Complexity of low-frequency blood oxygen level-dependent fluctuations covaries with local connectivity

Very low‐frequency blood oxygen level‐dependent (BOLD) fluctuations have emerged as a valuable tool for describing brain anatomy, neuropathology, and development. Such fluctuations exhibit power law frequency dynamics, with largest amplitude at lowest frequencies. The biophysical mechanisms generati...

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Published inHuman brain mapping Vol. 35; no. 4; pp. 1273 - 1283
Main Authors Anderson, Jeffrey S., Zielinski, Brandon A., Nielsen, Jared A., Ferguson, Michael A.
Format Journal Article
LanguageEnglish
Published New York, NY Blackwell Publishing Ltd 01.04.2014
Wiley-Liss
John Wiley & Sons, Inc
John Wiley and Sons Inc
Subjects
Online AccessGet full text
ISSN1065-9471
1097-0193
1097-0193
DOI10.1002/hbm.22251

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Abstract Very low‐frequency blood oxygen level‐dependent (BOLD) fluctuations have emerged as a valuable tool for describing brain anatomy, neuropathology, and development. Such fluctuations exhibit power law frequency dynamics, with largest amplitude at lowest frequencies. The biophysical mechanisms generating such fluctuations are poorly understood. Using publicly available data from 1,019 subjects of age 7–30, we show that BOLD fluctuations exhibit temporal complexity that is linearly related to local connectivity (regional homogeneity), consistently and significantly covarying across subjects and across gray matter regions. This relationship persisted independently of covariance with gray matter density or standard deviation of BOLD signal. During late neurodevelopment, BOLD fluctuations were unchanged with age in association cortex while becoming more random throughout the rest of the brain. These data suggest that local interconnectivity may play a key role in establishing the complexity of low‐frequency BOLD fluctuations underlying functional magnetic resonance imaging connectivity. Stable low‐frequency power dynamics may emerge through segmentation and integration of connectivity during development of distributed large‐scale brain networks. Hum Brain Mapp 35:1273–1283, 2014. © 2013 Wiley Periodicals, Inc.
AbstractList Very low-frequency blood oxygen level-dependent (BOLD) fluctuations have emerged as a valuable tool for describing brain anatomy, neuropathology, and development. Such fluctuations exhibit power law frequency dynamics, with largest amplitude at lowest frequencies. The biophysical mechanisms generating such fluctuations are poorly understood. Using publicly available data from 1,019 subjects of age 7-30, we show that BOLD fluctuations exhibit temporal complexity that is linearly related to local connectivity (regional homogeneity), consistently and significantly covarying across subjects and across gray matter regions. This relationship persisted independently of covariance with gray matter density or standard deviation of BOLD signal. During late neurodevelopment, BOLD fluctuations were unchanged with age in association cortex while becoming more random throughout the rest of the brain. These data suggest that local interconnectivity may play a key role in establishing the complexity of low-frequency BOLD fluctuations underlying functional magnetic resonance imaging connectivity. Stable low-frequency power dynamics may emerge through segmentation and integration of connectivity during development of distributed large-scale brain networks.Very low-frequency blood oxygen level-dependent (BOLD) fluctuations have emerged as a valuable tool for describing brain anatomy, neuropathology, and development. Such fluctuations exhibit power law frequency dynamics, with largest amplitude at lowest frequencies. The biophysical mechanisms generating such fluctuations are poorly understood. Using publicly available data from 1,019 subjects of age 7-30, we show that BOLD fluctuations exhibit temporal complexity that is linearly related to local connectivity (regional homogeneity), consistently and significantly covarying across subjects and across gray matter regions. This relationship persisted independently of covariance with gray matter density or standard deviation of BOLD signal. During late neurodevelopment, BOLD fluctuations were unchanged with age in association cortex while becoming more random throughout the rest of the brain. These data suggest that local interconnectivity may play a key role in establishing the complexity of low-frequency BOLD fluctuations underlying functional magnetic resonance imaging connectivity. Stable low-frequency power dynamics may emerge through segmentation and integration of connectivity during development of distributed large-scale brain networks.
Very low‐frequency blood oxygen level‐dependent (BOLD) fluctuations have emerged as a valuable tool for describing brain anatomy, neuropathology, and development. Such fluctuations exhibit power law frequency dynamics, with largest amplitude at lowest frequencies. The biophysical mechanisms generating such fluctuations are poorly understood. Using publicly available data from 1,019 subjects of age 7–30, we show that BOLD fluctuations exhibit temporal complexity that is linearly related to local connectivity (regional homogeneity), consistently and significantly covarying across subjects and across gray matter regions. This relationship persisted independently of covariance with gray matter density or standard deviation of BOLD signal. During late neurodevelopment, BOLD fluctuations were unchanged with age in association cortex while becoming more random throughout the rest of the brain. These data suggest that local interconnectivity may play a key role in establishing the complexity of low‐frequency BOLD fluctuations underlying functional magnetic resonance imaging connectivity. Stable low‐frequency power dynamics may emerge through segmentation and integration of connectivity during development of distributed large‐scale brain networks. Hum Brain Mapp 35:1273–1283, 2014 . © 2013 Wiley Periodicals, Inc.
Very low-frequency blood oxygen level-dependent (BOLD) fluctuations have emerged as a valuable tool for describing brain anatomy, neuropathology, and development. Such fluctuations exhibit power law frequency dynamics, with largest amplitude at lowest frequencies. The biophysical mechanisms generating such fluctuations are poorly understood. Using publicly available data from 1,019 subjects of age 7-30, we show that BOLD fluctuations exhibit temporal complexity that is linearly related to local connectivity (regional homogeneity), consistently and significantly covarying across subjects and across gray matter regions. This relationship persisted independently of covariance with gray matter density or standard deviation of BOLD signal. During late neurodevelopment, BOLD fluctuations were unchanged with age in association cortex while becoming more random throughout the rest of the brain. These data suggest that local interconnectivity may play a key role in establishing the complexity of low-frequency BOLD fluctuations underlying functional magnetic resonance imaging connectivity. Stable low-frequency power dynamics may emerge through segmentation and integration of connectivity during development of distributed large-scale brain networks.
Very low-frequency blood oxygen level-dependent (BOLD) fluctuations have emerged as a valuable tool for describing brain anatomy, neuropathology, and development. Such fluctuations exhibit power law frequency dynamics, with largest amplitude at lowest frequencies. The biophysical mechanisms generating such fluctuations are poorly understood. Using publicly available data from 1,019 subjects of age 7-30, we show that BOLD fluctuations exhibit temporal complexity that is linearly related to local connectivity (regional homogeneity), consistently and significantly covarying across subjects and across gray matter regions. This relationship persisted independently of covariance with gray matter density or standard deviation of BOLD signal. During late neurodevelopment, BOLD fluctuations were unchanged with age in association cortex while becoming more random throughout the rest of the brain. These data suggest that local interconnectivity may play a key role in establishing the complexity of low-frequency BOLD fluctuations underlying functional magnetic resonance imaging connectivity. Stable low-frequency power dynamics may emerge through segmentation and integration of connectivity during development of distributed large-scale brain networks. Hum Brain Mapp 35:1273-1283, 2014. © 2013 Wiley Periodicals, Inc. [PUBLICATION ABSTRACT]
Very low‐frequency blood oxygen level‐dependent (BOLD) fluctuations have emerged as a valuable tool for describing brain anatomy, neuropathology, and development. Such fluctuations exhibit power law frequency dynamics, with largest amplitude at lowest frequencies. The biophysical mechanisms generating such fluctuations are poorly understood. Using publicly available data from 1,019 subjects of age 7–30, we show that BOLD fluctuations exhibit temporal complexity that is linearly related to local connectivity (regional homogeneity), consistently and significantly covarying across subjects and across gray matter regions. This relationship persisted independently of covariance with gray matter density or standard deviation of BOLD signal. During late neurodevelopment, BOLD fluctuations were unchanged with age in association cortex while becoming more random throughout the rest of the brain. These data suggest that local interconnectivity may play a key role in establishing the complexity of low‐frequency BOLD fluctuations underlying functional magnetic resonance imaging connectivity. Stable low‐frequency power dynamics may emerge through segmentation and integration of connectivity during development of distributed large‐scale brain networks. Hum Brain Mapp 35:1273–1283, 2014. © 2013 Wiley Periodicals, Inc.
Author Zielinski, Brandon A.
Nielsen, Jared A.
Anderson, Jeffrey S.
Ferguson, Michael A.
AuthorAffiliation 3 The Brain Institute at the University of Utah, Salt Lake City, Utah
2 Program in Neuroscience, University of Utah, Salt Lake City, Utah
5 Departments of Pediatrics and Neurology, University of Utah, Salt Lake City, Utah
6 Division of Child Neurology, University of Utah, Salt Lake City, Utah
4 Department of Bioengineering, University of Utah, Salt Lake City, Utah
1 Division of Neuroradiology, University of Utah, Salt Lake City, Utah
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  organization: Department of Bioengineering, University of Utah, Salt Lake City, Utah
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Issue 4
Keywords Chaos
brain development
chaos theory
Fluctuations
Oxygen
Nervous system diseases
Radiodiagnosis
Theory
Memory
Central nervous system
1/f
avalanche dynamics
fcMRI
resting state fMRI
Low frequency
Nuclear magnetic resonance imaging
Complexity
Encephalon
power law
fMRI
long memory
regional homogeneity
complexity
Language English
License http://onlinelibrary.wiley.com/termsAndConditions#vor
CC BY 4.0
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Bullmore E, Barnes A, Bassett DS, Fornito A, Kitzbichler M, Meunier D, Suckling J (2009): Generic aspects of complexity in brain imaging data and other biological systems. Neuroimage 47:1125-1134.
Caserta F, Eldred WD, Fernandez E, Hausman RE, Stanford LR, Bulderev SV, Schwarzer S, Stanley HE (1995): Determination of fractal dimension of physiologically characterized neurons in two and three dimensions. J Neurosci Methods 56:133-144.
Bullmore E, Brammer M, Harvey I, Persaud R, Murray R, Ron M (1994): Fractal analysis of the boundary between white matter and cerebral cortex in magnetic resonance images: A controlled study of schizophrenic and manic-depressive patients. Psychol Med 24:771-781.
Kiselev VG, Hahn KR, Auer DP (2003): Is the brain cortex a fractal?Neuroimage 20:1765-1774.
Anderson JS, Nielsen JA, Froehlich AL, DuBray MB, Druzgal TJ, Cariello AN, Cooperrider JR, Zielinski BA, Ravichandran C, Fletcher PT, Alexander AL, Bigler ED, Lange N, Lainhart JE (2011c): Functional connectivity magnetic resonance imaging classification of autism. Brain 134:3742-3754.
Bullmore E, Fadili J, Maxim V, Sendur L, Whitcher B, Suckling J, Brammer M, Breakspear M (2004): Wavelets and functional magnetic resonance imaging of the human brain. Neuroimage 23(Suppl 1):S234-S249.
Dosenbach NU, Nardos B, Cohen AL, Fair DA, Power JD, Church JA, Nelson SM, Wig GS, Vogel AC, Lessov-Schlaggar CN, Barnes KA, Dubis JW, Feczko E, Coalson RS, Pruett JR Jr, Barch DM, Petersen SE, Schlaggar BL (2010): Prediction of individual brain maturity using fMRI. Science 329:1358-1361.
Maxim V, Sendur L, Fadili J, Suckling J, Gould R, Howard R, Bullmore E (2005): Fractional Gaussian noise, functional MRI and Alzheimer's disease. Neuroimage 25:141-158.
Supekar K, Uddin LQ, Prater K, Amin H, Greicius MD, Menon V (2010): Development of functional and structural connectivity within the default mode network in young children. Neuroimage 52:290-301.
Mendez MA, Zuluaga P, Hornero R, Gomez C, Escudero J, Rodriguez-Palancas A, Ortiz T, Fernandez A (2011): Complexity analysis of spontaneous brain activity: Effects of depression and antidepressant treatment. J Psychopharmacol 26:636-643.
Anderson JS, Druzgal TJ, Lopez-Larson M, Jeong EK, Desai K, Yurgelun-Todd D (2011a): Network anticorrelations, global regression, and phase-shifted soft tissue correction. Hum Brain Mapp 32:919-934.
Zang Y, Jiang T, Lu Y, He Y, Tian L (2004): Regional homogeneity approach to fMRI data analysis. Neuroimage 22:394-400.
Beggs JM, Plenz D (2004): Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures. J Neurosci 24:5216-5229.
Poil SS, van Ooyen A, Linkenkaer-Hansen K (2008): Avalanche dynamics of human brain oscillations: Relation to critical branching processes and temporal correlations. Hum Brain Mapp 29:770-777.
Power JD, Fair DA, Schlaggar BL, Petersen SE (2010): The development of human functional brain networks. Neuron 67:735-748.
Christensen K, Olami Z, Bak P (1992): Deterministic 1/f noise in nonconserative models of self-organized criticality. Phys Rev Lett 68:2417-2420.
Uddin LQ, Supekar K, Menon V (2010): Typical and atypical development of functional human brain networks: Insights from resting-state FMRI. Front Syst Neurosci 4:21.
Ciuciu P, Varoquaux G, Abry P, Sadaghiani S, Kleinschmidt A (2012): Scale-free and multifractal time dynamics of fmri signals during rest and task. Front Physiol 3:186.
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 34:537-541.
Gordon EM, Lee PS, Maisog JM, Foss-Feig J, Billington ME, Vanmeter J, Vaidya CJ (2011): Strength of default mode resting-state connectivity relates to white matter integrity in children. Dev Sci 14:738-751.
Vogel AC, Power JD, Petersen SE, Schlaggar BL (2011): Development of the brain's functional network architecture. Neuropsychol Rev 20:362-375.
Zarahn E, Aguirre GK, D'Esposito M (1997): Empirical analyses of BOLD fMRI statistics. I. Spatially unsmoothed data collected under null-hypothesis conditions. Neuroimage 5:179-197.
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He Y, Wang L, Zang Y, Tian L, Zhang X, Li K, Jiang T (2007): Regional coherence changes in the early stages of Alzheimer's disease: A combined structural and resting-state functional MRI study. Neuroimage 35:488-500.
Kitzbichler MG, Smith ML, Christensen SR, Bullmore E (2009): Broadband criticality of human brain network synchronization. PLoS Comput Biol 5:e1000314.
Fair DA, Cohen AL, Dosenbach NU, Church JA, Miezin FM, Barch DM, Raichle ME, Petersen SE, Schlaggar BL (2008): The maturing architecture of the brain's default network. Proc Natl Acad Sci USA 105:4028-4032.
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 59:2142-2154.
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 49:1432-1445.
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Wink AM, Bullmore E, Barnes A, Bernard F, Suckling J (2008): Monofractal and multifractal dynamics of low frequency endogenous brain oscillations in functional MRI. Hum Brain Mapp 29:791-801.
Lopez-Larson MP, Anderson JS, Ferguson MA, Yurgelun-Todd D (2011): Local brain connectivity and associations with gender and age. Dev Cogn Neurosci 1:187-197.
Bullmore E, Fadili J, Breakspear M, Salvador R, Suckling J, Brammer M (2003): Wavelets and statistical analysis of functional magnetic resonance images of the human brain. Stat Methods Med Res 12:375-399.
Beggs JM, Plenz D (2003): Neuronal avalanches in neocortical circuits. J Neurosci 23:11167-11177.
Paakki JJ, Rahko J, Long X, Moilanen I, Tervonen O, Nikkinen J, Starck T, Remes J, Hurtig T, Haapsamo H, Jussila K, Kuusikko-Gauffin S, Mattila ML, Zang Y, Kiviniemi V (2010): Alterations in regional homogeneity of resting-state brain activity in autism spectrum disorders. Brain Res 1321:169-179.
Supekar K, Musen M, Menon V (2009): Development of large-scale functional brain networks in children. PLoS Biol 7:e1000157.
Rombouts SA, Goekoop R, Stam CJ, Barkhof F, Scheltens P (2005): Delayed rather than decreased BOLD response as a marker for early Alzheimer's disease. Neuroimage 26:1078-1085.
Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, Quigley MA, Meyerand ME (2001): Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. AJNR Am J Neuroradiol 22:1326-1333.
Barnes A, Bullmore ET, Suckling J (2009): Endogenous human brain dynamics recover slowly following cognitive effort. PloS One 4:e6626.
Fair DA, Dosenbach NU, Church JA, Cohen AL, Brahmbhatt S, Miezin FM, Barch DM, Raichle ME, Petersen SE, Schlaggar BL (2007): Development of distinct control networks through segregation and integration. Proc Natl Acad Sci USA 104:13507-13512.
Anderson JS, Ferguson MA, Lopez-Larson M, Yurgelun-Todd D (2010): Topographic maps of multisensory attention. Proc Natl Acad Sci USA 107:20110-20114.
Fair DA, Cohen AL, Power JD, Dosenbach NU, Church JA, Miezin FM, Schlaggar BL, Petersen SE (2009): Functional brain networks develop from a "local to distributed" organization. PLoS Comput Biol 5:e1000381.
Ferguson MA, Anderson JS (2012): Dynamical stability of intrinsic connectivity networks. Neuroimage 59:4022-4031.
He BJ (2011): Scale-free propert
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Snippet Very low‐frequency blood oxygen level‐dependent (BOLD) fluctuations have emerged as a valuable tool for describing brain anatomy, neuropathology, and...
Very low-frequency blood oxygen level-dependent (BOLD) fluctuations have emerged as a valuable tool for describing brain anatomy, neuropathology, and...
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SubjectTerms 1/f
Adolescent
Adult
avalanche dynamics
Biological and medical sciences
Brain - anatomy & histology
Brain - growth & development
Brain - physiology
brain development
Brain Mapping - methods
Cardiovascular system
Cerebrovascular Circulation - physiology
chaos theory
Child
complexity
Databases, Factual
fcMRI
Female
fMRI
Head
Humans
Investigative techniques, diagnostic techniques (general aspects)
long memory
Magnetic Resonance Imaging - methods
Male
Medical sciences
Motion
Nerve Fibers, Unmyelinated - physiology
Nervous system
Neural Pathways - anatomy & histology
Neural Pathways - growth & development
Neural Pathways - physiology
Oxygen - blood
power law
Radiodiagnosis. Nmr imagery. Nmr spectrometry
regional homogeneity
resting state fMRI
Signal Processing, Computer-Assisted
Young Adult
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Title Complexity of low-frequency blood oxygen level-dependent fluctuations covaries with local connectivity
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