A Bayesian spatial model for neuroimaging data based on biologically informed basis functions

Abstract The dominant approach to neuroimaging data analysis employs the voxel as the unit of computation. While convenient, voxels lack biological meaning and their size is arbitrarily determined by the resolution of the image. Here, we propose a multivariate spatial model in which neuroimaging data are characterised as a linearly weighted combination of multiscale basis functions which map onto underlying brain nuclei or networks or nuclei. In this model, the elementary building blocks are derived to reflect the functional anatomy of the brain during the resting state. This model is estimated using a Bayesian framework which accurately quantifies uncertainty and automatically finds the most accurate and parsimonious combination of basis functions describing the data. We demonstrate the utility of this framework by predicting quantitative SPECT images of striatal dopamine function and we compare a variety of basis sets including generic isotropic functions, anatomical representations of the striatum derived from structural MRI, and two different soft functional parcellations of the striatum derived from resting‐state fMRI (rfMRI). We found that a combination of ˜50 multiscale functional basis functions accurately represented the striatal dopamine activity, and that functional basis functions derived from an advanced parcellation technique known as Instantaneous Connectivity Parcellation (ICP) provided the most parsimonious models of dopamine function. Importantly, functional basis functions derived from resting fMRI were more accurate than both structural and generic basis sets in representing dopamine function in the striatum for a fixed model order. We demonstrate the translational validity of our framework by constructing classification models for discriminating parkinsonian disorders and their subtypes. Here, we show that ICP approach is the only basis set that performs well across all comparisons and performs better overall than the classical voxel‐based approach. This spatial model constitutes an elegant alternative to voxel‐based approaches in neuroimaging studies; not only are their atoms biologically informed, they are also adaptive to high resolutions, represent high dimensions efficiently, and capture long‐range spatial dependencies, which are important and challenging objectives for neuroimaging data. HighlightsA multivariate spatial model using brain parcellations as basis functions is proposed.Brain regions can be modeled as a superposition of multiscale basis functions.These basis functions are biologically meaningful and capture spatial dependencies.Our framework allows to develop accurate and parsimonious clinical models.The model is computationally efficient, enhances power and adapts to high resolutions.

[1]  Koenraad Van Leemput,et al.  A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: Application to adaptive segmentation of in vivo MRI , 2015, NeuroImage.

[2]  S. Chib,et al.  Bayesian analysis of binary and polychotomous response data , 1993 .

[3]  Rich Caruana,et al.  Multitask Learning , 1998, Encyclopedia of Machine Learning and Data Mining.

[4]  Mark W. Woolrich,et al.  Combined spatial and non-spatial prior for inference on MRI time-series , 2009, NeuroImage.

[5]  Jan K Buitelaar,et al.  Attention-Deficit/Hyperactivity Disorder symptoms coincide with altered striatal connectivity. , 2016, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[6]  Michael E. Tipping Bayesian Inference: An Introduction to Principles and Practice in Machine Learning , 2003, Advanced Lectures on Machine Learning.

[7]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[8]  A. Lees,et al.  Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson's syndrome and PSP-parkinsonism. , 2005, Brain : a journal of neurology.

[9]  Dorit Hammerling,et al.  Explorer A Multi-resolution Gaussian process model for the analysis of large spatial data sets , 2012 .

[10]  Hongtu Zhu,et al.  Spatially Varying Coefficient Model for Neuroimaging Data With Jump Discontinuities , 2013, Journal of the American Statistical Association.

[11]  B. Franke,et al.  From estimating activation locality to predicting disorder: A review of pattern recognition for neuroimaging-based psychiatric diagnostics , 2015, Neuroscience & Biobehavioral Reviews.

[12]  Edwin V. Bonilla,et al.  Multi-task Gaussian Process Prediction , 2007, NIPS.

[13]  D. Nychka,et al.  A Multiresolution Gaussian Process Model for the Analysis of Large Spatial Datasets , 2015 .

[14]  Brian Caffo,et al.  A Bayesian hierarchical framework for spatial modeling of fMRI data , 2008, NeuroImage.

[15]  Hans Knutsson,et al.  Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates , 2016, Proceedings of the National Academy of Sciences.

[16]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[17]  I. Rezek,et al.  Understanding Heterogeneity in Clinical Cohorts Using Normative Models: Beyond Case-Control Studies , 2016, Biological Psychiatry.

[18]  Martin Styner,et al.  SGPP: spatial Gaussian predictive process models for neuroimaging data , 2014, NeuroImage.

[19]  Benson Mwangi,et al.  A Review of Feature Reduction Techniques in Neuroimaging , 2013, Neuroinformatics.

[20]  Bertrand Thirion,et al.  Multiscale Mining of fMRI Data with Hierarchical Structured Sparsity , 2012, SIAM J. Imaging Sci..

[21]  Michael J. Brammer,et al.  Bayesian multi-task learning for decoding multi-subject neuroimaging data , 2014, NeuroImage.

[22]  D. Rubin,et al.  Inference from Iterative Simulation Using Multiple Sequences , 1992 .

[23]  Angelo Arleo,et al.  How Synaptic Release Probability Shapes Neuronal Transmission: Information-Theoretic Analysis in a Cerebellar Granule Cell , 2010, Neural Computation.

[24]  Kim F. Nimon,et al.  Tools to Support Interpreting Multiple Regression in the Face of Multicollinearity , 2012, Front. Psychology.

[25]  Daniel E. Huddleston,et al.  Multimodal Imaging Signatures of Parkinson's Disease , 2016, Front. Neurosci..

[26]  Gaël Varoquaux,et al.  Multi-subject Dictionary Learning to Segment an Atlas of Brain Spontaneous Activity , 2011, IPMI.

[27]  Timothy O. Laumann,et al.  Generation and Evaluation of a Cortical Area Parcellation from Resting-State Correlations. , 2016, Cerebral cortex.

[28]  R Cameron Craddock,et al.  A whole brain fMRI atlas generated via spatially constrained spectral clustering , 2012, Human brain mapping.

[29]  David R Williams,et al.  Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges , 2009, The Lancet Neurology.

[30]  Maria Petrou,et al.  Learning in Pattern Recognition , 1999, MLDM.

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

[32]  Jesper Andersson,et al.  A multi-modal parcellation of human cerebral cortex , 2016, Nature.

[33]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[34]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[35]  C. Rasmussen,et al.  Approximations for Binary Gaussian Process Classification , 2008 .

[36]  David Mackay,et al.  Probable networks and plausible predictions - a review of practical Bayesian methods for supervised neural networks , 1995 .

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

[38]  Stefan Haufe,et al.  On the interpretation of weight vectors of linear models in multivariate neuroimaging , 2014, NeuroImage.

[39]  F. Carrillo,et al.  Machine learning models for the differential diagnosis of vascular parkinsonism and Parkinson’s disease using [123I]FP-CIT SPECT , 2014, European Journal of Nuclear Medicine and Molecular Imaging.

[40]  Isabelle Guyon,et al.  An Introduction to Variable and Feature Selection , 2003, J. Mach. Learn. Res..

[41]  N. Cressie,et al.  Fixed rank kriging for very large spatial data sets , 2008 .

[42]  Bertrand Thirion,et al.  Multi-scale Mining of fMRI Data with Hierarchical Structured Sparsity , 2011, 2011 International Workshop on Pattern Recognition in NeuroImaging.

[43]  Thomas E. Nichols Multiple testing corrections, nonparametric methods, and random field theory , 2012, NeuroImage.

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

[45]  Thomas E. Nichols,et al.  Twelfth Annual Meeting of the Organization for Human Brain Mapping , 2006, NeuroImage.

[46]  Wolfgang Grodd,et al.  Human brain parcellation using time courses of instantaneous correlations , 2016 .

[47]  J Sempau,et al.  Study of the point spread function (PSF) for 123I SPECT imaging using Monte Carlo simulation. , 2004, Physics in medicine and biology.

[48]  Carl E. Rasmussen,et al.  Gaussian processes for machine learning , 2005, Adaptive computation and machine learning.

[49]  Pierre Bellec,et al.  Mining the Hierarchy of Resting-State Brain Networks: Selection of Representative Clusters in a Multiscale Structure , 2013, 2013 International Workshop on Pattern Recognition in Neuroimaging.

[50]  J. Andrew Royle Spatial Statistical Modeling in Biology , 2002 .

[51]  George Eastman House,et al.  Sparse Bayesian Learning and the Relevan e Ve tor Ma hine , 2001 .

[52]  Max C. Keuken,et al.  Quantifying inter-individual anatomical variability in the subcortex using 7T structural MRI , 2014, NeuroImage.

[53]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[54]  Radford M. Neal Pattern Recognition and Machine Learning , 2007, Technometrics.

[55]  Xenophon Papademetris,et al.  Groupwise whole-brain parcellation from resting-state fMRI data for network node identification , 2013, NeuroImage.

[56]  Klaus Tatsch,et al.  Nigrostriatal Dopamine Terminal Imaging with Dopamine Transporter SPECT: An Update , 2013, The Journal of Nuclear Medicine.

[57]  Stephen M. Smith,et al.  Temporally-independent functional modes of spontaneous brain activity , 2012, Proceedings of the National Academy of Sciences.