Abstract
As a complex dynamic system, the brain exhibits spatially organized recurring patterns of activity over time. Coactivation patterns (CAPs), which analyzes data from each single frame, have been utilized to detect transient brain activity states recently. However, previous CAP analyses have been conducted at the group level, which might neglect meaningful individual differences. Here, we estimated individual CAP states at both subject- and scan-level based on a densely sampled dataset: Midnight Scan Club. We used differential identifiability, which measures the gap between intra- and inter-subject similarity, to evaluate individual differences. We found individual CAPs at the subject-level achieved the best fingerprinting ability by maintaining high intra-subject similarity and enlarging inter-subject differences, and brain regions of association networks mainly contributed to the identifiability. On the other hand, scan-level CAP states were unstable across scans for the same participant. Expectedly, we found subject-specific CAPs became more reliable and discriminative with more data (i.e., longer duration). As the acquisition time of each participant is limited in practice, our results recommend a data collection strategy that collects more scans with appropriate duration (e.g., 12 ~ 15 min/scan) to obtain more reliable subject-specific CAPs, when total acquisition time is fixed (e.g., 150 min). In summary, this work has constructed reliable subject-specific CAP states with meaningful individual differences, and recommended an appropriate data collection strategy, which can guide subsequent investigations into individualized brain dynamics.
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Data availability
The preprocessed Midnight Scan Club (MSC) data used in this study are available in the OpenfMRI data repository at https://openneuro.org/datasets/ds000224. The code used for CAP state can be found in https://github.com/davidyoung1994/CoactivationPattern.
References
Akhrif A, Romanos M, Domschke K, Schmitt-Boehrer A, Neufang S (2018) Fractal analysis of BOLD time series in a network associated with waiting impulsivity. Front Physiol 9:1378. https://doi.org/10.3389/fphys.2018.01378
Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD (2014) Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex 24(3):663–676. https://doi.org/10.1093/cercor/bhs352
Amico E, Goni J (2018) The quest for identifiability in human functional connectomes. Sci Rep 8(1):8254. https://doi.org/10.1038/s41598-018-25089-1
Bari S, Amico E, Vike N, Talavage TM, Goni J (2019) Uncovering multi-site identifiability based on resting-state functional connectomes. Neuroimage 202:115967. https://doi.org/10.1016/j.neuroimage.2019.06.045
Betzel RF, Cutts SA, Greenwell S, Faskowitz J, Sporns O (2022) Individualized event structure drives individual differences in whole-brain functional connectivity. Neuroimage 252:118993. https://doi.org/10.1016/j.neuroimage.2022.118993
Cash RFH, Cocchi L, Lv J, Wu Y, Fitzgerald PB, Zalesky A (2021) Personalized connectivity-guided DLPFC-TMS for depression: advancing computational feasibility, precision and reproducibility. Hum Brain Mapp 42(13):4155–4172. https://doi.org/10.1002/hbm.25330
Chen JE, Chang C, Greicius MD, Glover GH (2015) Introducing co-activation pattern metrics to quantify spontaneous brain network dynamics. Neuroimage 111:476–488. https://doi.org/10.1016/j.neuroimage.2015.01.057
Cho JW, Korchmaros A, Vogelstein JT, Milham MP, Xu T (2021) Impact of concatenating fMRI data on reliability for functional connectomics. Neuroimage 226:117549. https://doi.org/10.1016/j.neuroimage.2020.117549
Cole MW, Reynolds JR, Power JD, Repovs G, Anticevic A, Braver TS (2013) Multi-task connectivity reveals flexible hubs for adaptive task control. Nat Neurosci 16(9):1348-U1247. https://doi.org/10.1038/nn.3470
Cole MW, Bassett DS, Power JD, Braver TS, Petersen SE (2014) Intrinsic and task-evoked network architectures of the human brain. Neuron 83(1):238–251. https://doi.org/10.1016/j.neuron.2014.05.014
Cui ZX, Li HM, Xia CH, Larsen B, Adebimpe A, Baum GL, Satterthwaite TD (2020) Individual variation in functional topography of association networks in youth. Neuron 106(2):340. https://doi.org/10.1016/j.neuron.2020.01.029
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(12):1644–1654. https://doi.org/10.1038/s41593-020-00719-y
Finn ES, Shen XL, Scheinost D, Rosenberg MD, Huang J, Chun MM, Constable RT (2015) Functional connectome fingerprinting: identifying individuals using patterns of brain connectivity. Nat Neurosci 18(11):1664–1671. https://doi.org/10.1038/nn.4135
Finn ES, Scheinost D, Finn DM, Shen XL, Papademetris X, Constable RT (2017) Can brain state be manipulated to emphasize individual differences in functional connectivity? Neuroimage 160:140–151. https://doi.org/10.1016/j.neuroimage.2017.03.064
Gordon EM, Laumann TO, Adeyemo B, Gilmore AW, Nelson SM, Dosenbach NUF, Petersen SE (2017a) Individual-specific features of brain systems identified with resting state functional correlations. Neuroimage 146:918–939. https://doi.org/10.1016/j.neuroimage.2016.08.032
Gordon EM, Laumann TO, Gilmore AW, Newbold DJ, Greene DJ, Berg JJ, Dosenbach NUF (2017b) Precision functional mapping of individual human brains. Neuron 95(4):791–807. https://doi.org/10.1016/j.neuron.2017.07.011
Gratton C, Laumann TO, Nielsen AN, Greene DJ, Gordon EM, Gilmore AW, Petersen SE (2018) Functional brain networks are dominated by stable group and individual factors, not cognitive or daily variation. Neuron 98(2):439-452 e435. https://doi.org/10.1016/j.neuron.2018.03.035
Greene DJ, Marek S, Gordon EM, Siegel JS, Gratton C, Laumann TO, Dosenbach NUF (2020) Integrative and network-specific connectivity of the basal ganglia and thalamus defined in individuals. Neuron 105(4):742-758 e746. https://doi.org/10.1016/j.neuron.2019.11.012
Gutierrez-Barragan D, Basson MA, Panzeri S, Gozzi A (2019) Infraslow state fluctuations govern spontaneous fMRI network dynamics. Curr Biol 29(14):2295–2306. https://doi.org/10.1016/j.cub.2019.06.017
Horien C, Shen XL, Scheinost D, Constable RT (2019) The individual functional connectome is unique and stable over months to years. Neuroimage 189:676–687. https://doi.org/10.1016/j.neuroimage.2019.02.002
Huang Z, Zhang J, Wu J, Mashour GA, Hudetz AG (2020) Temporal circuit of macroscale dynamic brain activity supports human consciousness. Sci Adv 6(11):aaz0087. https://doi.org/10.1126/sciadv.aaz0087
Hutchison RM, Womelsdorf T, Allen EA, Bandettini PA, Calhoun VD, Corbetta 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
Jo Y, Faskowitz J, Esfahlani FZ, Sporns O, Betzel RF (2021) Subject identification using edge-centric functional connectivity. Neuroimage 238:118204. https://doi.org/10.1016/j.neuroimage.2021.118204
Kaiser RH, Kang MS, Lew Y, Van Der Feen J, Aguirre B, Clegg R, Pizzagalli DA (2019) Abnormal frontoinsular-default network dynamics in adolescent depression and rumination: a preliminary resting-state co-activation pattern analysis. Neuropsychopharmacology 44(9):1604–1612. https://doi.org/10.1038/s41386-019-0399-3
Kaufmann T, Alnaes D, Doan NT, Brandt CL, Andreassen OA, Westlye LT (2017) Delayed stabilization and individualization in connectome development are related to psychiatric disorders. Nat Neurosci 20(4):513. https://doi.org/10.1038/nn.4511
Kong R, Li J, Orban C, Sabuncu MR, Liu H, Schaefer A, Yeo BTT (2019) Spatial topography of individual-specific cortical networks predicts human cognition, personality, and emotion. Cereb Cortex 29(6):2533–2551. https://doi.org/10.1093/cercor/bhy123
Krienen FM, Yeo BT, Buckner RL (2014) Reconfigurable task-dependent functional coupling modes cluster around a core functional architecture. Philos Trans R Soc Lond B Biol Sci. https://doi.org/10.1098/rstb.2013.0526
Kuhn HW (1955) The Hungarian method for the assignment problem. Naval Res Logist Q 2(1–2):83–97
Kumar K, Desrosiers C, Siddiqi K, Colliot O, Toews M (2017) Fiberprint: a subject fingerprint based on sparse code pooling for white matter fiber analysis. Neuroimage 158:242–259. https://doi.org/10.1016/j.neuroimage.2017.06.083
Kupis L, Goodman ZT, Kornfeld S, Hoang S, Romero C, Dirks B, Uddin LQ (2021) Brain dynamics underlying cognitive flexibility across the lifespan. Cereb Cortex 31(11):5263–5274. https://doi.org/10.1093/cercor/bhab156
Laumann TO, Gordon EM, Adeyemo B, Snyder AZ, Joo SJ, Chen MY, Petersen SE (2015) Functional system and areal organization of a highly sampled individual human brain. Neuron 87(3):657–670. https://doi.org/10.1016/j.neuron.2015.06.037
Liu X, Duyn JH (2013) Time-varying functional network information extracted from brief instances of spontaneous brain activity. Proc Natl Acad Sci USA 110(11):4392–4397. https://doi.org/10.1073/pnas.1216856110
Liu X, Chang C, Duyn JH (2013) Decomposition of spontaneous brain activity into distinct fMRI co-activation patterns. Front Syst Neurosci 7:101. https://doi.org/10.3389/fnsys.2013.00101
Liu X, Zhang N, Chang C, Duyn JH (2018) Co-activation patterns in resting-state fMRI signals. Neuroimage 180(Pt B):485–494. https://doi.org/10.1016/j.neuroimage.2018.01.041
Lynch CJ, Breeden AL, Gordon EM, Cherry JBC, Turkeltaub PE, Vaidya CJ (2019) Precision inhibitory stimulation of individual-specific cortical hubs disrupts information processing in humans. Cereb Cortex 29(9):3912–3921. https://doi.org/10.1093/cercor/bhy270
Marek S, Tervo-Clemmens B, Calabro FJ, Montez DF, Kay BP, Hatoum AS, Dosenbach NUF (2022) Reproducible brain-wide association studies require thousands of individuals. Nature 603(7902):654–660. https://doi.org/10.1038/s41586-022-04492-9
Marquand AF, Rezek I, Buitelaar J, Beckmann CF (2016) Understanding heterogeneity in clinical cohorts using normative models: beyond case-control studies. Biol Psychiat 80(7):552–561. https://doi.org/10.1016/j.biopsych.2015.12.023
Meer JNV, Breakspear M, Chang LJ, Sonkusare S, Cocchi L (2020) Movie viewing elicits rich and reliable brain state dynamics. Nat Commun 11(1):5004. https://doi.org/10.1038/s41467-020-18717-w
Meissner TW, Walbrin J, Nordt M, Koldewyn K, Weigelt S (2020) Head motion during fMRI tasks is reduced in children and adults if participants take breaks. Dev Cogn Neurosci 44:100803
Menon SS, Krishnamurthy K (2019) A comparison of static and dynamic functional connectivities for identifying subjects and biological sex using intrinsic individual brain connectivity. Sc Rep 9:5729. https://doi.org/10.1038/s41598-019-42090-4
Mueller S, Wang D, Fox MD, Yeo BT, Sepulcre J, Sabuncu MR, Liu H (2013) Individual variability in functional connectivity architecture of the human brain. Neuron 77(3):586–595. https://doi.org/10.1016/j.neuron.2012.12.028
Murray L, Maurer JM, Peechatka AL, Frederick BB, Kaiser RH, Janes AC (2021) Sex differences in functional network dynamics observed using coactivation pattern analysis. Cogn Neurosci 12(3–4):120–130. https://doi.org/10.1080/17588928.2021.1880383
Pallares V, Insabato A, Sanjuan A, Kuhn S, Mantini D, Deco G, Gilson M (2018) Extracting orthogonal subject- and condition-specific signatures from fMRI data using whole-brain effective connectivity. Neuroimage 178:238–254. https://doi.org/10.1016/j.neuroimage.2018.04.070
Peng X, Liu Q, Hubbard CS, Wang D, Zhu W, Fox MD, Liu H (2023) Robust dynamic brain coactivation states estimated in individuals. Sci Adv 9(3):eabq8566. https://doi.org/10.1126/sciadv.abq8566
Piguet C, Karahanoglu FI, Saccaro LF, Van De Ville D, Vuilleumier P (2021) Mood disorders disrupt the functional dynamics, not spatial organization of brain resting state networks. Neuroimage Clin 32:102833. https://doi.org/10.1016/j.nicl.2021.102833
Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59(3):2142–2154. https://doi.org/10.1016/j.neuroimage.2011.10.018
Preti MG, Bolton TAW, Van De Ville D (2017) The dynamic functional connectome: state-of-the-art and perspectives. Neuroimage 160:41–54. https://doi.org/10.1016/j.neuroimage.2016.12.061
Price RB, Lane S, Gates K, Kraynak TE, Horner MS, Thase ME, Siegle GJ (2017) Parsing heterogeneity in the brain connectivity of depressed and healthy adults during positive mood. Biol Psychiat 81(4):347–357. https://doi.org/10.1016/j.biopsych.2016.06.023
Rey G, Bolton TAW, Gaviria J, Piguet C, Preti MG, Favre S, Vuilleumier P (2021) Dynamics of amygdala connectivity in bipolar disorders: a longitudinal study across mood states. Neuropsychopharmacology 46(9):1693–1701. https://doi.org/10.1038/s41386-021-01038-x
Salehi M, Greene AS, Karbasi A, Shen XL, Scheinost D, Constable RT (2020a) There is no single functional atlas even for a single individual: Functional parcel definitions change with task. Neuroimage 208:116366. https://doi.org/10.1016/j.neuroimage.2019.116366
Salehi M, Karbasi A, Barron DS, Scheinost D, Constable RT (2020b) Individualized functional networks reconfigure with cognitive state. Neuroimage 206:116233. https://doi.org/10.1016/j.neuroimage.2019.116233
Satterthwaite TD, Xia CH, Bassett DS (2018) Personalized neuroscience: common and individual-specific features in functional brain networks. Neuron 98(2):243–245. https://doi.org/10.1016/j.neuron.2018.04.007
Schaefer A, Kong R, Gordon EM, Laumann TO, Zuo XN, Holmes AJ, Yeo BTT (2018) Local-global parcellation of the human cerebral cortex from intrinsic functional connectivity MRI. Cereb Cortex 28(9):3095–3114. https://doi.org/10.1093/cercor/bhx179
Seitzman BA, Gratton C, Laumann TO, Gordon EM, Adeyemo B, Dworetsky A, Petersen SE (2019) Trait-like variants in human functional brain networks. Proc Natl Acad Sci USA 116(45):22851–22861. https://doi.org/10.1073/pnas.1902932116
Sepulcre J, Liu H, Talukdar T, Martincorena I, Yeo BT, Buckner RL (2010) The organization of local and distant functional connectivity in the human brain. PLoS Comput Biol 6(6):e1000808. https://doi.org/10.1371/journal.pcbi.1000808
Sorrentino P, Rucco R, Lardone A, Liparoti M, Lopez ET, Cavaliere C, Amico E (2021) Clinical connectome fingerprints of cognitive decline. Neuroimage 238:118253. https://doi.org/10.1016/j.neuroimage.2021.118253
Sui J, Jiang R, Bustillo J, Calhoun V (2020) Neuroimaging-based individualized prediction of cognition and behavior for mental disorders and health: methods and promises. Biol Psychiatry 88(11):818–828. https://doi.org/10.1016/j.biopsych.2020.02.016
Tarun A, Behjat H, Bolton T, Abramian D, Van De Ville D (2020) Structural mediation of human brain activity revealed by white-matter interpolation of fMRI. Neuroimage 213:116718. https://doi.org/10.1016/j.neuroimage.2020.116718
Van Dijk KR, Sabuncu MR, Buckner RL (2012) The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 59(1):431–438. https://doi.org/10.1016/j.neuroimage.2011.07.044
Vanderwal T, Eilbott J, Finn ES, Craddock RC, Turnbull A, Castellanos FX (2017) Individual differences in functional connectivity during naturalistic viewing conditions. Neuroimage 157:521–530. https://doi.org/10.1016/j.neuroimage.2017.06.027
Wang DH, Li ML, Wang MY, Schoeppe F, Ren JX, Chen HF, Liu HS (2018) Individual-specific functional connectivity markers track dimensional and categorical features of psychotic illness (vol 25, 2119, 2020). Mol Psychiatry 25(9):2200–2200. https://doi.org/10.1038/s41380-018-0340-x
Xu T, Kiar G, Cho JW, Bridgeford EW, Nikolaidis A, Vogelstein JT, Milham MP (2023) ReX: an integrative tool for quantifying and optimizing measurement reliability for the study of individual differences. Nat Methods. https://doi.org/10.1038/s41592-023-01901-3
Yang H, Zhang H, Di X, Wang S, Meng C, Tian L, Biswal B (2021) Reproducible coactivation patterns of functional brain networks reveal the aberrant dynamic state transition in schizophrenia. Neuroimage. https://doi.org/10.1016/j.neuroimage.2021.118193
Yang H, Zhang H, Meng C, Wohlschläger A, Brandl F, Di X, Biswal B (2022) Frequency-specific coactivation patterns in resting-state and their alterations in schizophrenia: an fMRI study. Hum Brain Mapp 43(12):3792–3808
Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Buckner RL (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 106(3):1125–1165. https://doi.org/10.1152/jn.00338.2011
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
Acknowledgements
We thank Evan M. Gordon and his team for collecting and sharing the midnight scan club data. This work was supported by the National Natural Science Foundation of China (NSFC) grant (No. 61871420 and 62071109).
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This work was supported by the National Natural Science Foundation of China (NSFC) grant (No. 61871420 and 62071109).
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HY: conceptualization, methodology, software, data analysis, writing original draft, revision, and editing. XY: data analysis, and reviewing. HZ: data analysis, and reviewing. CM: reviewing, methodology and editing. BB: conceptualization, methodology, software, revision, and editing.
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Yang, H., Yao, X., Zhang, H. et al. Estimating dynamic individual coactivation patterns based on densely sampled resting-state fMRI data and utilizing it for better subject identification. Brain Struct Funct 228, 1755–1769 (2023). https://doi.org/10.1007/s00429-023-02689-w
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DOI: https://doi.org/10.1007/s00429-023-02689-w