Modeling Semantic Encoding in a Common Neural Representational Space

Encoding models for mapping voxelwise semantic tuning are typically estimated separately for each individual, limiting their generalizability. In the current report, we develop a method for estimating semantic encoding models that generalize across individuals. Functional MRI was used to measure brain responses while participants freely viewed a naturalistic audiovisual movie. Word embeddings capturing agent-, action-, object-, and scene-related semantic content were assigned to each imaging volume based on an annotation of the film. We constructed both conventional within-subject semantic encoding models and between-subject models where the model was trained on a subset of participants and validated on a left-out participant. Between-subject models were trained using cortical surface-based anatomical normalization or surface-based whole-cortex hyperalignment. We used hyperalignment to project group data into an individual’s unique anatomical space via a common representational space, thus leveraging a larger volume of data for out-of-sample prediction while preserving the individual’s fine-grained functional–anatomical idiosyncrasies. Our findings demonstrate that anatomical normalization degrades the spatial specificity of between-subject encoding models relative to within-subject models. Hyperalignment, on the other hand, recovers the spatial specificity of semantic tuning lost during anatomical normalization, and yields model performance exceeding that of within-subject models.

[1]  Evan M. Gordon,et al.  Functional System and Areal Organization of a Highly Sampled Individual Human Brain , 2015, Neuron.

[2]  Jack L. Gallant,et al.  Pyrcca: Regularized Kernel Canonical Correlation Analysis in Python and Its Applications to Neuroimaging , 2015, Front. Neuroinform..

[3]  Russell A Poldrack,et al.  Precision Neuroscience: Dense Sampling of Individual Brains , 2017, Neuron.

[4]  Rodrigo M. Braga,et al.  Parallel Interdigitated Distributed Networks within the Individual Estimated by Intrinsic Functional Connectivity , 2017, Neuron.

[5]  Essa Yacoub,et al.  Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex , 2014, PLoS Comput. Biol..

[6]  J. S. Guntupalli,et al.  Decoding neural representational spaces using multivariate pattern analysis. , 2014, Annual review of neuroscience.

[7]  Nikolaus Kriegeskorte,et al.  Unique semantic space in the brain of each beholder predicts perceived similarity , 2014, Proceedings of the National Academy of Sciences.

[8]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[9]  Satrajit S. Ghosh,et al.  The brain imaging data structure, a format for organizing and describing outputs of neuroimaging experiments , 2016, Scientific Data.

[10]  Nancy Kanwisher,et al.  Toward a universal decoder of linguistic meaning from brain activation , 2018, Nature Communications.

[11]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

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

[13]  Satrajit S. Ghosh,et al.  Evaluation of volume-based and surface-based brain image registration methods , 2010, NeuroImage.

[14]  Frédéric E Theunissen,et al.  The Hierarchical Cortical Organization of Human Speech Processing , 2017, The Journal of Neuroscience.

[15]  Hao Xu,et al.  Regularized hyperalignment of multi-set fMRI data , 2012, 2012 IEEE Statistical Signal Processing Workshop (SSP).

[16]  Satrajit S. Ghosh,et al.  Nipype: A Flexible, Lightweight and Extensible Neuroimaging Data Processing Framework in Python , 2011, Front. Neuroinform..

[17]  Hervé Abdi,et al.  How the Human Brain Represents Perceived Dangerousness or “Predacity” of Animals , 2016, The Journal of Neuroscience.

[18]  Moritz F. Wurm,et al.  Decoding Concrete and Abstract Action Representations During Explicit and Implicit Conceptual Processing. , 2016, Cerebral cortex.

[19]  Paul E. Downing,et al.  A comparison of volume-based and surface-based multi-voxel pattern analysis , 2011, NeuroImage.

[20]  Po-Hsuan Chen,et al.  A Reduced-Dimension fMRI Shared Response Model , 2015, NIPS.

[21]  Bruce Fischl,et al.  FreeSurfer , 2012, NeuroImage.

[22]  Taicheng Huang,et al.  Quantifying the variability of scene‐selective regions: Interindividual, interhemispheric, and sex differences , 2017, Human brain mapping.

[23]  Lorenzo Torresani,et al.  Learning Spatiotemporal Features with 3D Convolutional Networks , 2014, 2015 IEEE International Conference on Computer Vision (ICCV).

[24]  Feilong Ma,et al.  A computational model of shared fine-scale structure in the human connectome , 2017, bioRxiv.

[25]  C C Wood,et al.  Retinotopic organization of human visual cortex: departures from the classical model. , 1996, Cerebral cortex.

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

[27]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

[28]  Samuel A. Nastase,et al.  Attention Selectively Reshapes the Geometry of Distributed Semantic Representation , 2016, bioRxiv.

[29]  Satrajit S. Ghosh,et al.  Prediction as a Humanitarian and Pragmatic Contribution from Human Cognitive Neuroscience , 2015, Neuron.

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

[31]  Jack L. Gallant,et al.  Encoding and decoding in fMRI , 2011, NeuroImage.

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

[33]  D. Heeger,et al.  Reliability of cortical activity during natural stimulation , 2010, Trends in Cognitive Sciences.

[34]  Rainer Goebel,et al.  Measuring structural–functional correspondence: Spatial variability of specialised brain regions after macro-anatomical alignment , 2012, NeuroImage.

[35]  J. Gallant,et al.  Reconstructing Visual Experiences from Brain Activity Evoked by Natural Movies , 2011, Current Biology.

[36]  Kentaro Yamada,et al.  Inter-subject neural code converter for visual image representation , 2015, NeuroImage.

[37]  Brian Murphy,et al.  Simultaneously Uncovering the Patterns of Brain Regions Involved in Different Story Reading Subprocesses , 2014, PloS one.

[38]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[39]  R. Adolphs,et al.  Building a Science of Individual Differences from fMRI , 2016, Trends in Cognitive Sciences.

[40]  Marcel A. J. van Gerven,et al.  Deep Neural Networks Reveal a Gradient in the Complexity of Neural Representations across the Ventral Stream , 2014, The Journal of Neuroscience.

[41]  Thomas L. Griffiths,et al.  Supplementary Information for Natural Speech Reveals the Semantic Maps That Tile Human Cerebral Cortex , 2022 .

[42]  Paul E. Downing,et al.  Crossmodal and action-specific: neuroimaging the human mirror neuron system , 2013, Trends in Cognitive Sciences.

[43]  R. Cameron Craddock,et al.  Individual differences in functional connectivity during naturalistic viewing conditions , 2016, NeuroImage.

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

[45]  Gidon Felsen,et al.  A natural approach to studying vision , 2005, Nature Neuroscience.

[46]  Xu Wang,et al.  Quantifying interindividual variability and asymmetry of face-selective regions: A probabilistic functional atlas , 2015, NeuroImage.

[47]  Xia Zhu,et al.  A Convolutional Autoencoder for Multi-Subject fMRI Data Aggregation , 2016, ArXiv.

[48]  Bryan R. Conroy,et al.  Function-based Intersubject Alignment of Human Cortical Anatomy , 2009, Cerebral cortex.

[49]  Michael Guerzhoy,et al.  Deep Neural Networks , 2013 .

[50]  J. S. Guntupalli,et al.  The Representation of Biological Classes in the Human Brain , 2012, The Journal of Neuroscience.

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

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

[53]  Daoqiang Zhang,et al.  Deep Hyperalignment , 2017, NIPS.

[54]  Moritz F. Wurm,et al.  Decoding Actions at Different Levels of Abstraction , 2015, The Journal of Neuroscience.

[55]  Sanjeev Arora,et al.  Mapping between fMRI responses to movies and their natural language annotations , 2016, NeuroImage.

[56]  Guowei Huang,et al.  Maternal Folic Acid Supplementation During Pregnancy Promotes Neurogenesis and Synaptogenesis in Neonatal Rat Offspring. , 2018, Cerebral cortex.

[57]  Satrajit S. Ghosh,et al.  BIDS apps: Improving ease of use, accessibility, and reproducibility of neuroimaging data analysis methods , 2016, bioRxiv.

[58]  Jonathan W. Peirce,et al.  PsychoPy—Psychophysics software in Python , 2007, Journal of Neuroscience Methods.

[59]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

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

[61]  Brenna Argall,et al.  SUMA: an interface for surface-based intra- and inter-subject analysis with AFNI , 2004, 2004 2nd IEEE International Symposium on Biomedical Imaging: Nano to Macro (IEEE Cat No. 04EX821).

[62]  Yaroslav O. Halchenko,et al.  The Animacy Continuum in the Human Ventral Vision Pathway , 2015, Journal of Cognitive Neuroscience.

[63]  D. Purves,et al.  Individual variation and lateral asymmetry of the rat primary somatosensory cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  Wei Chen,et al.  Transferring and generalizing deep-learning-based neural encoding models across subjects , 2017, NeuroImage.

[65]  J. Gower Generalized procrustes analysis , 1975 .

[66]  Peter J. Ramadge,et al.  Inter-subject alignment of human cortical anatomy using functional connectivity , 2013, NeuroImage.

[67]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[68]  Marcel van Gerven,et al.  Increasingly complex representations of natural movies across the dorsal stream are shared between subjects , 2017, NeuroImage.

[69]  Jeffrey Dean,et al.  Distributed Representations of Words and Phrases and their Compositionality , 2013, NIPS.

[70]  Jack L. Gallant,et al.  A Continuous Semantic Space Describes the Representation of Thousands of Object and Action Categories across the Human Brain , 2012, Neuron.

[71]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[72]  J. S. Guntupalli,et al.  A Model of Representational Spaces in Human Cortex , 2016, Cerebral cortex.

[73]  Evan M. Gordon,et al.  Precision Functional Mapping of Individual Human Brains , 2017, Neuron.