Functional Connectivity Mapping in the Animal Model: Principles and Applications of Resting-State fMRI
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‘Resting-state’ fMRI has substantially contributed to the understanding of human and non-human functional brain organization by the analysis of correlated patterns in spontaneous activity within dedicated brain systems. Spontaneous neural activity is indirectly measured from the blood oxygenation level dependent (BOLD) signal as acquired by echo planar imaging, when subjects quietly ‘resting’ in the scanner. Animal models including disease or knockout models allow a broad spectrum of experimental manipulations not applicable in humans. The noninvasive fMRI approach provides a promising tool for cross-species comparative investigations. This review focuses on the principles of ‘resting-state’ functional connectivity analysis and its applications to living animals. The translational aspect from in vivo animal models towards clinical applications in humans is emphasized. We introduce the fMRI-based investigation of the non-human brain’s hemodynamics, the methodological issues in the data postprocessing, and the functional data interpretation from different abstraction levels. The longer-term goal of integrating fMRI connectivity data with structural connectomes obtained with tracing and optical imaging approaches is presented and will allow the interrogation of fMRI data in terms of directional flow of information and may identify the structural underpinnings of observed functional connectivity patterns.
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Connectome properties have been shown to be preserved across species and therefore provide a unique translational bridge between preclinical and clinical studies.
“Connectome properties have been shown to be preserved across species and therefore provide a unique translational bridge between preclinical and clinical studies (Gorges et al., 2017; Oh et al., 2014; Stafford et al., 2014; van den Heuvel, Bullmore, & Sporns, 2016).”
From Functional and structural connectome properties in the 5XFAD transgenic mouse model of Alzheimer’s disease (2018) · cites this paper as Gorges et al., 2017
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Exploring the brain network: A review on resting-state fMRI functional connectivity
van den Heuvel, M. P., & Hulshoff Pol, H. E. (2010) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2010.03.008 · Cited by 3,326 · see citing works
Functional connectome fingerprinting: Identifying individuals using patterns of brain connectivity
Finn, E. S., Shen, X., Scheinost, D., Rosenberg, M. D., Huang, J., Chun, M. M., Papademetris, X., & Constable, R. T. (2015) · Nature Neuroscience · doi:10.1038/nn.4135 · Cited by 2,747 · see citing works
Buckner, R. L., Snyder, A. Z., Shannon, B. J., LaRossa, G., Sachs, R., Fotenos, A. F., Sheline, Y. I., Klunk, W. E., Mathis, C. A., Morris, J. C., et al. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2177-05.2005 · Cited by 2,140 · see citing works
Network hubs in the human brain
van den Heuvel, M. P., & Sporns, O. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.09.012 · Cited by 2,123 · cited 1× · see citing works
“Features such as highly connected neuron populations (“hubs”) (122), modularity (116), rich-club organization (123), and efficient small-world topology (70) can be systematically quantified by means of graph theory (124) across species.”
BackgroundElectrophysiological signatures of resting state networks in the human brain
Mantini, D., Perrucci, M. G., Del Gratta, C., Romani, G. L., & Corbetta, M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700668104 · Cited by 1,938 · see citing works
Self-propagation of pathogenic protein aggregates in neurodegenerative diseases
Jucker, M., & Walker, L. C. (2013) · Nature · doi:10.1038/nature12481 · Cited by 1,663 · see citing works
Raichle, M. E. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.01.008 · Cited by 1,111 · see citing works
Behavioral interpretations of intrinsic connectivity networks
Laird, A. R., Fox, P. M., Eickhoff, S. B., Turner, J. A., Ray, K. L., McKay, D. R., Glahn, D. C., Beckmann, C. F., Smith, S. M., & Fox, P. T. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00077 · Cited by 1,023 · see citing works
Allen Brain Atlas: an integrated spatio-temporal portal for exploring the central nervous system
Sunkin, S. M., Ng, L., Lau, C., Dolbeare, T., Gilbert, T. L., Thompson, C. L., Hawrylycz, M., & Dang, C. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1042 · Cited by 796 · see citing works
The restless brain: How intrinsic activity organizes brain function
Raichle, M. E. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0172 · Cited by 433 · see citing works
Yang, C.-C., Barrós-Loscertales, A., Pinazo, D., Ventura-Campos, N., Borchardt, V., Bustamante, J.-C., Rodríguez-Pujadas, A., Fuentes-Claramonte, P., Balaguer, R., Ávila, C., et al. (2016) · Neural Plasticity · doi:10.1155/2016/9504642 · Cited by 284 · see citing works
Resting State Networks and Consciousness
Heine, L., Soddu, A., Gómez, F., Vanhaudenhuyse, A., Tshibanda, L., Thonnard, M., Charland-Verville, V., Kirsch, M., Laureys, S., & Demertzi, A. (2012) · Frontiers in Psychology · doi:10.3389/fpsyg.2012.00295 · Cited by 272 · see citing works
Imaging of Functional Connectivity in the Mouse Brain
White, B. R., Bauer, A. Q., Snyder, A. Z., Schlaggar, B. L., Lee, J.-M., & Culver, J. P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016322 · Cited by 253 · see citing works
Large-scale topology and the default mode network in the mouse connectome
Stafford, J. M., Jarrett, B. R., Miranda-Dominguez, O., Mills, B. D., Cain, N., Mihalas, S., Lahvis, G. P., Lattal, K. M., Mitchell, S. H., David, S. V., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1404346111 · Cited by 229 · see citing works
A Dietary Treatment Improves Cerebral Blood Flow and Brain Connectivity in Aging apoE4 Mice
Wiesmann, M., Zerbi, V., Jansen, D., Haast, R., Lütjohann, D., Broersen, L. M., Heerschap, A., & Kiliaan, A. J. (2016) · Neural Plasticity · doi:10.1155/2016/6846721 · Cited by 60 · see citing works
Flagged first, then by citations
Research works printed but not linked: 139
- [1]Biswal BB. Resting state fMRI: a personal history. Neuroimage (2012) 62: 938– 44. 10.1016/j.neuroimage.2012.01.090 22326802 PMC12911935 · DOI
- [3]Biswal B Yetkin FZ Haughton VM Hyde JS. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med (1995) 34: 537– 41. 10.1002/mrm.1910340409 8524021 · DOI · Paper page
- [4]Van Dijk KRA Hedden T Venkataraman A Evans KC Lazar SW Buckner RL. Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J Neurophysiol (2010) 103: 297– 321. 10.1152/jn.00783.2009 19889849 PMC2807224 · DOI · Paper page
- [6]Oeltermann A Augath MA Logothetis NK. Simultaneous recording of neuronal signals and functional NMR imaging. Magn Reson Imaging (2007) 25: 760– 74. 10.1016/j.mri.2007.03.015 17478070 · DOI
- [8]Park H-J Friston K. Structural and functional brain networks: from connections to cognition. Science (2013) 342: 1238411. 10.1126/science.1238411 24179229 · DOI · Paper page
- [9]Smith SM Fox PT Miller KL Glahn DC Fox PM Mackay CE Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci U S A (2009) 106: 13040– 5. 10.1073/pnas.0905267106 19620724 PMC2722273 · DOI · Paper page
- [10]van den Heuvel MP Bullmore ET Sporns O. Comparative connectomics. Trends Cogn Sci (2016) 20: 345– 61. 10.1016/j.tics.2016.03.001 27026480 · DOI · Paper page
- [11]Raichle ME MacLeod AM Snyder AZ Powers WJ Gusnard DA Shulman GL. A default mode of brain function. Proc Natl Acad Sci U S A (2001) 98: 676– 82. 10.1073/pnas.98.2.676 11209064 PMC14647 · DOI · Paper page
- [12]Shulman GL Fiez JA Corbetta M Buckner RL Miezin FM Raichle ME Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J Cogn Neurosci (1997) 9: 648– 63. 10.1162/jocn.1997.9.5.624 23965122 · DOI
- [13]Wehrl HF Hossain M Lankes K Liu C-C Bezrukov I Martirosian P Simultaneous PET-MRI reveals brain function in activated and resting state on metabolic, hemodynamic and multiple temporal scales. Nat Med (2013) 19: 1184– 9. 10.1038/nm.3290 23975025 · DOI
- [14]Allen EA Erhardt EB Damaraju E Gruner W Segall JM Silva RF A baseline for the multivariate comparison of resting-state networks. Front Syst Neurosci (2011) 5: 2. 10.3389/fnsys.2011.00002 21442040 PMC3051178 · DOI
- [15]Guevara E Sadekova N Girouard H Lesage F. Optical imaging of resting-state functional connectivity in a novel arterial stiffness model. Biomed Opt Express (2013) 4: 2332– 46. 10.1364/BOE.4.002332 24298398 PMC3829531 · DOI
- [16]Schölvinck ML Maier A Ye FQ Duyn JH Leopold DA. Neural basis of global resting-state fMRI activity. Proc Natl Acad Sci U S A (2010) 107: 10238– 43. 10.1073/pnas.0913110107 20439733 PMC2890438 · DOI · Paper page
- [17]Laufs H Multimodal analysis of resting state cortical activity: what does EEG add to our knowledge of resting state BOLD networks? Neuroimage (2010) 52: 1171– 2. 10.1016/j.neuroimage.2010.05.034 20493268 · DOI
- [18]Pizoli CE Shah MN Snyder AZ Shimony JS Limbrick DD Raichle ME Resting-state activity in development and maintenance of normal brain function. Proc Natl Acad Sci U S A (2011) 108: 11638– 43. 10.1073/pnas.1109144108 21709227 PMC3136307 · DOI
- [19]Power JD Barnes KA Snyder AZ Schlaggar BL Petersen SE. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage (2012) 59: 2142– 54. 10.1016/j.neuroimage.2011.10.018 22019881 PMC3254728 · DOI · Paper page
- [20]Kassubek J The application of neuroimaging to healthy and diseased brains: present and future. Front Neurol (2017) 8: 61 10.3389/fneur.2017.00061 28286495 PMC5323372 · DOI
- [21]Mitra A Snyder AZ Tagliazucchi E Laufs H Raichle ME. Propagated infra-slow intrinsic brain activity reorganizes across wake and slow wave sleep. Elife (2015) 4: R774– 88. 10.7554/eLife.10781 26551562 PMC4737658 · DOI
- [22]Tagliazucchi E Laufs H. Decoding wakefulness levels from typical fMRI resting-state data reveals reliable drifts between wakefulness and sleep. Neuron (2014) 82: 695– 708. 10.1016/j.neuron.2014.03.020 24811386 · DOI
- [23]Kiviniemi V Jauhiainen J Tervonen O Pääkkö E Oikarinen J Vainionpää V Slow vasomotor fluctuation in fMRI of anesthetized child brain. Magn Reson Med (2000) 44: 373– 8. 10.1002/1522-2594(200009)44:3<373::AID-MRM5>3.0.CO;2-P 10975887 · DOI · Paper page
- [25]Smyser CD Snyder AZ Neil JJ. Functional connectivity MRI in infants: exploration of the functional organization of the developing brain. Neuroimage (2011) 56: 1437– 52. 10.1016/j.neuroimage.2011.02.073 21376813 PMC3089442 · DOI
- [26]Dosenbach NUF Nardos B Cohen AL Fair DA Power JD Church JA Prediction of individual brain maturity using fMRI. Science (2010) 329: 1358– 61. 10.1126/science.1194144 20829489 PMC3135376 · DOI · Paper page
- [27]Fornito A Zalesky A Bassett DS Meunier D Ellison-Wright I Yucel M Genetic influences on cost-efficient organization of human cortical functional networks. J Neurosci (2011) 31: 3261– 70. 10.1523/JNEUROSCI.4858-10.2011 21368038 PMC6623940 · DOI
- [28]Markett S de Reus MA Reuter M Montag C Weber B Schoene-Bake J-C Serotonin and the brain’s rich club-association between molecular genetic variation on the TPH2 gene and the structural connectome. Cereb Cortex (2016) 27(3): 2166– 74. 10.1093/cercor/bhw059 26975194 · DOI
- [29]Jonckers E Van Audekerke J De Visscher G Van der Linden A Verhoye M. Functional connectivity fMRI of the rodent brain: comparison of functional connectivity networks in rat and mouse. PLoS One (2011) 6: e18876. 10.1371/journal.pone.0018876 21533116 PMC3078931 · DOI
- [30]Liska A Galbusera A Schwarz AJ Gozzi A. Functional connectivity hubs of the mouse brain. Neuroimage (2015) 115: 281– 91. 10.1016/j.neuroimage.2015.04.033 25913701 · DOI · Paper page
- [31]Maier FC Wehrl HF Schmid AM Mannheim JG Wiehr S Lerdkrai C Longitudinal PET-MRI reveals β-amyloid deposition and rCBF dynamics and connects vascular amyloidosis to quantitative loss of perfusion. Nat Med (2014) 20: 1485– 92. 10.1038/nm.3734 25384087 · DOI
- [32]Sforazzini F Schwarz AJ Galbusera A Bifone A Gozzi A. Distributed BOLD and CBV-weighted resting-state networks in the mouse brain. Neuroimage (2014) 87: 403– 15. 10.1016/j.neuroimage.2013.09.050 24080504 · DOI
- [34]Tobin JE Xie M Le TQ Song S-K Armstrong RC. Reduced axonopathy and enhanced remyelination after chronic demyelination in fibroblast growth factor 2 (Fgf2)-null mice: differential detection with diffusion tensor imaging. J Neuropathol Exp Neurol (2011) 70: 157– 65. 10.1097/NEN.0b013e31820937e4 21343885 PMC3072283 · DOI
- [36]Hutchison RM Mirsattari SM Jones CK Gati JS Leung LS. Functional networks in the anesthetized rat brain revealed by independent component analysis of resting-state fMRI. J Neurophysiol (2010) 103: 3398– 406. 10.1152/jn.00141.2010 20410359 · DOI
- [37]Hyde JS Li R Functional connectivity in rat brain at 200 µm resolution. Brain Connect (2014) 4: 470– 80. 10.1089/brain.2014.0281 25112943 PMC4146383 · DOI
- [38]Liang Z King J Zhang N. Uncovering intrinsic connectional architecture of functional networks in awake rat brain. J Neurosci (2011) 31: 3776– 83. 10.1523/JNEUROSCI.4557-10.2011 21389232 PMC3073070 · DOI
- [39]Lu H Zou Q Gu H Raichle ME Stein EA Yang Y. Rat brains also have a default mode network. Proc Natl Acad Sci U S A (2012) 109: 3979– 84. 10.1073/pnas.1200506109 22355129 PMC3309754 · DOI
- [40]Majeed W Magnuson M Keilholz SD. Spatiotemporal dynamics of low frequency fluctuations in BOLD fMRI of the rat. J Magn Reson Imaging (2009) 30: 384– 93. 10.1002/jmri.21848 19629982 PMC2758521 · DOI
- [41]Pawela CP Biswal BB Cho YR Kao DS Li R Jones SR Resting-state functional connectivity of the rat brain. Magn Reson Med (2008) 59: 1021– 9. 10.1002/mrm.21524 18429028 PMC2562321 · DOI
- [42]Sierakowiak A Monnot C Aski SN Uppman M Li T-Q Damberg P Default mode network, motor network, dorsal and ventral basal ganglia networks in the rat brain: comparison to human networks using resting state-fMRI. PLoS One (2015) 10: e0120345. 10.1371/journal.pone.0120345 25789862 PMC4366046 · DOI
- [43]Schroeder MP Weiss C Procissi D Disterhoft JF Wang L. Intrinsic connectivity of neural networks in the awake rabbit. Neuroimage (2016) 129: 260– 7. 10.1016/j.neuroimage.2016.01.010 26774609 PMC4803608 · DOI
- [44]Berns GS Brooks AM Spivak M. Functional MRI in awake unrestrained dogs. PLoS One (2012) 7: e38027. 10.1371/journal.pone.0038027 22606363 PMC3350478 · DOI
- [45]De Groof G Jonckers E Güntürkün O Denolf P Van Auderkerke J Van der Linden A. Functional MRI and functional connectivity of the visual system of awake pigeons. Behav Brain Res (2013) 239: 43– 50. 10.1016/j.bbr.2012.10.044 23137696 · DOI
- [46]Hutchison RM Everling S. Monkey in the middle: why non-human primates are needed to bridge the gap in resting-state investigations. Front Neuroanat (2012) 6: 29. 10.3389/fnana.2012.00029 22855672 PMC3405297 · DOI
- [47]Hutchison RM Leung LS Mirsattari SM Gati JS Menon RS Everling S. Resting-state networks in the macaque at 7T. Neuroimage (2011) 56: 1546– 55. 10.1016/j.neuroimage.2011.02.063 21356313 · DOI
- [48]Hutchison RM Womelsdorf T Gati JS Everling S Menon RS. Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Hum Brain Mapp (2013) 34: 2154– 77. 10.1002/hbm.22058 22438275 PMC6870538 · DOI
- [49]Liu JV Hirano Y Nascimento GC Stefanovic B Leopold DA Silva AC. fMRI in the awake marmoset: somatosensory-evoked responses, functional connectivity, and comparison with propofol anesthesia. Neuroimage (2013) 78: 186– 95. 10.1016/j.neuroimage.2013.03.038 23571417 PMC3778909 · DOI
- [50]Mantini D Gerits A Nelissen K Durand J-B Joly O Simone L Default mode of brain function in monkeys. J Neurosci (2011) 31: 12954– 62. 10.1523/JNEUROSCI.2318-11.2011 21900574 PMC3686636 · DOI
- [51]Moeller S Nallasamy N Tsao DY Freiwald WA. Functional connectivity of the macaque brain across stimulus and arousal states. J Neurosci (2009) 29: 5897– 909. 10.1523/JNEUROSCI.0220-09.2009 19420256 PMC6665231 · DOI
- [52]Rilling JK Barks SK Parr LA Preuss TM Faber TL Pagnoni G A comparison of resting-state brain activity in humans and chimpanzees. Proc Natl Acad Sci U S A (2007) 104: 17146– 51. 10.1073/pnas.0705132104 17940032 PMC2040430 · DOI
- [53]Vincent JL Patel GH Fox MD Snyder AZ Baker JT Van Essen DC Intrinsic functional architecture in the anaesthetized monkey brain. Nature (2007) 447: 83– 6. 10.1038/nature05758 17476267 · DOI · Paper page
- [54]Gozzi A Schwarz AJ Large-scale functional connectivity networks in the rodent brain. Neuroimage (2015) 127: 496– 509. 10.1016/j.neuroimage.2015.12.017 26706448 · DOI
- [55]Bennett AJ Ringach DL. Animal research in neuroscience: a duty to engage. Neuron (2016) 92: 653– 7. 10.1016/j.neuron.2016.10.034 27810011 · DOI
- [56]Snyder AZ Raichle ME. A brief history of the resting state: the Washington University perspective. Neuroimage (2012) 62: 902– 10. 10.1016/j.neuroimage.2012.01.044 22266172 PMC3342417 · DOI
- [57]Müller H-P Kassubek J Vernikouskaya I Ludolph AC Stiller D Rasche V. Diffusion tensor magnetic resonance imaging of the brain in APP transgenic mice: a cohort study. PLoS One (2013) 8: e67630. 10.1371/journal.pone.0067630 23840754 PMC3695895 · DOI · Paper page
- [58]Pawela CP Biswal BB Hudetz AG Li R Jones SR Cho YR Interhemispheric neuroplasticity following limb deafferentation detected by resting-state functional connectivity magnetic resonance imaging (fcMRI) and functional magnetic resonance imaging (fMRI). Neuroimage (2010) 49: 2467– 78. 10.1016/j.neuroimage.2009.09.054 19796693 PMC2818026 · DOI
- [59]Pan W-J Billings JCW Grooms JK Shakil S Keilholz SD. Considerations for resting state functional MRI and functional connectivity studies in rodents. Front Neurosci (2015) 9: 269. 10.3389/fnins.2015.00269 26300718 PMC4525377 · DOI
- [60]Buckner RL Vincent JL. Unrest at rest: default activity and spontaneous network correlations. Neuroimage (2007) 37: 1091– 6. 10.1016/j.neuroimage.2007.01.010 17368915 · DOI · Paper page
- [61]Raichle ME The restless brain. Brain Connect (2011) 1: 3– 12. 10.1089/brain.2011.0019 22432951 PMC3621343 · DOI · Paper page
- [62]Nallasamy N Tsao DY Functional connectivity in the brain: effects of anesthesia. Neuroscientist (2011) 17: 94– 106. 10.1177/1073858410374126 21343409 · DOI
- [63]Buckner RL Andrews-Hanna JR Schacter DL. The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci (2008) 1124: 1– 38. 10.1196/annals.1440.011 18400922 · DOI · Paper page
- [64]Liang Z King J Zhang N. Intrinsic organization of the anesthetized brain. J Neurosci (2012) 32: 10183– 91. 10.1523/JNEUROSCI.1020-12.2012 22836253 PMC3422560 · DOI · Paper page
- [65]Bullmore E Sporns O. The economy of brain network organization. Nat Rev Neurosci (2012) 13: 336– 49. 10.1038/nrn3214 22498897 · DOI · Paper page
- [66]Buzsáki G Logothetis N Singer W. Scaling brain size, keeping timing: evolutionary preservation of brain rhythms. Neuron (2013) 80: 751– 64. 10.1016/j.neuron.2013.10.002 24183025 PMC4009705 · DOI · Paper page
- [67]Chen LM Yang P-F Wang F Mishra A Shi Z Wu R Biophysical and neural basis of resting state functional connectivity: evidence from non-human primates. Magn Reson Imaging (2017) 39: 71– 81. 10.1016/j.mri.2017.01.020 28161319 PMC5410395 · DOI
- [69]Festing S Wilkinson R The ethics of animal research. Talking point on the use of animals in scientific research. EMBO Rep (2007) 8: 526– 30. 10.1038/sj.embor.7400993 17545991 PMC2002542 · DOI
- [71]Zhan Y Paolicelli RC Sforazzini F Weinhard L Bolasco G Pagani F Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat Neurosci (2014) 17: 400– 6. 10.1038/nn.3641 24487234 · DOI · Paper page
- [73]Zerbi V Wiesmann M Emmerzaal TL Jansen D Van Beek M Mutsaers MPC Resting-state functional connectivity changes in aging apoE4 and apoE-KO mice. J Neurosci (2014) 34: 13963– 75. 10.1523/JNEUROSCI.0684-14.2014 25319693 PMC6705289 · DOI
- [75]Squillace M Dodero L Federici M Migliarini S Errico F Napolitano F Dysfunctional dopaminergic neurotransmission in asocial BTBR mice. Transl Psychiatry (2014) 4: e427. 10.1038/tp.2014.69 25136890 PMC4150243 · DOI
- [76]Harris NG Verley DR Gutman BA Thompson PM Yeh HJ Brown JA Disconnection and hyper-connectivity underlie reorganization after TBI: a rodent functional connectomic analysis. Exp Neurol (2015) 277: 124– 38. 10.1016/j.expneurol.2015.12.020 26730520 PMC4761291 · DOI
- [77]Tehranian R Rose ME Vagni V Griffith RP Wu S Maits S Transgenic mice that overexpress the anti-apoptotic Bcl-2 protein have improved histological outcome but unchanged behavioral outcome after traumatic brain injury. Brain Res (2006) 1101: 126– 35. 10.1016/j.brainres.2006.05.049 16782076 · DOI
- [78]Zhang D Raichle ME. Disease and the brain’s dark energy. Nat Rev Neurol (2010) 6: 15– 28. 10.1038/nrneurol.2009.198 20057496 · DOI
- [79]Logothetis NK. What we can do and what we cannot do with fMRI. Nature (2008) 453: 869– 78. 10.1038/nature06976 18548064 · DOI · Paper page
- [80]Hiltunen T Kantola J Abou Elseoud A Lepola P Suominen K Starck T Infra-slow EEG fluctuations are correlated with resting-state network dynamics in fMRI. J Neurosci (2014) 34: 356– 62. 10.1523/JNEUROSCI.0276-13.2014 24403137 PMC6608153 · DOI
- [81]Hughes JR. Gamma, fast, and ultrafast waves of the brain: their relationships with epilepsy and behavior. Epilepsy Behav (2008) 13: 25– 31. 10.1016/j.yebeh.2008.01.011 18439878 · DOI
- [82]Feinberg DA Yacoub E. The rapid development of high speed, resolution and precision in fMRI. Neuroimage (2012) 62: 720– 5. 10.1016/j.neuroimage.2012.01.049 22281677 PMC3389295 · DOI
- [83]Hutchison RM Womelsdorf T Gati JS Leung LS Menon RS Everling S. Resting-state connectivity identifies distinct functional networks in macaque cingulate cortex. Cereb Cortex (2012) 22: 1294– 308. 10.1093/cercor/bhr181 21840845 · DOI
- [84]Choi EY Yeo BTT Buckner RL. The organization of the human striatum estimated by intrinsic functional connectivity. J Neurophysiol (2012) 108: 2242– 63. 10.1152/jn.00270.2012 22832566 PMC3545026 · DOI · Paper page
- [85]Van Essen DC Ugurbil K Auerbach E Barch D Behrens TEJ Bucholz R The Human Connectome Project: a data acquisition perspective. Neuroimage (2012) 62: 2222– 31. 10.1016/j.neuroimage.2012.02.018 22366334 PMC3606888 · DOI
- [86]Marcus DS Harms MP Snyder AZ Jenkinson M Wilson JA Glasser MF Human Connectome Project informatics: quality control, database services, and data visualization. Neuroimage (2013) 80: 202– 19. 10.1016/j.neuroimage.2013.05.077 23707591 PMC3845379 · DOI · Paper page
- [87]Gorges M Müller H-P Ludolph AC Rasche V Kassubek J. Intrinsic functional connectivity networks in healthy elderly subjects: a multiparametric approach with structural connectivity analysis. Biomed Res Int (2014) 2014: 947252. 10.1155/2014/947252 24971361 PMC4058120 · DOI
- [88]Hutchison RM Gallivan JP Culham JC Gati JS Menon RS Everling S. Functional connectivity of the frontal eye fields in humans and macaque monkeys investigated with resting-state fMRI. J Neurophysiol (2012) 107: 2463– 74. 10.1152/jn.00891.2011 22298826 · DOI
- [89]Lemieux L Salek-Haddadi A Lund TE Laufs H Carmichael D. Modelling large motion events in fMRI studies of patients with epilepsy. Magn Reson Imaging (2007) 25: 894– 901. 10.1016/j.mri.2007.03.009 17490845 · DOI
- [90]Müller H-P Kassubek J Multimodal imaging in neurology: special focus on MRI applications and MEG. Synth Lect Biomed Eng (2007) 2: 1– 75. 10.2200/S00099ED1V01Y200710BME016 · DOI
- [91]Power JD Mitra A Laumann TO Snyder AZ Schlaggar BL Petersen SE. Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage (2014) 84: 320– 41. 10.1016/j.neuroimage.2013.08.048 23994314 PMC3849338 · DOI · Paper page
- [92]Ashby FG Statistical Analysis of fMRI Data. Cambridge, MA: MIT Press (2011).
- [93]Friman O Borga M Lundberg P Knutsson H. Detection and detrending in fMRI data analysis. Neuroimage (2004) 22: 645– 55. 10.1016/j.neuroimage.2004.01.033 15193593 · DOI
- [94]Song XW Dong ZY Long XY Li SF Zuo XN Zhu CZ REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One (2011) 6(9): e25031. 10.1371/journal.pone.0025031 21949842 PMC3176805 · DOI
- [95]Satterthwaite TD Elliott MA Gerraty RT Ruparel K Loughead J Calkins ME An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage (2013) 64: 240– 56. 10.1016/j.neuroimage.2012.08.052 22926292 PMC3811142 · DOI
- [96]Caballero-Gaudes C Reynolds RC. Methods for cleaning the BOLD fMRI signal. Neuroimage (2016). 10.1016/j.neuroimage.2016.12.018 27956209 PMC5466511 · DOI · Paper page
- [97]Becerra L Bishop J Barmettler G Kainz V Burstein R Borsook D. Brain network alterations in the inflammatory soup animal model of migraine. Brain Res (2017) 1660: 36– 46. 10.1016/j.brainres.2017.02.001 28167076 PMC5731648 · DOI · Paper page
- [98]Chan RW Ho LC Zhou IY Gao PP Chan KC Wu EX. Structural and functional brain remodeling during pregnancy with diffusion tensor MRI and resting-state functional MRI. PLoS One (2015) 10: e0144328. 10.1371/journal.pone.0144328 26658306 PMC4675543 · DOI
- [99]Westphal R Simmons C Mesquita MB Wood TC Williams SCR Vernon AC Characterization of the resting-state brain network topology in the 6-hydroxydopamine rat model of Parkinson’s disease. PLoS One (2017) 12: e0172394. 10.1371/journal.pone.0172394 28249008 PMC5382982 · DOI
- [100]Van Essen DC. Cartography and connectomes. Neuron (2013) 80: 775– 90. 10.1016/j.neuron.2013.10.027 24183027 PMC3855872 · DOI
- [101]Brett M Johnsrude IS Owen AM. The problem of functional localization in the human brain. Nat Rev Neurosci (2002) 3: 243– 9. 10.1038/nrn756 11994756 · DOI
- [102]Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage (2007) 38: 95– 113. 10.1016/j.neuroimage.2007.07.007 17761438 · DOI · Paper page
- [104]Oh SW Harris JA Ng L Winslow B Cain N Mihalas S A mesoscale connectome of the mouse brain. Nature (2014) 508: 207– 14. 10.1038/nature13186 24695228 PMC5102064 · DOI · Paper page
- [105]Sporns O Bullmore ET. From connections to function: the mouse brain connectome atlas. Cell (2014) 157: 773– 5. 10.1016/j.cell.2014.04.023 24813604 · DOI
- [106]Schwarz AJ Danckaert A Reese T Gozzi A Paxinos G Watson C A stereotaxic MRI template set for the rat brain with tissue class distribution maps and co-registered anatomical atlas: application to pharmacological MRI. Neuroimage (2006) 32: 538– 50. 10.1016/j.neuroimage.2006.04.214 16784876 · DOI
- [107]Ashburner J Friston KJ Voxel-based morphometry—the methods. Neuroimage (2000) 11: 805– 21. 10.1006/nimg.2000.0582 10860804 · DOI · Paper page
- [108]Müller H-P Unrath A Ludolph AC Kassubek J. Preservation of diffusion tensor properties during spatial normalization by use of tensor imaging and fibre tracking on a normal brain database. Phys Med Biol (2007) 52: N99– 109. 10.1088/0031-9155/52/6/N01 17327646 · DOI
- [109]Holmes CJ Hoge R Collins L Woods R Toga AW Evans AC. Enhancement of MR images using registration for signal averaging. J Comput Assist Tomogr (1998) 22: 324– 33. 10.1097/00004728-199803000-00032 9530404 · DOI
- [110]Müller H-P Unrath A Riecker A Pinkhardt EH Ludolph AC Kassubek J. Intersubject variability in the analysis of diffusion tensor images at the group level: fractional anisotropy mapping and fiber tracking techniques. Magn Reson Imaging (2009) 27: 324– 34. 10.1016/j.mri.2008.07.003 18701228 · DOI
- [111]Whitwell JL Voxel-based morphometry: an automated technique for assessing structural changes in the brain. J Neurosci (2009) 29: 9661– 4. 10.1523/JNEUROSCI.2160-09.2009 19657018 PMC6666603 · DOI
- [112]Müller H-P Vernikouskaya I Ludolph AC Kassubek J Rasche V. Fast diffusion tensor magnetic resonance imaging of the mouse brain at ultrahigh-field: aiming at cohort studies. PLoS One (2012) 7: e53389. 10.1371/journal.pone.0053389 23285289 PMC3532447 · DOI
- [113]Shen X Tokoglu F Papademetris X Constable RT. Groupwise whole-brain parcellation from resting-state fMRI data for network node identification. Neuroimage (2013) 82: 403– 15. 10.1016/j.neuroimage.2013.05.081 23747961 PMC3759540 · DOI
- [114]Beckmann CF Smith SM. Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging (2004) 23: 137– 52. 10.1109/TMI.2003.822821 14964560 · DOI
- [115]Beckmann CF DeLuca M Devlin JT Smith SM. Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci (2005) 360: 1001– 13. 10.1098/rstb.2005.1634 16087444 PMC1854918 · DOI · Paper page
- [116]Valencia M Pastor MA Fernandez-Seara M Artieda J Martinerie J Chavez M Modular Organization as a Basis for the Functional Integration/Segregation in Large-Scale Brain Networks (2009). arXiv:0901.1605. Available from: https://arxiv.org/abs/0901.1605 19566254 · arXiv
- [117]Shen X Papademetris X Constable RT. Graph-theory based parcellation of functional subunits in the brain from resting-state fMRI data. Neuroimage (2010) 50: 1027– 35. 10.1016/j.neuroimage.2009.12.119 20060479 PMC3062848 · DOI
- [118]Bastos AM Schoffelen J-M A tutorial review of functional connectivity analysis methods and their interpretational pitfalls. Front Syst Neurosci (2015) 9: 175 10.3389/fnsys.2015.00175 26778976 PMC4705224 · DOI
- [119]Cole DM Smith SM Beckmann CF. Advances and pitfalls in the analysis and interpretation of resting-state FMRI data. Front Syst Neurosci (2010) 4: 8. 10.3389/fnsys.2010.00008 20407579 PMC2854531 · DOI
- [120]Sporns O. Structure and function of complex brain networks. Dialogues Clin Neurosci (2013) 15(3): 247– 62. 24174898 PMC3811098
- [121]Bullmore E Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci (2009) 10: 186– 98. 10.1038/nrn2575 19190637 · DOI · Paper page
- [123]van den Heuvel MP Sporns O. Rich-club organization of the human connectome. J Neurosci (2011) 31: 15775– 86. 10.1523/JNEUROSCI.3539-11.2011 22049421 PMC6623027 · DOI · Paper page
- [124]Rubinov M Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage (2010) 52: 1059– 69. 10.1016/j.neuroimage.2009.10.003 19819337 · DOI · Paper page
- [125]Ortiz A Munilla J Álvarez-Illán I Górriz JM Ramírez J Alzheimer’s Disease Neuroimaging Initiative Exploratory graphical models of functional and structural connectivity patterns for Alzheimer’s disease diagnosis. Front Comput Neurosci (2015) 9: 132 10.3389/fncom.2015.00132 26578945 PMC4630314 · DOI
- [126]Munilla J Ortiz A Górriz JM Ramírez J Alzheimer’s Disease Neuroimaging Initiative. Construction and analysis of weighted brain networks from SICE for the study of Alzheimer’s disease. Front Neuroinform (2017) 11: 19. 10.3389/fninf.2017.00019 28344551 PMC5344925 · DOI
- [127]Ortiz A Gorriz JM Ramirez J Salas-Gonzalez D Improving MR brain image segmentation using self-organising maps and entropy-gradient clustering. Inf Sci (2014) 262: 117– 36. 10.1016/j.ins.2013.10.002 · DOI
- [128]Ortiz A Martínez-Murcia FJ García-Tarifa MJ Lozano F Górriz JM Ramírez J Automated diagnosis of parkinsonian syndromes by deep sparse filtering-based features. In: Chen YW Tanaka S Howlett R Jain L, editors. Innovation in Medicine and Healthcare 2016. Smart Innovation, Systems and Technologies. (Vol. 60), Cham: Springer (2016). p. 249– 58.
- [129]Silva AC Liu JV Hirano Y Leoni RF Merkle H Mackel JB Longitudinal functional magnetic resonance imaging in animal models. Methods Mol Biol (2011) 711: 281– 302. 10.1007/978-1-61737-992-5_14 21279608 PMC4748954 · DOI
- [130]Deco G Jirsa VK McIntosh AR. Resting brains never rest: computational insights into potential cognitive architectures. Trends Neurosci (2013) 36: 268– 74. 10.1016/j.tins.2013.03.001 23561718 · DOI
- [131]Hillary FG Roman CA Venkatesan U Rajtmajer SM Bajo R Castellanos ND Hyperconnectivity is a fundamental response to neurological disruption. Neuropsychology (2014) 29: 59– 75. 10.1037/neu0000110 24933491 · DOI
- [133]Douaud G Filippini N Knight S Talbot K Turner MR Integration of structural and functional magnetic resonance imaging in amyotrophic lateral sclerosis. Brain (2011) 134: 3470– 9. 10.1093/brain/awr279 22075069 · DOI
- [134]Gorges M Müller H-P Lulé D Ludolph AC Pinkhardt EH Kassubek J. Functional connectivity within the default mode network is associated with saccadic accuracy in Parkinson’s disease: a resting-state FMRI and videooculographic study. Brain Connect (2013) 3: 265– 72. 10.1089/brain.2013.0146 23627641 · DOI
- [135]Gorges M Müller HP Lulé D LANDSCAPE Consortium Pinkhardt EH Ludolph AC To rise and to fall: functional connectivity in cognitively normal and cognitively impaired patients with Parkinson’s disease. Neurobiol Aging (2015) 36: 1727– 35. 10.1016/j.neurobiolaging.2014.12.026 25623332 · DOI
- [136]Mevel K Chételat G Eustache F Desgranges B The default mode network in healthy aging and Alzheimer’s disease. Int J Alzheimers Dis (2011) 2011: 535816 10.4061/2011/535816 21760988 PMC3132539 · DOI · Paper page
- [137]Schulthess I Gorges M Müller H-P Lulé D Del Tredici K Ludolph AC Functional connectivity changes resemble patterns of pTDP-43 pathology in amyotrophic lateral sclerosis. Sci Rep (2016) 6: 38391 10.1038/srep38391 27929102 PMC5144012 · DOI
- [138]Baliki MN Chang PC Baria AT Centeno MV Apkarian AV. Resting-sate functional reorganization of the rat limbic system following neuropathic injury. Sci Rep (2014) 4: 6186. 10.1038/srep06186 25178478 PMC4151103 · DOI
- [139]Mishra AM Bai X Motelow JE DeSalvo MN Danielson N Sanganahalli BG Increased resting functional connectivity in spike-wave epilepsy in WAG/Rij rats. Epilepsia (2013) 54: 1214– 22. 10.1111/epi.12227 23815571 PMC3703864 · DOI
- [140]Menke RAL Proudfoot M Wuu J Andersen PM Talbot K Benatar M Increased functional connectivity common to symptomatic amyotrophic lateral sclerosis and those at genetic risk. J Neurol Neurosurg Psychiatry (2016) 87: 580– 8. 10.1136/jnnp-2015-311945 26733601 PMC4893149 · DOI
- [141]Petri G Expert P Turkheimer F Carhart-Harris R Nutt D Hellyer PJ Homological scaffolds of brain functional networks. J R Soc Interface (2014) 11: 20140873. 10.1098/rsif.2014.0873 25401177 PMC4223908 · DOI · Paper page
- [142]Fornito A Zalesky A Breakspear M. Graph analysis of the human connectome: promise, progress, and pitfalls. Neuroimage (2013) 80: 426– 44. 10.1016/j.neuroimage.2013.04.087 23643999 · DOI · Paper page
- [143]Gass N Becker R Schwarz AJ Weber-Fahr W Clemm von Hohenberg C Vollmayr B Brain network reorganization differs in response to stress in rats genetically predisposed to depression and stress-resilient rats. Transl Psychiatry (2016) 6: e970. 10.1038/tp.2016.233 27922640 PMC5315561 · DOI
- [144]Power JD Schlaggar BL Petersen SE. Studying brain organization via spontaneous fMRI signal. Neuron (2014) 84: 681– 96. 10.1016/j.neuron.2014.09.007 25459408 PMC4254503 · DOI
- [145]Glasser MF Sotiropoulos SN Wilson JA Coalson TS Fischl B Andersson JL The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage (2013) 80: 105– 24. 10.1016/j.neuroimage.2013.04.127 23668970 PMC3720813 · DOI · Paper page
- [146]Logothetis NK Wandell BA. Interpreting the BOLD signal. Annu Rev Physiol (2004) 66: 735– 69. 10.1146/annurev.physiol.66.082602.092845 14977420 · DOI · Paper page
- [147]Burgess GC Kandala S Nolan D Laumann TO Power JD Adeyemo B Evaluation of denoising strategies to address motion-correlated artifacts in resting-state functional magnetic resonance imaging data from the human connectome project. Brain Connect (2016) 6: 669– 80. 10.1089/brain.2016.0435 27571276 PMC5105353 · DOI · Paper page
- [148]Garrison KA Scheinost D Finn ES Shen X Constable RT. The (in)stability of functional brain network measures across thresholds. Neuroimage (2015) 118: 651– 61. 10.1016/j.neuroimage.2015.05.046 26021218 PMC4554838 · DOI
- [150]Zingg B Hintiryan H Gou L Song MY Bay M Bienkowski MS Neural networks of the mouse neocortex. Cell (2014) 156: 1096– 111. 10.1016/j.cell.2014.02.023 24581503 PMC4169118 · DOI · Paper page
- [151]Hintiryan H Foster NN Bowman I Bay M Song MY Gou L The mouse cortico-striatal projectome. Nat Neurosci (2016) 19: 1100– 14. 10.1038/nn.4332 27322419 PMC5564682 · DOI
- [152]Ghanem A Conzelmann K-K. G gene-deficient single-round rabies viruses for neuronal circuit analysis. Virus Res (2016) 216: 41– 54. 10.1016/j.virusres.2015.05.023 26065596 · DOI
- [153]Wertz A Trenholm S Yonehara K Hillier D Raics Z Leinweber M Single-cell-initiated monosynaptic tracing reveals layer-specific cortical network modules. Science (2015) 349: 70– 4. 10.1126/science.aab1687 26138975 · DOI
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Kesler, S. R., Acton, P., Rao, V., & Ray, W. J. (2018) · Network Neuroscience · doi:10.1162/netn_a_00048 · Cited by 34 · see citing works
“shown to be preserved across species and therefore provide a unique translational bridge between preclinical and clinical studies (Gorges et al., 2017; Oh et al., 2014; Stafford et al., 2014; van den Heuvel, Bullmore, & Sporns, 2016).”
BackgroundMüller, H.-P., Roselli, F., Rasche, V., & Kassubek, J. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00734 · Cited by 12 · see citing works
Self-citation
- Authors
- Gorges, M., Roselli, F., Müller, H.-P., Ludolph, A. C., Rasche, V., & Kassubek, J.
- Affiliations
- Universität Ulm (DE)
- Corresponding author
- Kassubek, Jan
- Venue
- Frontiers in Neurology
- Publisher
- Frontiers Media SA
- Published
- 2017-05-10
- Volume
- 8
- Pages
- 200-200
- ISSN
- 1664-2295 (ISSN-L)
- PMC
- PMC5423907
- OpenAlex
- W2612129909
- Cited by
- 76
- References
- 15
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 5 · 2023: 7 · 2022: 7 · 2021: 14 · 2020: 13 · 2019: 8 · 2018: 18
- FWCI
- 1.19
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Neurology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- OPen Access Repositorium der Universität Ulm (OPARU) (Ulm University) (submittedVersion, other-oa)
- Universität Ulm, Kommunikations- und Informationszentrum (kiz) (cc-by)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Keywords
- resting-state fMRI, functional connectivity, animal models, spontaneous neuronal activity, BOLD signal, hemodynamics, structural connectome, translational research, knockout models, cross-species comparison, echo planar imaging, data post-processing, information flow
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