What Makes Different People's Representations Alike: Neural Similarity Space Solves the Problem of Across-subject fMRI Decoding

A central goal in neuroscience is to interpret neural activation and, moreover, to do so in a way that captures universal principles by generalizing across individuals. Recent research in multivoxel pattern-based fMRI analysis has led to considerable success at decoding within individual subjects. However, the goal of being able to decode across subjects is still challenging: It has remained unclear what population-level regularities of neural representation there might be. Here, we present a novel and highly accurate solution to this problem, which decodes across subjects between eight different stimulus conditions. The key to finding this solution was questioning the seemingly obvious idea that neural decoding should work directly on neural activation patterns. On the contrary, to decode across subjects, it is beneficial to abstract away from subject-specific patterns of neural activity and, instead, to operate on the similarity relations between those patterns: Our new approach performs decoding purely within similarity space. These results demonstrate a hitherto unknown population-level regularity in neural representation and also reveal a striking convergence between our empirical findings in fMRI and discussions in the philosophy of mind addressing the problem of conceptual similarity across neural diversity.

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

[2]  Ernest Lepore,et al.  Holism: A Shopper's Guide , 1992 .

[3]  George A. Miller,et al.  WordNet: A Lexical Database for English , 1995, HLT.

[4]  D. Gentner,et al.  Respects for similarity , 1993 .

[5]  R. Shepard The analysis of proximities: Multidimensional scaling with an unknown distance function. I. , 1962 .

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

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

[8]  M. Ida Gobbini,et al.  Three Virtues of Similarity-based Multivariate Pattern Analysis : An example from the human object vision pathway , 2014 .

[9]  Jiawei Han,et al.  Data Mining: Concepts and Techniques , 2000 .

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

[11]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[12]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[13]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[14]  B. Mesquita,et al.  Adjustment to Chronic Diseases and Terminal Illness Health Psychology : Psychological Adjustment to Chronic Disease , 2006 .

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

[16]  P. Churchland Conceptual similarity across sensory and neural diversity : The Fodor/Lepore challenge answered , 1998 .

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

[18]  Scott A. Huettel,et al.  Within- and cross-participant classifiers reveal different neural coding of information , 2011, NeuroImage.

[19]  Juan José Rodríguez Diez,et al.  Random Subspace Ensembles for fMRI Classification , 2010, IEEE Transactions on Medical Imaging.

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

[21]  Roxana Josens,et al.  Calcium imaging in the ant Camponotus fellah reveals a conserved odour-similarity space in insects and mammals , 2010, BMC Neuroscience.

[22]  Stephen José Hanson,et al.  Decoding the Large-Scale Structure of Brain Function by Classifying Mental States Across Individuals , 2009, Psychological science.

[23]  R. Shepard The analysis of proximities: Multidimensional scaling with an unknown distance function. II , 1962 .

[24]  Paul M. Churchland,et al.  Some reductive Strategies in Cognitive Neurobiology , 1986, The Philosophy of Artificial Intelligence.

[25]  David Harel,et al.  A metric for odorant comparison , 2008, Nature Methods.

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

[27]  A. Caramazza,et al.  Domain-Specific Knowledge Systems in the Brain: The Animate-Inanimate Distinction , 1998, Journal of Cognitive Neuroscience.

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

[29]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[30]  I Daubechies,et al.  Independent component analysis for brain fMRI does not select for independence , 2009 .

[31]  Nikolaus Kriegeskorte,et al.  Pattern‐information fMRI: New questions which it opens up and challenges which face it , 2010, Int. J. Imaging Syst. Technol..

[32]  Daniel J Navarro,et al.  Introduction to the special issue on formal modeling of semantic concepts. , 2010, Acta psychologica.

[33]  J. Fodor,et al.  All at sea in semantic space : Churchland on meaning similarity , 1999 .

[34]  Robert P. W. Duin,et al.  The Dissimilarity Representation for Pattern Recognition - Foundations and Applications , 2005, Series in Machine Perception and Artificial Intelligence.

[35]  Robert O. Duncan,et al.  Cortical Magnification within Human Primary Visual Cortex Correlates with Acuity Thresholds , 2003, Neuron.

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

[37]  Sheng He,et al.  Similarity representation of pattern-information fMRI , 2013 .

[38]  Tom M. Mitchell,et al.  Training fMRI Classifiers to Detect Cognitive States across Multiple Human Subjects , 2003, NIPS 2003.

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

[40]  Maya R. Gupta,et al.  Similarity-based Classification: Concepts and Algorithms , 2009, J. Mach. Learn. Res..

[41]  Alice J. O'Toole,et al.  Theoretical, Statistical, and Practical Perspectives on Pattern-based Classification Approaches to the Analysis of Functional Neuroimaging Data , 2007, Journal of Cognitive Neuroscience.

[42]  Ted Pedersen,et al.  WordNet::Similarity - Measuring the Relatedness of Concepts , 2004, NAACL.

[43]  N. Kriegeskorte,et al.  Author ' s personal copy Representational geometry : integrating cognition , computation , and the brain , 2013 .

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

[45]  Robert L. Goldstone,et al.  Using relations within conceptual systems to translate across conceptual systems , 2002, Cognition.

[46]  John-Dylan Haynes,et al.  Odor quality coding and categorization in human posterior piriform cortex , 2009, Nature Neuroscience.

[47]  M. Giurfa,et al.  Perceptual and Neural Olfactory Similarity in Honeybees , 2005, PLoS biology.

[48]  T. Landauer,et al.  A Solution to Plato's Problem: The Latent Semantic Analysis Theory of Acquisition, Induction, and Representation of Knowledge. , 1997 .

[49]  A. Tversky Features of Similarity , 1977 .

[50]  Tom Michael Mitchell,et al.  From the SelectedWorks of Marcel Adam Just 2008 Using fMRI brain activation to identify cognitive states associated with perception of tools and dwellings , 2016 .

[51]  Thomas A. Cleland,et al.  Behavioral models of odor similarity. , 2002, Behavioral neuroscience.

[52]  Marcel Adam Just,et al.  Exploring commonalities across participants in the neural representation of objects , 2012, Human brain mapping.

[53]  R. Suganya,et al.  Data Mining Concepts and Techniques , 2010 .

[54]  J. Haynes Brain Reading: Decoding Mental States From Brain Activity In Humans , 2011 .

[55]  Geraint Rees,et al.  Early Visual Responses Predict Conscious Face Perception within and between Subjects during Binocular Rivalry , 2013, Journal of Cognitive Neuroscience.

[56]  J. Mumford,et al.  Greater Neural Pattern Similarity Across Repetitions Is Associated with Better Memory , 2010, Science.

[57]  T. Shallice,et al.  Category specific semantic impairments , 1984 .

[58]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[59]  Bryan R. Conroy,et al.  A Common, High-Dimensional Model of the Representational Space in Human Ventral Temporal Cortex , 2011, Neuron.

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

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