Increased hippocampus-medial prefrontal cortex resting-state functional connectivity and memory function after Tai Chi Chuan practice in elder adults

Frontiers in Aging Neuroscience

Volumn 8, Issue FEB, 2016, Pages

  Tao, Jing ^a,b,c   Liu, Jiao ^a   Egorova, Natalia ^c   Chen, Xiangli ^d   Sun, Sharon ^c   Xue, Xiehua ^a   Huang, Jia ^a,b   Zheng, Guohua ^a   Wang, Qin ^a   Chen, Lidian ^a,b   Kong, Jian ^c  

^a FUJIAN NORMAL UNIVERSITY   (China)

^b Fujian Key Laboratory of Microelectronic IC   (China)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Aging; Baduanjin exercise; Hippocampus; Medial prefrontal cortex; Memory function; Tai Chi Chuan exercise

Indexed keywords

ADULT; AGED; ARTICLE; BADUANJIN; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; KINESIOTHERAPY; LEFT HEMISPHERE; MALE; MEDIAL PREFRONTAL CORTEX; MEMORY; NORMAL HUMAN; RANDOMIZED CONTROLLED TRIAL; RESTING STATE NETWORK; RIGHT HEMISPHERE; TAI CHI; WECHSLER MEMORY SCALE;

EID: 84960128218     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2016.00025     Document Type: Article

References (74)

1. Aggleton, J. (2014). Looking beyond the hippocampus: old and new neurological targets for understanding memory disorders. Proc. Biol. Sci. 281, 1-9. doi: 10.1098/rspb.2014.0565.
2. Amodio, D. M., and Frith, C. D. (2006). Meeting of minds: the medial frontal cortex and social cognition. Nat. Rev. Neurosci. 7, 268-277. doi:10.1038/nrn1884.
3. Babakchanian, S., Woo, E., Kebets, V., Green, A., Zoumalan, C., Wang, B., et al. (2012). Age effects on cortical thickness in cognitively normal elderly individuals (P03.103). Neurology 78, 03.103. doi:10.1212/WNL.78.1_MeetingAbstracts. P03.103.
4. Bañuelos, C., Beas, B. S., McQuail, J. A., Gilbert, R. J., Frazier, C. J., Setlow, B., et al. (2014). Prefrontal cortical GABAergic dysfunction contributes to -age-related working memory impairment. J. Neurosci. 34, 3457-3466. doi:10.1523/JNEUROSCI.5192-13.2014.
5. Bein, O., Reggev, N., and Maril, A. (2014). Prior knowledge influences on hippocampus and medial prefrontal cortex interactions in subsequent memory. Neuropsychologia 64, 320-330. doi:10.1016/j.neuropsychologia.2014.09.046.
6. Bird, C. M., and Burgess, N. (2008). The hippocampus and memory: insights from spatial processing. Nat. Rev. Neurosci. 9, 182-194. doi:10.1038/nrn2335.
7. Black, D. S., Irwin, M. R., Olmstead, R., Ji, E., Crabb Breen, E., and Motivala, S. J. (2014). Tai Chi meditation effects on nuclear factor-κB signaling in lonely older adults: a randomized controlled trial. Psychother. Psychosom. 83, 315-317. doi:10.1159/000359956.
8. Brod, G., Werkle-Bergner, M., and Shing, Y. L. (2013). The influence of prior knowledge on memory: a developmental cognitive neuroscience perspective. Front. Behav. Neurosci. 7:139. doi:10.3389/fnbeh.2013.00139.
9. Buckner, R. L., Andrews-Hanna, J. R., and Schacter, D. L. (2008). The brain's default network: anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 1124, 1-38. doi:10.1196/annals.1440.011.
10. Burdette, J. H., Laurienti, P. J., Espeland, M. A., Morgan, A., Telesford, Q., Vechlekar, C. D., et al. (2010). Using network science to evaluate -exercise-associated brain changes in older adults. Front. Aging Neurosci. 2:23. doi:10.3389/fnagi.2010.00023.
11. Burgess, N., Maguire, E. A., and O'Keefe, J. (2002). The human hippocampus and spatial and episodic memory. Neuron 35, 625-641. doi:10.1016/S0896-6273(02)00830-9.
12. Cheng, F. K. (2015). Effects of Baduanjin on mental health: a comprehensive review. J. Bodyw. Mov. Ther. 19, 138-149. doi:10.1016/j.jbmt.2014.11.001.
13. China National Sports Commission. (1983). Simplified Taijiquan. Beijing: People's Sports Press.
14. Churchwell, J. C., and Kesner, R. P. (2011). Hippocampal-prefrontal dynamics in spatial working memory: interactions and independent parallel processing. Behav. Brain Res. 225, 389-395. doi:10.1016/j.bbr.2011.07.045.
15. Corbetta, M., and Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201-215. doi:10.1038/nrn755.
16. Erickson, K. I., Voss, M. W., Prakash, R. S., Basak, C., Szabo, A., Chaddock, L., et al. (2011). Exercise training increases size of hippocampus and improves memory. Proc. Natl. Acad. Sci. U.S.A. 108, 3017-3022. doi:10.1073/pnas.1015950108.
17. Flöel, A., Ruscheweyh, R., Krüger, K., Willemer, C., Winter, B., Völker, K., et al. (2010). Physical activity and memory functions: are neurotrophins and cerebral gray matter volume the missing link? Neuroimage 49, 2756-2763. doi:10.1016/j.neuroimage.2009.10.043.
18. Folstein, M. F., Folstein, S. E., and McHugh, P. R. (1975). "Mini-Mental State". A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189-198. doi:10.1016/0022-3956(75)90026-6.
19. Fong, D.-Y., Chi, L.-K., Li, F., and Chang, Y.-K. (2014). The benefits of endurance exercise and Tai Chi Chuan for the task-switching aspect of executive function in older adults: an ERP study. Front. Aging Neurosci. 6:295. doi:10.3389/fnagi.2014.00295.
20. Gong, Y., and Wang, D. J. (1989). Handbook of Wechsler Memory Scale-Revised. Changsha: Bulletin.
21. Griffin, A. L. (2015). Role of the thalamic nucleus reuniens in mediating interactions between the hippocampus and medial prefrontal cortex during spatial working memory. Front. Syst. Neurosci. 9:29. doi:10.3389/fnsys.2015.00029.
22. Gutchess, A. H., Kensinger, E. A., and Schacter, D. L. (2007). Aging, self-referencing, and medial prefrontal cortex. Soc. Neurosci. 2, 117-133. doi:10.1080/17470910701399029.
23. Hayes, S. M., Hayes, J. P., Cadden, M., and Verfaellie, M. (2013). A review of cardiorespiratory fitness-related neuroplasticity in the aging brain. Front. Aging Neurosci. 5:31. doi:10.3389/fnagi.2013.00031.
24. Health Qigong Management Center of General Administration of Sport of China. (2003). Health Qigong-Baduanjin. Beijing: People's Sports Publishing House of China.
25. Hölzel, B. K., Ott, U., Gard, T., Hempel, H., Weygandt, M., Morgen, K., et al. (2008). Investigation of mindfulness meditation practitioners with voxel-based morphometry. Soc. Cogn. Affect. Neurosci. 3, 55-61. doi:10.1093/scan/nsm038.
26. Hyman, J. M., Hasselmo, M. E., and Seamans, J. K. (2011). What is the functional relevance of prefrontal cortex entrainment to hippocampal theta rhythms? Front. Neurosci. 5:24. doi:10.3389/fnins.2011.00024.
27. Kaplan, R., Bush, D., Bonnefond, M., Bandettini, P. A., Barnes, G. R., Doeller, C. F., et al. (2014). Medial prefrontal theta phase coupling during spatial memory retrieval. Hippocampus 24, 656-665. doi:10.1002/hipo.22255.
28. Kelly, M. E., Loughrey, D., Lawlor, B. A., Robertson, I. H., Walsh, C., and Brennan, S. (2014). The impact of exercise on the cognitive functioning of healthy older adults: a systematic review and meta-analysis. Aging Res. Rev. 16, 12-31. doi:10.1016/j.arr.2014.05.002.
29. Kim, S., Dede, A. J. O., Hopkins, R. O., and Squire, L. R. (2015). Memory, scene construction, and the human hippocampus. Proc. Natl. Acad. Sci. U.S.A. 112, 201503863. doi:10.1073/pnas.1503863112.
30. Kumaran, D., and Maguire, E. A. (2005). The human hippocampus: cognitive maps or relational memory? J. Neurosci. 25, 7254-7259. doi:10.1523/JNEUROSCI.1103-05.2005.
31. Kurczek, J., Wechsler, E., Ahuja, S., Jensen, U., Cohen, N. J., Tranel, D., et al. (2015). Differential contributions of hippocampus and medial prefrontal cortex to self-projection and self-referential processing. Neuropsychologia 73, 116-126. doi:10.1016/j.neuropsychologia.2015.05.002.
32. Lam, L. C. W., Chau, R. C. M., Wong, B. M. L., Fung, A. W. T., Lui, V. W. C., Tam, C. C. W., et al. (2011). Interim follow-up of a randomized controlled trial comparing Chinese style mind body (Tai Chi) and stretching exercises on cognitive function in subjects at risk of progressive cognitive decline. Int. J. Geriatr. Psychiatry 26, 733-740. doi:10.1002/gps.2602.
33. Lan, C., Chen, S.-Y., Lai, J.-S., and Wong, A. M.-K. (2013). Tai Chi Chuan in medicine and health promotion. Evid. Based Complement. Alternat. Med. 2013, 502131. doi:10.1155/2013/502131.
34. Li, F., Harmer, P., Fitzgerald, K., Eckstrom, E., Stock, R., Galver, J., et al. (2012). Tai Chi and postural stability in patients with Parkinson's disease. N. Engl. J. Med. 366, 511-519. doi:10.1056/NEJMoa1107911.
35. Li, F., Harmer, P., Liu, Y., and Chou, L.-S. (2014a). Tai Ji Quan and global cognitive function in older adults with cognitive impairment: a pilot study. Arch. Gerontol. Geriatr. 58, 434-439. doi:10.1016/j.archger.2013.12.003.
36. Li, R., Zhu, X., Yin, S., Niu, Y., Zheng, Z., Huang, X., et al. (2014b). Multimodal intervention in older adults improves resting-state functional connectivity between the medial prefrontal cortex and medial temporal lobe. Front. Aging Neurosci. 6:39. doi:10.3389/fnagi.2014.00039.
37. 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.
38. MacDonald, C. J. (2014). Prospective and retrospective duration memory in the hippocampus: is time in the foreground or background? Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20120463. doi:10.1098/rstb.2012.0463.
39. Macrae, C. N., Moran, J. M., Heatherton, T. F., Banfield, J. F., and Kelley, W. M. (2004). Medial prefrontal activity predicts memory for self. Cereb. Cortex 14, 647-654. doi:10.1093/cercor/bhh025.
40. Maldjian, J. A., Laurienti, P. J., Kraft, R. A., and Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19, 1233-1239. doi:10.1016/S1053-8119(03)00169-1.
41. Man, D. W. K., Tsang, W. W. N., and Hui-Chan, C. W. Y. (2010). Do older T'ai Chi practitioners have better attention and memory function? J. Altern. Complement. Med. 16, 1259-1264. doi:10.1089/acm.2009.0462.
42. Manson, J., Rotondi, M., Jamnik, V., Ardern, C., and Tamim, H. (2013). Effect of Tai Chi on musculoskeletal health-related fitness and self-reported physical health changes in low income, multiple ethnicity mid to older adults. BMC Geriatr. 13:114. doi:10.1186/1471-2318-13-114.
43. Mattfeld, A. T., and Stark, C. E. L. (2015). Functional contributions and interactions between the human hippocampus and subregions of the striatum during arbitrary associative learning and memory. Hippocampus 25, 900-911. doi:10.1002/hipo.22411.
44. Mei, L., Chen, Q., Ge, L., Zheng, G., and Chen, J. (2012). Systematic review of Chinese traditional exercise Baduanjin modulating the blood lipid metabolism. Evid. Based Complement. Alternat. Med. 2012, 282131. doi:10.1155/2012/282131.
45. Miller, E. K. (2000). The prefrontal cortex and cognitive control. Nat. Rev. Neurosci. 1, 59-65. doi:10.1038/35036228.
46. Miller, S. L., Celone, K., DePeau, K., Diamond, E., Dickerson, B. C., Rentz, D., et al. (2008). Age-related memory impairment associated with loss of parietal deactivation but preserved hippocampal activation. Proc. Natl. Acad. Sci. U.S.A. 105, 2181-2186. doi:10.1073/pnas.0706818105.
47. Mortimer, J. A., Ding, D., Borenstein, A. R., Decarli, C., Guo, Q., Wu, Y., et al. (2012). Changes in brain volume and cognition in a randomized trial of exercise and social interaction in a community-based sample of non-demented Chinese elders. J. Alzheimers Dis. 30, 757-766. doi:10.3233/JAD-2012-120079.
48. O'Neill, P.-K., Gordon, J. A., and Sigurdsson, T. (2013). Theta oscillations in the medial prefrontal cortex are modulated by spatial working memory and synchronize with the hippocampus through its ventral subregion. J. Neurosci. 33, 14211-14224. doi:10.1523/JNEUROSCI.2378-13.2013.
49. Preston, A. R., and Eichenbaum, H. (2013). Interplay of hippocampus and prefrontal cortex in memory. Curr. Biol. 23, R764-R773. doi:10.1016/j.cub.2013.05.041.
50. Roche, R. A., Mullally, S. L., McNulty, J. P., Hayden, J., Brennan, P., Doherty, C. P., et al. (2009). Prolonged rote learning produces delayed memory facilitation and metabolic changes in the hippocampus of the ageing human brain. BMC Neurosci. 10:136. doi:10.1186/1471-2202-10-136.
51. Salami, A., Pudas, S., and Nyberg, L. (2014). Elevated hippocampal resting-state connectivity underlies deficient neurocognitive function in aging. Proc. Natl. Acad. Sci. U.S.A. 111, 17654-17659. doi:10.1073/pnas.1410233111.
52. Takehara-Nishiuchi, K., and McNaughton, B. L. (2008). Spontaneous changes of neocortical code for associative memory during consolidation. Science 960, 960-963. doi:10.1126/science.1161299.
53. Taylor-Piliae, R. E., Hoke, T. M., Hepworth, J. T., Latt, L. D., Najafi, B., and Coull, B. M. (2014). Effect of Tai Chi on physical function, fall rates and quality of life among older stroke survivors. Arch. Phys. Med. Rehabil. 95, 816-824. doi:10.1016/j.apmr.2014.01.001.
54. Tsai, P.-F., Chang, J. Y., Beck, C., Kuo, Y.-F., and Keefe, F. J. (2013). A pilot cluster-randomized trial of a 20-week Tai Chi program in elders with cognitive impairment and osteoarthritic knee: effects on pain and other health outcomes. J. Pain Symptom Manage. 45, 660-669. doi:10.1016/j.jpainsymman.2012.04.009.
55. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273-289. doi:10.1006/nimg.2001.0978.
56. Unverzagt, F. W., Gao, S., Baiyewu, O., Ogunniyi, A. O., Gureje, O., Perkins, A., et al. (2001). Prevalence of cognitive impairment: data from the Indianapolis Study of Health and Aging. Neurology 57, 1655-1662. doi:10.1212/WNL.57.9.1655.
57. Van de Vijver, I., Cohen, M. X., and Ridderinkhof, K. R. (2014). Aging affects medial but not anterior frontal learning-related theta oscillations. Neurobiol. Aging 35, 692-704. doi:10.1016/j.neurobiolaging.2013.09.006.
58. van Kesteren, M. T. R., Beul, S. F., Takashima, A., Henson, R. N., Ruiter, D. J., and Fernández, G. (2013). Differential roles for medial prefrontal and medial temporal cortices in schema-dependent encoding: from congruent to incongruent. Neuropsychologia 51, 2352-2359. doi:10.1016/j.neuropsychologia.2013.05.027.
59. van Kesteren, M. T. R., Rijpkema, M., Ruiter, D. J., and Fernández, G. (2010). Retrieval of associative information congruent with prior knowledge is related to increased medial prefrontal activity and connectivity. J. Neurosci. 30, 15888-15894. doi:10.1523/JNEUROSCI.2674-10.2010.
60. van Kesteren, M. T. R., Ruiter, D. J., Fernández, G., and Henson, R. N. (2012). How schema and novelty augment memory formation. Trends Neurosci. 35, 211-219. doi:10.1016/j.tins.2012.02.001.
61. Van Overwalle, F. (2009). Social cognition and the brain: a meta-analysis. Hum. Brain Mapp. 30, 829-858. doi:10.1002/hbm.20547.
62. Voss, M. W., Heo, S., Prakash, R. S., Erickson, K. I., Alves, H., Chaddock, L., et al. (2013). 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.
63. Wang, C., Schmid, C. H., Rones, R., Kalish, R., Yinh, J., Goldenberg, D. L., et al. (2010). A randomized trial of Tai Chi for fibromyalgia. N. Engl. J. Med. 363, 743-754. doi:10.1056/NEJMoa0912611.
64. Wang, S. T. (2007). Effect of Baduanjin on physiological age of intelligence for old people. J. Clin. Rehabil. Tissue Eng. Res. 11, 7910-7913.
65. Wayne, P. M., Walsh, J. N., Taylor-Piliae, R. E., Wells, R. E., Papp, K. V., Donovan, N. J., et al. (2014). Effect of Tai Chi on cognitive performance in older adults: systematic review and meta-analysis. J. Am. Geriatr. Soc. 62, 25-39. doi:10.1111/jgs.12611.
66. Wei, G.-X., Dong, H.-M., Yang, Z., Luo, J., and Zuo, X.-N. (2014). Tai Chi Chuan optimizes the functional organization of the intrinsic human brain architecture in older adults. Front. Aging Neurosci. 6:74. doi:10.3389/fnagi.2014.00074.
67. 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.
68. Wells, R. E., Yeh, G. Y., Kerr, C. E., Wolkin, J., Davis, R. B., Tan, Y., et al. (2013). Meditation's impact on default mode network and hippocampus in mild cognitive impairment: a pilot study. Neurosci. Lett. 556, 15-19. doi:10.1016/j.neulet.2013.10.001.
69. Whitfield-Gabrieli, S., and Nieto-Castanon, A. (2012). A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2, 125-141. doi:10.1089/brain.2012.0073.
70. Wixted, J. T., Squire, L. R., Jang, Y., Papesh, M. H., Goldinger, S. D., Kuhn, J. R., et al. (2014). Sparse and distributed coding of episodic memory in neurons of the human hippocampus. Proc. Natl. Acad. Sci. U.S.A. 111, 9621-9626. doi:10.1073/pnas.1408365111.
71. Woodard, J. L., and Axelrod, B. N. (1987). Parsimonious prediction of the Wechsler MemoryScale-revised memory indices. Psychol. Assess. 7, 445-449. doi:10.1037/1040-3590.7.4.445.
72. Xiong, X., Wang, P., Li, S., Zhang, Y., and Li, X. (2015). Effect of Baduanjin exercise for hypertension: a systematic review and meta-analysis of randomized controlled trials. Maturitas 80, 370-378. doi:10.1016/j.maturitas.2015.01.002.
73. Yin, S., Zhu, X., Li, R., Niu, Y., Wang, B., Zheng, Z., et al. (2014). Intervention-induced enhancement in intrinsic brain activity in healthy older adults. Sci. Rep. 4, 7309. doi:10.1038/srep07309.
74. Zheng, G., Chen, B., Fang, Q., Yi, H., Lin, Q., Chen, L., et al. (2014). Primary prevention for risk factors of ischemic stroke with Baduanjin exercise intervention in the community elder population: study protocol for a randomized controlled trial. Trials 15, 113. doi:10.1186/1745-6215-15-113.