Decoding subject-driven cognitive states with whole-brain connectivity patterns.

Decoding specific cognitive states from brain activity constitutes a major goal of neuroscience. Previous studies of brain-state classification have focused largely on decoding brief, discrete events and have required the timing of these events to be known. To date, methods for decoding more continuous and purely subject-driven cognitive states have not been available. Here, we demonstrate that free-streaming subject-driven cognitive states can be decoded using a novel whole-brain functional connectivity analysis. Ninety functional regions of interest (ROIs) were defined across 14 large-scale resting-state brain networks to generate a 3960 cell matrix reflecting whole-brain connectivity. We trained a classifier to identify specific patterns of whole-brain connectivity as subjects rested quietly, remembered the events of their day, subtracted numbers, or (silently) sang lyrics. In a leave-one-out cross-validation, the classifier identified these 4 cognitive states with 84% accuracy. More critically, the classifier achieved 85% accuracy when identifying these states in a second, independent cohort of subjects. Classification accuracy remained high with imaging runs as short as 30-60 s. At all temporal intervals assessed, the 90 functionally defined ROIs outperformed a set of 112 commonly used structural ROIs in classifying cognitive states. This approach should enable decoding a myriad of subject-driven cognitive states from brief imaging data samples.

[1]  Dimitri Van De Ville,et al.  Decoding brain states from fMRI connectivity graphs , 2011, NeuroImage.

[2]  Michael Esterman,et al.  Decoding Task-based Attentional Modulation during Face Categorization , 2011, Journal of Cognitive Neuroscience.

[3]  Edward T. Bullmore,et al.  Whole-brain anatomical networks: Does the choice of nodes matter? , 2010, NeuroImage.

[4]  D. Hassabis,et al.  Decoding Individual Episodic Memory Traces in the Human Hippocampus , 2010, Current Biology.

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

[6]  Xiangyu Long,et al.  Functional segmentation of the brain cortex using high model order group PICA , 2009, Human brain mapping.

[7]  Benjamin J. Tamber-Rosenau,et al.  Decoding cognitive control in human parietal cortex , 2009, Proceedings of the National Academy of Sciences.

[8]  Catie Chang,et al.  Effects of model-based physiological noise correction on default mode network anti-correlations and correlations , 2009, NeuroImage.

[9]  Dirk B. Walther,et al.  Natural Scene Categories Revealed in Distributed Patterns of Activity in the Human Brain , 2009, The Journal of Neuroscience.

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

[11]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

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

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

[14]  Daniel L. Rubin,et al.  Network Analysis of Intrinsic Functional Brain Connectivity in Alzheimer's Disease , 2008, PLoS Comput. Biol..

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

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

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

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

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

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

[21]  Timothy Edward John Behrens,et al.  Connection patterns distinguish 3 regions of human parietal cortex. , 2006, Cerebral cortex.

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

[23]  Matthew H. Davis,et al.  Detecting Awareness in the Vegetative State , 2006, Science.

[24]  G. Rees,et al.  Neuroimaging: Decoding mental states from brain activity in humans , 2006, Nature Reviews Neuroscience.

[25]  Habib Benali,et al.  Identification of large-scale networks in the brain using fMRI , 2006, NeuroImage.

[26]  Vaidehi S. Natu,et al.  Category-Specific Cortical Activity Precedes Retrieval During Memory Search , 2005, Science.

[27]  Janaina Mourão Miranda,et al.  Classifying brain states and determining the discriminating activation patterns: Support Vector Machine on functional MRI data , 2005, NeuroImage.

[28]  Dinggang Shen,et al.  Classifying spatial patterns of brain activity with machine learning methods: Application to lie detection , 2005, NeuroImage.

[29]  G. Rees,et al.  Predicting the Stream of Consciousness from Activity in Human Visual Cortex , 2005, Current Biology.

[30]  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.

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

[32]  G. Rees,et al.  Predicting the orientation of invisible stimuli from activity in human primary visual cortex , 2005, Nature Neuroscience.

[33]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[34]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

[35]  Eric R. Ziegel,et al.  The Elements of Statistical Learning , 2003, Technometrics.

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

[37]  Tom M. Mitchell,et al.  Classifying Instantaneous Cognitive States from fMRI Data , 2003, AMIA.

[38]  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.

[39]  G. Glover,et al.  Regularized higher‐order in vivo shimming , 2002, Magnetic resonance in medicine.

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

[41]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[42]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[43]  G. Glover,et al.  Spiral‐in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts , 2001, Magnetic resonance in medicine.

[44]  V. Haughton,et al.  Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. , 2001, AJNR. American journal of neuroradiology.

[45]  A. Kleinschmidt,et al.  Dissociating neural correlates of cognitive components in mental calculation. , 2001, Cerebral cortex.

[46]  B. Mazoyer,et al.  Neural Correlates of Simple and Complex Mental Calculation , 2001, NeuroImage.

[47]  N. Kanwisher,et al.  Mental Imagery of Faces and Places Activates Corresponding Stimulus-Specific Brain Regions , 2000, Journal of Cognitive Neuroscience.

[48]  Anthony Randal McIntosh,et al.  Towards a network theory of cognition , 2000, Neural Networks.

[49]  G. Glover,et al.  Dissociating Prefrontal and Parietal Cortex Activation during Arithmetic Processing , 2000, NeuroImage.

[50]  E. Spelke,et al.  Sources of mathematical thinking: behavioral and brain-imaging evidence. , 1999, Science.

[51]  G. Glover,et al.  Self‐navigated spiral fMRI: Interleaved versus single‐shot , 1998, Magnetic resonance in medicine.

[52]  Karl J. Friston Imaging neuroscience: principles or maps? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Jean-Baptiste Poline,et al.  Inferring behavior from functional brain images , 1998, Nature Neuroscience.

[54]  Karl J. Friston,et al.  Combining Spatial Extent and Peak Intensity to Test for Activations in Functional Imaging , 1997, NeuroImage.

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

[56]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[57]  D. Spalding The Principles of Psychology , 1873, Nature.