Differential transient MEG and fMRI responses to visual stimulation onset rate

While recent analysis of functional magnetic resonance imaging (fMRI) data utilize a generalized nonlinear convolution model (e.g., dynamic causal modeling), most conventional analyses of local responses utilize a linear convolution model (e.g., the general linear model). These models assume a linear relationship between the blood oxygenated level dependent (BOLD) signal and the underlying neuronal response. While previous studies have shown that this “neurovascular coupling” process is approximately linear, short stimulus durations are known to produce a larger fMRI response than expected from a linear system. This divergence from linearity between the stimulus time‐course and BOLD signal could be caused by neuronal onset and offset transients, rather than a nonlinearity in the hemodynamics related to BOLD contrast. We tested this hypothesis by measuring MEG and fMRI responses to stimuli with ramped contrast onsets and offsets in place of abrupt transitions. MEG results show that the ramp successfully reduced the transient onset of neural activity. However, the nonlinearity in the fMRI response, while also reduced, remained. Predictions of fMRI responses from MEG signals show a weaker nonlinearity than observed in the actual fMRI data. These results suggest that the fMRI BOLD nonlinearity seen with short duration stimuli is not solely due to transient neuronal activity. © 2008 Wiley Periodicals, Inc. Int J Imaging Syst Technol, 18, 17–28, 2008

[1]  Karl J. Friston,et al.  Nonlinear Responses in fMRI: The Balloon Model, Volterra Kernels, and Other Hemodynamics , 2000, NeuroImage.

[2]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[3]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[4]  M. Doughty Consideration of Three Types of Spontaneous Eyeblink Activity in Normal Humans: during Reading and Video Display Terminal Use, in Primary Gaze, and while in Conversation , 2001, Optometry and vision science : official publication of the American Academy of Optometry.

[5]  Karl J. Friston,et al.  The temporal dynamics of reading: a PET study , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  P. Bandettini,et al.  Spatial Heterogeneity of the Nonlinear Dynamics in the FMRI BOLD Response , 2001, NeuroImage.

[7]  J. Gore,et al.  Measurements of the Temporal fMRI Response of the Human Auditory Cortex to Trains of Tones , 1998, NeuroImage.

[8]  Dominique Hasboun,et al.  A multitrial analysis for revealing significant corticocortical networks in magnetoencephalography and electroencephalography , 2003, NeuroImage.

[9]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[10]  Arjan Hillebrand,et al.  The temporal frequency tuning of human visual cortex investigated using synthetic aperture magnetometry , 2004, NeuroImage.

[11]  Abraham Z. Snyder,et al.  Transient BOLD responses at block transitions , 2005, NeuroImage.

[12]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

[13]  A. B. Bonds Temporal dynamics of contrast gain in single cells of the cat striate cortex , 1991, Visual Neuroscience.

[14]  Antígona Martínez,et al.  Nonlinear temporal dynamics of the cerebral blood flow response , 2001, Human brain mapping.

[15]  Karl J. Friston Imaging neuroscience: principles or maps? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Karl J. Friston,et al.  Nonlinear Coupling between Evoked rCBF and BOLD Signals: A Simulation Study of Hemodynamic Responses , 2001, NeuroImage.

[17]  Bradley G Goodyear,et al.  Removal of phase artifacts from fMRI data using a Stockwell transform filter improves brain activity detection , 2004, Magnetic resonance in medicine.

[18]  D. Noll,et al.  Nonlinear Aspects of the BOLD Response in Functional MRI , 1998, NeuroImage.

[19]  G. Glover Deconvolution of Impulse Response in Event-Related BOLD fMRI1 , 1999, NeuroImage.

[20]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[21]  T. Maddess,et al.  Factors governing the adaptation of cells in area-17 of the cat visual cortex , 1988, Biological Cybernetics.

[22]  Abraham Z. Snyder,et al.  The BOLD onset transient: identification of novel functional differences in schizophrenia , 2005, NeuroImage.

[23]  R. Hari,et al.  Magnetoencephalography in the study of human somatosensory cortical processing. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[24]  D. Heeger,et al.  Neuronal basis of contrast discrimination , 1999, Vision Research.

[25]  Scott A. Huettel,et al.  Regional Differences in the Refractory Period of the Hemodynamic Response: An Event-Related fMRI Study , 2001, NeuroImage.

[26]  A W Toga,et al.  Refractory periods observed by intrinsic signal and fluorescent dye imaging. , 1998, Journal of neurophysiology.

[27]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[28]  P Pasik,et al.  Extrageniculostriate vision in the monkey. VII. Contrast sensitivity functions. , 1980, Journal of neurophysiology.

[29]  Josef Pfeuffer,et al.  Spatial dependence of the nonlinear BOLD response at short stimulus duration , 2002, NeuroImage.

[30]  Peter A. Bandettini,et al.  The effect of stimulus duty cycle and “off” duration on BOLD response linearity , 2005, NeuroImage.

[31]  C M Michel,et al.  Mapping of the neuronal networks of human cortical brain functions. , 2003, Advances and technical standards in neurosurgery.

[32]  Aysenil Belger,et al.  Hemodynamic correlates of stimulus repetition in the visual and auditory cortices: an fMRI study , 2004, NeuroImage.

[33]  R. S. Hinks,et al.  Time course EPI of human brain function during task activation , 1992, Magnetic resonance in medicine.

[34]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[35]  Clara A. Scholl,et al.  Synchronized delta oscillations correlate with the resting-state functional MRI signal , 2007, Proceedings of the National Academy of Sciences.

[36]  Mark S. Cohen,et al.  Parametric Analysis of fMRI Data Using Linear Systems Methods , 1997, NeuroImage.

[37]  Lalu Mansinha,et al.  Localization of the complex spectrum: the S transform , 1996, IEEE Trans. Signal Process..

[38]  W W Orrison,et al.  Anatomic localization of cerebral cortical function by magnetoencephalography combined with MR imaging and CT. , 1990, AJNR. American journal of neuroradiology.

[39]  Frorn tltc lepartnent,et al.  SPATIAL CONTRAST ADAPTATION CHARACTERISTICS OF NEURONES RECORDED IN THE CAT ' S VISUAL CORTEX , 2002 .

[40]  E. Seidemann,et al.  Color Signals in Area MT of the Macaque Monkey , 1999, Neuron.

[41]  G. McCarthy,et al.  Evidence for a Refractory Period in the Hemodynamic Response to Visual Stimuli as Measured by MRI , 2000, NeuroImage.

[42]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[43]  D. Heeger,et al.  In this issue , 2002, Nature Reviews Drug Discovery.

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

[45]  P. Lennie,et al.  Rapid adaptation in visual cortex to the structure of images. , 1999, Science.

[46]  Thomas T. Liu,et al.  Discrepancies between BOLD and flow dynamics in primary and supplementary motor areas: application of the balloon model to the interpretation of BOLD transients , 2004, NeuroImage.

[47]  P. Lennie,et al.  Information Conveyed by Onset Transients in Responses of Striate Cortical Neurons , 2001, The Journal of Neuroscience.

[48]  B. Rosen,et al.  Functional mapping of the human visual cortex by magnetic resonance imaging. , 1991, Science.