Untangling the relatedness among correlations, part I: Nonparametric approaches to inter-subject correlation analysis at the group level

FMRI data acquisition under naturalistic and continuous stimuli (e.g., watching a video or listening to music) has become popular recently due to the fact that it entails less manipulation and more realistic/complex contexts involved in the task, compared to the conventional task-based experimental designs. The synchronization or response similarities among subjects are typically measured through inter-subject correlation (ISC) between any pair of subjects. At the group level, summarizing the collection of ISC values is complicated by their intercorrelations, which necessarily lead to the violation of independence assumed in typical parametric approaches such as Student's t-test. Nonparametric methods, such as bootstrapping and permutation testing, have previously been adopted for testing purposes by resampling the time series of each subject, but the quantitative validity of these specific approaches in terms of controllability of false positive rate (FPR) has never been explored before. Here we survey the methods of ISC group analysis that have been employed in the literature, and discuss the issues involved in those methods. We then propose less computationally intensive nonparametric methods that can be performed at the group level (for both one- and two-sample analyses), as compared to the popular method of circularly shifting the EPI time series at the individual level. As part of the new approaches, subject-wise (SW) resampling is adopted instead of element-wise (EW) resampling, so that exchangeability and independence assumptions are satisfied, and the patterned correlation structure among the ISC values can be more accurately captured. We examine the FPR controllability and power achievement of all the methods through simulations, as well as their performance when applied to a real experimental dataset.

[1]  N. C. Silver,et al.  Averaging Correlation Coefficients: Should Fishers z Transformation Be Used? , 1987 .

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

[3]  Mikko Sams,et al.  Inter-Subject Correlation of Brain Hemodynamic Responses During Watching a Movie: Localization in Space and Frequency , 2009, Front. Neuroinform..

[4]  John C. Gower,et al.  Analysis of distance for structured multivariate data and extensions to multivariate analysis of variance , 1999 .

[5]  Mark S. Cohen,et al.  Parametric Analysis of fMRI Data Using Linear Systems Methods , 1997, NeuroImage.

[6]  R. Buxton,et al.  Modeling the hemodynamic response to brain activation , 2004, NeuroImage.

[7]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[8]  Stephen M. Smith,et al.  Multi-level block permutation , 2015, NeuroImage.

[9]  Matthew A. Zapala,et al.  Multivariate regression analysis of distance matrices for testing associations between gene expression patterns and related variables , 2006, Proceedings of the National Academy of Sciences.

[10]  Eva Petkova,et al.  Web-Based Supplementary Materials for “ On Distance-Based Permutation Tests for Between-Group Comparisons ” , 2009 .

[11]  Frank E. Pollick,et al.  Differences in fMRI intersubject correlation while viewing unedited and edited videos of dance performance , 2015, Cortex.

[12]  Patrik Vuilleumier,et al.  Temporal dynamics of musical emotions examined through intersubject synchrony of brain activity. , 2015, Social cognitive and affective neuroscience.

[13]  Vince D. Calhoun,et al.  Impact of autocorrelation on functional connectivity , 2014, NeuroImage.

[14]  George A. F. Seber,et al.  A matrix handbook for statisticians , 2007 .

[15]  Katie L. McMahon,et al.  A multivariate distance-based analytic framework for connectome-wide association studies , 2014, NeuroImage.

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

[17]  Uri Hasson,et al.  Not Lost in Translation: Neural Responses Shared Across Languages , 2012, The Journal of Neuroscience.

[18]  M. Corbetta,et al.  Inter-species activity correlations reveal functional correspondences between monkey and human brain areas , 2012, Nature Methods.

[19]  Wendy Van Moer,et al.  Fractional-Order Time Series Models for Extracting the Haemodynamic Response From Functional Magnetic Resonance Imaging Data , 2012, IEEE Transactions on Biomedical Engineering.

[20]  P. Wojtkowski Temporal Dynamics , 2017, Encyclopedia of GIS.

[21]  Jussi Tohka,et al.  A versatile software package for inter-subject correlation based analyses of fMRI , 2014, Front. Neuroinform..

[22]  Vince D. Calhoun,et al.  Cortical Response Similarities Predict which Audiovisual Clips Individuals Viewed, but Are Unrelated to Clip Preference , 2015, PloS one.

[23]  Christopher J Honey,et al.  Neural Correlates of Risk Perception during Real-Life Risk Communication , 2013, The Journal of Neuroscience.

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

[25]  Thomas E. Nichols,et al.  Nonparametric Permutation Tests for Functional Neuroimaging , 2003 .

[26]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[27]  Jussi Tohka,et al.  Post-print: Effects of spatial smoothing on inter-subject correlation based analysis of FMRI , 2014 .

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

[29]  Anja Thiede Magnetoencephalographic (MEG) Inter-subject Correlation using Continuous Music Stimuli , 2015 .

[30]  Marti J. Anderson,et al.  A new method for non-parametric multivariate analysis of variance in ecology , 2001 .

[31]  L. Davachi,et al.  Enhanced Intersubject Correlations during Movie Viewing Correlate with Successful Episodic Encoding , 2008, Neuron.

[32]  R. Hari,et al.  Emotions promote social interaction by synchronizing brain activity across individuals , 2012, Proceedings of the National Academy of Sciences.

[33]  Tapani Ristaniemi,et al.  From Vivaldi to Beatles and back: Predicting lateralized brain responses to music , 2013, NeuroImage.

[34]  Stephen M. Smith,et al.  Permutation inference for the general linear model , 2014, NeuroImage.

[35]  Uri Hasson,et al.  Engaged listeners: shared neural processing of powerful political speeches. , 2015, Social cognitive and affective neuroscience.

[36]  B. Thirion,et al.  Combined permutation test and mixed‐effect model for group average analysis in fMRI , 2006, Human brain mapping.

[37]  Gang Chen,et al.  Detecting the subtle shape differences in hemodynamic responses at the group level , 2015, Front. Neurosci..

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

[39]  Andreas Bartels,et al.  The chronoarchitecture of the human brain , 2004 .

[40]  Rafael Malach,et al.  Extrinsic and intrinsic systems in the posterior cortex of the human brain revealed during natural sensory stimulation. , 2007, Cerebral cortex.

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

[42]  F. Pollick,et al.  Uni- and multisensory brain areas are synchronised across spectators when watching unedited dance recordings , 2013, i-Perception.

[43]  Thomas E. Nichols,et al.  Can parametric statistical methods be trusted for fMRI based group studies? , 2015, 1511.01863.

[44]  Robert T. Knight,et al.  Spatial and temporal relationships of electrocorticographic alpha and gamma activity during auditory processing , 2014, NeuroImage.

[45]  Jessica F. Cantlon,et al.  Neural Activity during Natural Viewing of Sesame Street Statistically Predicts Test Scores in Early Childhood , 2013, PLoS biology.

[46]  Jukka-Pekka Kauppi,et al.  A versatile software package for inter-subject correlation based analyses of fMRI , 2014 .

[47]  Istvan Molnar-Szakacs,et al.  Beyond superior temporal cortex: intersubject correlations in narrative speech comprehension. , 2008, Cerebral cortex.

[48]  Rafael Malach,et al.  Vision Intersubject Synchronization of Cortical Activity During Natural , 2011 .

[49]  Parag Chordia,et al.  Inter‐subject synchronization of brain responses during natural music listening , 2013, The European journal of neuroscience.

[50]  Hang Joon Jo,et al.  Mapping sources of correlation in resting state FMRI, with artifact detection and removal , 2010, NeuroImage.