Embedding Anatomical or Functional Knowledge in Whole-Brain Multiple Kernel Learning Models

Pattern recognition models have been increasingly applied to neuroimaging data over the last two decades. These applications have ranged from cognitive neuroscience to clinical problems. A common limitation of these approaches is that they do not incorporate previous knowledge about the brain structure and function into the models. Previous knowledge can be embedded into pattern recognition models by imposing a grouping structure based on anatomically or functionally defined brain regions. In this work, we present a novel approach that uses group sparsity to model the whole brain multivariate pattern as a combination of regional patterns. More specifically, we use a sparse version of Multiple Kernel Learning (MKL) to simultaneously learn the contribution of each brain region, previously defined by an atlas, to the decision function. Our application of MKL provides two beneficial features: (1) it can lead to improved overall generalisation performance when the grouping structure imposed by the atlas is consistent with the data; (2) it can identify a subset of relevant brain regions for the predictive model. In order to investigate the effect of the grouping in the proposed MKL approach we compared the results of three different atlases using three different datasets. The method has been implemented in the new version of the open-source Pattern Recognition for Neuroimaging Toolbox (PRoNTo).

[1]  Michael J. Brammer,et al.  Bayesian multi-task learning for decoding multi-subject neuroimaging data , 2014, NeuroImage.

[2]  Nikolaus Kriegeskorte,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[3]  Eric M Reiman,et al.  Cortical atrophy in presymptomatic Alzheimer's disease presenilin 1 mutation carriers , 2012, Journal of Neurology, Neurosurgery & Psychiatry.

[4]  Janaina Mourão Miranda,et al.  PRoNTo: Pattern Recognition for Neuroimaging Toolbox , 2013, Neuroinformatics.

[5]  Jesper Andersson,et al.  A multi-modal parcellation of human cerebral cortex , 2016, Nature.

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

[7]  Jonathan Taylor,et al.  A family of interpretable multivariate models for regression and classification of whole-brain fMRI data , 2011 .

[8]  John G. Csernansky,et al.  Open Access Series of Imaging Studies (OASIS): Cross-sectional MRI Data in Young, Middle Aged, Nondemented, and Demented Older Adults , 2007, Journal of Cognitive Neuroscience.

[9]  Stefan Haufe,et al.  On the interpretation of weight vectors of linear models in multivariate neuroimaging , 2014, NeuroImage.

[10]  T. Shallice,et al.  Face repetition effects in implicit and explicit memory tests as measured by fMRI. , 2002, Cerebral cortex.

[11]  Hiroshi Honda,et al.  Automated method for identification of patients with Alzheimer's disease based on three-dimensional MR images. , 2008, Academic radiology.

[12]  Bernhard E. Boser,et al.  A training algorithm for optimal margin classifiers , 1992, COLT '92.

[13]  M. Buonocore,et al.  Remembering familiar people: the posterior cingulate cortex and autobiographical memory retrieval , 2001, Neuroscience.

[14]  Michael I. Jordan,et al.  Multiple kernel learning, conic duality, and the SMO algorithm , 2004, ICML.

[15]  Bilwaj Gaonkar,et al.  Deriving Statistical Significance Maps for SVM Based Image Classification and Group Comparisons , 2012, MICCAI.

[16]  J. Morris The Clinical Dementia Rating (CDR) , 1993, Neurology.

[17]  Clifford R. Jack,et al.  Alzheimer's disease diagnosis in individual subjects using structural MR images: Validation studies , 2008, NeuroImage.

[18]  Yudong Zhang,et al.  Detection of subjects and brain regions related to Alzheimer's disease using 3D MRI scans based on eigenbrain and machine learning , 2015, Front. Comput. Neurosci..

[19]  John Shawe-Taylor,et al.  Sparse Network-Based Models for Patient Classification Using fMRI , 2013, PRNI.

[20]  Luca Baldassarre,et al.  Sparsity Is Better with Stability: Combining Accuracy and Stability for Model Selection in Brain Decoding , 2017, Front. Neurosci..

[21]  Lila Davachi,et al.  Persistence of hippocampal multivoxel patterns into postencoding rest is related to memory , 2013, Proceedings of the National Academy of Sciences.

[22]  Nello Cristianini,et al.  Learning the Kernel Matrix with Semidefinite Programming , 2002, J. Mach. Learn. Res..

[23]  R. Tibshirani Regression Shrinkage and Selection via the Lasso , 1996 .

[24]  James V. Haxby,et al.  CoSMoMVPA: Multi-Modal Multivariate Pattern Analysis of Neuroimaging Data in Matlab/GNU Octave , 2016, bioRxiv.

[25]  E. Amaro,et al.  Use of SVM methods with surface-based cortical and volumetric subcortical measurements to detect Alzheimer's disease. , 2010, Journal of Alzheimer's disease : JAD.

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

[27]  Muhammad Abuzar Fahiem,et al.  An Ensemble-of-Classifiers Based Approach for Early Diagnosis of Alzheimer's Disease: Classification Using Structural Features of Brain Images , 2014, Comput. Math. Methods Medicine.

[28]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[29]  Vikas Singh,et al.  Predictive markers for AD in a multi-modality framework: An analysis of MCI progression in the ADNI population , 2011, NeuroImage.

[30]  A. Mechelli,et al.  Using Support Vector Machine to identify imaging biomarkers of neurological and psychiatric disease: A critical review , 2012, Neuroscience & Biobehavioral Reviews.

[31]  Roman Filipovych,et al.  Multi-Kernel Classification for Integration of Clinical and Imaging Data: Application to Prediction of Cognitive Decline in Older Adults , 2011, MLMI.

[32]  Jeffrey M. Zacks,et al.  Searchlight analysis: Promise, pitfalls, and potential , 2013, NeuroImage.

[33]  Daoqiang Zhang,et al.  Multimodal classification of Alzheimer's disease and mild cognitive impairment , 2011, NeuroImage.

[34]  Tso-Jung Yen,et al.  Discussion on "Stability Selection" by Meinshausen and Buhlmann , 2010 .

[35]  R. Passingham,et al.  Reading Hidden Intentions in the Human Brain , 2007, Current Biology.

[36]  John G. Csernansky,et al.  Open Access Series of Imaging Studies: Longitudinal MRI Data in Nondemented and Demented Older Adults , 2010, Journal of Cognitive Neuroscience.

[37]  Luca Baldassarre,et al.  Localizing and Comparing Weight Maps Generated from Linear Kernel Machine Learning Models , 2013, 2013 International Workshop on Pattern Recognition in Neuroimaging.

[38]  Martin Lepage,et al.  A face to remember: emotional expression modulates prefrontal activity during memory formation , 2005, NeuroImage.

[39]  Radoslaw Martin Cichy,et al.  The Neural Code for Face Orientation in the Human Fusiform Face Area , 2014, The Journal of Neuroscience.

[40]  Mark S. Seidenberg,et al.  Neural Systems Underlying the Recognition of Familiar and Newly Learned Faces , 2000, The Journal of Neuroscience.

[41]  John Shawe-Taylor,et al.  Sparse network-based models for patient classification using fMRI , 2013, NeuroImage.

[42]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[43]  H. Zou,et al.  Regularization and variable selection via the elastic net , 2005 .

[44]  D. Louis Collins,et al.  MRI-Based Automated Computer Classification of Probable AD Versus Normal Controls , 2008, IEEE Transactions on Medical Imaging.

[45]  Stephen C. Strother,et al.  Support vector machines for temporal classification of block design fMRI data , 2005, NeuroImage.

[46]  Arthur W. Toga,et al.  A wavelet-based statistical analysis of fMRI data , 2007, Neuroinformatics.

[47]  Clifford R. Jack,et al.  Diagnostic neuroimaging across diseases , 2011, NeuroImage.

[48]  Michael Eickenberg,et al.  Machine learning for neuroimaging with scikit-learn , 2014, Front. Neuroinform..

[49]  Huiguang He,et al.  Classification of ADHD children through multimodal magnetic resonance imaging , 2012, Front. Syst. Neurosci..

[50]  M Filippone,et al.  PROBABILISTIC PREDICTION OF NEUROLOGICAL DISORDERS WITH A STATISTICAL ASSESSMENT OF NEUROIMAGING DATA MODALITIES. , 2012, The annals of applied statistics.

[51]  A. J. Batista-Leyva,et al.  On the interpretation of , 2004 .

[52]  Garraux Gaëtan,et al.  Multiclass classification of FDG PET scans for the distinction between Parkinson’s Disease and Atypical Parkinsonian Syndromes , 2012 .

[53]  N. Meinshausen,et al.  Stability selection , 2008, 0809.2932.

[54]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[55]  J. Haynes A Primer on Pattern-Based Approaches to fMRI: Principles, Pitfalls, and Perspectives , 2015, Neuron.

[56]  Clifford R Jack,et al.  Automatic Prediction of Conversion from Mild Cognitive Impairment to Probable Alzheimer's Disease using Structural Magnetic Resonance Imaging. , 2010, AMIA ... Annual Symposium proceedings. AMIA Symposium.

[57]  Tonio Ball,et al.  Causal interpretation rules for encoding and decoding models in neuroimaging , 2015, NeuroImage.

[58]  Lars Kai Hansen,et al.  Model sparsity and brain pattern interpretation of classification models in neuroimaging , 2012, Pattern Recognit..

[59]  Louis Wehenkel,et al.  Decoding Semi-Constrained Brain Activity from fMRI Using Support Vector Machines and Gaussian Processes , 2012, PloS one.

[60]  Marie Chupin,et al.  Multidimensional classification of hippocampal shape features discriminates Alzheimer's disease and mild cognitive impairment from normal aging , 2009, NeuroImage.

[61]  Stephen José Hanson,et al.  Combinatorial codes in ventral temporal lobe for object recognition: Haxby (2001) revisited: is there a “face” area? , 2004, NeuroImage.

[62]  Stefan Pollmann,et al.  PyMVPA: a Python Toolbox for Multivariate Pattern Analysis of fMRI Data , 2009, Neuroinformatics.

[63]  Andrea Passerini,et al.  Interpretability of Multivariate Brain Maps in Linear Brain Decoding: Definition, and Heuristic Quantification in Multivariate Analysis of MEG Time-Locked Effects , 2017, Front. Neurosci..

[64]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

[65]  Andres Hoyos Idrobo,et al.  Assessing and tuning brain decoders: Cross-validation, caveats, and guidelines , 2016, NeuroImage.

[66]  John Shawe-Taylor,et al.  SCoRS—A Method Based on Stability for Feature Selection and Mapping in Neuroimaging , 2014, IEEE Transactions on Medical Imaging.

[67]  H. Benali,et al.  Support vector machine-based classification of Alzheimer’s disease from whole-brain anatomical MRI , 2009, Neuroradiology.

[68]  Luca Baldassarre,et al.  Structured Sparsity Models for Brain Decoding from fMRI Data , 2012, 2012 Second International Workshop on Pattern Recognition in NeuroImaging.

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

[70]  Francisco Pereira,et al.  Information mapping with pattern classifiers: A comparative study , 2011, NeuroImage.

[71]  William L. Gross,et al.  Common neural systems associated with the recognition of famous faces and names: An event-related fMRI study , 2010, Brain and Cognition.

[72]  Nick C Fox,et al.  Automatic classification of MR scans in Alzheimer's disease. , 2008, Brain : a journal of neurology.

[73]  Tom M. Mitchell,et al.  Machine learning classifiers and fMRI: A tutorial overview , 2009, NeuroImage.

[74]  Martin Klein,et al.  Precuneus atrophy in early-onset Alzheimer’s disease: a morphometric structural MRI study , 2007, Neuroradiology.

[75]  Alice J. O'Toole,et al.  Partially Distributed Representations of Objects and Faces in Ventral Temporal Cortex , 2005, Journal of Cognitive Neuroscience.

[76]  Martin N. Hebart,et al.  The Decoding Toolbox (TDT): a versatile software package for multivariate analyses of functional imaging data , 2015, Front. Neuroinform..

[77]  Volker Arolt,et al.  MANIA—A Pattern Classification Toolbox for Neuroimaging Data , 2014, Neuroinformatics.

[78]  David C. Alsop,et al.  Dissociable effects of methylphenidate, atomoxetine and placebo on regional cerebral blood flow in healthy volunteers at rest: A multi-class pattern recognition approach , 2012, NeuroImage.

[79]  Stefan Pollmann,et al.  Neuroinformatics Original Research Article Pymvpa: a Unifying Approach to the Analysis of Neuroscientifi C Data , 2022 .

[80]  M. Milham,et al.  The ADHD-200 Consortium: A Model to Advance the Translational Potential of Neuroimaging in Clinical Neuroscience , 2012, Front. Syst. Neurosci..

[81]  M. Brammer,et al.  Pattern Classification of Sad Facial Processing: Toward the Development of Neurobiological Markers in Depression , 2008, Biological Psychiatry.

[82]  Junzhou Huang,et al.  The Benefit of Group Sparsity , 2009 .

[83]  Denise A. Minnebusch,et al.  A bilateral occipitotemporal network mediates face perception , 2009, Behavioural Brain Research.

[84]  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.

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

[86]  Jie Tian,et al.  Seeing Jesus in toast: Neural and behavioral correlates of face pareidolia , 2014, Cortex.