Resting state functional connectivity changes induced by prior brain state are not network specific

Resting state functional connectivity (rFC) is used to identify functionally related brain areas without requiring subjects to perform specific tasks. Previous work suggests that prior brain state, as determined by the activity engaged in immediately prior to collection of resting state data, can influence the networks recovered by rFC analyses. We determined the prevalence and network specificity of rFC changes induced by manipulations of prior state (including an unstructured (unconstrained) state, and language and motor tasks). Three blocks of rest data (one after each of the specified prior states) were acquired on each of 25 subjects. We hypothesised that prior state induced changes in rFC would be greatest within the networks most actively recruited by that prior state. Changes in rFC were greatest following the motor task and, contrary to our hypothesis, were not network specific. This was demonstrated by comparing (1) the timecourses within a set of ROIs selected on the basis of task-related de/activation, and (2) seed-based whole brain voxel-wise connectivity maps, seeded from local maxima in the task-related de/activation maps. Changes in connectivity strength tended to manifest as increases in rFC relative to that in the unstructured rest state, with change maps resembling partially complete maps of the primary sensory cortices and the cognitive control network. The majority of rFC changes occurred in areas moderately (but not weakly) connected to the seeds. Constrained prior states were associated with lower across-participant variance in rFC. This systematic investigation of the effect of prior brain state on rFC indicates that the rFC changes induced by prior brain state occur both in brain networks related to that brain activity and in networks nominally unrelated to that brain activity.

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

[2]  Lee M. Miller,et al.  Functional connectivity of cortical networks involved in bimanual motor sequence learning. , 2006, Cerebral cortex.

[3]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

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

[5]  Yong He,et al.  Characterizing dynamic functional connectivity in the resting brain using variable parameter regression and Kalman filtering approaches , 2011, NeuroImage.

[6]  Mark A. Elliott,et al.  Impact of in-scanner head motion on multiple measures of functional connectivity: Relevance for studies of neurodevelopment in youth , 2012, NeuroImage.

[7]  Michael J. Prietula,et al.  Short- and Long-Term Effects of a Novel on Connectivity in the Brain , 2013, Brain Connect..

[8]  P. Bandettini,et al.  What's New in Neuroimaging Methods? , 2009, Annals of the New York Academy of Sciences.

[9]  Peter Fransson,et al.  Can resting‐state functional MRI serve as a complement to task‐based mapping of sensorimotor function? A test–retest reliability study in healthy volunteers , 2011, Journal of magnetic resonance imaging : JMRI.

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

[11]  Graeme D. Jackson,et al.  An Automated Method for Identifying Artifact in Independent Component Analysis of Resting-State fMRI , 2013, Front. Hum. Neurosci..

[12]  Graeme D. Jackson,et al.  Cortical and thalamic resting-state functional connectivity is altered in childhood absence epilepsy , 2012, Epilepsy Research.

[13]  Cheryl L. Grady,et al.  Task-Related Effects on the Temporal and Spatial Dynamics of Resting-State Functional Connectivity in the Default Network , 2010, PloS one.

[14]  L. Lemieux,et al.  Modelling large motion events in fMRI studies of patients with epilepsy. , 2007, Magnetic resonance imaging.

[15]  Hang Joon Jo,et al.  Trouble at Rest: How Correlation Patterns and Group Differences Become Distorted After Global Signal Regression , 2012, Brain Connect..

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

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

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

[19]  G. Jackson,et al.  A Neurocognitive Account of Frontal Lobe Involvement in Orthographic Lexical Retrieval: An fMRI Study , 2001, NeuroImage.

[20]  D. Yurgelun-Todd,et al.  Reproducibility of Single-Subject Functional Connectivity Measurements , 2011, American Journal of Neuroradiology.

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

[22]  Hang Joon Jo,et al.  The perils of global signal regression for group comparisons: a case study of Autism Spectrum Disorders , 2013, Front. Hum. Neurosci..

[23]  Rainer Goebel,et al.  Independent component model of the default-mode brain function: Assessing the impact of active thinking , 2006, Brain Research Bulletin.

[24]  Nuno Sousa,et al.  Stress Impact on Resting State Brain Networks , 2013, PloS one.

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

[26]  Peter A. Bandettini,et al.  Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI , 2006, NeuroImage.

[27]  O. Witte,et al.  Perceptual plasticity is mediated by connectivity changes of the medial thalamic nucleus , 2013, Human brain mapping.

[28]  Ning Zhong,et al.  Changes in the brain intrinsic organization in both on-task state and post-task resting state , 2012, NeuroImage.

[29]  J. Xiong,et al.  The power of spectral density analysis for mapping endogenous BOLD signal fluctuations , 2008, Human brain mapping.

[30]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[31]  Serge A R B Rombouts,et al.  Functional brain connectivity at rest changes after working memory training , 2013, Human brain mapping.

[32]  G. Jackson,et al.  Functional connectivity networks are disrupted in left temporal lobe epilepsy , 2006, Annals of neurology.

[33]  G. Jackson,et al.  Effect of prior cognitive state on resting state networks measured with functional connectivity , 2005, Human brain mapping.

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

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

[36]  O. Selnes A Compendium of Neuropsychological Tests , 1991, Neurology.

[37]  Tobias Otto,et al.  Spatially Distributed Effects of Mental Exhaustion on Resting-State FMRI Networks , 2014, PloS one.

[38]  Simon B. Eickhoff,et al.  One-year test–retest reliability of intrinsic connectivity network fMRI in older adults , 2012, NeuroImage.

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

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

[41]  Alex Fornito,et al.  What can spontaneous fluctuations of the blood oxygenation-level-dependent signal tell us about psychiatric disorders? , 2010, Current opinion in psychiatry.

[42]  Archana Venkataraman,et al.  Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. , 2010, Journal of neurophysiology.

[43]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[44]  Evan M. Gordon,et al.  Working memory‐related changes in functional connectivity persist beyond task disengagement , 2014, Human brain mapping.

[45]  Nicholas A. Ketz,et al.  Enhanced Brain Correlations during Rest Are Related to Memory for Recent Experiences , 2010, Neuron.

[46]  Karl J. Friston,et al.  Classical and Bayesian Inference in Neuroimaging: Applications , 2002, NeuroImage.

[47]  Catie Chang,et al.  Influence of heart rate on the BOLD signal: The cardiac response function , 2009, NeuroImage.

[48]  Yong He,et al.  Graph Theoretical Analysis of Functional Brain Networks: Test-Retest Evaluation on Short- and Long-Term Resting-State Functional MRI Data , 2011, PloS one.

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

[50]  D. Schacter,et al.  Correlated low-frequency BOLD fluctuations in the resting human brain are modulated by recent experience in category-preferential visual regions. , 2010, Cerebral cortex.

[51]  Guang H. Yue,et al.  Reductions in interhemispheric motor cortex functional connectivity after muscle fatigue , 2005, Brain Research.

[52]  R. Malach,et al.  The Day-After Effect: Long Term, Hebbian-Like Restructuring of Resting-State fMRI Patterns Induced by a Single Epoch of Cortical Activation , 2013, The Journal of Neuroscience.

[53]  J. Maldjian,et al.  Effect of resting-state functional MR imaging duration on stability of graph theory metrics of brain network connectivity. , 2011, Radiology.

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

[55]  Graeme Jackson,et al.  iBrain® — Software for analysis and visualisation of functional MR images , 2001, NeuroImage.

[56]  Rasmus M. Birn,et al.  The role of physiological noise in resting-state functional connectivity , 2012, NeuroImage.