Abstract
Characterization of the default mode network (DMN) as a complex network of functionally interacting dynamic systems has received great interest for the study of DMN neural mechanisms. In particular, understanding the relationship of intrinsic resting-state DMN brain network with cognitive behaviors is an important issue in healthy cognition and mental disorders. However, it is still unclear how DMN functional connectivity links to cognitive behaviors during resting-state. In this study, we hypothesize that static and dynamic DMN nodal topology is associated with upcoming cognitive task performance. We used graph theory analysis in order to understand better the relationship between the DMN functional connectivity and cognitive behavior during resting-state and task performance. Nodal degree of the DMN was calculated as a metric of network topology. We found that the static and dynamic posterior cingulate cortex (PCC) nodal degree within the DMN was associated with task performance (Reaction Time). Our results show that the core node PCC nodal degree within the DMN was significantly correlated with reaction time, which suggests that the PCC plays a key role in supporting cognitive function.
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Achard, S., Delon-Martin, C., Vertes, P. E., Renard, F., Schenck, M., Schneider, F., Heinrich, C., Kremer, S., & Bullmore, E. T. (2012). Hubs of brain functional networks are radically reorganized in comatose patients. Proceedings of the National Academy of Sciences of the United States of America, 109(50), 20608–20613.
Allen, E. A., Damaraju, E., Plis, S. M., Erhardt, E. B., Eichele, T., & Calhoun, V. D. (2014). Tracking whole-brain connectivity dynamics in the resting state. Cerebral Cortex, 24(3), 663–676.
Andrews-Hanna, J. R., Snyder, A. Z., Vincent, J. L., Lustig, C., Head, D., Raichle, M. E., & Buckner, R. L. (2007). Disruption of large-scale brain systems in advanced aging. Neuron, 56(5), 924–935.
Arenivas, A., Diaz-Arrastia, R., Spence, J., Cullum, C. M., Krishnan, K., Bosworth, C., Culver, C., Kennard, B., & Marquez de la Plata, C. (2014). Three approaches to investigating functional compromise to the default mode network after traumatic axonal injury. Brain Imaging and Behavior, 8(3), 407–419.
Bassett, D. S., Bullmore, E. T., Meyer-Lindenberg, A., Apud, J. A., Weinberger, D. R., & Coppola, R. (2009). Cognitive fitness of cost-efficient brain functional networks. Proceedings of the National Academy of Sciences of the United States of America, 106(28), 11747–11752.
Bonnelle, V., Ham, T. E., Leech, R., Kinnunen, K. M., Mehta, M. A., Greenwood, R. J., & Sharp, D. J. (2012). Salience network integrity predicts default mode network function after traumatic brain injury. Proceedings of the National Academy of Sciences of the United States of America, 109(12), 4690–4695.
Buckner, R. L., Andrews-Hanna, J. R., & Schacter, D. L. (2008). The brain’s default network: anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences, 1124, 1–38.
Buckner, R. L., Sepulcre, J., Talukdar, T., Krienen, F. M., Liu, H. S., Hedden, T., Andrews-Hanna, J. R., Sperling, R. A., & Johnson, K. A. (2009). Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer’s disease. Journal of Neuroscience, 29(6), 1860–1873.
Calhoun, V. D., Miller, R., Pearlson, G., & Adali, T. (2014). The chronnectome: time-varying connectivity networks as the next frontier in fMRI Data discovery. Neuron, 84(2), 262–274.
Castellanos, N. P., Paul, N., Ordonez, V. E., Demuynck, O., Bajo, R., Campo, P., Bilbao, A., Ortiz, T., Del-Pozo, F., & Maestu, F. (2010). Reorganization of functional connectivity as a correlate of cognitive recovery in acquired brain injury. Brain: A Journal of Neurology, 133(Pt 8), 2365–2381.
Chang, C., & Glover, G. H. (2010). Time-frequency dynamics of resting-state brain connectivity measured with fMRI. NeuroImage, 50(1), 81–98.
Chen, J. L., Ros, T., & Gruzelier, J. H. (2013). Dynamic changes of ICA-derived EEG functional connectivity in the resting state. Human Brain Mapping, 34(4), 852–868.
Chikazoe, J., Konishi, S., Asari, T., Jimura, K., & Miyashita, Y. (2007). Activation of right inferior frontal gyrus during response inhibition across response modalities. Journal of Cognitive Neuroscience, 19(1), 69–80.
Cocchi, L., Zalesky, A., Toepel, U., Whitford, T. J., De-Lucia, M., Murray, M. M., & Carter, O. (2011). Dynamic changes in brain functional connectivity during concurrent dual-task performance. PLoS One, 6(11), e28301.
Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3(3), 201–215.
Crossley, N. A., Mechelli, A., Vertes, P. E., Winton-Brown, T. T., Patel, A. X., Ginestet, C. E., McGuire, P., & Bullmore, E. T. (2013). Cognitive relevance of the community structure of the human brain functional coactivation network. Proceedings of the National Academy of Sciences of the United States of America, 110(28), 11583–11588.
De Pisapia, N., Turatto, M., Lin, P., Jovicich, J., & Caramazza, A. (2012). Unconscious priming instructions modulate activity in default and executive networks of the human brain. Cerebral Cortex, 22(3), 639–649.
Dosenbach, N. U. F., Fair, D. A., Miezin, F. M., Cohen, A. L., Wenger, K. K., Dosenbach, R. A. T., Fox, M. D., Snyder, A. Z., Vincent, J. L., Raichle, M. E., et al. (2007). Distinct brain networks for adaptive and stable task control in humans. Proceedings of the National Academy of Sciences of the United States of America, 104(26), 11073–11078.
Fair, D. A., Cohen, A. L., Dosenbach, N. U. F., Church, J. A., Miezin, F. M., Barch, D. M., Raichle, M. E., Petersen, S. E., & Schlaggar, B. L. (2008). The maturing architecture of the brain’s default network. Proceedings of the National Academy of Sciences of the United States of America, 105(10), 4028–4032.
Fornito, A., Harrison, B. J., Zalesky, A., & Simons, J. S. (2012). Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection. Proceedings of the National Academy of Sciences of the United States of America, 109(31), 12788–12793.
Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., & Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences of the United States of America, 102(27), 9673–9678.
Garrett, D. D., Kovacevic, N., McIntosh, A. R., & Grady, C. L. (2011). The importance of being variable. Journal of Neuroscience, 31(12), 4496–4503.
Gong, G., He, Y., Concha, L., Lebel, C., Gross, D. W., Evans, A. C., & Beaulieu, C. (2009). Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cerebral Cortex (New York, N Y : 1991), 19(3), 524–536.
Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences of the United States of America, 100(1), 253–258.
Greicius, M. D., Supekar, K., Menon, V., & Dougherty, R. F. (2009). Resting-state functional connectivity reflects structural connectivity in the default mode network. Cerebral Cortex (New York, N Y : 1991), 19(1), 72–78.
Hagmann, P., Sporns, O., Madan, N., Cammoun, L., Pienaar, R., Wedeen, V. J., Meuli, R., Thiran, J. P., & Grant, P. E. (2010). White matter maturation reshapes structural connectivity in the late developing human brain. Proceedings of the National Academy of Sciences of the United States of America, 107(44), 19067–19072.
Handwerker, D. A., Roopchansingh, V., Gonzalez-Castillo, J., & Bandettini, P. A. (2012). Periodic changes in fMRI connectivity. NeuroImage, 63(3), 1712–1719.
Hellyer, P. J., Shanahan, M., Scott, G., Wise, R. J., Sharp, D. J., & Leech, R. (2014). The control of global brain dynamics: opposing actions of frontoparietal control and default mode networks on attention. Journal of Neuroscience, 34(2), 451–461.
Hutchison, R. M., Womelsdorf, T., Allen, E. A., Bandettini, P. A., Calhoun, V. D., Corbetta, M., Penna, S., Duyn, J. H., Glover, G. H., Gonzalez-Castillo, J., et al. (2013a). Dynamic functional connectivity: promise, issues, and interpretations. NeuroImage, 80, 360–378.
Hutchison, R. M., Womelsdorf, T., Gati, J. S., Everling, S., & Menon, R. S. (2013b). Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Human Brain Mapping, 34(9), 2154–2177.
Kelly, A. M. C., Uddin, L. Q., Biswal, B. B., Castellanos, F. X., & Milham, M. P. (2008). Competition between functional brain networks mediates behavioral variability. NeuroImage, 39(1), 527–537.
Konishi, S., Hayashi, T., Uchida, I., Kikyo, H., Takahashi, E., & Miyashita, Y. (2002). Hemispheric asymmetry in human lateral prefrontal cortex during cognitive set shifting. Proceedings of the National Academy of Sciences of the United States of America, 99(11), 7803–7808.
Kucyi, A., & Davis, K. D. (2014). Dynamic functional connectivity of the default mode network tracks daydreaming. NeuroImage, 100, 471–480.
Kucyi, A., & Davis, K. D. (2015). The dynamic pain connectome. Trends in Neurosciences, 38(2), 86–95.
Kucyi, A., Salomons, T. V., & Davis, K. D. (2013). Mind wandering away from pain dynamically engages antinociceptive and default mode brain networks. Proceedings of the National Academy of Sciences of the United States of America, 110(46), 18692–18697.
Lee, H. L., Zahneisen, B., Hugger, T., Levan, P., & Hennig, J. (2013). Tracking dynamic resting-state networks at higher frequencies using MR-encephalography. NeuroImage, 65, 216–222.
Leech, R., Kamourieh, S., Beckmann, C. F., & Sharp, D. J. (2011). Fractionating the default mode network: distinct contributions of the ventral and dorsal posterior cingulate cortex to cognitive control. Journal of Neuroscience, 31(9), 3217–3224.
Leech, R., Sharp, DJ. (2013). The role of the posterior cingulate cortex in cognition and disease. Brain.
Leonardi, N., Richiardi, J., Gschwind, M., Simioni, S., Annoni, J. M., Schluep, M., Vuilleumier, P., & Van De Ville, D. (2013). Principal components of functional connectivity: a new approach to study dynamic brain connectivity during rest. NeuroImage, 83, 937–950.
Liang, X., Zou, Q. H., He, Y., & Yang, Y. H. (2013). Coupling of functional connectivity and regional cerebral blood flow reveals a physiological basis for network hubs of the human brain. Proceedings of the National Academy of Sciences of the United States of America, 110(5), 1929–1934.
Lin, P., Hasson, U., Jovicich, J., & Robinson, S. (2011). A neuronal basis for task-negative responses in the human brain. Cerebral Cortex (New York, N Y : 1991), 21(4), 821–830.
Lin, P., Sun, J. B., Yu, G., Wu, Y., Yang, Y., Liang, M. L., & Liu, X. (2014). Global and local brain network reorganization in attention-deficit/hyperactivity disorder. Brain Imaging and Behavior, 8(4), 558–569.
Ma, S., Calhoun, V. D., Phlypo, R., & Adali, T. (2014). Dynamic changes of spatial functional network connectivity in healthy individuals and schizophrenia patients using independent vector analysis. NeuroImage, 90, 196–206.
Mantini, D., & Vanduffel, W. (2013). Emerging roles of the brain’s default network. The Neuroscientist, 19(1), 76–87.
Marchant, J. L., & Driver, J. (2013). Visual and audiovisual effects of isochronous timing on visual perception and brain activity. Cerebral Cortex, 23(6), 1290–1298.
Mayhew, S. D., Hylands-White, N., Porcaro, C., Derbyshire, S. W. G., & Bagshaw, A. P. (2013). Intrinsic variability in the human response to pain is assembled from multiple, dynamic brain processes. NeuroImage, 75, 68–78.
McKiernan, K. A., Kaufman, J. N., Kucera-Thompson, J., & Binder, J. R. (2003). A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. Journal of Cognitive Neuroscience, 15(3), 394–408.
Murphy, K., Birn, R. M., Handwerker, D. A., Jones, T. B., & Bandettini, P. A. (2009). The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? NeuroImage, 44(3), 893–905.
Park, H. J., & Friston, K. (2013). Structural and functional brain networks: from connections to cognition. Science, 342(6158), 1238411.
Patel, K. T., Stevens, M. C., Pearlson, G. D., Winkler, A. M., Hawkins, K. A., Skudlarski, P., & Bauer, L. O. (2013). Default mode network activity and white matter integrity in healthy middle-aged ApoE4 carriers. Brain Imaging and Behavior, 7(1), 60–67.
Pfefferbaum, A., Chanraud, S., Pitel, A. L., Muller-Oehring, E., Shankaranarayanan, A., Alsop, D. C., Rohlfing, T., & Sullivan, E. V. (2011). Cerebral blood flow in posterior cortical nodes of the default mode network decreases with task engagement but remains higher than in most brain regions. Cerebral Cortex, 21(1), 233–244.
Philip, N. S., Sweet, L. H., Tyrka, A. R., Price, L. H., Carpenter, L. L., Kuras, Y. I., Clark, U. S., & Niaura, R. S. (2013). Early life stress is associated with greater default network deactivation during working memory in healthy controls: a preliminary report. Brain Imaging and Behavior, 7(2), 204–212.
Power, J. D., Schlaggar, B. L., Lessov-Schlaggar, C. N., & Petersen, S. E. (2013). Evidence for hubs in human functional brain networks. Neuron, 79(4), 798–813.
Raichle, M. E., & Gusnard, D. A. (2002). Appraising the brain’s energy budget. Proceedings of the National Academy of Sciences of the United States of America, 99(16), 10237–10239.
Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98(2), 676–682.
Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: uses and interpretations. NeuroImage, 52(3), 1059–1069.
Scholvinck, M. L., Maier, A., Ye, F. Q., Duyn, J. H., & Leopold, D. A. (2010). Neural basis of global resting-state fMRI activity. Proceedings of the National Academy of Sciences of the United States of America, 107(22), 10238–10243.
Sharp, D. J., Beckmann, C. F., Greenwood, R., Kinnunen, K. M., Bonnelle, V., De Boissezon, X., Powell, J. H., Counsell, S. J., Patel, M. C., & Leech, R. (2011). Default mode network functional and structural connectivity after traumatic brain injury. Brain, 134(Pt 8), 2233–2247.
Sharp, D. J., Scott, G., & Leech, R. (2014). Network dysfunction after traumatic brain injury. Nature Reviews Neurology, 10(3), 156–166.
Sporns, O., Tononi, G., & Edelman, G. M. (2000). Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. Cerebral Cortex, 10(2), 127–141.
Street, J. O., Carroll, R. J., & Ruppert, D. (1988). A note on computing robust regression estimates via iteratively reweighted least-squares. American Statistician, 42(2), 152–154.
Supekar, K., Musen, M., & Menon, V. (2009). Development of large-scale functional brain networks in children. PLoS Biology, 7(7), e1000157.
Supekar, K., Uddin, L. Q., Prater, K., Amin, H., Greicius, M. D., & Menon, V. (2010). Development of functional and structural connectivity within the default mode network in young children. NeuroImage, 52(1), 290–301.
Tagliazucchi, E., & Laufs, H. (2014). Decoding wakefulness levels from typical fMRI resting-state data reveals reliable drifts between wakefulness and sleep. Neuron, 82(3), 695–708.
Tagliazucchi, E., von Wegner, F., Morzelewski, A., Brodbeck, V., & Laufs, H. (2012). Dynamic BOLD functional connectivity in humans and its electrophysiological correlates. Frontiers in Human Neuroscience, 6, 339.
Tam, A., Luedke, AC., Walsh, JJ., Fernandez-Ruiz, J., Garcia, A. (2014). Effects of reaction time variability and age on brain activity during Stroop task performance. Brain Imaging and Behav
Thompson, G. J., Merritt, M. D., Pan, W. J., Magnuson, M. E., Grooms, J. K., Jaeger, D., & Keilholz, S. D. (2013). Neural correlates of time-varying functional connectivity in the rat. NeuroImage, 83, 826–836.
Utevsky, A. V., Smith, D. V., & Huettel, S. A. (2014). Precuneus is a functional core of the default-mode network. Journal of Neuroscience, 34(3), 932–940.
van den Bos, W., Talwar, A., & McClure, S. M. (2013). Neural correlates of reinforcement learning and social preferences in competitive bidding. Journal of Neuroscience, 33(5), 2137–2146.
van den Heuvel, M., Mandl, R., Luigjes, J., & Hulshoff, P. H. (2008). Microstructural organization of the cingulum tract and the level of default mode functional connectivity. Journal of Neuroscience, 28(43), 10844–10851.
van den Heuvel, M. P., Stam, C. J., Kahn, R. S., & Hulshoff Pol, H. E. (2009). Efficiency of functional brain networks and intellectual performance. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 29(23), 7619–7624.
Van Dijk, K. R. A., Hedden, T., Venkataraman, A., Evans, K. C., Lazar, S. W., & Buckner, R. L. (2010). Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. Journal of Neurophysiology, 103(1), 297–321.
van Veluw, S. J., & Chance, S. A. (2014). Differentiating between self and others: an ALE meta-analysis of fMRI studies of self-recognition and theory of mind. Brain Imaging and Behavior, 8(1), 24–38.
Weissman, D. H., Roberts, K. C., Visscher, K. M., & Woldorff, M. G. (2006). The neural bases of momentary lapses in attention. Nature Neuroscience, 9(7), 971–978.
Yan, Y., Rasch, M. J., Chen, M., Xiang, X., Huang, M., Wu, S., & Li, W. (2014). Perceptual training continuously refines neuronal population codes in primary visual cortex. Nature Neuroscience, 17(10), 1380–1387.
Zaitsev, M., Hennig, J., & Speck, O. (2004). Point spread function mapping with parallel imaging techniques and high acceleration factors: Fast, robust, and flexible method for echo-planar imaging distortion correction. Magnetic Resonance in Medicine, 52(5), 1156–1166.
Acknowledgments
Government of the Provincia Autonoma di Trento, Italy, Project PAT Post-doc 2006; Fondazione Cassa di Risparmio di Trento e Rovereto; and University of Trento, Italy. This work was supported by the National Natural Science Foundation of China (61473221, 61462031, 61262034, 31271061), by Doctoral Fund of Ministry of Education of China (20120201120071), by the Young Scientist Foundation of Jiangxi Province (20122BCB23017), by the Project of the Education Department of Jiangxi Province (KJLD14031), by the Fundamental Research Funds for the Central Universities of China, by the Program for New Century Excellent Talents in University of China (NCET-12-0557 to XW).
Competing interests
Pan Lin, Yong Yang, Jorge Jovicich, Nicola De Pisapia, Xiang Wang, Chun S. Zuo, and James Jonathan Levitt declare that they have no conflicts of interest.
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All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.
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Lin, P., Yang, Y., Jovicich, J. et al. Static and dynamic posterior cingulate cortex nodal topology of default mode network predicts attention task performance. Brain Imaging and Behavior 10, 212–225 (2016). https://doi.org/10.1007/s11682-015-9384-6
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DOI: https://doi.org/10.1007/s11682-015-9384-6