Relations between BOLD fMRI-Derived Resting Brain Activity and Cerebral Blood Flow

Consistent resting brain activity patterns have been repeatedly demonstrated using measures derived from resting BOLD fMRI data. While those metrics are presumed to reflect underlying spontaneous brain activity (SBA), it is challenging to prove that association because resting BOLD fMRI metrics are purely model-free and scale-free variables. Cerebral blood flow (CBF) is typically closely coupled to brain metabolism and is used as a surrogate marker for quantifying regional brain function, including resting function. Assessing the correlations between resting BOLD fMRI measures and CBF correlation should provide a means of linking of those measures to the underlying SBA, and a means to quantify those scale-free measures. The purpose of this paper was to examine the CBF correlations of 3 widely used neuroimaging-based SBA measures, including seed-region based functional connectivity (FC), regional homogeneity (ReHo), and amplitude of low frequency fluctuation (ALFF). Test-retest data were acquired to check the stability of potential correlations across time. Reproducible posterior cingulate cortex (PCC) FC vs regional CBF correlations were found in much of the default mode network and visual cortex. Dorsal anterior cingulate cortex (ACC) FC vs CBF correlations were consistently found in bilateral prefrontal cortex. Both ReHo and ALFF were found to be reliably correlated with CBF in most of brain cortex. None of the assessed SBA measures was correlated with whole brain mean CBF. These findings suggest that resting BOLD fMRI-derived measures are coupled with regional CBF and are therefore linked to regional SBA.

[1]  P. Molinoff,et al.  Basic Neurochemistry: Molecular, Cellular and Medical Aspects , 1989 .

[2]  Jeff H. Duyn,et al.  Mapping resting-state functional connectivity using perfusion MRI , 2008, NeuroImage.

[3]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[4]  P. Fransson.  Spontaneous low‐frequency BOLD signal fluctuations: An fMRI investigation of the resting‐state default mode of brain function hypothesis , 2005, Human brain mapping.

[5]  B. Biswal,et al.  Blind source separation of multiple signal sources of fMRI data sets using independent component analysis. , 1999, Journal of computer assisted tomography.

[6]  Hengyi Rao,et al.  Arterial spin-labeled perfusion MRI in basic and clinical neuroscience , 2009, Current opinion in neurology.

[7]  E. Bullmore,et al.  Adaptive reconfiguration of fractal small-world human brain functional networks , 2006, Proceedings of the National Academy of Sciences.

[8]  J. Detre,et al.  Nicotine abstinence-induced cerebral blood flow changes by genotype , 2008, Neuroscience Letters.

[9]  Donald S. Williams,et al.  Perfusion imaging , 1992, Magnetic resonance in medicine.

[10]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  John Pluta,et al.  Test–retest stability analysis of resting brain activity revealed by blood oxygen level‐dependent functional MRI , 2012, Journal of magnetic resonance imaging : JMRI.

[12]  R. Ehrman,et al.  Limbic Activation to Cigarette Smoking Cues Independent of Nicotine Withdrawal: A Perfusion fMRI Study , 2007, Neuropsychopharmacology.

[13]  J. Detre,et al.  Neural Substrates of Abstinence-Induced Cigarette Cravings in Chronic Smokers , 2007, The Journal of Neuroscience.

[14]  Daniel S. Margulies,et al.  Mapping the functional connectivity of anterior cingulate cortex , 2007, NeuroImage.

[15]  Ze Wang,et al.  Empirical optimization of ASL data analysis using an ASL data processing toolbox: ASLtbx. , 2008, Magnetic resonance imaging.

[16]  John A. Detre,et al.  SPEECH PRODUCTION : AN fMRI STUDY USING CONTINUOUS ARTERIAL SPIN LABELING , 2008 .

[17]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[18]  Jeffrey R. Binder,et al.  Interrupting the “stream of consciousness”: An fMRI investigation , 2006, NeuroImage.

[19]  S. Debener,et al.  Default-mode brain dysfunction in mental disorders: A systematic review , 2009, Neuroscience & Biobehavioral Reviews.

[20]  S. Kety,et al.  THE DETERMINATION OF CEREBRAL BLOOD FLOW IN MAN BY THE USE OF NITROUS OXIDE IN LOW CONCENTRATIONS , 1945 .

[21]  Bruce R. Rosen,et al.  Spatio-temporal characteristics of low-frequency BOLD signal fluctuations in isoflurane-anesthetized rat brain , 2008, NeuroImage.

[22]  S. Kety,et al.  The circulation and energy metabolism of the brain. , 1963, Clinical neurosurgery.

[23]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[24]  Hengyi Rao,et al.  Applications of arterial spin labeled MRI in the brain , 2012, Journal of magnetic resonance imaging : JMRI.

[25]  S. Petersen,et al.  The maturing architecture of the brain's default network , 2008, Proceedings of the National Academy of Sciences.

[26]  Yufen Chen,et al.  Test–retest reliability of arterial spin labeling with common labeling strategies , 2011, Journal of magnetic resonance imaging : JMRI.

[27]  David C. Alsop,et al.  Assessment of functional development in normal infant brain using arterial spin labeled perfusion MRI , 2008, NeuroImage.

[28]  Ze Wang,et al.  Improving cerebral blood flow quantification for arterial spin labeled perfusion MRI by removing residual motion artifacts and global signal fluctuations. , 2012, Magnetic resonance imaging.

[29]  Yingli Lu,et al.  Regional homogeneity approach to fMRI data analysis , 2004, NeuroImage.

[30]  T. L. Davis,et al.  Calibrated functional MRI: mapping the dynamics of oxidative metabolism. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[31]  C. Sherrington,et al.  On the Regulation of the Blood‐supply of the Brain , 1890, The Journal of physiology.

[32]  Louis Sokoloff,et al.  Circulation and Energy Metabolism of the Brain , 1999 .

[33]  Bharat B. Biswal,et al.  Competition between functional brain networks mediates behavioral variability , 2008, NeuroImage.

[34]  M. Raichle.  Behind the scenes of functional brain imaging: a historical and physiological perspective. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[35]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[36]  Kendall Lee,et al.  Principles of Neurosurgery , 1991, The Yale Journal of Biology and Medicine.

[37]  Egill Rostrup,et al.  Determination of relative CMRO2 from CBF and BOLD changes: Significant increase of oxygen consumption rate during visual stimulation , 1999, Magnetic resonance in medicine.

[38]  Peter T Fox,et al.  Nonlinear coupling between cerebral blood flow, oxygen consumption, and ATP production in human visual cortex , 2010, Proceedings of the National Academy of Sciences.

[39]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[40]  R J Roman,et al.  Spontaneous Flow Oscillations in the Cerebral Cortex during Acute Changes in Mean Arterial Pressure , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[41]  Gary H. Glover,et al.  Changes of Cerebral Blood Flow, Oxygenation, and Oxidative Metabolism during Graded Motor Activation , 2002, NeuroImage.

[42]  M. Greicius.  Resting-state functional connectivity in neuropsychiatric disorders , 2008, Current opinion in neurology.

[43]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[44]  S Marrett,et al.  Changes of blood flow and oxygen consumption in visual cortex of living humans. , 1997, Advances in experimental medicine and biology.

[45]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[46]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[47]  R G Shulman,et al.  A model for the regulation of cerebral oxygen delivery. , 1998, Journal of applied physiology.

[48]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[49]  Yihong Yang,et al.  Static and dynamic characteristics of cerebral blood flow during the resting state , 2009, NeuroImage.

[50]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[51]  Yufeng Zang,et al.  Alterations in regional homogeneity of resting-state brain activity in autism spectrum disorders , 2010, Brain Research.

[52]  Tianzi Jiang,et al.  Regional coherence changes in the early stages of Alzheimer’s disease: A combined structural and resting-state functional MRI study , 2007, NeuroImage.

[53]  Thomas T. Liu,et al.  Coupling of cerebral blood flow and oxygen consumption during physiological activation and deactivation measured with fMRI , 2004, NeuroImage.

[54]  John A. Detre,et al.  Continuous ASL perfusion fMRI investigation of higher cognition: Quantification of tonic CBF changes during sustained attention and working memory tasks , 2006, NeuroImage.

[55]  M. Raichle,et al.  Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Chaozhe Zhu,et al.  Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI , 2007, NeuroImage.

[57]  M. Mintun,et al.  Brain work and brain imaging. , 2006, Annual review of neuroscience.

[58]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[59]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[60]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[61]  G. Crelier,et al.  Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[62]  M. Mintun,et al.  Nonoxidative glucose consumption during focal physiologic neural activity. , 1988, Science.

[63]  P. Skudlarski,et al.  Detection of functional connectivity using temporal correlations in MR images , 2002, Human brain mapping.

[64]  H. Gu,et al.  Association of nicotine addiction and nicotine's actions with separate cingulate cortex functional circuits. , 2009, Archives of general psychiatry.

[65]  V. Haughton,et al.  Mapping functionally related regions of brain with functional connectivity MR imaging. , 2000, AJNR. American journal of neuroradiology.

[66]  J. Detre,et al.  Amplitude-modulated continuous arterial spin-labeling 3.0-T perfusion MR imaging with a single coil: feasibility study. , 2005, Radiology.