Robust and Gaussian spatial functional regression models for analysis of event-related potentials

ABSTRACT Event‐related potentials (ERPs) summarize electrophysiological brain response to specific stimuli. They can be considered as correlated functions of time with both spatial correlation across electrodes and nested correlations within subjects. Commonly used analytical methods for ERPs often focus on pre‐determined extracted components and/or ignore the correlation among electrodes or subjects, which can miss important insights, and tend to be sensitive to outlying subjects, time points or electrodes. Motivated by ERP data in a smoking cessation study, we introduce a Bayesian spatial functional regression framework that models the entire ERPs as spatially correlated functional responses and the stimulus types as covariates. This novel framework relies on mixed models to characterize the effects of stimuli while simultaneously accounting for the multilevel correlation structure. The spatial correlation among the ERP profiles is captured through basis‐space Matérn assumptions that allow either separable or nonseparable spatial correlations over time. We induce both adaptive regularization over time and spatial smoothness across electrodes via a correlated normal‐exponential‐gamma (CNEG) prior on the fixed effect coefficient functions. Our proposed framework includes both Gaussian models as well as robust models using heavier‐tailed distributions to make the regression automatically robust to outliers. We introduce predictive methods to select among Gaussian vs. robust models and models with separable vs. non‐separable spatiotemporal correlation structures. Our proposed analysis produces global tests for stimuli effects across entire time (or time‐frequency) and electrode domains, plus multiplicity‐adjusted pointwise inference based on experiment‐wise error rate or false discovery rate to flag spatiotemporal (or spatio‐temporal‐frequency) regions that characterize stimuli differences, and can also produce inference for any prespecified waveform components. Our analysis of the smoking cessation ERP data set reveals numerous effects across different types of visual stimuli. HIGHLIGHTSEstimates spatiotemporal effects of various stimuli on Event‐related potentials.Models separable or nonseparable inter‐electrode spatial correlation over time.Accounts for multilevel data structures through Bayesian functional mixed models.Achieves adaptive regularization over time and spatial smoothness over electrodes.Enables robust modeling, model selection, global test and pointwise inference.

[1]  Hernando Ombao,et al.  The SLEX Model of a Non-Stationary Random Process , 2002 .

[2]  Claudio Carvalhaes,et al.  The surface Laplacian technique in EEG: Theory and methods. , 2014, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[3]  Jeffrey S. Morris Functional Regression , 2014, 1406.4068.

[4]  Raymond J Carroll,et al.  A Study of Mexican Free-Tailed Bat Chirp Syllables: Bayesian Functional Mixed Models for Nonstationary Acoustic Time Series , 2013, Journal of the American Statistical Association.

[5]  H. Müller,et al.  Modeling Repeated Functional Observations , 2012 .

[6]  D. Lehmann,et al.  Event-related potentials of the brain and cognitive processes: Approaches and applications , 1986, Neuropsychologia.

[7]  Ana-Maria Staicu,et al.  Functional Additive Mixed Models , 2012, Journal of computational and graphical statistics : a joint publication of American Statistical Association, Institute of Mathematical Statistics, Interface Foundation of North America.

[8]  Jürgen Kayser,et al.  On the benefits of using surface Laplacian (current source density) methodology in electrophysiology. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[9]  Arnab Maity,et al.  Reduced Rank Mixed Effects Models for Spatially Correlated Hierarchical Functional Data , 2010, Journal of the American Statistical Association.

[10]  Ana-Maria Staicu,et al.  Bootstrap‐based inference on the difference in the means of two correlated functional processes , 2012, Statistics in medicine.

[11]  Fabian Scheipl,et al.  Generalized Functional Additive Mixed Models , 2015, 1506.05384.

[12]  John Hughes,et al.  Fast, fully Bayesian spatiotemporal inference for fMRI data. , 2016, Biostatistics.

[13]  M Cagy,et al.  Statistical analysis of event-related potential elicited by verb-complement merge in Brazilian Portuguese. , 2006, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[14]  Jeffrey S. Morris,et al.  AUTOMATED ANALYSIS OF QUANTITATIVE IMAGE DATA USING ISOMORPHIC FUNCTIONAL MIXED MODELS, WITH APPLICATION TO PROTEOMICS DATA. , 2011, The annals of applied statistics.

[15]  D. J. Davidson,et al.  Functional Mixed-Effect Models for Electrophysiological Responses , 2009, Neurophysiology.

[16]  Ana-Maria Staicu,et al.  Longitudinal functional data analysis , 2015, Stat.

[17]  Kristin L. Sainani The Importance of Accounting for Correlated Observations , 2010, PM & R : the journal of injury, function, and rehabilitation.

[18]  Michael I. Jordan,et al.  Variational inference for Dirichlet process mixtures , 2006 .

[19]  Wensheng Guo Functional Mixed Effects Models , 2002 .

[20]  Charlotte DiStefano,et al.  A multi‐dimensional functional principal components analysis of EEG data , 2017, Biometrics.

[21]  Wensheng Guo,et al.  Functional mixed effects models , 2012, Biometrics.

[22]  E. Vaquero,et al.  Cluster analysis of behavioural and event-related potentials during a contingent negative variation paradigm in remitting-relapsing and benign forms of multiple sclerosis , 2011, BMC neurology.

[23]  H. Müller,et al.  Modelling function‐valued stochastic processes, with applications to fertility dynamics , 2017 .

[24]  Francesco Versace,et al.  Brain reactivity to emotional, neutral and cigarette‐related stimuli in smokers , 2011, Addiction biology.

[25]  Brian Caffo,et al.  Longitudinal functional principal component analysis. , 2010, Electronic journal of statistics.

[26]  Guillaume A. Rousselet,et al.  LIMO EEG: A Toolbox for Hierarchical LInear MOdeling of ElectroEncephaloGraphic Data , 2011, Comput. Intell. Neurosci..

[27]  R C Burgess,et al.  Event related potentials I , 1992, Clinical Neurophysiology.

[28]  B. Jørgensen Statistical Properties of the Generalized Inverse Gaussian Distribution , 1981 .

[29]  Can event-related potentials be evoked by extra-cochlear stimulation and used for selection purposes in cochlear implantation? , 1998, Clinical otolaryngology and allied sciences.

[30]  Dietrich Lehmann,et al.  EEG microstates , 2009, Scholarpedia.

[31]  Jeffrey S. Morris,et al.  Bayesian Analysis of Mass Spectrometry Proteomic Data Using Wavelet‐Based Functional Mixed Models , 2008, Biometrics.

[32]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[33]  Jeffrey S. Morris,et al.  Functional CAR Models for Large Spatially Correlated Functional Datasets , 2016, Journal of the American Statistical Association.

[34]  Karl J. Friston,et al.  Statistical parametric mapping for event-related potentials (II): a hierarchical temporal model , 2004, NeuroImage.

[35]  Christopher K Wikle,et al.  Modeling Complex Phenotypes: Generalized Linear Models Using Spectrogram Predictors of Animal Communication Signals , 2010, Biometrics.

[36]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[37]  Terrence J. Sejnowski,et al.  Neural Network Analysis of Event Related Potentials and Electroencephalogram Predicts Vigilance , 1991, NIPS.

[38]  Jeffrey S. Morris,et al.  Journal of the American Statistical Association Using Wavelet-based Functional Mixed Models to Characterize Population Heterogeneity in Accelerometer Profiles Using Wavelet-based Functional Mixed Models to Characterize Population Heterogeneity in Accelerometer Profiles: a Case Study , 2022 .

[39]  Margot J. Taylor,et al.  Spatiotemporal analysis of event-related potentials to upright, inverted, and contrast-reversed faces: effects on encoding and recognition. , 2004, Psychophysiology.

[40]  Dietrich Lehmann,et al.  The functional significance of EEG microstates—Associations with modalities of thinking , 2016, NeuroImage.

[41]  Rae. Z.H. Aliyev,et al.  Interpolation of Spatial Data , 2018, Biomedical Journal of Scientific & Technical Research.

[42]  Jim E. Griffin,et al.  Structuring shrinkage: some correlated priors for regression , 2012 .

[43]  Hongxiao Zhu,et al.  Robust, Adaptive Functional Regression in Functional Mixed Model Framework , 2011, Journal of the American Statistical Association.

[44]  G. Yue,et al.  Assessing time-dependent association between scalp EEG and muscle activation: A functional random-effects model approach , 2009, Journal of Neuroscience Methods.

[45]  S. Luck,et al.  Best Practices for Event-Related Potential Research in Clinical Populations. , 2016, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[46]  Ana-Maria Staicu,et al.  Fast methods for spatially correlated multilevel functional data. , 2010, Biostatistics.

[47]  Jeffrey S. Morris,et al.  Wavelet‐based functional mixed models , 2006, Journal of the Royal Statistical Society. Series B, Statistical methodology.

[48]  B. Mallick,et al.  Bayesian Hierarchical Spatially Correlated Functional Data Analysis with Application to Colon Carcinogenesis , 2008, Biometrics.

[49]  Torsten Hothorn,et al.  The functional linear array model , 2015 .

[50]  Jeffrey M. Engelmann,et al.  Effects of varenicline and bupropion sustained-release use plus intensive smoking cessation counseling on prolonged abstinence from smoking and on depression, negative affect, and other symptoms of nicotine withdrawal. , 2013, JAMA psychiatry.

[51]  Ci-Ren Jiang,et al.  Multi-dimensional functional principal component analysis , 2015, Stat. Comput..

[52]  H. Hermens,et al.  More potential in statistical analyses of event‐related potentials: a mixed regression approach , 2011, International journal of methods in psychiatric research.

[53]  C. Gonsalvez,et al.  Can event-related potentials serve as neural markers for wins, losses, and near-wins in a gambling task? A principal components analysis. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[54]  Xingyu Wang,et al.  Aggregation of Sparse Linear Discriminant analyses for Event-Related potential Classification in Brain-Computer Interface , 2014, Int. J. Neural Syst..

[55]  T. Louis,et al.  General methods for analysing repeated measures. , 1988, Statistics in medicine.

[56]  Jeffrey S. Morris,et al.  Wavelet-Based Functional Mixed Models to characterize Population Heterogeneity in Accelerometer Profiles: A Case Study. , 2006 .

[57]  B. Hjorth An on-line transformation of EEG scalp potentials into orthogonal source derivations. , 1975, Electroencephalography and clinical neurophysiology.

[58]  B. Silverman,et al.  Functional Data Analysis , 1997 .

[59]  Dominique Lamy,et al.  Neural Correlates of Subjective Awareness and Unconscious Processing: An ERP Study , 2009, Journal of Cognitive Neuroscience.

[60]  Karl J. Friston,et al.  Statistical parametric mapping for event-related potentials: I. Generic considerations , 2004, NeuroImage.

[61]  Sean L. Simpson,et al.  Kronecker Product Linear Exponent AR(1) Correlation Structures for Multivariate Repeated Measures , 2010, PloS one.

[62]  Jeffrey S. Morris,et al.  Bayesian function‐on‐function regression for multilevel functional data , 2015, Biometrics.

[63]  M. Bradley,et al.  Large-scale neural correlates of affective picture processing. , 2002, Psychophysiology.

[64]  M. Wand,et al.  Semiparametric Regression: Parametric Regression , 2003 .