Estimating the transfer function from neuronal activity to BOLD using simultaneous EEG-fMRI

Previous studies using combined electrical and hemodynamic measurements of brain activity, such as EEG and (BOLD) fMRI, have yielded discrepant results regarding the relationship between neuronal activity and the associated BOLD response. In particular, some studies suggest that this link, or transfer function, depends on the frequency content of neuronal activity, while others suggest that total neuronal power accounts for the changes in BOLD. Here we explored this dependency by comparing different frequency-dependent and -independent transfer functions, using simultaneous EEG-fMRI. Our results suggest that changes in BOLD are indeed associated with changes in the spectral profile of neuronal activity and that these changes do not arise from one specific spectral band. Instead they result from the dynamics of the various frequency components together, in particular, from the relative power between high and low frequencies. Understanding the nature of the link between neuronal activity and BOLD plays a crucial role in improving the interpretability of BOLD images as well as on the design of more robust and realistic models for the integration of EEG and fMRI.

[1]  S. Debener,et al.  Mining EEG-fMRI using independent component analysis. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[2]  M. Lauritzen,et al.  Relationship of Spikes, Synaptic Activity, and Local Changes of Cerebral Blood Flow , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[3]  Louis Lemieux,et al.  EEG/Functional MRI in Epilepsy: The Queen Square Experience , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[4]  Mark S. Cohen,et al.  Simultaneous EEG and fMRI of the alpha rhythm , 2002, Neuroreport.

[5]  William D. Penny,et al.  Bayesian model selection maps for group studies , 2009, NeuroImage.

[6]  Nelson J. Trujillo-Barreto,et al.  Biophysical model for integrating neuronal activity, EEG, fMRI and metabolism , 2008, NeuroImage.

[7]  D. Nair.  About being BOLD , 2005, Brain Research Reviews.

[8]  Karl Friston.  Neurophysiology: The Brain at Work , 2008, Current Biology.

[9]  Robert Turner,et al.  A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI , 2000, NeuroImage.

[10]  Kenneth Hugdahl,et al.  Assessing the spatiotemporal evolution of neuronal activation with single-trial event-related potentials and functional MRI. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Nikolas Offenhauser,et al.  Principal neuron spiking: neither necessary nor sufficient for cerebral blood flow in rat cerebellum , 2004, The Journal of physiology.

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

[13]  Mark S. Cohen,et al.  Acquiring simultaneous EEG and functional MRI , 2000, Clinical Neurophysiology.

[14]  Krish D. Singh,et al.  Functional decoupling of BOLD and gamma‐band amplitudes in human primary visual cortex , 2009, Human brain mapping.

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

[16]  Rajesh P. N. Rao,et al.  Spectral Changes in Cortical Surface Potentials during Motor Movement , 2007, The Journal of Neuroscience.

[17]  R. Turner,et al.  Characterizing Evoked Hemodynamics with fMRI , 1995, NeuroImage.

[18]  Nelson J. Trujillo-Barreto,et al.  A symmetrical Bayesian model for fMRI and EEG/MEG neuroimage fusion , 2001 .

[19]  R. Freeman,et al.  Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity , 2007, Nature Neuroscience.

[20]  Andreas Kleinschmidt,et al.  EEG-correlated fMRI of human alpha activity , 2003, NeuroImage.

[21]  Makoto Takahashi,et al.  The neural basis of the hemodynamic response nonlinearity in human primary visual cortex: Implications for neurovascular coupling mechanism , 2006, NeuroImage.

[22]  G. Ermentrout,et al.  Gamma rhythms and beta rhythms have different synchronization properties. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  N. Logothetis,et al.  Neurophysiology of the BOLD fMRI Signal in Awake Monkeys , 2008, Current Biology.

[24]  P. Nunez,et al.  On the Relationship of Synaptic Activity to Macroscopic Measurements: Does Co-Registration of EEG with fMRI Make Sense? , 2004, Brain Topography.

[25]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[26]  A. Kleinschmidt,et al.  Linking Generalized Spike‐and‐Wave Discharges and Resting State Brain Activity by Using EEG/fMRI in a Patient with Absence Seizures , 2006, Epilepsia.

[27]  Karl J. Friston,et al.  Hemodynamic correlates of EEG: A heuristic , 2005, NeuroImage.

[28]  Christian M Kerskens,et al.  Reduced BOLD response to periodic visual stimulation , 2004, NeuroImage.

[29]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

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

[31]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

[32]  Fred Tam,et al.  A novel method for integrating MEG and BOLD fMRI signals with the linear convolution model in human primary somatosensory cortex , 2008, Human brain mapping.

[33]  W. Penny,et al.  Random-Effects Analysis , 2002 .

[34]  N. Logothetis.  What we can do and what we cannot do with fMRI , 2008, Nature.

[35]  Guillaume Flandin,et al.  Bayesian comparison of spatially regularised general linear models , 2007, Human brain mapping.

[36]  W. D. Penny,et al.  Random-Effects Analysis , 2002 .

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

[38]  Afraim Salek-Haddadi,et al.  Simultaneous EEG-Correlated Ictal fMRI , 2002, NeuroImage.

[39]  Manbir Singh,et al.  Correlation between BOLD‐fMRI and EEG signal changes in response to visual stimulus frequency in humans , 2003, Magnetic resonance in medicine.

[40]  M R Symms,et al.  Spatio-temporal imaging of focal interictal epileptiform activity using EEG-triggered functional MRI. , 2001, Epileptic disorders : international epilepsy journal with videotape.

[41]  Helmut Laufs,et al.  Endogenous brain oscillations and related networks detected by surface EEG‐combined fMRI , 2008, Human brain mapping.

[42]  O. Bertrand,et al.  Relationship between task‐related gamma oscillations and BOLD signal: New insights from combined fMRI and intracranial EEG , 2007, Human brain mapping.

[43]  Helmut Laufs,et al.  Where the BOLD signal goes when alpha EEG leaves , 2006, NeuroImage.

[44]  R Turner,et al.  Optimisation of the 3D MDEFT sequence for anatomical brain imaging: technical implications at 1.5 and 3 T , 2004, NeuroImage.

[45]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[46]  Hamid Soltanian-Zadeh,et al.  Integrated MEG/EEG and fMRI model based on neural masses , 2006, IEEE Transactions on Biomedical Engineering.

[47]  Afraim Salek-Haddadi,et al.  Event-Related fMRI with Simultaneous and Continuous EEG: Description of the Method and Initial Case Report , 2001, NeuroImage.

[48]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[49]  Erkki Oja,et al.  Independent component approach to the analysis of EEG and MEG recordings , 2000, IEEE Transactions on Biomedical Engineering.

[50]  I. Fried,et al.  Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex , 2005, Science.

[51]  Anthony B Waites,et al.  fMRI “deactivation” of the posterior cingulate during generalized spike and wave , 2003, NeuroImage.

[52]  W. Skrandies.  Visual information processing: topography of brain electrical activity , 1995, Biological Psychology.

[53]  R. Silberstein,et al.  Steady-state visual evoked potentials and travelling waves , 2000, Clinical Neurophysiology.

[54]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[55]  Hellmuth Obrig,et al.  Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy , 2003, NeuroImage.

[56]  Natasha M. Maurits,et al.  Correlating the alpha rhythm to BOLD using simultaneous EEG/fMRI: Inter-subject variability , 2006, NeuroImage.

[57]  Daniel Brandeis,et al.  Synchronization facilitates removal of MRI artefacts from concurrent EEG recordings and increases usable bandwidth , 2006, NeuroImage.