Frontiers in Systems Neuroscience Systems Neuroscience

A fundamental challenge for systems neuroscience is to quantitatively relate its three major branches of research: brain-activity measurement, behavioral measurement, and computational modeling. Using measured brain-activity patterns to evaluate computational network models is complicated by the need to define the correspondency between the units of the model and the channels of the brain-activity data, e.g., single-cell recordings or voxels from functional magnetic resonance imaging (fMRI). Similar correspondency problems complicate relating activity patterns between different modalities of brain-activity measurement (e.g., fMRI and invasive or scalp electrophysiology), and between subjects and species. In order to bridge these divides, we suggest abstracting from the activity patterns themselves and computing representational dissimilarity matrices (RDMs), which characterize the information carried by a given representation in a brain or model. Building on a rich psychological and mathematical literature on similarity analysis, we propose a new experimental and data-analytical framework called representational similarity analysis (RSA), in which multi-channel measures of neural activity are quantitatively related to each other and to computational theory and behavior by comparing RDMs. We demonstrate RSA by relating representations of visual objects as measured with fMRI in early visual cortex and the fusiform face area to computational models spanning a wide range of complexities. The RDMs are simultaneously related via second-level application of multidimensional scaling and tested using randomization and bootstrap techniques. We discuss the broad potential of RSA, including novel approaches to experimental design, and argue that these ideas, which have deep roots in psychology and neuroscience, will allow the integrated quantitative analysis of data from all three branches, thus contributing to a more unified systems neuroscience.

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

[2]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

[3]  Amir Shmuel,et al.  Multi-resolution classification analysis of ocular dominance columns obtained at 7 Tesla from human V1: mechanisms underlying decoding signals , 2007 .

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

[5]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[6]  Dae-Shik Kim,et al.  Localized cerebral blood flow response at submillimeter columnar resolution , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[9]  T. Carlson,et al.  Patterns of Activity in the Categorical Representations of Objects , 2003, Journal of Cognitive Neuroscience.

[10]  R. Shepard,et al.  Second-order isomorphism of internal representations: Shapes of states ☆ , 1970 .

[11]  Garrison W. Cottrell,et al.  Content and cluster analysis: Assessing representational similarity in neural systems , 2000 .

[12]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

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

[14]  Thomas Serre,et al.  A feedforward architecture accounts for rapid categorization , 2007, Proceedings of the National Academy of Sciences.

[15]  S. Edelman,et al.  Toward direct visualization of the internal shape representation space by fMRI , 1998, Psychobiology.

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

[17]  Vivien A. Casagrande,et al.  Biophysics of Computation: Information Processing in Single Neurons , 1999 .

[18]  S Edelman,et al.  Faithful representation of similarities among three-dimensional shapes in human vision. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[19]  R. Shepard,et al.  The internal representation of numbers , 1975, Cognitive Psychology.

[20]  L. K. Hansen,et al.  The Quantitative Evaluation of Functional Neuroimaging Experiments: The NPAIRS Data Analysis Framework , 2000, NeuroImage.

[21]  Shimon Edelman,et al.  Similarity, Connectionism, and the Problem of Representation in Vision , 1997, Neural Computation.

[22]  Tomaso Poggio,et al.  Fast Readout of Object Identity from Macaque Inferior Temporal Cortex , 2005, Science.

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

[24]  S. Edelman,et al.  Representation of object similarity in human vision: psychophysics and a computational model , 1998, Vision Research.

[25]  B. Biswal,et al.  High‐resolution fMRI using multislice partial k‐space GR‐EPI with cubic voxels , 2001, Magnetic resonance in medicine.

[26]  A. Kraskov,et al.  Estimating mutual information. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  R. S. Hinks,et al.  Time course EPI of human brain function during task activation , 1992, Magnetic resonance in medicine.

[28]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[29]  Geoffrey Karl Aguirre,et al.  Continuous carry-over designs for fMRI , 2007, NeuroImage.

[30]  Lars Kai Hansen,et al.  The Quantitative Evaluation of Functional Neuroimaging Experiments: The NPAIRS Data Analysis Framework , 2000, NeuroImage.

[31]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[32]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

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

[34]  R N Shepard,et al.  Multidimensional Scaling, Tree-Fitting, and Clustering , 1980, Science.

[35]  F. Tong,et al.  Decoding Seen and Attended Motion Directions from Activity in the Human Visual Cortex , 2006, Current Biology.

[36]  T. Poggio,et al.  Neural mechanisms of object recognition , 2002, Current Opinion in Neurobiology.

[37]  Michael Schmitt,et al.  Neuroimaging databases as a resource for scientific discovery. , 2005, International review of neurobiology.

[38]  R. Buckner,et al.  Human Brain Mapping 6:373–377(1998) � Event-Related fMRI and the Hemodynamic Response , 2022 .

[39]  J. Tenenbaum,et al.  A global geometric framework for nonlinear dimensionality reduction. , 2000, Science.

[40]  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.

[41]  Peter A. Bandettini,et al.  From neuron to BOLD: new connections , 2001, Nature Neuroscience.

[42]  Walter Schneider,et al.  A Virtual Reality System for Neurobehavioral and Functional MRI Studies , 2003, Cyberpsychology Behav. Soc. Netw..

[43]  Sharon L. Thompson-Schill,et al.  Item analysis in functional magnetic resonance imaging , 2007, NeuroImage.

[44]  Thomas Serre,et al.  Object recognition with features inspired by visual cortex , 2005, 2005 IEEE Computer Society Conference on Computer Vision and Pattern Recognition (CVPR'05).

[45]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

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

[47]  Keiji Tanaka,et al.  Human Ocular Dominance Columns as Revealed by High-Field Functional Magnetic Resonance Imaging , 2001, Neuron.

[48]  Karl J. Friston,et al.  Analysis of functional MRI time‐series , 1994, Human Brain Mapping.

[49]  Karl J. Friston,et al.  Bayesian decoding of brain images , 2008, NeuroImage.

[50]  L. Pessoa,et al.  Decoding near-threshold perception of fear from distributed single-trial brain activation. , 2006, Cerebral cortex.

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

[52]  T. Carlson,et al.  Patterns of Activity in the Categorical Representations of Objects , 2003 .

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

[54]  S T Roweis,et al.  Nonlinear dimensionality reduction by locally linear embedding. , 2000, Science.

[55]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[56]  N. Kanwisher,et al.  How Distributed Is Visual Category Information in Human Occipito-Temporal Cortex? An fMRI Study , 2002, Neuron.

[57]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[58]  Essa Yacoub,et al.  Frontiers of brain mapping using MRI , 2006, Journal of magnetic resonance imaging : JMRI.

[59]  Geoffrey M Boynton,et al.  The Representation of Behavioral Choice for Motion in Human Visual Cortex , 2007, The Journal of Neuroscience.

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

[61]  S. C. Johnson Hierarchical clustering schemes , 1967, Psychometrika.

[62]  R. Malach,et al.  Intersubject Synchronization of Cortical Activity During Natural Vision , 2004, Science.

[63]  S Edelman,et al.  A model of visual recognition and categorization. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[65]  Shimon Edelman,et al.  Representation of Similarity in Three-Dimensional Object Discrimination , 1995, Neural Computation.

[66]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Keiji Tanaka,et al.  Object category structure in response patterns of neuronal population in monkey inferior temporal cortex. , 2007, Journal of neurophysiology.

[68]  Thomas E. Nichols,et al.  Optimization of experimental design in fMRI: a general framework using a genetic algorithm , 2003, NeuroImage.

[69]  Joseph L. Zinnes,et al.  Theory and Methods of Scaling. , 1958 .

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

[71]  S. C. Strother,et al.  The Quantitative Evaluation of Functional Neuroimaging Experiments: Mutual Information Learning Curves , 2002, NeuroImage.

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

[73]  N. Kanwisher,et al.  Only some spatial patterns of fMRI response are read out in task performance , 2007, Nature Neuroscience.

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

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

[76]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[77]  Patrick J. F. Groenen,et al.  Modern Multidimensional Scaling: Theory and Applications , 2003 .

[78]  Tomaso Poggio,et al.  Intracellular measurements of spatial integration and the MAX operation in complex cells of the cat primary visual cortex. , 2004, Journal of neurophysiology.

[79]  R. Vogels,et al.  Inferotemporal neurons represent low-dimensional configurations of parameterized shapes , 2001, Nature Neuroscience.

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

[81]  J. Gallant,et al.  Predicting neuronal responses during natural vision , 2005, Network.

[82]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[83]  S. Brison The Intentional Stance , 1989 .

[84]  Ulrike von Luxburg,et al.  A tutorial on spectral clustering , 2007, Stat. Comput..

[85]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[86]  S Edelman,et al.  Representation is representation of similarities , 1996, Behavioral and Brain Sciences.

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