Abstract
Spatially remote brain regions show synchronized activity as typically revealed by correlated functional MRI (fMRI) signals. An emerging line of research has focused on the temporal fluctuations of connectivity; however, its relationships with stationary connectivity have not been clearly illustrated. We examined dynamic and stationary connectivity when the participants watched four different movie clips. We calculated point-by-point multiplication between two regional time series to estimate the time-resolved dynamic connectivity, and estimated the inter-individual consistency of the dynamic connectivity time series. Widespread consistent dynamic connectivity was observed for each movie clip, which also showed differences between the clips. For example, a cartoon movie clip, Wall-E, showed more consistent of dynamic connectivity with the posterior cingulate cortex and supramarginal gyrus, while a court drama clip, A Few Good Men, showed more consistent of dynamic connectivity with the auditory cortex and temporoparietal junction, which might suggest the involvement of specific brain processing for different movie contents. In contrast, the stationary connectivity as measured by the correlations between regional time series was highly similar among the movie clips, and showed fewer statistically significant differences. The patterns of consistent dynamic connectivity could be used to classify different movie clips with higher accuracy than the stationary connectivity and regional activity. These results support the functional significance of dynamic connectivity in reflecting functional brain changes, which could provide more functionally relevant information than stationary connectivity.
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Data availability
This study is a secondary analysis of publicly available data sets. The download links for the data sets are provided in the manuscript. No personal identifiable information was used in the current study.
References
Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD (2014) Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex N Y 1991(24):663–676. https://doi.org/10.1093/cercor/bhs352
Baldassano C, Chen J, Zadbood A, Pillow JW, Hasson U, Norman KA (2017) Discovering event structure in continuous narrative perception and memory. Neuron 95:709-721.e5. https://doi.org/10.1016/j.neuron.2017.06.041
Bartels A, Zeki S, Logothetis NK (2008) Natural vision reveals regional specialization to local motion and to contrast-invariant, global flow in the human brain. Cereb Cortex 18:705–717. https://doi.org/10.1093/cercor/bhm107
Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med off J Soc Magn Reson Med Soc Magn Reson Med 34:537–541. https://doi.org/10.1002/mrm.1910340409
Biswal BB, Mennes M, Zuo X-N, Gohel S, Kelly C, Smith SM, Beckmann CF, Adelstein JS, Buckner RL, Colcombe S, Dogonowski A-M, Ernst M, Fair D, Hampson M, Hoptman MJ, Hyde JS, Kiviniemi VJ, Kötter R, Li S-J, Lin C-P, Lowe MJ, Mackay C, Madden DJ, Madsen KH, Margulies DS, Mayberg HS, McMahon K, Monk CS, Mostofsky SH, Nagel BJ, Pekar JJ, Peltier SJ, Petersen SE, Riedl V, Rombouts SARB, Rypma B, Schlaggar BL, Schmidt S, Seidler RD, Siegle GJ, Sorg C, Teng G-J, Veijola J, Villringer A, Walter M, Wang L, Weng X-C, Whitfield-Gabrieli S, Williamson P, Windischberger C, Zang Y-F, Zhang H-Y, Castellanos FX, Milham MP (2010) Toward discovery science of human brain function. Proc Natl Acad Sci USA 107:4734–4739. https://doi.org/10.1073/pnas.0911855107
Bullmore E, Sporns O (2012) The economy of brain network organization. Nat Rev Neurosci 13:336–349. https://doi.org/10.1038/nrn3214
Cai Q, Van der Haegen L, Brysbaert M (2013) Complementary hemispheric specialization for language production and visuospatial attention. Proc Natl Acad Sci USA 110:E322–E330. https://doi.org/10.1073/pnas.1212956110
Calhoun VD, Adali T, Pearlson GD, Pekar JJ (2001) A method for making group inferences from functional MRI data using independent component analysis. Hum Brain Mapp 14:140–151
Chen G, Shin Y-W, Taylor PA, Glen DR, Reynolds RC, Israel RB, Cox RW (2016) Untangling the relatedness among correlations, part I: nonparametric approaches to inter-subject correlation analysis at the group level. Neuroimage 142:248–259. https://doi.org/10.1016/j.neuroimage.2016.05.023
Chen JE, Lewis LD, Chang C, Tian Q, Fultz NE, Ohringer NA, Rosen BR, Polimeni JR (2020) Resting-state “physiological networks.” Neuroimage 213:116707. https://doi.org/10.1016/j.neuroimage.2020.116707
Cole MW, Bassett DS, Power JD, Braver TS, Petersen SE (2014) Intrinsic and task-evoked network architectures of the human brain. Neuron 83:238–251. https://doi.org/10.1016/j.neuron.2014.05.014
Cooper RA, Kurkela KA, Davis SW, Ritchey M (2021) Mapping the organization and dynamics of the posterior medial network during movie watching. Neuroimage 236:118075. https://doi.org/10.1016/j.neuroimage.2021.118075
Di Martino A, Scheres A, Margulies DS, Kelly MC, Uddin LQ, Shehzad Z, Biswal B, Walters JR, Castellanos FX, Milham MP (2008) Functional connectivity of human striatum: a resting state FMRI study. Cereb. Cortex NY 1991(18):2735–2747. https://doi.org/10.1093/cercor/bhn041
Di X, Biswal BB (2015) Characterizations of resting-state modulatory interactions in the human brain. J Neurophysiol 114:2785–2796. https://doi.org/10.1152/jn.00893.2014
Di X, Biswal BB (2019) Toward task connectomics: examining whole-brain task modulated connectivity in different task domains. Cereb Cortex 29:1572–1583. https://doi.org/10.1093/cercor/bhy055
Di X, Biswal BB (2020) Intersubject consistent dynamic connectivity during natural vision revealed by functional MRI. Neuroimage 216:1166982. https://doi.org/10.1016/j.neuroimage.2020.116698
Di X, Biswal BB (2022) Principal component analysis reveals multiple consistent responses to naturalistic stimuli in children and adults. Hum Brain Mapp. https://doi.org/10.1002/hbm.25568
Di X, Kim EH, Chen P, Biswal BB (2014) Lateralized resting-state functional connectivity in the task-positive and task-negative networks. Brain Connect 4:641–648. https://doi.org/10.1089/brain.2013.0215
Di X, Zhang Z, Biswal BB (2020) Understanding psychophysiological interaction and its relations to beta series correlation. Brain Imaging Behav 15:958–973. https://doi.org/10.1007/s11682-020-00304-8
Eichenbaum A, Pappas I, Lurie D, Cohen JR, D’Esposito M (2021) Differential contributions of static and time-varying functional connectivity to human behavior. Netw Neurosci 5:145–165. https://doi.org/10.1162/netn_a_00172
Faskowitz J, Esfahlani FZ, Jo Y, Sporns O, Betzel RF (2020) Edge-centric functional network representations of human cerebral cortex reveal overlapping system-level architecture. Nat Neurosci 23:1644–1654. https://doi.org/10.1038/s41593-020-00719-y
Finn ES, Bandettini PA (2021) Movie-watching outperforms rest for functional connectivity-based prediction of behavior. Neuroimage 235:117963. https://doi.org/10.1016/j.neuroimage.2021.117963
Finn ES, Shen X, Scheinost D, Rosenberg MD, Huang J, Chun MM, Papademetris X, Constable RT (2015) Functional connectome fingerprinting: identifying individuals using patterns of brain connectivity. Nat Neurosci 18:1664–1671. https://doi.org/10.1038/nn.4135
Fornito A, Harrison BJ, Zalesky A, Simons JS (2012) Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection. Proc Natl Acad Sci U S A 109:12788–12793. https://doi.org/10.1073/pnas.1204185109
Freitas LGA, Bolton TAW, Krikler BE, Jochaut D, Giraud A-L, Hüppi PS, Van De Ville D (2020) Time-resolved effective connectivity in task fMRI: psychophysiological interactions of Co-activation patterns. Neuroimage 212:116635. https://doi.org/10.1016/j.neuroimage.2020.116635
Friston KJ (1994) Functional and effective connectivity in neuroimaging: a synthesis. Hum Brain Mapp 2:56–78. https://doi.org/10.1002/hbm.460020107
Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6:218–229
Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R (1996) Movement-related effects in fMRI time-series. Magn Reson Med off J Soc Magn Reson Med Soc Magn Reson Med 35:346–355. https://doi.org/10.1002/mrm.1910350312
Fu Z, Chan S-C, Di X, Biswal B, Zhang Z (2014) Adaptive covariance estimation of non-stationary processes and its application to infer dynamic connectivity from fMRI. IEEE Trans Biomed Circuits Syst 8:228–239. https://doi.org/10.1109/TBCAS.2014.2306732
Fu Z, Tu Y, Di X, Biswal BB, Calhoun VD, Zhang Z (2017) Associations between functional connectivity dynamics and bold dynamics are heterogeneous across brain networks. Front Hum Neurosci 11:593. https://doi.org/10.3389/fnhum.2017.00593
Hasson U, Nir Y, Levy I, Fuhrmann G, Malach R (2004) Intersubject synchronization of cortical activity during natural vision. Science 303:1634–1640. https://doi.org/10.1126/science.1089506
Hutchison RM, Womelsdorf T, Allen EA, Bandettini PA, Calhoun VD, Corbetta M, Della Penna S, Duyn JH, Glover GH, Gonzalez-Castillo J, Handwerker DA, Keilholz S, Kiviniemi V, Leopold DA, de Pasquale F, Sporns O, Walter M, Chang C (2013) Dynamic functional connectivity: promise, issues, and interpretations. Neuroimage 80:360–378. https://doi.org/10.1016/j.neuroimage.2013.05.079
Kauppi J-P, Jääskeläinen IP, Sams M, Tohka J (2010) Inter-subject correlation of brain hemodynamic responses during watching a movie: localization in space and frequency. Front Neuroinformatics 4:5. https://doi.org/10.3389/fninf.2010.00005
Koster-Hale J, Saxe R (2013) Theory of mind: a neural prediction problem. Neuron 79:836–848. https://doi.org/10.1016/j.neuron.2013.08.020
Krienen FM, Yeo BTT, Buckner RL (2014) Reconfigurable task-dependent functional coupling modes cluster around a core functional architecture. Philos Trans R Soc Lond B Biol Sci 369:20130526. https://doi.org/10.1098/rstb.2013.0526
Laumann TO, Snyder AZ (2021) Brain activity is not only for thinking. Curr Opin Behav Sci Deep Imaging Personalized Neurosci 40:130–136. https://doi.org/10.1016/j.cobeha.2021.04.002
Lindquist MA, Xu Y, Nebel MB, Caffo BS (2014) Evaluating dynamic bivariate correlations in resting-state fMRI: a comparison study and a new approach. Neuroimage 101:531–546. https://doi.org/10.1016/j.neuroimage.2014.06.052
Lurie DJ, Kessler D, Bassett DS, Betzel RF, Breakspear M, Kheilholz S, Kucyi A, Liégeois R, Lindquist MA, McIntosh AR, Poldrack RA, Shine JM, Thompson WH, Bielczyk NZ, Douw L, Kraft D, Miller RL, Muthuraman M, Pasquini L, Razi A, Vidaurre D, Xie H, Calhoun VD (2020) Questions and controversies in the study of time-varying functional connectivity in resting fMRI. Netw Neurosci 4:30–69. https://doi.org/10.1162/netn_a_00116
Margulies DS, Ghosh SS, Goulas A, Falkiewicz M, Huntenburg JM, Langs G, Bezgin G, Eickhoff SB, Castellanos FX, Petrides M, Jefferies E, Smallwood J (2016) Situating the default-mode network along a principal gradient of macroscale cortical organization. Proc Natl Acad Sci 113:12574–12579. https://doi.org/10.1073/pnas.1608282113
McAvoy M, Mitra A, Coalson RS, d’Avossa G, Keidel JL, Petersen SE, Raichle ME (2016) Unmasking language lateralization in human brain intrinsic activity. Cereb Cortex 26:1733–1746. https://doi.org/10.1093/cercor/bhv007
Nastase SA, Gazzola V, Hasson U, Keysers C (2019) Measuring shared responses across subjects using intersubject correlation. Soc Cogn Affect Neurosci 14:667–685. https://doi.org/10.1093/scan/nsz037
Nishimoto S, Vu AT, Naselaris T, Benjamini Y, Yu B, Gallant JL (2011) Reconstructing visual experiences from brain activity evoked by natural movies. Curr Biol 21:1641–1646. https://doi.org/10.1016/j.cub.2011.08.031
O’Connor D, Potler NV, Kovacs M, Xu T, Ai L, Pellman J, Vanderwal T, Parra LC, Cohen S, Ghosh S, Escalera J, Grant-Villegas N, Osman Y, Bui A, Craddock RC, Milham MP (2017) The healthy brain network serial scanning initiative: a resource for evaluating inter-individual differences and their reliabilities across scan conditions and sessions. GigaScience 6:1–14. https://doi.org/10.1093/gigascience/giw011
Poldrack RA (2006) Can cognitive processes be inferred from neuroimaging data? Trends Cogn Sci 10:59–63. https://doi.org/10.1016/j.tics.2005.12.004
Richardson H, Lisandrelli G, Riobueno-Naylor A, Saxe R (2018) Development of the social brain from age three to twelve years. Nat Commun 9:1–12. https://doi.org/10.1038/s41467-018-03399-2
Salvador R, Suckling J, Coleman MR, Pickard JD, Menon D, Bullmore E (2005) Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb Cortex NY 1991(15):1332–1342. https://doi.org/10.1093/cercor/bhi016
Schurz M, Radua J, Tholen MG, Maliske L, Margulies DS, Mars RB, Sallet J, Kanske P (2021) Toward a hierarchical model of social cognition: a neuroimaging meta-analysis and integrative review of empathy and theory of mind. Psychol Bull 147:293–327. https://doi.org/10.1037/bul0000303
Silk TJ, Bellgrove MA, Wrafter P, Mattingley JB, Cunnington R (2010) Spatial working memory and spatial attention rely on common neural processes in the intraparietal sulcus. Neuroimage 53:718–724. https://doi.org/10.1016/j.neuroimage.2010.06.068
Simony E, Chang C (2020) Analysis of stimulus-induced brain dynamics during naturalistic paradigms. Neuroimage 216:116461. https://doi.org/10.1016/j.neuroimage.2019.116461
Simony E, Honey CJ, Chen J, Lositsky O, Yeshurun Y, Wiesel A, Hasson U (2016) Dynamic reconfiguration of the default mode network during narrative comprehension. Nat Commun 7:12141. https://doi.org/10.1038/ncomms12141
Sun Y, Ma J, Huang M, Yi Y, Wang Y, Gu Y, Lin Y, Li LMW, Dai Z (2022) Functional connectivity dynamics as a function of the fluctuation of tension during film watching. Brain Imaging Behav 16(3):1260–1274. https://doi.org/10.1007/s11682-021-00593-7
Thompson WH, Fransson P (2015) The mean–variance relationship reveals two possible strategies for dynamic brain connectivity analysis in fMRI. Front Hum Neurosci 9:398. https://doi.org/10.3389/fnhum.2015.00398
Tian L, Ye M, Chen C, Cao X, Shen T (2021) Consistency of functional connectivity across different movies. Neuroimage 233:117926. https://doi.org/10.1016/j.neuroimage.2021.117926
Tian Y, Margulies DS, Breakspear M, Zalesky A (2020) Topographic organization of the human subcortex unveiled with functional connectivity gradients. Nat Neurosci 23:1421–1432. https://doi.org/10.1038/s41593-020-00711-6
Vanderwal T, Eilbott J, Castellanos FX (2019) Movies in the magnet: naturalistic paradigms in developmental functional neuroimaging. Dev Cogn Neurosci 36:100600. https://doi.org/10.1016/j.dcn.2018.10.004
Vos de Wael R, Benkarim O, Paquola C, Lariviere S, Royer J, Tavakol S, Xu T, Hong S-J, Langs G, Valk S, Misic B, Milham M, Margulies D, Smallwood J, Bernhardt BC (2020) BrainSpace: a toolbox for the analysis of macroscale gradients in neuroimaging and connectomics datasets. Commun Biol 3:1–10. https://doi.org/10.1038/s42003-020-0794-7
Wang Y, Metoki A, Xia Y, Zang Y, He Y, Olson IR (2021) A large-scale structural and functional connectome of social mentalizing. Neuroimage 236:118115. https://doi.org/10.1016/j.neuroimage.2021.118115
Yeo BTT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Roffman JL, Smoller JW, Zöllei L, Polimeni JR, Fischl B, Liu H, Buckner RL (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 106:1125–1165. https://doi.org/10.1152/jn.00338.2011
Yuan R, Di X, Taylor PA, Gohel S, Tsai Y-H, Biswal BB (2016) Functional topography of the thalamocortical system in human. Brain Struct Funct 221:1971–1984. https://doi.org/10.1007/s00429-015-1018-7
Zhang C, Baum SA, Adduru VR, Biswal BB, Michael AM (2018) Test-retest reliability of dynamic functional connectivity in resting state fMRI. Neuroimage 183:907–918. https://doi.org/10.1016/j.neuroimage.2018.08.021
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This study was supported by (US) National Institutes of Health Grants R15MH125332 (XD), R01MH131335 (BB), and R01AT009829 (BB).
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XD contributed to the study conception and data analysis. All authors have discussed the results. The first draft of the manuscript was written by XD and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Di, X., Zhang, Z., Xu, T. et al. Dynamic and stationary brain connectivity during movie watching as revealed by functional MRI. Brain Struct Funct 227, 2299–2312 (2022). https://doi.org/10.1007/s00429-022-02522-w
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DOI: https://doi.org/10.1007/s00429-022-02522-w