Modeling habituation in rat EEG-evoked responses via a neural mass model with feedback

Habituation is a generic property of the neural response to repeated stimuli. Its strength often increases as inter-stimuli relaxation periods decrease. We propose a simple, broadly applicable control structure that enables a neural mass model of the evoked EEG response to exhibit habituated behavior. A key motivation for this investigation is the ongoing effort to develop model-based reconstruction of multi-modal functional neuroimaging data. The control structure proposed here is illustrated and validated in the context of a biophysical neural mass model, developed by Riera et al. (Hum Brain Mapp 27(11):896–914, 2006; 28(4):335–354, 2007), and of simplifications thereof, using data from rat EEG response to medial nerve stimuli presented at frequencies from 1 to 8 Hz. Performance was tested by predictions of both the response to the next stimulus based on the current one, and also of continued stimuli trains over 4-s time intervals based on the first stimulus in the interval, with similar success statistics. These tests demonstrate the ability of simple generative models to capture key features of the evoked response, including habituation.

[1]  Karl J. Friston,et al.  Dynamic causal modelling of evoked responses in EEG/MEG with lead field parameterization , 2006, NeuroImage.

[2]  J. T. Stuart.  Nonlinear Stability Theory , 1971, Handbook of Marine Craft Hydrodynamics and Motion Control.

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

[4]  Ben H. Jansen,et al.  Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns , 1995, Biological Cybernetics.

[5]  Jean-Baptiste Poline,et al.  Fusion of simultaneous fMRI/EEG data based on the electro-metabolic coupling , 2004, 2004 2nd IEEE International Symposium on Biomedical Imaging: Nano to Macro (IEEE Cat No. 04EX821).

[6]  Hinrich Schütze,et al.  Introduction to information retrieval , 2008 .

[7]  Karl J. Friston,et al.  Dynamic causal modeling , 2010, Scholarpedia.

[8]  Donald A. Wilson,et al.  Habituation revisited: An updated and revised description of the behavioral characteristics of habituation , 2009, Neurobiology of Learning and Memory.

[9]  Jérémie Mattout,et al.  Symmetrical event-related EEG/fMRI information fusion in a variational Bayesian framework , 2007, NeuroImage.

[10]  Nikolai F. Rulkov,et al.  Subthreshold oscillations in a map-based neuron model , 2004, q-bio/0406007.

[11]  Mathew P. Dafilis,et al.  A spatially continuous mean field theory of electrocortical activity , 2002, Network.

[12]  R R Hoy,et al.  Habituation of the ultrasound-induced acoustic startle response in flying crickets. , 1991, The Journal of experimental biology.

[13]  J. C. Jimenez,et al.  Nonlinear local electrovascular coupling. I: A theoretical model , 2006, Human brain mapping.

[14]  Lawrence C Katz,et al.  Noradrenergic Induction of Odor-Specific Neural Habituation and Olfactory Memories , 2008, The Journal of Neuroscience.

[15]  Philip Holmes,et al.  Minimal Models of Bursting Neurons: How Multiple Currents, Conductances, and Timescales Affect Bifurcation Diagrams , 2004, SIAM J. Appl. Dyn. Syst..

[16]  Petre Stoica,et al.  Introduction to spectral analysis , 1997 .

[17]  J. Bower,et al.  An active membrane model of the cerebellar Purkinje cell II. Simulation of synaptic responses. , 1994, Journal of neurophysiology.

[18]  James M. Bower,et al.  The Book of GENESIS , 1994, Springer New York.

[19]  O. Nelles.  Nonlinear System Identification: From Classical Approaches to Neural Networks and Fuzzy Models , 2000 .

[20]  J.C. Mosher,et al.  Recursive MUSIC: A framework for EEG and MEG source localization , 1998, IEEE Transactions on Biomedical Engineering.

[21]  Koji Inui,et al.  Temporal dynamics of neural adaptation effect in the human visual ventral stream , 2005 .

[22]  R. Zucker.  Crayfish escape behavior and central synapses. II. Physiological mechanisms underlying behavioral habituation. , 1972, Journal of neurophysiology.

[23]  Karl J. Friston,et al.  Mechanisms of evoked and induced responses in MEG/EEG , 2006, NeuroImage.

[24]  Chris J. Martin,et al.  Hemodynamic Response in the Unanesthetized Rat: Intrinsic Optical Imaging and Spectroscopy of the Barrel Cortex , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[25]  David Poeppel,et al.  How can EEG/MEG and fMRI/PET data be combined? , 2002, Human brain mapping.

[26]  R D Hall,et al.  Habituation of evoked potentials in the rat under conditions of behavioral control. , 1968, Electroencephalography and clinical neurophysiology.

[27]  Andrei Zinovyev,et al.  Principal Manifolds for Data Visualization and Dimension Reduction , 2007 .

[28]  T. Goldberg,et al.  Isolating the Mnemonic Component in Spatial Delayed Response: A Controlled PET15O-Labeled Water Regional Cerebral Blood Flow Study in Normal Humans , 1996, NeuroImage.

[29]  B. R. Noack,et al.  Galerkin Models Enhancements for Flow Control , 2011 .

[30]  Pierre-Antoine Absil,et al.  Principal Manifolds for Data Visualization and Dimension Reduction , 2007 .

[31]  David A. Boas,et al.  Coupling between somatosensory evoked potentials and hemodynamic response in the rat , 2008, NeuroImage.

[32]  R Kawashima,et al.  Nonlinear local electrovascular coupling. II: From data to neuronal masses , 2007, Human brain mapping.

[33]  M W Luttges,et al.  Neural habituation in garter snakes. , 1972, Physiology & behavior.

[34]  Pablo Laguna,et al.  Bioelectrical Signal Processing in Cardiac and Neurological Applications , 2005 .

[35]  D. Liley,et al.  Modeling electrocortical activity through improved local approximations of integral neural field equations. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[36]  Karl J. Friston,et al.  Repetition suppression and plasticity in the human brain , 2009, NeuroImage.

[37]  Oliver Nelles.  Dynamic Neural and Fuzzy Models , 2001 .

[38]  Adam S Bristol,et al.  Differential role of inhibition in habituation of two independent afferent pathways to a common motor output. , 2005, Learning & memory.

[39]  R. F. Thompson,et al.  Habituation: a model phenomenon for the study of neuronal substrates of behavior. , 1966, Psychological review.

[40]  J. Woods,et al.  Probability and Random Processes with Applications to Signal Processing , 2001 .

[41]  J. Bower,et al.  An active membrane model of the cerebellar Purkinje cell. I. Simulation of current clamps in slice. , 1994, Journal of neurophysiology.

[42]  James M. Bower,et al.  Neural Modeling with GENESIS , 1998 .

[43]  Karl J. Friston,et al.  A neural mass model for MEG/EEG: coupling and neuronal dynamics , 2003, NeuroImage.