Optimizing methods for linking cinematic features to fMRI data

One of the challenges of naturalistic neurosciences using movie-viewing experiments is how to interpret observed brain activations in relation to the multiplicity of time-locked stimulus features. As previous studies have shown less inter-subject synchronization across viewers of random video footage than story-driven films, new methods need to be developed for analysis of less story-driven contents. To optimize the linkage between our fMRI data collected during viewing of a deliberately non-narrative silent film 'At Land' by Maya Deren (1944) and its annotated content, we combined the method of elastic-net regularization with the model-driven linear regression and the well-established data-driven independent component analysis (ICA) and inter-subject correlation (ISC) methods. In the linear regression analysis, both IC and region-of-interest (ROI) time-series were fitted with time-series of a total of 36 binary-valued and one real-valued tactile annotation of film features. The elastic-net regularization and cross-validation were applied in the ordinary least-squares linear regression in order to avoid over-fitting due to the multicollinearity of regressors, the results were compared against both the partial least-squares (PLS) regression and the un-regularized full-model regression. Non-parametric permutation testing scheme was applied to evaluate the statistical significance of regression. We found statistically significant correlation between the annotation model and 9 ICs out of 40 ICs. Regression analysis was also repeated for a large set of cubic ROIs covering the grey matter. Both IC- and ROI-based regression analyses revealed activations in parietal and occipital regions, with additional smaller clusters in the frontal lobe. Furthermore, we found elastic-net based regression more sensitive than PLS and un-regularized regression since it detected a larger number of significant ICs and ROIs. Along with the ISC ranking methods, our regression analysis proved a feasible method for ordering the ICs based on their functional relevance to the annotated cinematic features. The novelty of our method is - in comparison to the hypothesis-driven manual pre-selection and observation of some individual regressors biased by choice - in applying data-driven approach to all content features simultaneously. We found especially the combination of regularized regression and ICA useful when analyzing fMRI data obtained using non-narrative movie stimulus with a large set of complex and correlated features.

[1]  Kaustubh Supekar,et al.  Estimation of functional connectivity in fMRI data using stability selection-based sparse partial correlation with elastic net penalty , 2012, NeuroImage.

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

[3]  F. R. Gantmakher The Theory of Matrices , 1984 .

[4]  Ravi S. Menon,et al.  Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements. , 2001, Journal of neurophysiology.

[5]  Peter Lancaster,et al.  The theory of matrices , 1969 .

[6]  Jeffrey M. Zacks,et al.  Human brain activity time-locked to perceptual event boundaries , 2001, Nature Neuroscience.

[7]  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.

[8]  M. Gold,et al.  Human Functional Magnetic Resonance Imaging of Eating and Satiety in Eating Disorders and Obesity , 2003 .

[9]  Mikko Sams,et al.  Naturalistic fMRI Mapping Reveals Superior Temporal Sulcus as the Hub for the Distributed Brain Network for Social Perception , 2012, Front. Hum. Neurosci..

[10]  Angela R. Laird,et al.  ALE meta-analysis of action observation and imitation in the human brain , 2010, NeuroImage.

[11]  A. Owen,et al.  A common neural code for similar conscious experiences in different individuals , 2014, Proceedings of the National Academy of Sciences.

[12]  V. Calhoun,et al.  Multisubject Independent Component Analysis of fMRI: A Decade of Intrinsic Networks, Default Mode, and Neurodiagnostic Discovery , 2012, IEEE Reviews in Biomedical Engineering.

[13]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

[14]  R. O’Brien,et al.  A Caution Regarding Rules of Thumb for Variance Inflation Factors , 2007 .

[15]  G. Orban,et al.  Common and segregated processing of observed actions in human SPL. , 2013, Cerebral cortex.

[16]  Timothy O. Laumann,et al.  Methods to detect, characterize, and remove motion artifact in resting state fMRI , 2014, NeuroImage.

[17]  Vinoo Alluri,et al.  Capturing the musical brain with Lasso: Dynamic decoding of musical features from fMRI data , 2014, NeuroImage.

[18]  T. Martin McGinnity,et al.  A least angle regression method for fMRI activation detection in phase-encoded experimental designs , 2010, NeuroImage.

[19]  Hennie Brugman,et al.  Annotating Multi-media/Multi-modal Resources with ELAN , 2004, LREC.

[20]  Steven Laureys,et al.  Resting State Networks and Consciousness , 2012, Front. Psychology.

[21]  D. Perrett,et al.  A region of right posterior superior temporal sulcus responds to observed intentional actions , 2004, Neuropsychologia.

[22]  J. Pekar,et al.  A method for making group inferences from functional MRI data using independent component analysis , 2001, Human brain mapping.

[23]  D. Heeger,et al.  A Hierarchy of Temporal Receptive Windows in Human Cortex , 2008, The Journal of Neuroscience.

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

[25]  T. Allison,et al.  Functional anatomy of biological motion perception in posterior temporal cortex: an FMRI study of eye, mouth and hand movements. , 2005, Cerebral cortex.

[26]  A. R. McIntosh,et al.  Spatiotemporal analysis of event-related fMRI data using partial least squares , 2004, NeuroImage.

[27]  A. Ravishankar Rao,et al.  Prediction and interpretation of distributed neural activity with sparse models , 2009, NeuroImage.

[28]  R. Tibshirani,et al.  Regression shrinkage and selection via the lasso: a retrospective , 2011 .

[29]  Janne Kauttonen,et al.  Model of Narrative Nowness for Neurocinematic Experiments , 2014, CMN.

[30]  Riitta Hari,et al.  Intersubject consistency of cortical MEG signals during movie viewing , 2014, NeuroImage.

[31]  Jukka-Pekka Kauppi,et al.  Inter-Subject Correlation in fMRI: Method Validation against Stimulus-Model Based Analysis , 2012, PloS one.

[32]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[33]  Huafu Chen,et al.  Discussion on the choice of separated components in fMRI data analysis by spatial independent component analysis. , 2004, Magnetic resonance imaging.

[34]  Jean-Baptiste Poline,et al.  Ambiguous Results in Functional Neuroimaging Data Analysis Due to Covariate Correlation , 1999, NeuroImage.

[35]  N. Logothetis,et al.  Natural vision reveals regional specialization to local motion and to contrast-invariant, global flow in the human brain. , 2008, Cerebral cortex.

[36]  D. Heeger,et al.  Retinotopy and Functional Subdivision of Human Areas MT and MST , 2002, The Journal of Neuroscience.

[37]  Aapo Hyvärinen,et al.  Validating the independent components of neuroimaging time series via clustering and visualization , 2004, NeuroImage.

[38]  S. D. Jong SIMPLS: an alternative approach to partial least squares regression , 1993 .

[39]  Rex E. Jung,et al.  A Baseline for the Multivariate Comparison of Resting-State Networks , 2011, Front. Syst. Neurosci..

[40]  Toshio Aoyagi,et al.  Estimation of functional connectivity between bursting electrodes , 2008 .

[41]  Riitta Hari,et al.  Data-based functional template for sorting independent components of fMRI activity , 2011, Neuroscience Research.

[42]  Jeffrey M. Zacks,et al.  The Brain's Cutting-Room Floor: Segmentation of Narrative Cinema , 2010, Front. Hum. Neurosci..

[43]  S. Zeki,et al.  Functional brain mapping during free viewing of natural scenes , 2004, Human brain mapping.

[44]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[45]  Jouko Lampinen,et al.  Stimulus-Related Independent Component and Voxel-Wise Analysis of Human Brain Activity during Free Viewing of a Feature Film , 2012, PloS one.

[46]  Bernard Ng,et al.  Generalized Sparse Regularization with Application to fMRI Brain Decoding , 2011, IPMI.

[47]  S. Wold,et al.  PLS-regression: a basic tool of chemometrics , 2001 .

[48]  F. Gómez,et al.  Alterations of multiple resting state network connectivity in physiological, pharmacological, and pathological consciousness states , 2012 .

[49]  Jody C. Culham,et al.  The neural correlates of change detection in the face perception network , 2008, Neuropsychologia.

[50]  Andrea Bergmann,et al.  Statistical Parametric Mapping The Analysis Of Functional Brain Images , 2016 .

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

[52]  S Makeig,et al.  Analysis of fMRI data by blind separation into independent spatial components , 1998, Human brain mapping.

[53]  J. Hair Multivariate data analysis , 1972 .

[54]  Riitta Hari,et al.  Towards natural stimulation in fMRI—Issues of data analysis , 2007, NeuroImage.

[55]  Sylvain Arlot,et al.  A survey of cross-validation procedures for model selection , 2009, 0907.4728.

[56]  Peter J. Ramadge,et al.  The Pairwise Elastic Net support vector machine for automatic fMRI feature selection , 2013, 2013 IEEE International Conference on Acoustics, Speech and Signal Processing.

[57]  N. Kanwisher,et al.  The fusiform face area: a cortical region specialized for the perception of faces , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

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

[60]  M. Sams,et al.  Inter-Subject Synchronization of Prefrontal Cortex Hemodynamic Activity During Natural Viewing , 2008, The open neuroimaging journal.

[61]  G. Rizzolatti,et al.  Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. , 2014, Physiological reviews.

[62]  Richard G. F. Visser,et al.  Comparison of Regularized Regression Methods for ~Omics Data , 2012 .

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

[64]  Mikko Sams,et al.  Large-scale brain networks emerge from dynamic processing of musical timbre, key and rhythm , 2012, NeuroImage.

[65]  Peter Bühlmann Regression shrinkage and selection via the Lasso: a retrospective (Robert Tibshirani): Comments on the presentation , 2011 .

[66]  Pingmei Xu,et al.  Detecting stimulus driven changes in functional brain connectivity , 2013, 2013 IEEE International Conference on Acoustics, Speech and Signal Processing.

[67]  D. Heeger,et al.  Neurocinematics: The Neuroscience of Film , 2008 .

[68]  Andreas Bartels,et al.  The chronoarchitecture of the human brain—natural viewing conditions reveal a time-based anatomy of the brain , 2004, NeuroImage.

[69]  Dezhong Yao,et al.  Analysis of fMRI Data by Blind Separation of Data in a Tiny Spatial Domain into Independent Temporal Component , 2004, Brain Topography.

[70]  Jianfeng Feng,et al.  Voxel Selection in fMRI Data Analysis Based on Sparse Representation , 2009, IEEE Transactions on Biomedical Engineering.

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

[72]  Alexander G. Huth,et al.  Attention During Natural Vision Warps Semantic Representation Across the Human Brain , 2013, Nature Neuroscience.

[73]  P. Downing,et al.  Within‐subject reproducibility of category‐specific visual activation with functional MRI , 2005, Human brain mapping.

[74]  Damaris Zurell,et al.  Collinearity: a review of methods to deal with it and a simulation study evaluating their performance , 2013 .

[75]  G. Orban,et al.  Human Functional Magnetic Resonance Imaging Reveals Separation and Integration of Shape and Motion Cues in Biological Motion Processing , 2009, The Journal of Neuroscience.

[76]  Petia Koprinkova-Hristova,et al.  Artificial Neural Networks and Machine Learning , 2016 .

[77]  Pia Tikka,et al.  Functional Subdivision of Group-ICA Results of fMRI Data Collected during Cinema Viewing , 2012, PloS one.

[78]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[79]  Ryan J. Prenger,et al.  Bayesian Reconstruction of Natural Images from Human Brain Activity , 2009, Neuron.