Inter-individual differences in resting-state functional connectivity predict task-induced BOLD activity

The resting brain exhibits coherent patterns of spontaneous low-frequency BOLD fluctuations. These so-called resting-state functional connectivity (RSFC) networks are posited to reflect intrinsic representations of functional systems commonly implicated in cognitive function. Yet, the direct relationship between RSFC and the BOLD response induced by task performance remains unclear. Here we examine the relationship between a region's pattern of RSFC across participants and that same region's level of BOLD activation during an Eriksen Flanker task. To achieve this goal we employed a voxel-matched regression method, which assessed whether the magnitude of task-induced activity at each brain voxel could be predicted by measures of RSFC strength for the same voxel, across 26 healthy adults. We examined relationships between task-induced activation and RSFC strength for six different seed regions [Fox, M.D., Snyder, A.Z., Vincent, J.L., Corbetta, M., Van Essen, D.C., Raichle, M.E., 2005. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 102, 9673-9678.], as well as the "default mode" and "task-positive" resting-state networks in their entirety. Our results indicate that, for a number of brain regions, inter-individual differences in task-induced BOLD activity were predicted by one of two resting-state properties: (1) the region's positive connectivity strength with the task-positive network, or (2) its negative connectivity with the default mode network. Strikingly, most of the regions exhibiting a significant relationship between their RSFC properties and task-induced BOLD activity were located in transition zones between the default mode and task-positive networks. These results suggest that a common mechanism governs many brain regions' neural activity during rest and its neural activity during task performance.

[1]  J. Gallant,et al.  Identifying natural images from human brain activity , 2008, Nature.

[2]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[3]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[4]  B. Harrison,et al.  Modulation of Brain Resting-State Networks by Sad Mood Induction , 2008, PloS one.

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

[6]  Catie Chang,et al.  Time–frequency dynamics of resting-state brain connectivity measured with fMRI , 2010, NeuroImage.

[7]  M. Jenkinson Non-linear registration aka Spatial normalisation , 2007 .

[8]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[9]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[10]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[11]  H. Nusbaum,et al.  Task-dependent organization of brain regions active during rest , 2009, Proceedings of the National Academy of Sciences.

[12]  C. Kelly,et al.  L-Dopa Modulates Functional Connectivity in Striatal Cognitive and Motor Networks: A Double-Blind Placebo-Controlled Study , 2009, NeuroImage.

[13]  M. Greicius,et al.  Default-Mode Activity during a Passive Sensory Task: Uncoupled from Deactivation but Impacting Activation , 2004, Journal of Cognitive Neuroscience.

[14]  C. J. Honeya,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009 .

[15]  Gary H. Glover,et al.  Default-mode function and task-induced deactivation have overlapping brain substrates in children , 2008, NeuroImage.

[16]  Johannes Schultz,et al.  BOLD signal in intraparietal sulcus covaries with magnitude of implicitly driven attention shifts , 2009, NeuroImage.

[17]  Justin L. Vincent,et al.  Intrinsic Fluctuations within Cortical Systems Account for Intertrial Variability in Human Behavior , 2007, Neuron.

[18]  R. Todd Constable,et al.  Effects of estrogen variation on neural correlates of emotional response inhibition , 2006, NeuroImage.

[19]  E. Bullmore,et al.  Endogenous Human Brain Dynamics Recover Slowly Following Cognitive Effort , 2008, PloS one.

[20]  Justin L. Vincent,et al.  Disruption of Large-Scale Brain Systems in Advanced Aging , 2007, Neuron.

[21]  J. Schultz,et al.  BOLD signal in intraparietal sulcus covaries with magnitude of implicitly driven attention shifts , 2009 .

[22]  B. J. Casey,et al.  Differential patterns of striatal activation in young children with and without ADHD , 2003, Biological Psychiatry.

[23]  A. Roebroeck,et al.  Behavioural Brain Research , 2015 .

[24]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[25]  Xi-Nian Zuo,et al.  Reliable intrinsic connectivity networks: Test–retest evaluation using ICA and dual regression approach , 2010, NeuroImage.

[26]  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.

[27]  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.

[28]  P. Fransson How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations , 2006, Neuropsychologia.

[29]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[30]  T. Paus,et al.  Functional coactivation map of the human brain. , 2008, Cerebral cortex.

[31]  Joshua W. Brown,et al.  Conflict effects without conflict in anterior cingulate cortex: Multiple response effects and context specific representations , 2009, NeuroImage.

[32]  D. Alistair Steyn-Ross,et al.  Modeling brain activation patterns for the default and cognitive states , 2009, NeuroImage.

[33]  R. Kahn,et al.  Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain , 2009, Human brain mapping.

[34]  P. Skudlarski,et al.  Brain Connectivity Related to Working Memory Performance , 2006, The Journal of Neuroscience.

[35]  Edwin M. Robertson,et al.  The Resting Human Brain and Motor Learning , 2009, Current Biology.

[36]  Gary F. Egan,et al.  Long-term motor training induced changes in regional cerebral blood flow in both task and resting states , 2009, NeuroImage.

[37]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[38]  Damien A. Fair,et al.  Defining functional areas in individual human brains using resting functional connectivity MRI , 2008, NeuroImage.

[39]  Kevin N. Ochsner,et al.  Neural Systems Supporting the Control of Affective and Cognitive Conflicts , 2009, Journal of Cognitive Neuroscience.

[40]  D. Margulies,et al.  Development of anterior cingulate functional connectivity from late childhood to early adulthood. , 2009, Cerebral cortex.

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

[42]  Sarah Durston,et al.  A shift from diffuse to focal cortical activity with development. , 2006, Developmental science.

[43]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[44]  M. Fukunaga,et al.  Low frequency BOLD fluctuations during resting wakefulness and light sleep: A simultaneous EEG‐fMRI study , 2008, Human brain mapping.

[45]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

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

[47]  P. Matthews,et al.  Distinct patterns of brain activity in young carriers of the APOE e4 allele , 2009, NeuroImage.

[48]  Todd S. Braver,et al.  Age-related changes in neural activity during performance matched working memory manipulation , 2008, NeuroImage.

[49]  Lori Haase,et al.  Cortical activation in response to pure taste stimuli during the physiological states of hunger and satiety , 2009, NeuroImage.

[50]  Vince D. Calhoun,et al.  Measuring brain connectivity: Diffusion tensor imaging validates resting state temporal correlations , 2008, NeuroImage.

[51]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[52]  David Silbersweig,et al.  Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[54]  Jeffrey M. Zacks,et al.  Coherent spontaneous activity accounts for trial-to-trial variability in human evoked brain responses , 2006, Nature Neuroscience.

[55]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

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

[57]  C. Kelly,et al.  Relationship between cingulo-insular functional connectivity and autistic traits in neurotypical adults. , 2009, The American journal of psychiatry.

[58]  Aapo Hyvärinen,et al.  Independent component analysis of nondeterministic fMRI signal sources , 2003, NeuroImage.

[59]  B. Biswal,et al.  The resting brain: unconstrained yet reliable. , 2009, Cerebral cortex.

[60]  Joshua W. Brown Con fl ict effects without con fl ict in anterior cingulate cortex : Multiple response effects and context speci fi c representations , 2009 .

[61]  M. Greicius,et al.  Persistent default‐mode network connectivity during light sedation , 2008, Human brain mapping.

[62]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[63]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[64]  James J. Pekar,et al.  Atypical Motor and Sensory Cortex Activation in Attention-Deficit/Hyperactivity Disorder: A Functional Magnetic Resonance Imaging Study of Simple Sequential Finger Tapping , 2006, Biological Psychiatry.

[65]  Eliot Hazeltine,et al.  Dissociable Contributions of Prefrontal and Parietal Cortices to Response Selection , 2002, NeuroImage.

[66]  O. Tervonen,et al.  Functional segmentation of the brain cortex using high model order group-PICA. , 2009, NeuroImage.

[67]  Richard J. Davidson,et al.  Individual differences in some (but not all) medial prefrontal regions reflect cognitive demand while regulating unpleasant emotion , 2009, NeuroImage.