Comparison of multivariate classifiers and response normalizations for pattern-information fMRI

A popular method for investigating whether stimulus information is present in fMRI response patterns is to attempt to "decode" the stimuli from the response patterns with a multivariate classifier. The sensitivity for detecting the information depends on the particular classifier used. However, little is known about the relative performance of different classifiers on fMRI data. Here we compared six multivariate classifiers and investigated how the response-amplitude estimate used (beta- or t-value) and different pattern normalizations affect classification performance. The compared classifiers were a pattern-correlation classifier, a k-nearest-neighbors classifier, Fisher's linear discriminant, Gaussian naïve Bayes, and linear and nonlinear (radial-basis-function kernel) support vector machines. We compared these classifiers' accuracy at decoding the category of visual objects from response patterns in human early visual and inferior temporal cortex acquired in an event-related design with BOLD fMRI at 3T using SENSE and isotropic voxels of about 2-mm width. Overall, Fisher's linear discriminant (with an optimal-shrinkage covariance estimator) and the linear support vector machine performed best. The pattern-correlation classifier often performed similarly as those two classifiers. The nonlinear classifiers never performed better and sometimes significantly worse than the linear classifiers, suggesting overfitting. Defining response patterns by t-values (or in error-standard-deviation units) rather than by beta estimates (in % signal change) to define the patterns appeared advantageous. Cross-validation by a leave-one-stimulus-pair-out method gave higher accuracies than a leave-one-run-out method, suggesting that generalization to independent runs (which more safely ensures independence of the test set) is more challenging than generalization to novel stimuli within the same category. Independent selection of fewer more visually responsive voxels tended to yield better decoding performance for all classifiers. Normalizing mean and standard deviation of the response patterns either across stimuli or across voxels had no significant effect on decoding performance. Overall our results suggest that linear decoders based on t-value patterns may perform best in the present scenario of visual object representations measured for about 60min per subject with 3T fMRI.

[1]  Radford M. Neal Pattern Recognition and Machine Learning , 2007, Technometrics.

[2]  R. Goebel,et al.  Individual faces elicit distinct response patterns in human anterior temporal cortex , 2007, Proceedings of the National Academy of Sciences.

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

[4]  Nikolaus Kriegeskorte,et al.  Functional magnetic resonance imaging of the human object-vision system : methodological and empirical contributions , 2004 .

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

[6]  Nikolaus Kriegeskorte,et al.  Artifactual time‐course correlations in echo‐planar fMRI with implications for studies of brain function , 2008, Int. J. Imaging Syst. Technol..

[7]  Rafael Malach,et al.  Faculty Opinions recommendation of Distributed and overlapping representations of faces and objects in ventral temporal cortex. , 2002 .

[8]  Thomas G. Dietterich Adaptive computation and machine learning , 1998 .

[9]  Alexander J. Smola,et al.  Learning with Kernels: support vector machines, regularization, optimization, and beyond , 2001, Adaptive computation and machine learning series.

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

[11]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[12]  Rainer Goebel,et al.  Combining multivariate voxel selection and support vector machines for mapping and classification of fMRI spatial patterns , 2008, NeuroImage.

[13]  David D. Cox,et al.  Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex , 2003, NeuroImage.

[14]  Vladimir N. Vapnik,et al.  The Nature of Statistical Learning Theory , 2000, Statistics for Engineering and Information Science.

[15]  K. Strimmer,et al.  Statistical Applications in Genetics and Molecular Biology A Shrinkage Approach to Large-Scale Covariance Matrix Estimation and Implications for Functional Genomics , 2011 .

[16]  R. Quiroga,et al.  Extracting information from neuronal populations : information theory and decoding approaches , 2022 .

[17]  Nikolaus Kriegeskorte,et al.  Analyzing for information, not activation, to exploit high-resolution fMRI , 2007, NeuroImage.

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

[19]  Yoshua Bengio,et al.  Inference for the Generalization Error , 1999, Machine Learning.

[20]  Janez Demsar,et al.  Statistical Comparisons of Classifiers over Multiple Data Sets , 2006, J. Mach. Learn. Res..

[21]  Johan Wessberg,et al.  An Evolutionary Approach to Multivariate Feature Selection for FMRI Pattern Analysis , 2008, BIOSIGNALS.

[22]  Manel Martínez-Ramón,et al.  fMRI pattern classification using neuroanatomically constrained boosting , 2006, NeuroImage.

[23]  A. Ishai,et al.  Recollection- and Familiarity-Based Decisions Reflect Memory Strength , 2008, Frontiers in systems neuroscience.

[24]  Tom Michael Mitchell,et al.  Predicting Human Brain Activity Associated with the Meanings of Nouns , 2008, Science.

[25]  Thomas G. Dietterich Approximate Statistical Tests for Comparing Supervised Classification Learning Algorithms , 1998, Neural Computation.

[26]  Arthur Gretton,et al.  Comparison of Pattern Recognition Methods in Classifying High-resolution Bold Signals Obtained at High Magnetic Field in Monkeys , 2008 .

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

[28]  Thomas G. Dietterich What is machine learning? , 2020, Archives of Disease in Childhood.

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

[30]  Isabelle Guyon,et al.  An Introduction to Variable and Feature Selection , 2003, J. Mach. Learn. Res..

[31]  Robert Tibshirani,et al.  The Elements of Statistical Learning: Data Mining, Inference, and Prediction, 2nd Edition , 2001, Springer Series in Statistics.

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

[33]  Nello Cristianini,et al.  An introduction to Support Vector Machines , 2000 .

[34]  A. Atiya,et al.  Learning with Kernels: Support Vector Machines, Regularization, Optimization, and Beyond , 2005, IEEE Transactions on Neural Networks.

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

[36]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[37]  James R. Schott,et al.  Principles of Multivariate Analysis: A User's Perspective , 2002 .

[38]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[39]  Olivier Ledoit,et al.  Improved estimation of the covariance matrix of stock returns with an application to portfolio selection , 2003 .

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

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

[42]  Trevor Hastie,et al.  The Elements of Statistical Learning , 2001 .

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

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

[45]  David G. Stork,et al.  Pattern Classification , 1973 .

[46]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[47]  David G. Stork,et al.  Pattern Classification (2nd ed.) , 1999 .

[48]  Lawrence Carin,et al.  Sparse multinomial logistic regression: fast algorithms and generalization bounds , 2005, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[49]  Tom M. Mitchell,et al.  Learning to Decode Cognitive States from Brain Images , 2004, Machine Learning.

[50]  N. Kriegeskorte,et al.  Revealing representational content with pattern-information fMRI--an introductory guide. , 2009, Social cognitive and affective neuroscience.

[51]  Klaus Nordhausen,et al.  The Elements of Statistical Learning: Data Mining, Inference, and Prediction, Second Edition by Trevor Hastie, Robert Tibshirani, Jerome Friedman , 2009 .