Resting connectivity predicts task activation in pre-surgical populations

Injury and disease affect neural processing and increase individual variations in patients when compared with healthy controls. Understanding this increased variability is critical for identifying the anatomical location of eloquent brain areas for pre-surgical planning. Here we show that precise and reliable language maps can be inferred in patient populations from resting scans of idle brain activity. We trained a predictive model on pairs of resting-state and task-evoked data and tested it to predict activation of unseen patients and healthy controls based on their resting-state data alone. A well-validated language task (category fluency) was used in acquiring the task-evoked fMRI data. Although patients showed greater variation in their actual language maps, our models successfully learned variations in both patient and control responses from the individual resting-connectivity features. Importantly, we further demonstrate that a model trained exclusively on the more-homogenous control group can be used to predict task activations in patients. These results are the first to show that resting connectivity robustly predicts individual differences in neural response in cases of pathological variability.

[1]  John Suckling,et al.  Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[2]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

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

[4]  Katrin Amunts,et al.  Cortical Folding Patterns and Predicting Cytoarchitecture , 2007, Cerebral cortex.

[5]  Mark W. Woolrich,et al.  Resting-state fMRI in the Human Connectome Project , 2013, NeuroImage.

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

[7]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[8]  Brian Everitt,et al.  A systematic review and quantitative appraisal of fMRI studies of verbal fluency: Role of the left inferior frontal gyrus , 2006, Human brain mapping.

[9]  Jonathan D. Power,et al.  Intrinsic and Task-Evoked Network Architectures of the Human Brain , 2014, Neuron.

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

[11]  Zeynep M. Saygin,et al.  Anatomical connectivity patterns predict face-selectivity in the fusiform gyrus , 2011, Nature Neuroscience.

[12]  M. Chun,et al.  A neuromarker of sustained attention from whole-brain functional connectivity , 2015, Nature Neuroscience.

[13]  S. Cobb Speech and Brain-Mechanisms. , 1960 .

[14]  Thomas E. Nichols,et al.  Combining voxel intensity and cluster extent with permutation test framework , 2004, NeuroImage.

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

[16]  Timothy Edward John Behrens,et al.  Task-free MRI predicts individual differences in brain activity during task performance , 2016, Science.

[17]  Nancy Kanwisher,et al.  Structural Connectivity Fingerprints Predict Cortical Selectivity for Multiple Visual Categories across Cortex. , 2016, Cerebral cortex.

[18]  M. Chun,et al.  Functional connectome fingerprinting: Identifying individuals based on patterns of brain connectivity , 2015, Nature Neuroscience.

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

[20]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[21]  L. R. Dice Measures of the Amount of Ecologic Association Between Species , 1945 .

[22]  Aapo Hyvärinen,et al.  Group-PCA for very large fMRI datasets , 2014, NeuroImage.

[23]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[24]  D. Perani,et al.  Functional heterogeneity of left inferior frontal cortex as revealed by fMRI , 1997, Neuroreport.

[25]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[26]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. , 1989, Journal of neurosurgery.

[27]  Kevin Murphy,et al.  How long to scan? The relationship between fMRI temporal signal to noise ratio and necessary scan duration , 2007, NeuroImage.