Spatial–temporal modelling of fMRI data through spatially regularized mixture of hidden process models

Previous work investigated a range of spatio-temporal constraints for fMRI data analysis to provide robust detection of neural activation. We present a mixture-based method for the spatio-temporal modelling of fMRI data. This approach assumes that fMRI time series are generated by a probabilistic superposition of a small set of spatio-temporal prototypes (mixture components). Each prototype comprises a temporal model that explains fMRI signals on a single voxel and the model's “region of influence” through a spatial prior over the voxel space. As the key ingredient of our temporal model, the Hidden Process Model (HPM) framework proposed in Hutchinson et al. (2009) is adopted to infer the overlapping cognitive processes triggered by stimuli. Unlike the original HPM framework, we use a parametric model of Haemodynamic Response Function (HRF) so that biological constraints are naturally incorporated in the HRF estimation. The spatial priors are defined in terms of a parameterised distribution. Thus, the total number of parameters in the model does not depend on the number of voxels. The resulting model provides a conceptually principled and computationally efficient approach to identify spatio-temporal patterns of neural activation from fMRI data, in contrast to most conventional approaches in the literature focusing on the detection of spatial patterns. We first verify the proposed model in a controlled experimental setting using synthetic data. The model is further validated on real fMRI data obtained from a rapid event-related visual recognition experiment (Mayhew et al., 2012). Our model enables us to evaluate in a principled manner the variability of neural activations within individual regions of interest (ROIs). The results strongly suggest that, compared with occipitotemporal regions, the frontal ones are less homogeneous, requiring two HPM prototypes per region. Despite the rapid event-related experimental design, the model is capable of disentangling the perceptual judgement and motor response processes that are both activated in the frontal ROIs. Spatio-temporal heterogeneity in the frontal regions seems to be associated with diverse dynamic localizations of the two hidden processes in different subregions of frontal ROIs.

[1]  Karl J. Friston Models of brain function in neuroimaging. , 2005, Annual review of psychology.

[2]  Nava Rubin,et al.  Cluster-based analysis of FMRI data , 2006, NeuroImage.

[3]  P. Green,et al.  Corrigendum: On Bayesian analysis of mixtures with an unknown number of components , 1997 .

[4]  Jean-Baptiste Poline,et al.  Are fMRI event-related response constant in time? A model selection answer , 2006, NeuroImage.

[5]  Charles H. Bennett,et al.  Efficient estimation of free energy differences from Monte Carlo data , 1976 .

[6]  Duane,et al.  Hybrid stochastic differential equations applied to quantum chromodynamics. , 1985, Physical review letters.

[7]  Jun S. Liu,et al.  The Wang-Landau algorithm in general state spaces: Applications and convergence analysis , 2010 .

[8]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[9]  Bernd Fritzke Growing Grid — a self-organizing network with constant neighborhood range and adaptation strength , 1995, Neural Processing Letters.

[10]  Gary F. Egan,et al.  Complex spatio-temporal dynamics of fMRI BOLD: A study of motor learning , 2007, NeuroImage.

[11]  William D. Penny,et al.  Bayesian fMRI data analysis with sparse spatial basis function priors , 2007, NeuroImage.

[12]  Chunming Zhang,et al.  Computational Statistics and Data Analysis Efficient Modeling and Inference for Event-related Fmri Data , 2022 .

[13]  Michalis Vazirgiannis,et al.  c ○ 2001 Kluwer Academic Publishers. Manufactured in The Netherlands. On Clustering Validation Techniques , 2022 .

[14]  Paul J. Laurienti,et al.  The impact of temporal regularization on estimates of the BOLD hemodynamic response function: A comparative analysis , 2008, NeuroImage.

[15]  Iven Van Mechelen,et al.  A Bayesian approach to the selection and testing of mixture models , 2003 .

[16]  David M. Blei,et al.  A topographic latent source model for fMRI data , 2011, NeuroImage.

[17]  C Gössl,et al.  Bayesian Spatiotemporal Inference in Functional Magnetic Resonance Imaging , 2001, Biometrics.

[18]  Gordana Derado,et al.  Modeling the Spatial and Temporal Dependence in fMRI Data , 2010, Biometrics.

[19]  Nick F. Ramsey,et al.  Within-subject variation in BOLD-fMRI signal changes across repeated measurements: Quantification and implications for sample size , 2008, NeuroImage.

[20]  Indrayana Rustandi,et al.  Modeling fMRI data generated by overlapping cognitive processes with unknown onsets using Hidden Process Models , 2009, NeuroImage.

[21]  Jens Ledet Jensen,et al.  Spatial mixture modelling of fMRI data , 2000 .

[22]  Kathleen A. Hansen,et al.  Modeling low‐frequency fluctuation and hemodynamic response timecourse in event‐related fMRI , 2008, Human brain mapping.

[23]  C. Kilts,et al.  Predicting the brain response to treatment using a Bayesian hierarchical model with application to a study of schizophrenia , 2008, Human brain mapping.

[24]  Hans Knutsson,et al.  Adaptive analysis of fMRI data , 2003, NeuroImage.

[25]  Thomas Vincent,et al.  A joint detection-estimation framework for analysing within-subject fMRI data , 2010 .

[26]  Charles E. Clark,et al.  Monte Carlo , 2006 .

[27]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[28]  M. Lindquist The Statistical Analysis of fMRI Data. , 2008, 0906.3662.

[29]  Karl J. Friston,et al.  Mixtures of general linear models for functional neuroimaging , 2003, IEEE Transactions on Medical Imaging.

[30]  Karl J. Friston,et al.  Bayesian fMRI time series analysis with spatial priors , 2005, NeuroImage.

[31]  J. -B. Poline,et al.  Estimating the Delay of the fMRI Response , 2002, NeuroImage.

[32]  William D. Penny,et al.  CHAPTER 25 – Spatio-temporal models for fMRI , 2007 .

[33]  Stephen D. Mayhew,et al.  Learning Acts on Distinct Processes for Visual Form Perception in the Human Brain , 2012, The Journal of Neuroscience.

[34]  Karl J. Friston,et al.  Analysis of functional MRI time‐series , 1994, Human Brain Mapping.

[35]  Topi Tanskanen,et al.  From local to global: Cortical dynamics of contour integration. , 2008, Journal of vision.

[36]  Mark W. Woolrich,et al.  Constrained linear basis sets for HRF modelling using Variational Bayes , 2004, NeuroImage.

[37]  Ming Jiang,et al.  Blind deblurring of spiral CT images , 2003, Conference Record of Thirty-Fifth Asilomar Conference on Signals, Systems and Computers (Cat.No.01CH37256).

[38]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Nicholas Ayache,et al.  A multisubject anatomo-functional parcellation of the brain , 2003 .

[40]  Geoffrey E. Hinton,et al.  SMEM Algorithm for Mixture Models , 1998, Neural Computation.

[41]  M. D’Esposito,et al.  The variability of human BOLD hemodynamic responses , 1998, NeuroImage.

[42]  P. N. Suganthan,et al.  Robust growing neural gas algorithm with application in cluster analysis , 2004, Neural Networks.

[43]  P. Green,et al.  On Bayesian Analysis of Mixtures with an Unknown Number of Components (with discussion) , 1997 .

[44]  Hal S. Stern,et al.  A Bayesian Mixture Approach to Modeling Spatial Activation Patterns in Multisite fMRI Data , 2010, IEEE Transactions on Medical Imaging.

[45]  Markus Svensén,et al.  Probabilistic modeling of single-trial fMRI data , 2000, IEEE Transactions on Medical Imaging.

[46]  Mark W. Woolrich,et al.  Fully Bayesian spatio-temporal modeling of FMRI data , 2004, IEEE Transactions on Medical Imaging.

[47]  Xuemei Huang,et al.  Nonparametric Estimation of Hemodynamic Response Function: A Frequency Domain Approach , 2016 .

[48]  Laurent Risser,et al.  Spatially adaptive mixture modeling for analysis of fMRI time series , 2009, NeuroImage.

[49]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[50]  K. Fujii,et al.  Visualization for the analysis of fluid motion , 2005, J. Vis..

[51]  H. Benali,et al.  Robust Bayesian estimation of the hemodynamic response function in event‐related BOLD fMRI using basic physiological information , 2003, Human brain mapping.

[52]  Christoph S. Herrmann,et al.  Circles are different: The perception of Glass patterns modulates early event-related potentials , 2005, Vision Research.

[53]  Thomas Martinetz,et al.  'Neural-gas' network for vector quantization and its application to time-series prediction , 1993, IEEE Trans. Neural Networks.

[54]  S. Duane,et al.  Hybrid Monte Carlo , 1987 .

[55]  Miguel P. Eckstein,et al.  Predicting variations of perceptual performance across individuals from neural activity using pattern classifiers , 2010, NeuroImage.

[56]  Bruno A Olshausen,et al.  Timecourse of neural signatures of object recognition. , 2003, Journal of vision.