The exercising brain: Changes in functional connectivity induced by an integrated multimodal cognitive and whole-body coordination training

Neural Plasticity

Volumn 2016, Issue , 2016, Pages

  Demirakca, Traute ^a   Cardinale, Vita ^a   Dehn, Sven ^a   Ruf, Matthias ^a   Ende, Gabriele ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; COORDINATION; DEFAULT MODE NETWORK; DIENCEPHALON; EXERCISE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MEDIAL FRONTAL CORTEX; PLANT SEED; PLASTICITY; POSTERIOR CINGULATE; REST; VISUAL CORTEX; WORKING MEMORY; ADULT; BRAIN MAPPING; COGNITION; CONNECTOME; FEMALE; IMAGE PROCESSING; MALE; MIDDLE AGED; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; SHORT TERM MEMORY;

ADULT; BRAIN; BRAIN MAPPING; COGNITION; CONNECTOME; EXERCISE; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; MIDDLE AGED; NERVE NET;

EID: 84957083522     PISSN: 20905904     EISSN: 16875443     Source Type: Journal    
DOI: 10.1155/2016/8240894     Document Type: Article

References (80)

1. D. O. Hebb, The Organization of Behavior: A Neuropsychological Theory, Psychology Press, New York, NY, USA, 1949.
2. G. Kempermann, H. G. Kuhn, and F. H. Gage, "More hippocampal neurons in adult mice living in an enriched environment," Nature, vol. 386, no. 6624, pp. 493-495, 1997.
3. C. S. Green and D. Bavelier, "Exercising your brain: a review of human brain plasticity and training-induced learning," Psychology and Aging, vol. 23, no. 4, pp. 692-701, 2008.
4. D. Bavelier, D. M. Levi, R. W. Li, Y. Dan, and T. K. Hensch, "Removing brakes on adult brain plasticity: from molecular to behavioral interventions," Journal of Neuroscience, vol. 30, no. 45, pp. 14964-14971, 2010.
5. A. Gutchess, "Plasticity of the aging brain: new directions in cognitive neuroscience," Science, vol. 346, no. 6209, pp. 579-582, 2014.
6. R. J. Zatorre, R. D. Fields, and H. Johansen-Berg, "Plasticity in gray andwhite: neuroimaging changes in brain structure during learning," Nature Neuroscience, vol. 15, no. 4, pp. 528-536, 2012.
7. A. May, "Experience-dependent structural plasticity in the adult human brain," Trends in Cognitive Sciences, vol. 15, no. 10, pp. 475-482, 2011.
8. M. Spolidoro, A. Sale, N. Berardi, and L. Maffei, "Plasticity inthe adult brain:lessons from the visual system," Experimental Brain Research, vol. 192, no. 3, pp. 335-341, 2009.
9. B. Guerra-Carrillo, A. P. MacKey, and S. A. Bunge, "Restingstate fMRI: a window into human brain plasticity," Neuroscientist, vol. 20, no. 5, pp. 522-533, 2014.
10. C. Kelly and F. X. Castellanos, "Strengthening connections: functional connectivity and brain plasticity," Neuropsychology Review, vol. 24, no. 1, pp. 63-76, 2014.
11. B. Biswal, F. Z. Yetkin, V. M. Haughton, and J. S. Hyde, "Functional connectivity in the motor cortex of resting human brain using echo-planar MRI,"Magnetic Resonance inMedicine, vol. 34, no. 4, pp. 537-541, 1995.
12. M. J. Lowe, "The emergence of doing nothing as a viable paradigm design," Neuro Image, vol. 62, no. 2, pp. 1146-1151, 2012.
13. A. Z. Snyder and M. E. Raichle, "A brief history of the resting state: theWashington University perspective," Neuro Image, vol. 62, no. 2, pp. 902-910, 2012.
14. M. D. Fox and M. E. Raichle, "Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging," Nature Reviews Neuroscience, vol. 8, no. 9, pp. 700-711, 2007.
15. N. B. Albert, E. M. Robertson, and R. C. Miall, "The resting human brain and motor learning," Current Biology, vol. 19, no. 12, pp. 1023-1027, 2009.
16. K. Yoo, W. S. Sohn, and Y. Jeong, "Tool-use practice induces changes in intrinsic functional connectivity of parietal areas," Frontiers in Human Neuroscience, vol. 7, article 49, 2013.
17. L. Ma, S. Narayana, D. A. Robin, P. T. Fox, and J. Xiong, "Changes occur in resting state network of motor systemduring weeks of motor skill learning," Neuro Image, vol. 58, no. 1, pp. 226-233, 2011.
18. S. Vahdat, M. Darainy, T. E. Milner, and D. J. Ostry, "Functionally specific changes in resting-state sensorimotor networks after motor learning," Journal of Neuroscience, vol. 31, no. 47, pp. 16907-16915, 2011.
19. M. Taubert, G. Lohmann, D. S. Margulies, A. Villringer, and P. Ragert, "Long-term effects of motor training on resting-state networks and underlying brain structure," Neuro Image, vol. 57, no. 4, pp. 1492-1498, 2011.
20. M. W. Voss, R. S. Prakash, K. I. Erickson et al., "Plasticity of brain networks in a randomized intervention trial of exercise training in older adults," Frontiers in Aging Neuroscience, vol. 2, article 32, 2010.
21. H. Takeuchi, Y. Taki, R. Nouchi et al., "Effects of working memory training on functional connectivity and cerebral blood flow during rest," Cortex, vol. 49, no. 8, pp. 2106-2125, 2013.
22. D. D. Jolles, M. A. van Buchem, E. A. Crone, and S. A. R. B. Rombouts, "Functional brain connectivity at rest changes after working memory training," Human Brain Mapping, vol. 34, no. 2, pp. 396-406, 2013.
23. H. Takeuchi, Y. Taki, R. Nouchi et al., "Effects of multitaskingtraining on gray matter structure and resting state neural mechanisms," Human Brain Mapping, vol. 35, no. 8, pp. 3646-3660, 2014.
24. A. P. Mackey, A. T. M. Singley, and S. A. Bunge, "Intensive reasoning training alters patterns of brain connectivity at rest," Journal of Neuroscience, vol. 33, no. 11, pp. 4796-4803, 2013.
25. K. Martinez, A. B. Solana, M. Burgaleta et al., "Changes in resting-state functionally connected parietofrontal networks after videogame practice," Human Brain Mapping, vol. 34, no. 12, pp. 3143-3157, 2013.
26. T. Harmelech, S. Preminger, E. Wertman, and R. Malach, "The day-after effect: long term, hebbian-like restructuring of resting-state fMRI patterns induced by a single epoch of cortical activation," Journal of Neuroscience, vol. 33, no. 22, pp. 9488-9497, 2013.
27. F. Megumi, A. Yamashita, M. Kawato, and H. Imamizu, "Functional MRI neurofeedback training on connectivity between two regions induces long-lasting changes in intrinsic functional network," Frontiers in Human Neuroscience, vol. 9, article 160, 2015.
28. E. Kraft, "Cognitive function, physical activity, and aging: possible biological links and implications formultimodal interventions," Aging, Neuropsychology, andCognition, vol. 19, no. 1-2, pp. 248-263, 2012.
29. K. Hötting and B. Röder, "Beneficial effects of physical exercise on neuroplasticity and cognition," Neuroscience and Biobehavioral Reviews, vol. 37, no. 9, pp. 2243-2257, 2013.
30. R. Li, X. Zhu, S. Yin et al., "Multimodal intervention in older adults improves resting-state functional connectivity between the medial prefrontal cortex and medial temporal lobe," Frontiers in Aging Neuroscience, vol. 6, article 39, 2014.
31. K. Holzschneider, T. Wolbers, B. Röder, and K. Hötting, "Cardiovascular fitness modulates brain activation associated with spatial learning," Neuro Image, vol. 59, no. 3, pp. 3003-3014, 2012.
32. C. M. Lewis, A. Baldassarre, G. Committeri, G. L. Romani, and M. Corbetta, "Learning sculpts the spontaneous activity of the resting human brain," Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 41, pp. 17558-17563, 2009.
33. T. E. J. Behrens, H. Johansen-Berg, M. W. Woolrich et al., "Noninvasive mapping of connections between human thalamus and cortex using diffusion imaging," Nature Neuroscience, vol. 6, no. 7, pp. 750-757, 2003.
34. R. Fama and E. V. Sullivan, "Thalamic structures and associated cognitive functions: relations with age and aging," Neuroscience and Biobehavioral Reviews, vol. 54, pp. 29-37, 2015.
35. B. Zhou, Y. Liu, Z. Zhang et al., "Impaired functional connectivity of the thalamus in Alzheimer s disease and mild cognitive impairment: a resting-state FMRI study," Current Alzheimer Research, vol. 10, no. 7, pp. 754-766, 2013.
36. Z. Wang, X. Jia, P. Liang et al., "Changes in thalamus connectivity in mild cognitive impairment: evidence fromresting state fMRI," European Journal of Radiology, vol. 81, no. 2, pp. 277-285, 2012.
37. R. L. Buckner, F. M. Krienen, A. Castellanos, J. C. Diaz, and B. T. Thomas Yeo, "The organization of the human cerebellum estimated by intrinsic functional connectivity," Journal of Neurophysiology, vol. 106, no. 5, pp. 2322-2345, 2011.
38. J. X. OReilly, C. F. Beckmann, V. Tomassini, N. Ramnani, and H. Johansen-Berg, "Distinct and overlapping functional zones in the cerebellumdefined by resting state functional connectivity," Cerebral Cortex, vol. 20, no. 4, pp. 953-965, 2010.
39. J. Pa, S. Dutt, J. B. Mirsky et al., "The functional oculomotor network and saccadic cognitive control in healthy elders," Neuro Image, vol. 95, pp. 61-68, 2014.
40. R. M. Hutchison, J. P. Gallivan, J. C. Culham, J. S. Gati, R. S. Menon, and S. Everling, "Functional connectivity of the frontal eye fields in humans and macaque monkeys investigated with resting-state fMRI," Journal of Neurophysiology, vol. 107, no. 9, pp. 2463-2474, 2012.
41. E. J. Anderson, D. K. Jones, R. L. OGorman, A. Leemans, M. Catani, and M. Husain, "Cortical network for gaze control in humans revealed using multimodal MRI," Cerebral Cortex, vol. 22, no. 4, pp. 765-775, 2012.
42. J. Ashburner, "A fast diffeomorphic image registration algorithm," Neuro Image, vol. 38, no. 1, pp. 95-113, 2007.
43. S. Whitfield-Gabrieli and A. Nieto-Castanon, "Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks," Brain Connectivity, vol. 2, no. 3, pp. 125-141, 2012.
44. W. R. Shirer, H. Jiang, C. M. Price, B. Ng, and M. D. Greicius, "Optimization of rs-fMRI pre-processing for enhanced signalnoise separation, test-retest reliability, and group discrimination," Neuro Image, vol. 117, pp. 67-79, 2015.
45. Y. Behzadi, K. Restom, J. Liau, and T. T. Liu, "Acomponentbased noise correction method (CompCor) for BOLD and perfusion based fMRI," Neuro Image, vol. 37, no. 1, pp. 90-101, 2007.
46. Z. Qing, Z. Dong, S. Li, Y. Zang, and D. Liu, "Global signal regression has complex effects on regional homogeneity of resting state fMRI signal," Magnetic Resonance Imaging, 2015.
47. O. Agcaoglu, R. Miller, A. R. Mayer, K. Hugdahl, and V. D. Calhoun, "Lateralization of resting state networks and relationship to age and gender," Neuro Image, vol. 104, pp. 310-325, 2015.
48. C. Luo, Z.-W. Guo, Y.-X. Lai et al., "Musical training induces functional plasticity in perceptual andmotor networks: insights from resting-state fMRI," PLoS ONE, vol. 7, no. 5, Article ID e36568, 2012.
49. C. Sampaio-Baptista, A. A. Khrapitchev, S. Foxley et al., "Motor skill learning induces changes in white matter microstructure and myelination," Journal of Neuroscience, vol. 33, no. 50, pp. 19499-19503, 2013.
50. C. Sampaio-Baptista, N. Filippini, C. J. Stagg, J. Near, J. Scholz, And H. Johansen-Berg, "Changes in functional connectivity and GABA levels with long-term motor learning," Neuro Image, vol. 106, pp. 15-20, 2015.
51. B. Draganski, C. Gaser, V. Busch, G. Schuierer, U. Bogdahn, and A. May, "Neuroplasticity: changes in grey matter induced by training," Nature, vol. 427, no. 6972, pp. 311-312, 2004.
52. J. C. Culham and N. G. Kanwisher, "Neuroimaging of cognitive functions in human parietal cortex," Current Opinion in Neurobiology, vol. 11, no. 2, pp. 157-163, 2001.
53. O. Simon, J.-F. Mangin, L. Cohen, D. Le Bihan, and S. Dehaene, "Topographical layout of hand, eye, calculation, and languagerelated areas in the human parietal lobe," Neuron, vol. 33, no. 3, pp. 475-487, 2002.
54. A. Bartels and S. Zeki, "Brain dynamics during natural viewing conditions-a new guide for mapping connectivity in vivo," Neuro Image, vol. 24, no. 2, pp. 339-349, 2005.
55. M.-T. Herrero, C. Barcia, and J. M. Navarro, "Functional anatomy of thalamus and basal ganglia," Childs Nervous System, vol. 18, no. 8, pp. 386-404, 2002.
56. L. Hearne, L. Cocchi, A. Zalesky, and J. B. Mattingley, "Interactions between default mode and control networks as a function of increasing cognitive reasoning complexity," Human Brain Mapping, vol. 36, no. 7, pp. 2719-2731, 2015.
57. L. Bonzano, E. Palmaro, R. Teodorescu, L. Fleysher, M. Inglese, and M. Bove, "Functional connectivity in the resting-state motor networks influences the kinematic processes during motor sequence learning," European Journal of Neuroscience, vol. 41, no. 2, pp. 243-253, 2015.
58. N. C. Andreasen, "The role of the thalamus in schizophrenia," Canadian Journal of Psychiatry, vol. 42, no. 1, pp. 27-33, 1997.
59. J. D. Schmahmann and D. N. Pandya, "Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems," Cortex, vol. 44, no. 8, pp. 1037-1066, 2008.
60. H. S. Wang, C. Rau, Y. Li, Y. Chen, and R. Yu, "Disrupted thalamic resting-state functional networks in schizophrenia," Frontiers in Behavioral Neuroscience, vol. 9, article 45, 2015.
61. C. Solé-Padullés, D. Bartrés-Faz, C. Junqué et al., "Brain structure and function related to cognitive reserve variables in normal aging, mild cognitive impairment and Alzheimers disease," Neurobiology ofAging, vol. 30, no. 7, pp. 1114-1124, 2009.
62. C.-Y. C. Sylvester, T. D. Wager, S. C. Lacey et al., "Switching attention and resolving interference: fMRI measures of executive functions," Neuropsychologia, vol. 41, no. 3, pp. 357-370, 2003.
63. M. E. Raichle, "The restless brain: how intrinsic activity organizes brain function," Philosophical Transactions of the Royal Society of London Series B: Biological Sciences, vol. 370, no. 1668, 2015.
64. D. Zhang and M. E. Raichle, "Disease and the brains dark energy," Nature Reviews Neurology, vol. 6, no. 1, pp. 15-28, 2010.
65. E. Solesio-Jofre, L. Serbruyns, D. G. Woolley, D. Mantini, I. A. M. Beets, and S. P. Swinnen, "Aging effects on the resting statemotor network and interlimb coordination," Human Brain Mapping, vol. 35, no. 8, pp. 3945-3961, 2014.
66. R. Seidler, B. Erdeniz, V. Koppelmans, S. Hirsiger, S. Mérillat, and L. Jäncke, "Associations between age, motor function, and resting state sensorimotor network connectivity in healthy older adults," Neuro Image, vol. 108, pp. 47-59, 2015.
67. O. Ajilore, M. Lamar, and A. Kumar, "Association of brain network efficiency with aging, depression, and cognition," The American Journal of Geriatric Psychiatry, vol. 22, no. 2, pp. 102-110, 2014.
68. Z. Zheng, X. Zhu, S. Yin et al., "Combined cognitive-psychological-physical intervention induces reorganization of intrinsic functional brain architecture in older adults," Neural Plasticity, vol. 2015, Article ID713104, 11 pages, 2015.
69. A. Lampit, H. Hallock, C. Suo, S. L. Naismith, and M. Valenzuela, "Cognitive training-induced short-term functional and long-term structural plastic change is related to gains in global cognition in healthy older adults: a pilot study," Frontiers in Aging Neuroscience, vol. 7, article 014, 2015.
70. M. W. Cole, T. Yarkoni, G. Repovš, A. Anticevic, and T. S. Braver, "Global connectivity of prefrontal cortex predicts cognitive control and intelligence,"The Journal of Neuroscience, vol. 32, no. 26, pp. 8988-8999, 2012.
71. Y. I. Sheline, J. L. Price, Z. Yan, and M. A. Mintun, "Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus," Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 24, pp. 11020-11025, 2010.
72. M. W. Voss, K. I. Erickson, R. S. Prakash et al., "Functional connectivity: a source of variance in the association between cardiorespiratory fitness and cognition?" Neuropsychologia, vol. 48, no. 5, pp. 1394-1406, 2010.
73. T. D. Ben-Soussan, A. Berkovich-Ohana, J. Glicksohn, and A. Goldstein, "A suspended act: increased reflectivity and genderdependent electrophysiological change following Quadrato Motor Training," Frontiers in Psychology, vol. 5, article 55, 2014.
74. C. M. Bennett and M. B. Miller, "How reliable are the results from functional magnetic resonance imaging?" Annals of the New York Academy of Sciences, vol. 1191, pp. 133-155, 2010.
75. K. J. Gorgolewski, A. J. Storkey, M. E. Bastin, I. Whittle, and C. Pernet, "Single subject fMRI test-retest reliability metrics and confounding factors," Neuro Image, vol. 69, pp. 231-243, 2013.
76. R. Maitra, S. R. Roys, and R. P. Gullapalli, "Test-retest reliability estimation of functional MRI data," Magnetic Resonance in Medicine, vol. 48, no. 1, pp. 62-70, 2002.
77. M. Raemaekers, S. du Plessis, N. F. Ramsey, J. M. H. Weusten, And M. Vink, "Test-retest variability underlying fMRI measurements," Neuro Image, vol. 60, no. 1, pp. 717-727, 2012.
78. Z. Shehzad, A. M. C. Kelly, P. T. Reiss et al., "The resting brain: unconstrained yet reliable," Cerebral Cortex, vol. 19, no. 10, pp. 2209-2229, 2009.
79. K. Murphy, R. M. Birn, and P. A. Bandettini, "Resting-state fMRI confounds and cleanup," Neuro Image, vol. 80, pp. 349-359, 2013.
80. X.-N. Zuo and X.-X. Xing, "Test-retest reliabilities of restingstate FMRI measurements in human brain functional connectomics: a systems neuroscience perspective," Neuroscience and Biobehavioral Reviews C, vol. 45, pp. 100-118, 2014.