Skip to main content
Top
Published in: Brain Structure and Function 2/2021

01-03-2021 | Original Article

Integrated and segregated frequency architecture of the human brain network

Authors: Junji Ma, Ying Lin, Chuanlin Hu, Jinbo Zhang, Yangyang Yi, Zhengjia Dai

Published in: Brain Structure and Function | Issue 2/2021

Login to get access

Abstract

The frequency of brain activity modulates the relationship between the brain and human behavior. Insufficient understanding of frequency-specific features may thus lead to inconsistent explanations of human behavior. However, to date, the frequency-specific features of the human brain functional network at the whole-brain level remain poorly understood. Here, we used resting-state fMRI data and graph-theory analyses to investigate the frequency-specific characteristics of fMRI signals in 12 frequency bands (frequency range 0.01–0.7 Hz) in 75 healthy participants. We found that brain regions with higher level and more complex functions had a more variable functional connectivity pattern but engaged less in higher frequency ranges. Moreover, brain regions that engaged in fewer frequency bands played more integrated roles (i.e., higher network participation coefficient and lower within-module degree) in the functional network, whereas regions that engaged in broader frequency ranges exhibited more segregated functions (i.e., lower network participation coefficient and higher within-module degree). Finally, behavioral analyses revealed that regional frequency variability was associated with a spectrum of behavioral functions from sensorimotor functions to complex cognitive and social functions. Taken together, our results showed that segregated functions are executed in wide frequency ranges, whereas integrated functions are executed mainly in lower frequency ranges. These frequency-specific features of brain networks provided crucial insights into the frequency mechanism of fMRI signals, suggesting that signals in higher frequency ranges should be considered for their relation to cognitive functions.
Appendix
Available only for authorised users
Literature
go back to reference Baria AT, Baliki MN, Parrish T, Apkarian AV (2011) Anatomical and functional assemblies of brain BOLD oscillations. J Neurosci 31:7910–7919PubMedPubMedCentral Baria AT, Baliki MN, Parrish T, Apkarian AV (2011) Anatomical and functional assemblies of brain BOLD oscillations. J Neurosci 31:7910–7919PubMedPubMedCentral
go back to reference Birn RM, Diamond JB, Smith MA, Bandettini PA (2006) Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. NeuroImage 31:1536–1548PubMed Birn RM, Diamond JB, Smith MA, Bandettini PA (2006) Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. NeuroImage 31:1536–1548PubMed
go back to reference Birn RM, Smith MA, Jones TB, Bandettini PA (2008) The respiration response function: the temporal dynamics of fMRI signal fluctuations related to changes in respiration. NeuroImage 40:644–654PubMed Birn RM, Smith MA, Jones TB, Bandettini PA (2008) The respiration response function: the temporal dynamics of fMRI signal fluctuations related to changes in respiration. NeuroImage 40:644–654PubMed
go back to reference 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 34:537–541PubMed 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 34:537–541PubMed
go back to reference Boubela RN, Kalcher K, Huf W, Kronnerwetter C, Filzmoser P, Moser E (2013) Beyond noise: using temporal ICA to extract meaningful information from high-frequency fMRI signal fluctuations during rest. Front Hum Neurosci 7:168PubMedPubMedCentral Boubela RN, Kalcher K, Huf W, Kronnerwetter C, Filzmoser P, Moser E (2013) Beyond noise: using temporal ICA to extract meaningful information from high-frequency fMRI signal fluctuations during rest. Front Hum Neurosci 7:168PubMedPubMedCentral
go back to reference Braboszcz C, Delorme A (2011) Lost in thoughts: neural markers of low alertness during mind wandering. NeuroImage 54:3040–3047PubMed Braboszcz C, Delorme A (2011) Lost in thoughts: neural markers of low alertness during mind wandering. NeuroImage 54:3040–3047PubMed
go back to reference Bright MG, Tench CR, Murphy K (2017) Potential pitfalls when denoising resting state fMRI data using nuisance regression. NeuroImage 154:159–168PubMed Bright MG, Tench CR, Murphy K (2017) Potential pitfalls when denoising resting state fMRI data using nuisance regression. NeuroImage 154:159–168PubMed
go back to reference Brooks JC, Beckmann CF, Miller KL, Wise RG, Porro CA, Tracey I, Jenkinson M (2008) Physiological noise modelling for spinal functional magnetic resonance imaging studies. NeuroImage 39:680–692PubMed Brooks JC, Beckmann CF, Miller KL, Wise RG, Porro CA, Tracey I, Jenkinson M (2008) Physiological noise modelling for spinal functional magnetic resonance imaging studies. NeuroImage 39:680–692PubMed
go back to reference Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929PubMed Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929PubMed
go back to reference Chang C, Cunningham JP, Glover GH (2009) Influence of heart rate on the BOLD signal: the cardiac response function. NeuroImage 44:857–869PubMed Chang C, Cunningham JP, Glover GH (2009) Influence of heart rate on the BOLD signal: the cardiac response function. NeuroImage 44:857–869PubMed
go back to reference Chen JE, Glover GH (2015) BOLD fractional contribution to resting-state functional connectivity above 0.1 Hz. NeuroImage 107:207–218PubMed Chen JE, Glover GH (2015) BOLD fractional contribution to resting-state functional connectivity above 0.1 Hz. NeuroImage 107:207–218PubMed
go back to reference Chen JE, Jahanian H, Glover GH (2017) Nuisance regression of high-frequency functional magnetic resonance imaging data: denoising can be noisy. Brain Connectivity 7:13–24PubMedPubMedCentral Chen JE, Jahanian H, Glover GH (2017) Nuisance regression of high-frequency functional magnetic resonance imaging data: denoising can be noisy. Brain Connectivity 7:13–24PubMedPubMedCentral
go back to reference Chen JE, Polimeni JR, Bollmann S, Glover GH (2019) On the analysis of rapidly sampled fMRI data. NeuroImage 188:807–820PubMed Chen JE, Polimeni JR, Bollmann S, Glover GH (2019) On the analysis of rapidly sampled fMRI data. NeuroImage 188:807–820PubMed
go back to reference Christoff K, Gordon AM, Smallwood J, Smith R, Schooler JW (2009) Experience sampling during fMRI reveals default network and executive system contributions to mind wandering. Proc Natl Acad Sci 106:8719–8724PubMedPubMedCentral Christoff K, Gordon AM, Smallwood J, Smith R, Schooler JW (2009) Experience sampling during fMRI reveals default network and executive system contributions to mind wandering. Proc Natl Acad Sci 106:8719–8724PubMedPubMedCentral
go back to reference Cioli C, Abdi H, Beaton D, Burnod Y, Mesmoudi S (2014) Differences in human cortical gene expression match the temporal properties of large-scale functional networks. PLoS ONE 9:e115913PubMedPubMedCentral Cioli C, Abdi H, Beaton D, Burnod Y, Mesmoudi S (2014) Differences in human cortical gene expression match the temporal properties of large-scale functional networks. PLoS ONE 9:e115913PubMedPubMedCentral
go back to reference Coifman RR, Lafon S, Lee AB, Maggioni M, Nadler B, Warner F, Zucker SW (2005) Geometric diffusions as a tool for harmonic analysis and structure definition of data: diffusion maps. Proc Natl Acad Sci 102:7426–7431PubMedPubMedCentral Coifman RR, Lafon S, Lee AB, Maggioni M, Nadler B, Warner F, Zucker SW (2005) Geometric diffusions as a tool for harmonic analysis and structure definition of data: diffusion maps. Proc Natl Acad Sci 102:7426–7431PubMedPubMedCentral
go back to reference Collins CE, Airey DC, Young NA, Leitch DB, Kaas JH (2010) Neuron densities vary across and within cortical areas in primates. Proc Natl Acad Sci USA 107:15927–15932PubMedPubMedCentral Collins CE, Airey DC, Young NA, Leitch DB, Kaas JH (2010) Neuron densities vary across and within cortical areas in primates. Proc Natl Acad Sci USA 107:15927–15932PubMedPubMedCentral
go back to reference Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, Meyerand ME (2001) Frequencies contributing to functional connectivity in the cerebral cortex in “resting-state” data. Am J Neuroradiol 22:1326–1333PubMedPubMedCentral Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, Meyerand ME (2001) Frequencies contributing to functional connectivity in the cerebral cortex in “resting-state” data. Am J Neuroradiol 22:1326–1333PubMedPubMedCentral
go back to reference Crossley NA, Mechelli A, Vértes PE, Wintonbrown TT, Patel AX, Ginestet CE, Bullmore ET (2013) Cognitive relevance of the community structure of the human brain functional coactivation network. Proc Natl Acad Sci 110:11583–11588PubMedPubMedCentral Crossley NA, Mechelli A, Vértes PE, Wintonbrown TT, Patel AX, Ginestet CE, Bullmore ET (2013) Cognitive relevance of the community structure of the human brain functional coactivation network. Proc Natl Acad Sci 110:11583–11588PubMedPubMedCentral
go back to reference Curtis CE, D’Esposito M (2003) Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci 7:415–423PubMed Curtis CE, D’Esposito M (2003) Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci 7:415–423PubMed
go back to reference Dai Z, Lin Q, Li T, Wang X, Yuan H, Yu X, Wang H (2019) Disrupted structural and functional brain networks in Alzheimer’s disease. Neurobiol Aging 75:71–82PubMed Dai Z, Lin Q, Li T, Wang X, Yuan H, Yu X, Wang H (2019) Disrupted structural and functional brain networks in Alzheimer’s disease. Neurobiol Aging 75:71–82PubMed
go back to reference Davey CE, Grayden DB, Egan GF, Johnston LA (2013) Filtering induces correlation in fMRI resting state data. NeuroImage 64:728–740PubMed Davey CE, Grayden DB, Egan GF, Johnston LA (2013) Filtering induces correlation in fMRI resting state data. NeuroImage 64:728–740PubMed
go back to reference De Luca M, Beckmann C, De Stefano N, Matthews P, Smith SM (2006) fMRI resting state networks define distinct modes of long-distance interactions in the human brain. NeuroImage 29:1359–1367PubMed De Luca M, Beckmann C, De Stefano N, Matthews P, Smith SM (2006) fMRI resting state networks define distinct modes of long-distance interactions in the human brain. NeuroImage 29:1359–1367PubMed
go back to reference Desjardins AE, Kiehl KA, Liddle PF (2001) Removal of confounding effects of global signal in functional MRI analyses. NeuroImage 13:751–758PubMed Desjardins AE, Kiehl KA, Liddle PF (2001) Removal of confounding effects of global signal in functional MRI analyses. NeuroImage 13:751–758PubMed
go back to reference Donner TH, Siegel M, Fries P, Engel AK (2009) Buildup of choice-predictive activity in human motor cortex during perceptual decision making. Curr Biol 19:1581–1585PubMed Donner TH, Siegel M, Fries P, Engel AK (2009) Buildup of choice-predictive activity in human motor cortex during perceptual decision making. Curr Biol 19:1581–1585PubMed
go back to reference Feinberg DA, Moeller S, Smith SM, Auerbach E, Ramanna S, Glasser MF, Yacoub E (2010) Multiplexed echo planar imaging for sub-second whole brain FMRI and fast diffusion imaging. PLoS ONE 5:e15710PubMedPubMedCentral Feinberg DA, Moeller S, Smith SM, Auerbach E, Ramanna S, Glasser MF, Yacoub E (2010) Multiplexed echo planar imaging for sub-second whole brain FMRI and fast diffusion imaging. PLoS ONE 5:e15710PubMedPubMedCentral
go back to reference Finn ES, Shen X, Scheinost D, Rosenberg MD, Huang J, Chun MM, Constable RT (2015) Functional connectome fingerprinting: identifying individuals using patterns of brain connectivity. Nat Neurosci 18:1664–1671PubMedPubMedCentral Finn ES, Shen X, Scheinost D, Rosenberg MD, Huang J, Chun MM, Constable RT (2015) Functional connectome fingerprinting: identifying individuals using patterns of brain connectivity. Nat Neurosci 18:1664–1671PubMedPubMedCentral
go back to reference Fox MD, Zhang D, Snyder AZ, Raichle ME (2009) The global signal and observed anticorrelated resting state brain networks. J Neurophysiol 101:3270–3283PubMedPubMedCentral Fox MD, Zhang D, Snyder AZ, Raichle ME (2009) The global signal and observed anticorrelated resting state brain networks. J Neurophysiol 101:3270–3283PubMedPubMedCentral
go back to reference Garcés P, Pereda E, Hernández-Tamames JA, Del-Pozo F, Maestú F, Ángel Pineda-Pardo J (2016) Multimodal description of whole brain connectivity: a comparison of resting state MEG, fMRI, and DWI. Hum Brain Mapp 37:20–34PubMed Garcés P, Pereda E, Hernández-Tamames JA, Del-Pozo F, Maestú F, Ángel Pineda-Pardo J (2016) Multimodal description of whole brain connectivity: a comparison of resting state MEG, fMRI, and DWI. Hum Brain Mapp 37:20–34PubMed
go back to reference Glasser MF, Sotiropoulos SN, Wilson JA, Coalson TS, Fischl B, Andersson JL, Xu J, Jbabdi S, Webster M, Polimeni JR, Van Essen DC (2013) The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage 80:105–124PubMed Glasser MF, Sotiropoulos SN, Wilson JA, Coalson TS, Fischl B, Andersson JL, Xu J, Jbabdi S, Webster M, Polimeni JR, Van Essen DC (2013) The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage 80:105–124PubMed
go back to reference Glover GH, Li TQ, Ress D (2000) Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn Reson Med 44:162–167PubMed Glover GH, Li TQ, Ress D (2000) Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn Reson Med 44:162–167PubMed
go back to reference Gohel SR, Biswal BB (2015) Functional integration between brain regions at rest occurs in multiple-frequency bands. Brain Connectivity 5:23–34PubMedPubMedCentral Gohel SR, Biswal BB (2015) Functional integration between brain regions at rest occurs in multiple-frequency bands. Brain Connectivity 5:23–34PubMedPubMedCentral
go back to reference Guimera R, Amaral LAN (2005) Cartography of complex networks: modules and universal roles. J Stat Mech Theory Exp 2005:P02001 Guimera R, Amaral LAN (2005) Cartography of complex networks: modules and universal roles. J Stat Mech Theory Exp 2005:P02001
go back to reference Hallquist MN, Hwang K, Luna B (2013) The nuisance of nuisance regression: spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity. NeuroImage 82:208–225PubMed Hallquist MN, Hwang K, Luna B (2013) The nuisance of nuisance regression: spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity. NeuroImage 82:208–225PubMed
go back to reference Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL, Shen EH, Ng L, Miller JA, van de Lagemaat LN, Smith KA, Ebbert A, Riley ZL, Abajian C, Beckmann CF, Bernard A, Bertagnolli D, Boe AF, Cartagena PM, Chakravarty MM, Chapin M, Chong J, Dalley RA, Jones AR (2012) An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489:391–399PubMedPubMedCentral Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL, Shen EH, Ng L, Miller JA, van de Lagemaat LN, Smith KA, Ebbert A, Riley ZL, Abajian C, Beckmann CF, Bernard A, Bertagnolli D, Boe AF, Cartagena PM, Chakravarty MM, Chapin M, Chong J, Dalley RA, Jones AR (2012) An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489:391–399PubMedPubMedCentral
go back to reference Hennig J, Zhong K, Speck O (2007) MR-encephalography: fast multi-channel monitoring of brain physiology with magnetic resonance. NeuroImage 34:212–219PubMed Hennig J, Zhong K, Speck O (2007) MR-encephalography: fast multi-channel monitoring of brain physiology with magnetic resonance. NeuroImage 34:212–219PubMed
go back to reference Hipp JF, Siegel M (2015) BOLD fMRI correlation reflects frequency-specific neuronal correlation. Curr Biol 25:1368–1374PubMed Hipp JF, Siegel M (2015) BOLD fMRI correlation reflects frequency-specific neuronal correlation. Curr Biol 25:1368–1374PubMed
go back to reference Huntenburg JM, Bazin PL, Margulies DS (2018) Large-scale gradients in human cortical organization. Trends Cogn Sci 22:21–31PubMed Huntenburg JM, Bazin PL, Margulies DS (2018) Large-scale gradients in human cortical organization. Trends Cogn Sci 22:21–31PubMed
go back to reference Larkman DJ, Hajnal JV, Herlihy AH, Coutts GA, Young IR, Ehnholm G (2001) Use of multicoil arrays for separation of signal from multiple slices simultaneously excited. J Magn Reson Imaging 13:313–317PubMed Larkman DJ, Hajnal JV, Herlihy AH, Coutts GA, Young IR, Ehnholm G (2001) Use of multicoil arrays for separation of signal from multiple slices simultaneously excited. J Magn Reson Imaging 13:313–317PubMed
go back to reference Laufs H, Kleinschmidt A, Beyerle A, Eger E, Salek-Haddadi A, Preibisch C, Krakow K (2003) EEG-correlated fMRI of human alpha activity. NeuroImage 19:1463–1476PubMed Laufs H, Kleinschmidt A, Beyerle A, Eger E, Salek-Haddadi A, Preibisch C, Krakow K (2003) EEG-correlated fMRI of human alpha activity. NeuroImage 19:1463–1476PubMed
go back to reference Lee HL, Zahneisen B, Hugger T, LeVan P, Hennig J (2013) Tracking dynamic resting-state networks at higher frequencies using MR-encephalography. NeuroImage 65:216–222PubMed Lee HL, Zahneisen B, Hugger T, LeVan P, Hennig J (2013) Tracking dynamic resting-state networks at higher frequencies using MR-encephalography. NeuroImage 65:216–222PubMed
go back to reference Leopold DA, Murayama Y, Logothetis NK (2003) Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. Cereb Cortex 13:422–433PubMed Leopold DA, Murayama Y, Logothetis NK (2003) Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. Cereb Cortex 13:422–433PubMed
go back to reference Lewis LD, Setsompop K, Rosen BR, Polimeni JR (2016) Fast fMRI can detect oscillatory neural activity in humans. Proc Natl Acad Sci 113:E6679–E6685PubMedPubMedCentral Lewis LD, Setsompop K, Rosen BR, Polimeni JR (2016) Fast fMRI can detect oscillatory neural activity in humans. Proc Natl Acad Sci 113:E6679–E6685PubMedPubMedCentral
go back to reference Lin FH, Wald LL, Ahlfors SP, Hämäläinen MS, Kwong KK, Belliveau JW (2006) Dynamic magnetic resonance inverse imaging of human brain function. Magn Reson Med 56:787–802PubMed Lin FH, Wald LL, Ahlfors SP, Hämäläinen MS, Kwong KK, Belliveau JW (2006) Dynamic magnetic resonance inverse imaging of human brain function. Magn Reson Med 56:787–802PubMed
go back to reference Lin FH, Chu YH, Hsu YC, Lin JFL, Tsai KWK, Tsai SY, Kuo WJ (2015) Significant feed-forward connectivity revealed by high frequency components of BOLD fMRI signals. NeuroImage 121:69–77PubMed Lin FH, Chu YH, Hsu YC, Lin JFL, Tsai KWK, Tsai SY, Kuo WJ (2015) Significant feed-forward connectivity revealed by high frequency components of BOLD fMRI signals. NeuroImage 121:69–77PubMed
go back to reference Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150–157PubMed Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150–157PubMed
go back to reference Macey PM, Macey KE, Kumar R, Harper RM (2004) A method for removal of global effects from fMRI time series. NeuroImage 22(1):360–366PubMed Macey PM, Macey KE, Kumar R, Harper RM (2004) A method for removal of global effects from fMRI time series. NeuroImage 22(1):360–366PubMed
go back to reference Margulies DS, Ghosh SS, Goulas A, Falkiewicz M, Huntenburg JM, Langs G, Petrides M (2016) Situating the default-mode network along a principal gradient of macroscale cortical organization. Proc Natl Acad Sci 113:12574–12579PubMedPubMedCentral Margulies DS, Ghosh SS, Goulas A, Falkiewicz M, Huntenburg JM, Langs G, Petrides M (2016) Situating the default-mode network along a principal gradient of macroscale cortical organization. Proc Natl Acad Sci 113:12574–12579PubMedPubMedCentral
go back to reference Maris E, Fries P, van Ede F (2016) Diverse phase relations among neuronal rhythms and their potential function. Trends Neurosci 39:86–99PubMed Maris E, Fries P, van Ede F (2016) Diverse phase relations among neuronal rhythms and their potential function. Trends Neurosci 39:86–99PubMed
go back to reference Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN (2007) Wandering minds: the default network and stimulus-independent thought. Science 315:393–395PubMedPubMedCentral Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN (2007) Wandering minds: the default network and stimulus-independent thought. Science 315:393–395PubMedPubMedCentral
go back to reference Moeller S, Yacoub E, Olman CA, Auerbach E, Strupp J, Harel N, Uğurbil K (2010) Multiband multislice GE-EPI at 7 tesla, with 16-fold acceleration using partial parallel imaging with application to high spatial and temporal whole-brain fMRI. Magn Reson Med 63:1144–1153PubMedPubMedCentral Moeller S, Yacoub E, Olman CA, Auerbach E, Strupp J, Harel N, Uğurbil K (2010) Multiband multislice GE-EPI at 7 tesla, with 16-fold acceleration using partial parallel imaging with application to high spatial and temporal whole-brain fMRI. Magn Reson Med 63:1144–1153PubMedPubMedCentral
go back to reference Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA (2009) The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? NeuroImage 44:893–905CrossRefPubMed Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA (2009) The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? NeuroImage 44:893–905CrossRefPubMed
go back to reference Murray JD, Bernacchia A, Freedman DJ, Romo R, Wallis JD, Cai X, Lee D (2014) A hierarchy of intrinsic timescales across primate cortex. Nat Neurosci 17:1661PubMedPubMedCentral Murray JD, Bernacchia A, Freedman DJ, Romo R, Wallis JD, Cai X, Lee D (2014) A hierarchy of intrinsic timescales across primate cortex. Nat Neurosci 17:1661PubMedPubMedCentral
go back to reference Niazy RK, Xie J, Miller K, Beckmann CF, Smith SM (2011) Spectral characteristics of resting state networks. Prog Brain Res 193:259–276PubMed Niazy RK, Xie J, Miller K, Beckmann CF, Smith SM (2011) Spectral characteristics of resting state networks. Prog Brain Res 193:259–276PubMed
go back to reference Penttonen M, Buzsáki G (2003) Natural logarithmic relationship between brain oscillators. Thalamus Relat Syst 2:145–152 Penttonen M, Buzsáki G (2003) Natural logarithmic relationship between brain oscillators. Thalamus Relat Syst 2:145–152
go back to reference Power JD, Barnes K, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59:2142–2154PubMed Power JD, Barnes K, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59:2142–2154PubMed
go back to reference Preti MG, Van De Ville D (2019) Decoupling of brain function from structure reveals regional behavioral specialization in humans. Nat Commun 10:4747PubMedPubMedCentral Preti MG, Van De Ville D (2019) Decoupling of brain function from structure reveals regional behavioral specialization in humans. Nat Commun 10:4747PubMedPubMedCentral
go back to reference Saad ZS, Gotts SJ, Murphy K, Chen G, Jo HJ, Martin A, Cox RW (2012) Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain Connectivity 2:25–32PubMedPubMedCentral Saad ZS, Gotts SJ, Murphy K, Chen G, Jo HJ, Martin A, Cox RW (2012) Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain Connectivity 2:25–32PubMedPubMedCentral
go back to reference Salvador R, Martinez A, Pomarol-Clotet E, Gomar J, Vila F, Sarró S, Bullmore E (2008) A simple view of the brain through a frequency-specific functional connectivity measure. NeuroImage 39:279–289PubMed Salvador R, Martinez A, Pomarol-Clotet E, Gomar J, Vila F, Sarró S, Bullmore E (2008) A simple view of the brain through a frequency-specific functional connectivity measure. NeuroImage 39:279–289PubMed
go back to reference Siegel M, Donner TH, Engel AK (2012) Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci 13:121PubMed Siegel M, Donner TH, Engel AK (2012) Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci 13:121PubMed
go back to reference Smith-Collins AP, Luyt K, Heep A, Kauppinen RA (2015) High frequency functional brain networks in neonates revealed by rapid acquisition resting state fMRI. Hum Brain Mapp 36:2483–2494PubMedPubMedCentral Smith-Collins AP, Luyt K, Heep A, Kauppinen RA (2015) High frequency functional brain networks in neonates revealed by rapid acquisition resting state fMRI. Hum Brain Mapp 36:2483–2494PubMedPubMedCentral
go back to reference Sporns O (2013) Network attributes for segregation and integration in the human brain. Curr Opin Neurobiol 23:162–171PubMed Sporns O (2013) Network attributes for segregation and integration in the human brain. Curr Opin Neurobiol 23:162–171PubMed
go back to reference Sporns O, Betzel RF (2016) Modular brain networks. Annu Rev Psychol 67:613–640PubMed Sporns O, Betzel RF (2016) Modular brain networks. Annu Rev Psychol 67:613–640PubMed
go back to reference Störmer VS, Feng W, Martinez A, McDonald JJ, Hillyard SA (2016) Salient, irrelevant sounds reflexively induce alpha rhythm desynchronization in parallel with slow potential shifts in visual cortex. J Cogn Neurosci 28:433–445PubMed Störmer VS, Feng W, Martinez A, McDonald JJ, Hillyard SA (2016) Salient, irrelevant sounds reflexively induce alpha rhythm desynchronization in parallel with slow potential shifts in visual cortex. J Cogn Neurosci 28:433–445PubMed
go back to reference Thompson WH, Fransson P (2015) The frequency dimension of fMRI dynamic connectivity: network connectivity, functional hubs and integration in the resting brain. NeuroImage 121:227–242PubMed Thompson WH, Fransson P (2015) The frequency dimension of fMRI dynamic connectivity: network connectivity, functional hubs and integration in the resting brain. NeuroImage 121:227–242PubMed
go back to reference Thompson GJ, Merritt MD, Pan WJ, Magnuson ME, Grooms JK, Jaeger D, Keilholz SD (2013) Neural correlates of time-varying functional connectivity in the rat. NeuroImage 83:826–836PubMed Thompson GJ, Merritt MD, Pan WJ, Magnuson ME, Grooms JK, Jaeger D, Keilholz SD (2013) Neural correlates of time-varying functional connectivity in the rat. NeuroImage 83:826–836PubMed
go back to reference Thompson WH, Kastrati G, Finc K, Wright J, Shine JM, Poldrack RA (2019) Time-varying nodal measures with temporal community structure: a cautionary note to avoid misquantification. BioRxiv 659508 Thompson WH, Kastrati G, Finc K, Wright J, Shine JM, Poldrack RA (2019) Time-varying nodal measures with temporal community structure: a cautionary note to avoid misquantification. BioRxiv 659508
go back to reference Tomasi D, Volkow ND (2011) Functional connectivity hubs in the human brain. NeuroImage 57(3):908–917PubMed Tomasi D, Volkow ND (2011) Functional connectivity hubs in the human brain. NeuroImage 57(3):908–917PubMed
go back to reference Tsushima Y, Sasaki Y, Watanabe T (2006) Greater disruption due to failure of inhibitory control on an ambiguous distractor. Science 314:1786–1788PubMed Tsushima Y, Sasaki Y, Watanabe T (2006) Greater disruption due to failure of inhibitory control on an ambiguous distractor. Science 314:1786–1788PubMed
go back to reference Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15:273–289PubMed Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15:273–289PubMed
go back to reference van den Heuvel MP, Sporns O (2013) Network hubs in the human brain. Trends Cogn Sci 17:683–696PubMed van den Heuvel MP, Sporns O (2013) Network hubs in the human brain. Trends Cogn Sci 17:683–696PubMed
go back to reference van den Heuvel MP, de Lange SC, Zalesky A, Seguin C, Yeo BT, Schmidt R (2017) Proportional thresholding in resting-state fMRI functional connectivity networks and consequences for patient-control connectome studies: Issues and recommendations. NeuroImage 152:437–449PubMed van den Heuvel MP, de Lange SC, Zalesky A, Seguin C, Yeo BT, Schmidt R (2017) Proportional thresholding in resting-state fMRI functional connectivity networks and consequences for patient-control connectome studies: Issues and recommendations. NeuroImage 152:437–449PubMed
go back to reference van Den Heuvel MP, Pol HEH (2010) Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 20:519–534PubMed van Den Heuvel MP, Pol HEH (2010) Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 20:519–534PubMed
go back to reference Van Dijk KRA, Sabuncu MR, Buckner RL (2012) The influence of head motion on in-trinsic functional connectivity MRI. NeuroImage 59:431–438PubMed Van Dijk KRA, Sabuncu MR, Buckner RL (2012) The influence of head motion on in-trinsic functional connectivity MRI. NeuroImage 59:431–438PubMed
go back to reference Van Wijk BC, Stam CJ, Daffertshofer A (2010) Comparing brain networks of different size and connectivity density using graph theory. PLoS ONE 5:e13701PubMedPubMedCentral Van Wijk BC, Stam CJ, Daffertshofer A (2010) Comparing brain networks of different size and connectivity density using graph theory. PLoS ONE 5:e13701PubMedPubMedCentral
go back to reference van Essen DC, Smith SM, Barch DM, Behrens TE, Yacoub E, Ugurbil K, Consortium WMH (2013) The WU-Minn human connectome project: an overview. NeuroImage 80:62–79PubMed van Essen DC, Smith SM, Barch DM, Behrens TE, Yacoub E, Ugurbil K, Consortium WMH (2013) The WU-Minn human connectome project: an overview. NeuroImage 80:62–79PubMed
go back to reference Wagstyl K, Ronan L, Goodyer IM, Fletcher PC (2015) Cortical thickness gradients in structural hierarchies. NeuroImage 111:241–250PubMed Wagstyl K, Ronan L, Goodyer IM, Fletcher PC (2015) Cortical thickness gradients in structural hierarchies. NeuroImage 111:241–250PubMed
go back to reference Wang JH, Zuo XN, Gohel S, Milham MP, Biswal BB, He Y (2011) Graph theoretical analysis of functional brain networks: test-retest evaluation on short-and long-term resting-state functional MRI data. PLoS ONE 6:e21976PubMedPubMedCentral Wang JH, Zuo XN, Gohel S, Milham MP, Biswal BB, He Y (2011) Graph theoretical analysis of functional brain networks: test-retest evaluation on short-and long-term resting-state functional MRI data. PLoS ONE 6:e21976PubMedPubMedCentral
go back to reference Wang J, Wang X, Xia M, Liao X, Evans A, He Y (2015) GRETNA: a graph theoretical network analysis toolbox for imaging connectomics. Front Hum Neurosci 9:386PubMedPubMedCentral Wang J, Wang X, Xia M, Liao X, Evans A, He Y (2015) GRETNA: a graph theoretical network analysis toolbox for imaging connectomics. Front Hum Neurosci 9:386PubMedPubMedCentral
go back to reference Wang Y, Zhu L, Zou Q, Cui Q, Liao W, Duan X, Chen H (2018) Frequency dependent hub role of the dorsal and ventral right anterior insula. NeuroImage 165:112–117PubMed Wang Y, Zhu L, Zou Q, Cui Q, Liao W, Duan X, Chen H (2018) Frequency dependent hub role of the dorsal and ventral right anterior insula. NeuroImage 165:112–117PubMed
go back to reference Weissenbacher A, Kasess C, Gerstl F, Lanzenberger R, Moser E, Windischberger C (2009) Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies. NeuroImage 47:1408–1416PubMed Weissenbacher A, Kasess C, Gerstl F, Lanzenberger R, Moser E, Windischberger C (2009) Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies. NeuroImage 47:1408–1416PubMed
go back to reference Welvaert M, Rosseel Y (2013) On the definition of signal-to-noise ratio and contrast-to-noise ratio for fMRI data. PLoS ONE 8:e77089PubMedPubMedCentral Welvaert M, Rosseel Y (2013) On the definition of signal-to-noise ratio and contrast-to-noise ratio for fMRI data. PLoS ONE 8:e77089PubMedPubMedCentral
go back to reference Wu CW, Gu H, Lu H, Stein EA, Chen J-H, Yang Y (2008) Frequency specificity of functional connectivity in brain networks. NeuroImage 42:1047–1055PubMed Wu CW, Gu H, Lu H, Stein EA, Chen J-H, Yang Y (2008) Frequency specificity of functional connectivity in brain networks. NeuroImage 42:1047–1055PubMed
go back to reference Xia M, Wang J, He Y (2013) BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS ONE 8:e68910PubMedPubMedCentral Xia M, Wang J, He Y (2013) BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS ONE 8:e68910PubMedPubMedCentral
go back to reference Yan CG, Zang YF (2010) DPARSF: a MATLAB TOOLBOX for “pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 4:13 Yan CG, Zang YF (2010) DPARSF: a MATLAB TOOLBOX for “pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 4:13
go back to reference Yang GJ, Murray JD, Repovs G, Cole MW, Savic A, Glasser MF et al (2014) Altered global brain signal in schizophrenia. Proc Nat Acad Sci 111:7438–7443PubMedPubMedCentral Yang GJ, Murray JD, Repovs G, Cole MW, Savic A, Glasser MF et al (2014) Altered global brain signal in schizophrenia. Proc Nat Acad Sci 111:7438–7443PubMedPubMedCentral
go back to reference 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 106:1125–1165PubMed 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 106:1125–1165PubMed
go back to reference Zahneisen B, Grotz T, Lee KJ, Ohlendorf S, Reisert M, Zaitsev M, Hennig J (2011) Three-dimensional MR-encephalography: fast volumetric brain imaging using rosette trajectories. Magn Reson Med 65:1260–1268PubMed Zahneisen B, Grotz T, Lee KJ, Ohlendorf S, Reisert M, Zaitsev M, Hennig J (2011) Three-dimensional MR-encephalography: fast volumetric brain imaging using rosette trajectories. Magn Reson Med 65:1260–1268PubMed
go back to reference Zalesky A, Fornito A, Harding IH, Cocchi L, Yücel M, Pantelis C, Bullmore ET (2010) Whole-brain anatomical networks: does the choice of nodes matter? NeuroImage 50:970–983PubMed Zalesky A, Fornito A, Harding IH, Cocchi L, Yücel M, Pantelis C, Bullmore ET (2010) Whole-brain anatomical networks: does the choice of nodes matter? NeuroImage 50:970–983PubMed
go back to reference Zhang J, Cheng W, Liu Z, Zhang K, Lei X, Yao Y, Lu G (2016) Neural, electrophysiological and anatomical basis of brain-network variability and its characteristic changes in mental disorders. Brain 139:2307–2321PubMed Zhang J, Cheng W, Liu Z, Zhang K, Lei X, Yao Y, Lu G (2016) Neural, electrophysiological and anatomical basis of brain-network variability and its characteristic changes in mental disorders. Brain 139:2307–2321PubMed
go back to reference Zuo XN, Di Martino A, Kelly C, Shehzad ZE, Gee DG, Klein DF, Castellanos FX, Biswal BB, Milham MP (2010) The oscillating brain: complex and reliable. NeuroImage 49:1432–1445PubMed Zuo XN, Di Martino A, Kelly C, Shehzad ZE, Gee DG, Klein DF, Castellanos FX, Biswal BB, Milham MP (2010) The oscillating brain: complex and reliable. NeuroImage 49:1432–1445PubMed
go back to reference Zuo XN, Ehmke R, Mennes M, Imperati D, Castellanos FX, Sporns O, Milham MP (2012) Network centrality in the human functional connectome. Cereb Cortex 22:1862–1875PubMed Zuo XN, Ehmke R, Mennes M, Imperati D, Castellanos FX, Sporns O, Milham MP (2012) Network centrality in the human functional connectome. Cereb Cortex 22:1862–1875PubMed
Metadata
Title
Integrated and segregated frequency architecture of the human brain network
Authors
Junji Ma
Ying Lin
Chuanlin Hu
Jinbo Zhang
Yangyang Yi
Zhengjia Dai
Publication date
01-03-2021
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 2/2021
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-020-02174-8

Other articles of this Issue 2/2021

Brain Structure and Function 2/2021 Go to the issue