Non-parametric temporal modeling of the hemodynamic response function via a liquid state machine

Standard methods for the analysis of functional MRI data strongly rely on prior implicit and explicit hypotheses made to simplify the analysis. In this work the attention is focused on two such commonly accepted hypotheses: (i) the hemodynamic response function (HRF) to be searched in the BOLD signal can be described by a specific parametric model e.g., double-gamma; (ii) the effect of stimuli on the signal is taken to be linearly additive. While these assumptions have been empirically proven to generate high sensitivity for statistical methods, they also limit the identification of relevant voxels to what is already postulated in the signal, thus not allowing the discovery of unknown correlates in the data due to the presence of unexpected hemodynamics. This paper tries to overcome these limitations by proposing a method wherein the HRF is learned directly from data rather than induced from its basic form assumed in advance. This approach produces a set of voxel-wise models of HRF and, as a result, relevant voxels are filterable according to the accuracy of their prediction in a machine learning framework. This approach is instantiated using a temporal architecture based on the paradigm of Reservoir Computing wherein a Liquid State Machine is combined with a decoding Feed-Forward Neural Network. This splits the modeling into two parts: first a representation of the complex temporal reactivity of the hemodynamic response is determined by a universal global "reservoir" which is essentially temporal; second an interpretation of the encoded representation is determined by a standard feed-forward neural network, which is trained by the data. Thus the reservoir models the temporal state of information during and following temporal stimuli in a feed-back system, while the neural network "translates" this data to fit the specific HRF response as given, e.g. by BOLD signal measurements in fMRI. An empirical analysis on synthetic datasets shows that the learning process can be robust both to noise and to the varying shape of the underlying HRF. A similar investigation on real fMRI datasets provides evidence that BOLD predictability allows for discrimination between relevant and irrelevant voxels for a given set of stimuli.

[1]  Hananel Hazan,et al.  Decoding the Formation of New Semantics: MVPA Investigation of Rapid Neocortical Plasticity during Associative Encoding through Fast Mapping , 2015, Neural plasticity.

[2]  Martin M. Monti,et al.  Human Neuroscience , 2022 .

[3]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

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

[5]  Karl J. Friston,et al.  Convolution Models for fMRI , 2007 .

[6]  Liam McDaid,et al.  SWAT: A Spiking Neural Network Training Algorithm for Classification Problems , 2010, IEEE Transactions on Neural Networks.

[7]  R. Cox,et al.  Event‐related fMRI contrast when using constant interstimulus interval: Theory and experiment , 2000, Magnetic resonance in medicine.

[8]  Martin A. Lindquist,et al.  Detection of time-varying signals in event-related fMRI designs , 2008, NeuroImage.

[9]  Martin A. Riedmiller,et al.  A direct adaptive method for faster backpropagation learning: the RPROP algorithm , 1993, IEEE International Conference on Neural Networks.

[10]  David R. Hardoon,et al.  Classifying cognitive states of brain activity via one-class neural networks with feature selection by genetic algorithms , 2011, Int. J. Mach. Learn. Cybern..

[11]  Robert A. Legenstein,et al.  What Can a Neuron Learn with Spike-Timing-Dependent Plasticity? , 2005, Neural Computation.

[12]  Karl J. Friston,et al.  Nonlinear event‐related responses in fMRI , 1998, Magnetic resonance in medicine.

[13]  Hananel Hazan,et al.  Learning BOLD Response in fMRI by Reservoir Computing , 2011, 2011 International Workshop on Pattern Recognition in NeuroImaging.

[14]  O Josephs,et al.  Event-related functional magnetic resonance imaging: modelling, inference and optimization. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[15]  H. Berg,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S7 Tables S1 to S3 References Movies S1 to S6 Tuned Responses of Astrocytes and Their Influence on Hemodynamic Signals in the Visual Cortex , 2022 .

[16]  Janaina Mourão Miranda,et al.  Classifying brain states and determining the discriminating activation patterns: Support Vector Machine on functional MRI data , 2005, NeuroImage.

[17]  Benjamin Schrauwen,et al.  An experimental unification of reservoir computing methods , 2007, Neural Networks.

[18]  Lars Kai Hansen,et al.  Modeling the hemodynamic response in fMRI using smooth FIR filters , 2000, IEEE Transactions on Medical Imaging.

[19]  Karl J. Friston,et al.  Event-related fMRI , 1997 .

[20]  Albert,et al.  Topology of evolving networks: local events and universality , 2000, Physical review letters.

[21]  Henry Markram,et al.  Real-Time Computing Without Stable States: A New Framework for Neural Computation Based on Perturbations , 2002, Neural Computation.

[22]  Tom M. Mitchell,et al.  Learning to Decode Cognitive States from Brain Images , 2004, Machine Learning.

[23]  Hananel Hazan,et al.  Topological constraints and robustness in liquid state machines , 2012, Expert Syst. Appl..

[24]  Jos B. T. M. Roerdink,et al.  Data-driven haemodynamic response function extraction using Fourier-wavelet regularised deconvolution , 2008, BMC Medical Imaging.

[25]  Wolfgang Maass,et al.  Liquid State Machines: Motivation, Theory, and Applications , 2010 .

[26]  W. Maass,et al.  State-dependent computations: spatiotemporal processing in cortical networks , 2009, Nature Reviews Neuroscience.

[27]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[28]  Ze Wang,et al.  A hybrid SVM–GLM approach for fMRI data analysis , 2009, NeuroImage.

[29]  S E Petersen,et al.  Detection of cortical activation during averaged single trials of a cognitive task using functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Harald Haas,et al.  Harnessing Nonlinearity: Predicting Chaotic Systems and Saving Energy in Wireless Communication , 2004, Science.

[31]  Ying Zheng,et al.  A Model of the Hemodynamic Response and Oxygen Delivery to Brain , 2002, NeuroImage.

[32]  David D. Cox,et al.  Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex , 2003, NeuroImage.

[33]  Vladimir N. Vapnik,et al.  The Nature of Statistical Learning Theory , 2000, Statistics for Engineering and Information Science.

[34]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

[35]  Bernard Widrow,et al.  Improving the learning speed of 2-layer neural networks by choosing initial values of the adaptive weights , 1990, 1990 IJCNN International Joint Conference on Neural Networks.

[36]  Mark D'Esposito,et al.  The continuing challenge of understanding and modeling hemodynamic variation in fMRI , 2012, NeuroImage.

[37]  David R. Hardoon,et al.  fMRI Analysis via One-class Machine Learning Techniques , 2005, IJCAI.