Tai Chi Chuan optimizes the functional organization of the intrinsic human brain architecture in older adults

Frontiers in Aging Neuroscience

Volumn 6, Issue APR, 2014, Pages

  Wei, Gao Xia ^a   Dong, Hao Ming ^a,b   Yang, Zhi ^a   Luo, Jing ^a,c   Zuo, Xi Nian ^a  

^a INSTITUTE OF PSYCHOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c CAPITAL NORMAL UNIVERSITY   (China)

Author keywords

Aerobic exercise; Executive function; Functional homogeneity; Meditation; Tai Chi Chuan

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; ATTENTION; BEHAVIOR; BRAIN CORTEX; COGNITION; CONNECTOME; CONTROLLED STUDY; EXECUTIVE FUNCTION; EXPERIENCE; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MAJOR CLINICAL STUDY; MALE; NERVE CELL PLASTICITY; NEUROANATOMY; POSTCENTRAL GYRUS; POSTERIOR CINGULATE; PREFRONTAL CORTEX; RESTING STATE NETWORK; TAI CHI; TASK PERFORMANCE;

EID: 84901353462     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00074     Document Type: Article

References (62)

1. Biswal, B. B., Mennes, M., Zuo, X. N., Gohel, S., Kelly, C., Smith, S. M., et al. (2010). Toward discovery science of human brain function. Proc. Natl. Acad. Sci. U.S.A. 107, 4734-4739. doi: 10.1073/pnas.0911855107
2. Biswal, B., Yetkin, F. Z., Haughton, V. M., and Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537-541. doi: 10.1002/mrm.1910340409
3. Botvinick, M., Nystrom, L. E., Fissell, K., Carter, C. S., and Cohen, J. D. (1999). Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402, 179-181. doi: 10.1038/46035
4. Brewer, J. A., Worhunsky, P. D., Gray, J. R., Tang, Y. Y., Weber, J., and Kober, H. (2011). Meditation experience is associated with differences in default mode network activity and connectivity. Proc. Natl. Acad. Sci. U.S.A. 108, 20254-20259. doi: 10.1073/pnas.1112029108
5. Bush, G., Luu, P., and Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4, 215-222. doi: 10.1016/S1364-6613(00)01483-2
6. Cahn, B. R., and Polich, J. (2006). Meditation states and traits: EEG, ERP, and neuroimaging studies. Psychol. Bull. 132, 180-211. doi: 10.1037/0033-2909.132.2.180
7. Caldwell, K., Harrison, M., Adams, M., and Triplett, N. T. (2009). Effect of Pilates and taiji quan training on self-efficacy, sleep quality, mood, and physical performance of college students. J. Bodyw. Mov. Ther. 13, 155-163. doi: 10.1016/j.jbmt.2007.12.001
8. Chang, Y. K., Nien, Y. H., Tsai, C. L., and Etnier, J. L. (2010). Physical activity and cognition in older adults: the potential of Tai Chi Chuan. J. Aging Phys. Act. 18, 451-472. Pubmed Abstract | Pubmed Full Text
9. Colcombe, S. J., Kramer, A. F., Erickson, K. I., Scalf, P., McAuley, E., Cohen, N. J., et al. (2004a). Cardiovascular fitness, cortical plasticity, and aging. Proc. Natl. Acad. Sci. U.S.A. 101, 3316-3321. doi: 10.1073/pnas.0400266101
10. Colcombe, S. J., Kramer, A. F., McAuley, E., Erickson, K. I., and Scalf, P. (2004b). Neurocognitive aging and cardiovascular fitness: recent findings and future directions. J. Mol. Neurosci. 24, 9-14. doi: 10.1385/JMN:24:1:009
11. Cole, M. W., Reynolds, J. R., Power, J. D., Repovs, G., Anticevic, A., and Braver, T. S. (2013). Multi-task connectivity reveals flexible hubs for adaptive task control. Nat. Neurosci. 16, 1348-1355. doi: 10.1038/nn.3470
12. Cox, R. W. (2012). AFNI: what a long strange trip it's been. Neuroimage 62, 743-747. doi: 10.1016/j.neuroimage.2011.08.056
13. Davis, C. L., Tomporowski, P. D., McDowell, J. E., Miller, P. H., Yanasak, N. E., Allison, J. D., 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
14. Dijkhuizen, R. M., Ren, J., Mandeville, J. B., Wu, O., Ozdag, F. M., Moskowitz, M. A., et al. (2001). Functional magnetic resonance imaging of reorganization in rat brain after stroke. Proc. Natl. Acad. Sci. U.S.A. 98, 12766-12771. doi: 10.1073/pnas.231235598
15. Ding, M. (2012). Tai Chi for stroke rehabilitation: a focused review. Am. J. Phys. Med. Rehabil. 91, 1091-1096. doi: 10.1097/PHM.0b013e31826edd21
16. Fan, J., McCandliss, B. D., Sommer, T., Raz, A., and Posner, M. I. (2002). Testing the efficiency and independence of attentional networks. J. Cogn. Neurosci. 14, 340-347. doi: 10.1162/089892902317361886
17. Field, T., Diego, M., and Hernandez-Reif, M. (2010). Tai chi/yoga effects on anxiety, heartrate, EEG and math computations. Complement. Ther. Clin. Pract. 16, 235-238. doi: 10.1016/j.ctcp.2010.05.014
18. Fischl, B. (2012). FreeSurfer. Neuroimage 62, 774-781. doi: 10.1016/j.neuroimage.2012.01.021
19. Floyer-Lea, A., and Matthews, P. M. (2005). Distinguishable brain activation networks for short- and long-term motor skill learning. J. Neurophysiol. 94, 512-518. doi: 10.1152/jn.00717.2004
20. Fox, M. D., and Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700-711. doi: 10.1038/nrn2201
21. Gehring, W. J., Goss, B., Coles, M. G. H., Meyer, D. E., and Donchin, E. (1993). A neural system for error detection and compensation. Psychol. Sci. 4, 385-390. doi: 10.1111/j.1467-9280.1993.tb00586.x CrossRef Full Text
22. Glasser, M. F., and Van Essen, D. C. (2011). Mapping human cortical areas in vivo based on myelin content as revealed by T1-and T2-weighted MRI. J. Neurosci. 31, 11597-11616. doi: 10.1523/JNEUROSCI.2180-11.2011
23. Grafton, S. T., Hazeltine, E., and Ivry, R. (1995). Functional mapping of sequence learning in normal humans. J. Cogn. Neurosci. 7, 497-510. doi: 10.1162/jocn.1995.7.4.497
24. Greve, D. N., and Fischl, B. (2009). Accurate and robust brain image alignment using boundary-based registration. Neuroimage 48, 63-72. doi: 10.1016/j.neuroimage.2009.06.060
25. Jang, J. H., Jung, W. H., Kang, D. H., Byun, M. S., Kwon, S. J., Choi, C. H., et al. (2011). Increased default mode network connectivity associated with meditation. Neurosci. Lett. 487, 358-362. doi: 10.1016/j.neulet.2010.10.056
26. Jenkinson, M., Beckmann, C. F., Behrens, T. E., Woolrich, M. W., and Smith, S. M. (2012). FSL. Neuroimage 62, 782-790. doi: 10.1016/j.neuroimage.2011.09.015
27. Kerr, C. E., Shaw, J. R., Wasserman, R. H., Chen, V. W., Kanojia, A., Bayer, T., et al. (2008). Tactile acuity in experienced Tai Chi practitioners: evidence for use dependent plasticity as an effect of sensory-attentional training. Exp. Brain Res. 188, 317-322. doi: 10.1007/s00221-008-1409-6
28. Kramer, A. F., Hahn, S., Cohen, N. J., Banich, M. T., McAuley, E., Harrison, C. R., et al. (1999). Ageing, fitness and neurocognitive function. Nature 400, 418-419. doi: 10.1038/22682
29. Lee, M. S., and Ernst, E. (2012). Systematic reviews of t'ai chi: an overview. Br. J. Sports Med. 46, 713-718. doi: 10.1136/bjsm.2010.080622
30. Li, F., Harmer, P., Fisher, K. J., and McAuley, E. (2004). Tai Chi: improving functional balance and predicting subsequent falls in older persons. Med. Sci. Sports Exerc. 36, 2046-2052. doi: 10.1249/01.MSS.0000147590.54632.E7
31. Li, H. J., Cao, X. H., Zhu, X. T., Zhang, A. X., Hou, X. H., Xu, Y., et al. (2014). Surface-based regional homogeneity in first-episode, drug-naive major depression: a resting-state fMRI study. Biomed. Res. Int. 2014:374828. doi: 10.1155/2014/374828
32. Liu, Y., Mimura, K., Wang, L., and Ikuda, K. (2003). Physiological benefits of 24-style Taijiquan exercise in middle-aged women. J. Physiol. Anthropol. Appl. Human Sci. 22, 219-225. doi: 10.2114/jpa.22.219
33. Luders, E., Clark, K., Narr, K. L., and Toga, A. W. (2011). Enhanced brain connectivity in long-term meditation practitioners. Neuroimage 57, 1308-1316. doi: 10.1016/j.neuroimage.2011.05.075
34. Luders, E., Phillips, O. R., Clark, K., Kurth, F., Toga, A. W., and Narr, K. L. (2012). Bridging the hemispheres in meditation: thicker callosal regions and enhanced fractional anisotropy (FA) in long-term practitioners. Neuroimage 61, 181-187. doi: 10.1016/j.neuroimage.2012.02.026
35. Luders, E., Toga, A. W., Lepore, N., and Gaser, C. (2009). The underlying anatomical correlates of long-term meditation: larger hippocampal and frontal volumes of gray matter. Neuroimage 45, 672-678. doi: 10.1016/j.neuroimage.2008.12.061
36. Matthews, M. M., and Williams, H. G. (2008). Can Tai chi enhance cognitive vitality? A preliminary study of cognitive executive control in older adults after A Tai chi intervention. J. S. C. Med. Assoc. 104, 255-257. Pubmed Abstract | Pubmed Full Text
37. Patriat, R., Molloy, E. K., Meier, T. B., Kirk, G. R., Nair, V. A., Meyerand, M. E., et al. (2013). The effect of resting condition on resting-state fMRI reliability and consistency: a comparison between resting with eyes open, closed, and fixated. Neuroimage 78, 463-473. doi: 10.1016/j.neuroimage.2013.04.013
38. Petersen, S., and Posner, M. (2012). The attention system of the human brain: 20 years after. Annu. Rev. Neurosci. 35, 73-89. doi: 10.1146/annurev-neuro-062111-150525
39. Posner, M. I., and DiGirolamo, G. J. (1998). "Executive attention: Conflict, target detection and cognitive control," in The Attentive Brain, ed. R. Parasuraman (Cambridge, MA: MIT Press), 401-423.
40. Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., and Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59, 2142-2154. doi: 10.1016/j.neuroimage.2011.10.018
41. Raichle, M. E. (2010). Two views of brain function. Trends Cogn. Sci. 14, 180-190. doi: 10.1016/j.tics.2010.01.008
42. Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676-682. doi: 10.1073/pnas.98.2.676
43. Robins, J. L. W., Elswick, R. K., and McCain, N. L. (2012). The story of the evolution of a unique tai chi form: origins, philosophy, and research. J. Holist. Nurs. 30, 134-146. doi: 10.1177/0898010111429850
44. Satterthwaite, T. D., Elliott, M. A., Gerraty, R. T., Ruparel, K., Loughead, J., Calkins, M. E., et al. (2013). An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 64, 240-256. doi: 10.1016/j.neuroimage.2012.08.052
45. Szeszko, P. R., Bilder, R. M., Lencz, T., Ashtari, M., Goldman, R. S., Reiter, G., et al. (2000). Reduced anterior cingulate gyrus volume correlates with executive dysfunction in men with first-episode schizophrenia. Schizophr. Res. 43, 97-108. doi: 10.1016/S0920-9964(99)00155-3
46. Tang, Y. Y., Lu, Q., Geng, X., Stein, E. A., Yang, Y., and Posner, M. I. (2010). Short-term meditation induces white matter changes in the anterior cingulate. Proc. Natl. Acad. Sci. U.S.A. 107, 15649-15652. doi: 10.1073/pnas.1011043107
47. Tang, Y. Y., Ma, Y., Fan, Y., Feng, H., Wang, J., Feng, S., et al. (2009). Central and autonomic nervous system interaction is altered by short-term meditation. Proc. Natl. Acad. Sci. U.S.A. 106, 8865-8870. doi: 10.1073/pnas.0904031106
48. Taylor-Piliae, R. E., and Froelicher, E. S. (2004). Effectiveness of Tai Chi exercise in improving aerobic capacity: a meta-analysis. J. Cardiovasc. Nurs. 19, 48-57. doi: 10.1097/00005082-200401000-00009
49. Taylor-Piliae, R. E., Haskell, W. L., Waters, C. M., and Froelicher, E. S. (2006). Change in perceived psychosocial status following a 12-week Tai Chi exercise programme. J. Adv. Nurs. 54, 313-329. doi: 10.1111/j.1365-2648.2006.03809.x
50. Taylor-Piliae, R. E., Newell, K. A., Cherin, R., Lee, M. J., King, A. C., and Haskell, W. L. (2010). Effects of Tai Chi and Western exercise on physical and cognitive functioning in healthy community-dwelling older adults. J. Aging Phys. Act. 18, 261-279.
51. Taylor, V. A., Daneault, V., Grant, J., Scavone, G., Breton, E., Roffe-Vidal, S., et al. (2013). Impact of meditation training on the default mode network during a restful state. Soc. Cogn. Affect. Neurosci. 8, 4-14. doi: 10.1093/scan/nsr087
52. Travis, F., Haaga, D. A., Hagelin, J., Tanner, M., Arenander, A., Nidich, S., et al. (2010). A self-referential default brain state: patterns of coherence, power, and eLORETA sources during eyes-closed rest and Transcendental Meditation practice. Cogn. Process. 11, 21-30. doi: 10.1007/s10339-009-0343-2
53. Tsang, W. W., Wong, V. S., Fu, S. N., and Hui-Chan, C. W. (2004). Tai Chi improves standing balance control under reduced or conflicting sensory conditions. Arch. Phys. Med. Rehabil. 85, 129-137. doi: 10.1016/j.apmr.2003.02.002
54. Wei, G. X., Xu, T., Fan, F. M., Dong, H. M., Jiang, L. L., Li, H. J., et al. (2013). Can taichi reshape the brain? A brain morphometry study. PLoS ONE 8:e61038. doi: 10.1371/journal.pone.0061038
55. Weissman, D. H., Gopalakrishnan, A., Hazlett, C. J., and Woldorff, M. G. (2005). Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. Cereb. Cortex 15, 229-237. doi: 10.1093/cercor/bhh125
56. Wong, A. M., Pei, Y. C., Lan, C., Huang, S. C., Lin, Y. C., and Chou, S. W. (2009). Is Tai Chi Chuan effective in improving lower limb response time to prevent backward falls in the elderly? Age (Dordr.) 31, 163-170. doi: 10.1007/s11357-009-9094-3
57. Yan, C. G., Cheung, B., Kelly, C., Colcombe, S., Craddock, R. C., Di Martino, A., et al. (2013). A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage 76, 183-201. doi: 10.1016/j.neuroimage.2013.03.004
58. Yanagisawa, H., Dan, I., Tsuzuki, D., Kato, M., Okamoto, M., Kyutoku, Y., et al. (2010). Acute moderate exercise elicits increased dorsolateral prefrontal activation and improves cognitive performance with Stroop test. Neuroimage 50, 1702-1710. doi: 10.1016/j.neuroimage.2009.12.023
59. Zang, Y., Jiang, T., Lu, Y., He, Y., and Tian, L. (2004). Regional homogeneity approach to fMRI data analysis. Neuroimage 22, 394-400. doi: 10.1016/j.neuroimage.2003.12.030
60. Zhang, D., and Raichle, M. E. (2010). Disease and the brain's dark energy. Nat. Rev. Neurol. 6, 15-28. doi: 10.1038/nrneurol.2009.198
61. Zuo, X. N., Ehmke, R., Mennes, M., Imperati, D., Castellanos, F. X., Sporns, O., et al. (2012). Network centrality in the human functional connectome. Cereb. Cortex 22, 1862-1875. doi: 10.1093/cercor/bhr269
62. Zuo, X. N., Xu, T., Jiang, L., Yang, Z., Cao, X. Y., He, Y., et al. (2013). Toward reliable characterization of functional homogeneity in the human brain: preprocessing, scan duration, imaging resolution and computational space. Neuroimage 65, 374-386. doi: 10.1016/j.neuroimage.2012.10.017