. Rumsey and M. Ernst (Cambridge: Cambridge University Press), 22-37. doi: 10.1017/CBO9780511757402.005
12. Burzynska, A. Z., Preuschhof, C., Bäckman, L., Nyberg, L., Li, S. C., Lindenberger, U., et al. (2010). Age-related differences in white matter microstructure: region-specific patterns of diffusivity. Neuroimage 49, 2104-2112. doi: 10.1016/j.neuroimage.2009.09.041
13. Castelli, D. M., Hillman, C. H., Buck, S. M., and Erwin, H. E. (2007). Physical fitness and academic achievement in third-and fifth-grade students. J. Sport Exerc. Psychol. 29, 239-252.
14. Centers for Disease Control and Prevention. (2010). The Association Between School-Based Physical Activity, Including Physical Education, and Academic Performance. Available at: http: //www. cdc. gov/healthyyouth/health_and_academics/pdf/pape_executive_summary. pdf (accessed March 1, 2014).
15. Chaddock, L., Erickson, K. I., Prakash, R. S., Kim, J. S., Voss, M. W., VanPatter, M., et al. (2010a). A neuroimaging investigation of the association between aerobic fitness, hippocampal volume and memory performance in preadolescent children. Brain Res. 1358, 172-183. doi: 10.1016/j.brainres.2010.08.049
16. Chaddock, L., Erickson, K. I., Prakash, R. S., VanPatter, M., Voss, M. V., Pontifex, M. B., et al. (2010b). Basal ganglia volume is associated with aerobic fitness in preadolescent children. Dev. Neurosci. 32, 249-256. doi: 10.1159/000316648
17. Chaddock, L., Erickson, K. I., Prakash, R. S., Voss, M. V., VanPatter, M., Pontifex, M. B., et al. (2012a). A functional MRI investigation of the association between childhood aerobic fitness and neurocognitive control. Biol. Psychol. 89, 260-268. doi: 10.1016/j.biopsycho.2011.10.017
18. Chaddock, L., Voss, M. W., and Kramer, A. F. (2012b). Physical activity and fitness effects on cognition and brain health in children and older adults. Kinesiol. Rev. 1, 37-45.
19. Chaddock, L., Pontifex, M., Hillman, C. H., and Kramer, A. F. (2011). A review of the relation of aerobic fitness and physical activity to brain structure and function in children. J. Int. Neuropsychol. Soc. 17, 975-985. doi: 10.1017/S1355617711000567
20. Chaddock-Heyman, L., Erickson, K. I., Voss, M. W., Powers, J. P., Knecht, A. M., Pontifex, M. B., et al. (2013). White matter microstructure is associated with cognitive control in children. Biol. Psychol. 94, 109-115. doi: 10.1016/j.biopsycho.2013.05.008
21. Chomitz, V. R., Slining, M. M., McGowan, R. J., Mitchell, S. E., Dawson, G. F., and Hacker, K. A. (2009). Is there a relationship between physical fitness and academic achievement? Positive results from public school children in the northeastern United States. J. Sch. Health 79, 30-37. doi: 10.1111/j.1746-1561.2008.00371.x
22. Coe, D. P., Pivarnik, J. M., Womack, C. J., Reeves, M. J., and Malina, R. M. (2006). Effect of physical education and activity levels on academic achievement in children. Med. Sci. Sports Exerc. 38, 1515-1519. doi: 10.1249/01.mss.0000227537.13175.1b
23. Colcombe, S. J., Erickson, K. I., Scalf, P. E., Kim, J. S., Prakash, R., McAuley, E., et al. (2006). Aerobic exercise training increases brain volume in aging humans. J. Gerontol. A Biol. Sci. Med. Sci. 61, 1166-1170. doi: 10.1093/gerona/61.11.1166
24. Colcombe, S. J., and Kramer, A. F. (2003). Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol. Sci. 14, 125-130. doi: 10.1111/1467-9280.t01-1-01430
25. Colcombe, S. J., Kramer, A. F., Erickson, K. I., Scalf, P., McAuley, E., Cohen, N. J., et al. (2004). Cardiovascular fitness, cortical plasticity, and aging. Proc. Natl. Acad. Sci. U. S. A. 101, 3316-3321. doi: 10.1073/pnas.0400266101
26. Davis, C. L., Tomporowski, P. D., McDowell, J. E., Austin, B. P., Miller, P. H., Yanasak, N. E., et al. (2011). Exercise improves executive function and achievement and alters brain activation in overweight children: a randomized, controlled trial. Health Psychol. 30, 91-98. doi: 10.1037/a0021766
27. Diamond, A., and Lee, K. (2011). Interventions shown to aid executive function development in children 4-12 years old. Science 333, 959-964. doi: 10.1126/science.1204529
28. Ding, Y. H., Li, J., Zhou, Y., Rafols, J. A., Clark, J. C., and Ding, Y. (2006). Cerebral angiogenesis and expression of angiogenic factors in aging rats after exercise. Curr. Neurovasc. Res. 3, 15-23. doi: 10.2174/156720206775541787
29. DuPaul, G. J., Power, T. J., Anastopoulos, A., and Reid, R. (1998). ADHD Rating Scale-IV: Checklists, Norms, And Clinical Interpretation. New York, NY: Guilford Press.
30. Freedson, P. S., and Goodman, T. L. (1993). "Measurement of oxygen consumption, " in Pediatric Laboratory Exercise Testing: Clinical Guidelines, ed. T. W. Rowland (Champaign, IL: Human Kinetics), 91-113.
31. Gazzaniga, M. S. (1995). Principles of human brain organization derived from split-brain studies. Neuron 14, 217-228. doi: 10.1016/0896-6273(95)90280-5
32. Hillman, C. H., Buck, S. M., Themanson, J. R., Pontifex, M. B., and Castelli, D. M. (2009). Aerobic fitness and cognitive development: event-related brain potential and task performance of executive control in preadolescent children. Dev. Psychol. 45, 114-129. doi: 10.1037/a0014437
33. Hua, K., Zhang, J., Wakana, S., Jiang, H., Li, X., Reich, D. S., et al. (2008). Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantifcation. Neuroimage 39, 336-347. doi: 10.1016/j.neuroimage.2007.07.053
34. Johnson, N. F., Kim, C., Clasey, J. L., Bailey, A., and Gold, B. T. (2012). Cardiorespiratory fitness is positively correlated with cerebral white matter integrity in healthy seniors. Neuroimage 59, 1514-1523. doi: 10.1016/j.neuroimage.2011.08.032
35. Kaufman, A. S., and Kaufman, N. L. (1990). Kaufman Brief Intelligence Test. Circle Pines: AGS.
36. Kramer, A. F., Hahn, S., Cohen, N., Banich, M., McAuley, E., Harrison, C., et al. (1999). Aging, fitness, and neurocognitive function. Nature 400, 418-419. doi: 10.1038/22682
37. Liston, C., Watts, R., Tottenham, N., Davidson, M. C., Niogi, S., Ulug, A. M., et al. (2006). Fronto-striatal microstructure modulates efficient recruitment of cognitive control. Cereb. Cortex 16, 553-560. doi: 10.1093/cercor/bhj003
38. Madsen, K. S., Baare, W. F., Vestergaard, M., Skimminge, A., Ejersbo, L. R., Ramsøy, T. Z., et al. (2010). Response inhibition is associated with white matter microstructure in children. Neuropsychologia 48, 854-862. doi: 10.1016/j.neuropsychologia.2009.11.001
39. Marks, B. L., Madden, D. J., Bucur, B., Provenzale, J. M., White, L. E., Cabeza, R., et al. (2007). Role of aerobic fitness and aging on cerebral white matter integrity. Ann. N. Y. Acad. Sci. 1097, 171-174. doi: 10.1196/annals.1379.022
40. Mori, S., Wakana, S., and Van Zijl, P. C. M. (2005). MRI Atlas of Human White Matter. Amsterdam: Elsevier.
41. Muetzel, R. L., Collins, P. F., Mueller, B. A., Schissel, A. M., Lim, K. O., and Luciana, M. (2008). The development of corpus callosum microstructure and associations with bimanual task performance in healthy adolescents. Neuroimage 39, 1918-1925. doi: 10.1016/j.neuroimage.2007.10.018
42. Nagy, Z., Westerberg, H., and Klingberg, T. (2004). Maturation of white matter is associated with the development of cognitive functions during childhood. J. Cogn. Neurosci. 16, 1227-1233. doi: 10.1162/0898929041920441
43. Nair, G., Tanahashi, Y., Low, H. P., Billings-Gagliardi, S., Schwartz, W. J., and Duong, T. Q. (2005). Myelination and long diffusion times alter diffusion-tensor-imaging contrast in myelin-deficient shiverer mice. Neuroimage 28, 165-174. doi: 10.1016/j.neuroimage.2005.05.049
44. Niogi, S., Mukherjee, P., Ghajar, J., and McCandliss, B. D. (2010). Individual differences in distinct components of attention are linked to anatomical variations in distinct white matter tracts. Front. Neuroanat. 4: 2. doi: 10.3389/neuro.05.002.2010
45. Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97-113. doi: 10.1016/0028-3932(71)90067-4
46. Olesen, P., Nagy, Z., Westerberg, H., and Klingberg, T. (2003). Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network. Cogn. Brain Res. 18, 48-57. doi: 10.1016/j.cogbrainres.2003.09.003
47. Olson, E. A., Collins, P. F., Hooper, C. J., Muetzel, R., Lim, K. O., and Luciana, M. (2009). White matter integrity predicts delay discounting behavior in 9-to 23-year-olds: a diffusion tensor imaging study. J. Cogn. Neurosci. 21, 1406-1421. doi: 10.1162/jocn.2009.21107
48. Paus, T. (2010). Growth of white matter in the adolescent brain: myelin or axon? Brain Cogn. 72, 26-35. doi: 10.1016/j.bandc.2009.06.002
49. Petrides, M., and Pandya, D. N. (1984). Projections to the frontal cortex from the posterior parietal region in the rhesus monkey. J. Comp. Neurol. 228, 105-116. doi: 10.1002/cne.902280110
50. Pierpaoli, C., and Basser, P. J. (1996). Toward a quantitative assessment of diffusion anisotropy. Magn. Reson. Med. 36, 893-906. doi: 10.1002/mrm.1910360612
51. Pierpaoli, C., Jezzard, P., Basser, P. J., Barnett, A., and Di Chiro, G. (1996). Diffusion tensor MR imaging of the human brain. Radiology 201, 637-648. doi: 10.1148/radiology.201.3.8939209
52. Pontifex, M. B., Raine, L. B., Johnson, C. R., Chaddock, L., Voss, M. W., Cohen, N. J., et al. (2011). Cardiorespiratory fitness and the flexible modulation of cognitive control in preadolescent children. J. Cogn. Neurosci. 23, 1332-1345. doi: 10.1162/jocn.2010.21528
53. Rykhlevskaia, E., Gratton, G., and Fabiani, M. (2008). Combining structural and functional neuroimaging data for studying brain connectivity: a review. Psychophysiology 45, 173-187. doi: 10.1111/j.1469-8986.2007.00621.x
54. Schmahmann, J. D., and Pandya, D. N. (2006). Fiber Pathways of The Brain. New York: Oxford University Press. doi: 10.1093/acprof:oso/9780195104233.001.0001
55. Schmithorst, V. J., and Yuan, W. (2010). White matter development during adolescence as shown by diffusion MRI. Brain Cogn. 72, 16-25. doi: 10.1016/j.bandc.2009.06.005
56. Sen, P. N., and Basser, P. J. (2005). A model for diffusion in white matter in the brain. Biophys. J. 89, 2927-2938. doi: 10.1529/biophysj.105.063016
57. Shvartz, E., and Reibold, R. C. (1990). Aerobic fitness norms for males and females aged 6 to 75 years: a review. Aviat. Space Environ. Med. 61, 3-11.
58. Smith, S. M. (2002). Fast robust automated brain extraction. Hum. Brain Mapp. 17, 143-155. doi: 10.1002/hbm.10062
59. Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C., et al. (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31, 1487-1505. doi: 10.1016/j.neuroimage.2006.02.024
60. Song, S. K., Sun, S. W., Ju, W. K., Lin, S. J., Cross, A. H., and Neufeld, A. H. (2003). Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 20, 1714-1722. doi: 10.1016/j.neuroimage.2003.07.005
61. Song, S. K., Sun, S. W., Ramsbottom, M. J., Chang, C., Russell, J., and Cross, A. H. (2002). Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17, 1429-1436. doi: 10.1006/nimg.2002.1267
62. Song, S. K., Yoshino, J., Le, T. Q., Lin, S. J., Sun, S. W., Cross, A. H., et al. (2005). Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26, 132-140. doi: 10.1016/j.neuroimage.2005.01.028
63. Sun, S. W., Liang, H. F., Cross, A. H., and Song, S. K. (2008). Evolving Wallerian degeneration after transient retinal ischemia in mice characterized by diffusion tensor imaging. Neuroimage 40, 1-10. doi: 10.1016/j.neuroimage.2007.11.049
64. Sun, S. W., Liang, H. F., Le, T. Q., Armstrong, R. C., Cross, A. H., and Song, S. K. (2006). Differential sensitivity of In vivo and ex vivo diffusion tensor imaging to evolving optic nerve injury in mice with retinal ischemia. Neuroimage32, 1195-1204. doi: 10.1016/j.neuroimage.2006.04.212
65. Tamnes, C. K., Fjell, A. M., Westlye, L. T., Ostby, Y., and Walhovd, K. B. (2012). Becoming consistent: developmental reductions in intraindividual variability in reaction time are related to white matter integrity. J. Neurosci. 32, 972-892. doi: 10.1523/JNEUROSCI.4779-11.2012
66. Taylor, S. J. C., Whincup, P. H., Hindmarsh, P. C., Lampe, F., Odoki, K., and Cook, D. G. (2001). Performance of a new pubertal self-assessment questionnaire: a preliminary study. Paediatr. Perinat. Epidemiol. 15, 88-94. doi: 10.1046/j.1365-3016.2001.00317.x
67. Trudeau, F., and Shephard, R. J. (2008). Physical education, school physical activity, school sports and academic performance. Int. J. Behav. Nutr. Phys. Act. 5, 10. doi: 10.1186/1479-5868-5-10
68. Utter, A. C., Robertson, R. J., Nieman, D. C., and Kang, J. (2002). Children's OMNI scale of perceived exertion: walking/running evaluation. Med. Sci. Sporst Exerc. 34, 139-144. doi: 10.1097/00005768-200201000-00021
69. van Eimeren, L., Niogi, S. N., McCandliss, B. D., Holloway, I. D., and Ansari, D. (2008). White matter microstructures underlying mathematical abilities in children. Neuroreport 19, 1117-1121. doi: 10.1097/WNR.0b013e328307f5c1
70. Voss, M. W., Chaddock, L., Kim, J. S., VanPatter, M., Pontifex, M. B., Raine, L. B., et al. (2011). Aerobic fitness is associated with greater efficiency of the network underlying cognitive control in preadolescent children. Neuroscience 199, 166-176. doi: 10.1016/j.neuroscience.2011.10.009
71. Voss, M. W., Heo, S., Prakash, R. S., Erickson, K. I., Alves, H., Chaddock, L., et al. (2012). The influence of aerobic fitness on cerebral white matter integrity and cognitive function in older adults: results of a one-year exercise intervention. Hum. Brain Mapp. 34, 2972-2985. doi: 10.1002/hbm.22119
72. Wakana, S., Caprihan, A., Panzenboeck, M. M., Fallon, J. H., Perry, M., Gollub, R. L., et al. (2007). Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36, 630-644. doi: 10.1016/j.neuroimage.2007.02.049