Tai Chi Chuan and Baduanjin practice modulates functional connectivity of the cognitive control network in older adults

Jing Tao, Xiangli Chen, Natalia Egorova, Jiao Liu, Xiehua Xue, Qin Wang, Guohua Zheng, Moyi Li, Wenjun Hong, Sharon Sun, Lidian Chen, Jian Kong, Jing Tao, Xiangli Chen, Natalia Egorova, Jiao Liu, Xiehua Xue, Qin Wang, Guohua Zheng, Moyi Li, Wenjun Hong, Sharon Sun, Lidian Chen, Jian Kong

Abstract

Cognitive impairment is one of the most common problem saffecting older adults. In this study, we investigated whether Tai Chi Chuan and Baduanjin practice can modulate mental control functionand the resting state functional connectivity (rsFC) of the cognitive control network in older adults. Participants in the two exercise groups practiced either Tai Chi Chuan or Baduanjin for 12 weeks, and those in the control group received basic health education. Memory tests and fMRI scans were conducted at baseline and at the end of the study. Seed-based (bilateral dorsolateral prefrontal cortex, DLPFC) rsFC analysis was performed. We found that compared to the controls, 1) both Tai Chi Chuan and Baduanjin groups demonstrated significant improvements in mental control function; 2) the Tai Chi Chuan group showed a significant decrease in rsFC between the DLPFC and the left superior frontal gyrus (SFG) and anterior cingulate cortex; and 3) the Baduanjin group showed a significant decrease in rsFC between the DLPFC and the left putamen and insula. Mental control improvement was negatively associated with rsFC DLPFC-putamen changes across all subjects. These findings demonstrate the potential of Tai Chi Chuan and Baduanjin exercises in preventing cognitive decline.

Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1. Yellow indicates brain regions that…
Figure 1. Yellow indicates brain regions that showed significant FC decrease with in the cognitive control network (CCN) in the Tai Chi Chuan group as compared to the control group; Red indicates brain regions that showed significant FC decrease within the CCN in the Baduanjin group as compared to the control group; Blue indicates brain regions, in which the CCN FC changes (post-minus pre-treatment) were negatively associated with the mental control score across all subjects.
(A) The activation regions in the left SFG is the CCN FC changes in the Tai Chi Chuan group as compared to the control group; (B) The activation regions of dACC/rACC in the contract of Tai Chi Chuan group and control group. (C) The circle indicates an overlap of the results of the CCN FC changes in Baduanjin group and association between the mental control scores improvement and the CCN FC decrease in the left putamen across all subjects; (D) Scatter plots show the correlation between mental control and Fisher’s Z values at the peak (−39 0 18) of the significant cluster across all subjects. L, left; SFG, superior frontal gyrus; ACC, anterior cingulate cortex.

References

    1. Erickson K. I. et al.. Exercise training increases size of hippocampus and improves memory. Proc. Natl. Acad. Sci. USA. 108, 3017–3022 (2011).
    1. Gard T., Hölzel B. K. & Lazar S. W. The potential effects of meditation on age-related cognitive decline: A systematic review. Ann. N. Y. Acad. Sci. 1307, 89–103 (2014).
    1. National Institutes of Health. National Center for Complementary and Alternative Medicine (NCCAM) (2007). .
    1. Wayne P. M. et al.. Effect of tai chi on cognitive performance in older adults: Systematic review and meta-analysis. J. Am. Geriatr. Soc. 62, 25–39 (2014).
    1. Wang S. T. Effect of Baduanjin on physiological age of intelligence for old people. J. Clin. Rehabil. Tissue Eng. Res. 11, 7910–7913 (2007).
    1. Fong D. Y., Chi L. K., Li F. & Chang Y. K. 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, 1–11 (2014).
    1. Hakun J. G., Zhu Z., Brown C. A., Johnson N. F. & Gold B. T. Longitudinal alterations to brain function, structure, and cognitive performance in healthy older adults: A fMRI-DTI study. Neuropsychologia. 71, 225–235 (2015).
    1. Cole M. W. & Schneider W. The cognitive control network: Integrated cortical regions with dissociable functions. Neuroimage. 37, 343–360 (2007).
    1. Rizio A. A. & Dennis N. A. The cognitive control of memory: Age differences in the neural correlates of successful remembering and intentional forgetting. PLoS One. 9, e87010 (2014).
    1. Zanto T. P. & Gazzaley A. Fronto-parietal network: Flexible hub of cognitive control. Trends Cogn. Sci. 17, 602–603 (2013).
    1. Cole M. W., Repovš G. & Anticevic A. The Frontoparietal Control System: A Central Role in Mental Health. Neuroscientist, doi: 10.1177/1073858414525995 (2014).
    1. Rosen M. L., Stern C. E., Michalka S. W., Devaney K. J. & Somers D. C. Cognitive Control Network Contributions to Memory-Guided Visual Attention. Cereb. Cortex. 26, 2059–2073 (2016).
    1. Cieslik E. C. et al.. Is there one DLPFC in cognitive action control? Evidence for heterogeneity from Co-activation-based parcellation. Cereb. Cortex. 23, 2677–2689 (2013).
    1. Miller E. K. & Cohen J. D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).
    1. Sandrini M. et al.. Noninvasive stimulation of prefrontal cortex strengthens existing episodic memories and reduces forgetting in the elderly. Front. Aging Neurosci. 6, 289 (2014).
    1. Tao J. et al.. Increased hippocampus–medial prefrontal cortex resting state functional connectivity and memory function after Tai Chi Chuan practice in elder adults. Front. Aging Neurosci. 8, 25, doi: 10.3389/fnagi.2016.00025 (2016).
    1. Campbell K. L., Grady C. L., Ng C. & Hasher L. Age differences in the frontoparietal cognitive control network: Implications for distractibility. Neuropsychologia. 50, 2212–2223 (2012).
    1. Gutchess A. H. et al.. Contextual interference in recognition memory with age. Neuroimage. 35, 1338–1347 (2007).
    1. Grady C. L. et al.. A Multivariate Analysis of Age-Related Differences in Default Mode and Task Positive Networks Across Multiple Cognitive Domains. Cereb. Cortex. 20, 1432–1447 (2011).
    1. Small G. W. et al.. Effects of a 14-day healthy longevity lifestyle program on cognition and brain function. Am. J. Geriatr. Psychiatry. 14, 538–545 (2006).
    1. Bugg J. M. & Head D. Exercise moderates age-related atrophy of the medial temporal lobe. Neurobiol. Aging. 32, 506–514 (2011).
    1. Flöel A. et al.. Physical activity and memory functions: are neurotrophins and cerebral gray matter volume the missing link? Neuroimage. 49, 2756–2763 (2010).
    1. Yanagisawa H. et al.. Acute moderate exercise elicits increased dorsolateral prefrontal activation and improves cognitive performance with Stroop test. Neuroimage. 50, 1702–1710 (2010).
    1. Dietrich A. Transient hypofrontality as a mechanism for the psychological effects of exercise. Psychiatry Res. 145, 79–83 (2006).
    1. Schneider S. et al.. The influence of exercise on prefrontal cortex activity and cognitive performance during a simulated space flight to Mars (MARS500). Behav. Brain Res. 236, 1–7 (2013).
    1. MacDonald A. M., Cohen J. D., Stenger V. A. & Carter C. S. Dissociating the role of the dorsolateral prefrontal cortex and anterior cingulate cortex in cognitive control. Science. 288, 1835–1838 (2000).
    1. Woodcock E. A., White R. & Diwadkar V. A. The dorsal prefrontal and dorsal anterior cingulate cortices exert complementary network signatures during encoding and retrieval in associative memory. Behav. Brain Res. 290, 152–160(2015).
    1. Harding I. H., Yücel M., Harrison B. J., Pantelis C. & Breakspear M. Effective connectivity within the frontoparietal control network differentiates cognitive control and working memory. Neuroimage. 106, 144–153 (2015).
    1. Braver T. S., Barch D. M., Gray J. R., Molfese D. L. & Snyder A. Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. Cereb. Cortex. 11, 825–836 (2001).
    1. Diwadkar V. A. et al.. Dysfunctional Activation and Brain Network Profiles in Youth with Obsessive-Compulsive Disorder: A Focus on the Dorsal Anterior Cingulate during Working Memory. Front. Hum. Neurosci. 9, 149 (2015).
    1. Tang Y. Y. et al.. Short-term meditation induces white matter changes in the anterior cingulate. Proc. Natl. Acad. Sci. USA 107, 15649–15652 (2010).
    1. Baron Short E. et al.. Regional brain activation during meditation shows time and practice effects: an exploratory FMRI study. Evid. Based. Complement. Alternat. Med. 7, 121–127 (2010).
    1. Wei G. X., Dong H. M., Yang Z., Luo J. & Zuo X. N. Tai Chi Chuan optimizes the functional organization of the intrinsic human brain architecture in older adults. Front. Aging Neurosci. 6, 74 (2014).
    1. Boisgueheneuc F. D. et al.. Functions of the left superior frontal gyrus in humans: A lesion study. Brain. 129, 3315–3328 (2006).
    1. Darki F. & Klingberg T. The Role of Fronto-Parietal and Fronto-Striatal Networks in the Development of Working Memory: A Longitudinal Study. Cereb. cortex. 25, 1587–1595 (2015).
    1. Hopfinger J. B., Buonocore M. H. & Mangun G. R. The neural mechanisms of top-down attentional control. Nat. Neurosci. 3, 284–291 (2000).
    1. Turner G. R. & Spreng R. N. Executive functions and neurocognitive aging: Dissociable patterns of brain activity. Neurobiol. Aging. 33 (2012).
    1. Gutchess A. H. et al.. Aging and the neural correlates of successful picture encoding: frontal activations compensate for decreased medial-temporal activity. J. Cogn. Neurosci. 17, 84–96 (2005).
    1. Pagnoni G., Cekic M. & Guo Y. ‘Thinking about not-thinking’: Neural correlates of conceptual processing during Zen meditation. PLoS One. 3, e3083 (2008).
    1. Yin S. et al.. Intervention-induced enhancement in intrinsic brain activity in healthy older adults. Sci. Rep. 4, 7309 (2014).
    1. Leisman G., Braun-Benjamin O. & Melillo R. Cognitive-motor interactions of the basal ganglia in development. Front. Syst. Neurosci. 8, 16 (2014).
    1. Arsalidou M., Duerden E. G. & Taylor M. J. The centre of the brain: Topographical model of motor, cognitive, affective, and somatosensory functions of the basal ganglia. Hum. Brain Mapp. 34, 3031–3054 (2013).
    1. Baier B. et al.. Keeping memory clear and stable–the contribution of human basal ganglia and prefrontal cortex to working memory. J. Neurosci. 30, 9788–9792 (2010).
    1. Voytek B. & Knight R. T. Prefrontal cortex and basal ganglia contributions to visual working memory. Proc. Natl. Acad. Sci. USA 107, 18167–18172 (2010).
    1. Niemann C., Godde B., Staudinger U. M. & Voelcker-Rehage C. Exercise-induced changes in basal ganglia volume and cognition in older adults. Neuroscience. 281, 147–163 (2014).
    1. Gasquoine P. G. Contributions of the insula to cognition and emotion. Neuropsychol. Rev. 24, 77–87 (2014).
    1. Levens S. M. & Phelps E. A. Insula and Orbital Frontal Cortex Activity Underlying Emotion Interference Resolution in Working Memory. 22, 2790–2803 (2010).
    1. Power J. D. & Petersen S. E. Control-related systems in the human brain. Curr. Opin. Neurobiol. 23, 223–228 (2013).
    1. Froeliger B. et al.. Meditation-State Functional Connectivity (msFC): Strengthening of the Dorsal Attention Network and Beyond. Evid. Based. Complement. Alternat. Med. 2012, 680407 (2012).
    1. Health Qigong Management Center of General Administration of Sport of China. Health qigong–Baduanjin. (People’s Sports Publishing House of China, 2003).
    1. Lamar M., Price C. C., Davis K. L., Kaplan E. & Libon D. J. Capacity to maintain mental set in dementia. Neuropsychologia. 40, 435–445 (2002).
    1. Gong Y. &Wang D. J. Handbook of Wechsler Memory Scale-Revised (1989).
    1. ChaoGan Y. & YuFeng Z. DPARSF: A MATLAB Toolbox for ‘Pipeline’ Data Analysis of Resting-State fMRI. Front. Syst. Neurosci. 4, 13 (2010).
    1. Song X. W. et al.. REST: A Toolkit for Resting-State Functional Magnetic Resonance Imaging Data Processing. PLoS One. 6, e25031 (2011).
    1. Di Martino A. et al.. The autism brain imaging data exchange: towards a large-scale evaluation of the intrinsic brain architecture in autism. Mol. Psychiatry. 19, 659–667 (2014).
    1. Leonardi N. et al.. Principal components of functional connectivity: A new approach to study dynamic brain connectivity during rest. Neuroimage. 83, 937–950 (2013).
    1. Yan C. G. et al.. A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage. 76, 183–201 (2013).
    1. Li Z. et al.. Altered periaqueductal gray resting state functional connectivity in migraine and the modulation effect of treatment. Sci. Rep. 6, 20298 (2016).
    1. Sheline Y. I., Price J. L., Yan Z. & Mintun M. A. Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proc. Natl. Acad. Sci. USA 107, 11020–11025 (2010).
    1. Fales C. L. et al.. Altered Emotional Interference Processing in Affective and Cognitive-Control Brain Circuitry in Major Depression. Biol. Psychiatry. 63, 377–384 (2008).
    1. Hwang J. W. et al.. Subthreshold depression is associated with impaired resting-state functional connectivity of the cognitive control network. Transl. Psychiatry. 5, e683 (2015).

Source: PubMed

3
Abonnere