Study of neurovascular coupling in humans via simultaneous magnetoencephalography and diffuse optical imaging acquisition

By combining diffuse optical imaging (DOI) and magnetoencephalography (MEG) we investigate neurovascular coupling non-invasively in human subjects using median-nerve stimulation. Previous fMRI studies have shown a habituation effect in the hemodynamic blood oxygen level-dependent (BOLD) response for stimulation periods longer than 2 s. With DOI and MEG we can test whether this effect in hemodynamic response can be accounted for by a habituation effect in the neural response. Our experimental results show that the habituation effect in the hemodynamic response is stronger than that in the earliest cortical neural response (N20). Using a linear convolution model to predict hemodynamic responses we found that including late neural components (> or = 30 ms) improves the prediction of the hemoglobin response. This finding suggests that in addition to the initial evoked-response deflections related to the talamic afferent input, later cortical activity is needed to predict the hemodynamic response.

[1]  Anders M. Dale,et al.  Improved Localization of Cortical Activity By Combining EEG and MEG with MRI Cortical Surface Reconstruction , 2002 .

[2]  Ying Zheng,et al.  Long Duration Stimuli and Nonlinearities in the Neural–Haemodynamic Coupling , 2005, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[3]  A. Toga,et al.  Linear and Nonlinear Relationships between Neuronal Activity, Oxygen Metabolism, and Hemodynamic Responses , 2004, Neuron.

[4]  M. Lauritzen,et al.  Coupling and uncoupling of activity‐dependent increases of neuronal activity and blood flow in rat somatosensory cortex , 2001, The Journal of physiology.

[5]  M Hämäläinen,et al.  Early deflections of cerebral magnetic responses to median nerve stimulation. , 1989, Electroencephalography and clinical neurophysiology.

[6]  A. Villringer,et al.  Spontaneous Low Frequency Oscillations of Cerebral Hemodynamics and Metabolism in Human Adults , 2000, NeuroImage.

[7]  C Baumgartner,et al.  Laminar analysis of extracellular field potentials in rat vibrissa/barrel cortex. , 1990, Journal of neurophysiology.

[8]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

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

[10]  Ulrich Dirnagl,et al.  Functional imaging with Laser Speckle Contrast Analysis: Vascular compartment analysis and correlation with Laser Doppler Flowmetry and somatosensory evoked potentials , 2006, Brain Research.

[11]  R. Ilmoniemi,et al.  Effects of interstimulus interval on somatosensory evoked magnetic fields (SEFs): a hypothesis concerning SEF generation at the primary sensorimotor cortex. , 1996, Electroencephalography and clinical neurophysiology.

[12]  J.C. Mosher,et al.  Multiple dipole modeling and localization from spatio-temporal MEG data , 1992, IEEE Transactions on Biomedical Engineering.

[13]  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.

[14]  L. Kaufman,et al.  Somatically Evoked Magnetic Fields of the Human Brain , 1978, Science.

[15]  Peter A. Bandettini,et al.  Dynamic nonlinearities in BOLD contrast: neuronal or hemodynamic? , 2002 .

[16]  V. Jousmäki,et al.  Activation of a distributed somatosensory cortical network in the human brain. A dipole modelling study of magnetic fields evoked by median nerve stimulation. Part I: Location and activation timing of SEF sources. , 1997, Electroencephalography and clinical neurophysiology.

[17]  T. Allison,et al.  THE FUNCTIONAL NEUROANATOMY OF EVENT RELATED POTENTIALS , 1978 .

[18]  Iwao Kanno,et al.  Stimulus frequency dependence of the linear relationship between local cerebral blood flow and field potential evoked by activation of rat somatosensory cortex , 2004, Neuroscience Research.

[19]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[20]  Giorgio Bonmassar,et al.  EEG/(f)MRI measurements at 7 Tesla using a new EEG cap (“InkCap”) , 2006, NeuroImage.

[21]  O. Creutzfeldt,et al.  Extracellular and intracellular recordings from cat's cortical whisker projection area: thalamocortical response transformation. , 1977, Journal of neurophysiology.

[22]  M. Hämäläinen,et al.  Realistic conductivity geometry model of the human head for interpretation of neuromagnetic data , 1989, IEEE Transactions on Biomedical Engineering.

[23]  Richard M. Leahy,et al.  Electromagnetic brain mapping , 2001, IEEE Signal Process. Mag..

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

[25]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[26]  Ann-Christine Ehlis,et al.  Enhancement of activity of the primary visual cortex during processing of emotional stimuli as measured with event‐related functional near‐infrared spectroscopy and event‐related potentials , 2008, Human brain mapping.

[27]  U. Mitzdorf.  Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[28]  A. Dale,et al.  Coupling of Total Hemoglobin Concentration, Oxygenation, and Neural Activity in Rat Somatosensory Cortex , 2003, Neuron.

[29]  A. Villringer,et al.  Simultaneous EEG–fMRI , 2006, Neuroscience & Biobehavioral Reviews.

[30]  M Hämäläinen,et al.  Somatosensory evoked cerebral magnetic fields from SI and SII in man. , 1984, Electroencephalography and clinical neurophysiology.

[31]  Luigi Rovati,et al.  Optical and electrical recording of neural activity evoked by graded contrast visual stimulus , 2007, Biomedical engineering online.

[32]  Peter A. Bandettini,et al.  From neuron to BOLD: new connections , 2001, Nature Neuroscience.

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

[34]  C. Mathiesen,et al.  Modification of activity‐dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex , 1998, The Journal of physiology.

[35]  Peter Redgrave,et al.  Nonlinear coupling of neural activity and CBF in rodent barrel cortex , 2004, NeuroImage.

[36]  T Allison,et al.  SCALP AND CORTICAL RECORDINGS OF INITIAL SOMATOSENSORY CORTEX ACTIVITY TO MEDIAN NERVE STIMULATION IN MAN * , 1980, Annals of the New York Academy of Sciences.

[37]  H. Jasper,et al.  Laminar microelectrode studies of specific somatosensory cortical potentials. , 1956, Journal of neurophysiology.

[38]  David A. Boas,et al.  Factors affecting the accuracy of near-infrared spectroscopy concentration calculations for focal changes in oxygenation parameters , 2003, NeuroImage.

[39]  A. van Oosterom,et al.  Source parameter estimation in inhomogeneous volume conductors of arbitrary shape , 1989, IEEE Transactions on Biomedical Engineering.

[40]  C. Iadecola.  Neurovascular regulation in the normal brain and in Alzheimer's disease , 2004, Nature Reviews Neuroscience.

[41]  L. Kaufman,et al.  On the relation between somatic evoked potentials and fields. , 1981, The International journal of neuroscience.

[42]  L. Cauller,et al.  The neural basis of the behaviorally relevant N1 component of the somatosensory-evoked potential in SI cortex of awake monkeys: evidence that backward cortical projections signal conscious touch sensation , 2004, Experimental Brain Research.

[43]  Gian Luca Romani,et al.  Complete artifact removal for EEG recorded during continuous fMRI using independent component analysis , 2007, NeuroImage.

[44]  Hellmuth Obrig,et al.  Habituation of the Visually Evoked Potential and Its Vascular Response: Implications for Neurovascular Coupling in the Healthy Adult , 2002, NeuroImage.

[45]  Gabriel Curio,et al.  Neurovascular coupling analyzed non-invasively in the human brain , 2004, Neuroreport.

[46]  D. Delpy,et al.  Characterization of the near infrared absorption spectra of cytochrome aa3 and haemoglobin for the non-invasive monitoring of cerebral oxygenation. , 1988, Biochimica et biophysica acta.

[47]  Hellmuth Obrig,et al.  Individual alpha-frequency correlates with amplitude of visual evoked potential and hemodynamic response , 2008, NeuroImage.

[48]  Hellmuth Obrig,et al.  Separability and cross talk: optimizing dual wavelength combinations for near-infrared spectroscopy of the adult head , 2004, NeuroImage.

[49]  Arthur W. Toga,et al.  Evaluation of coupling between optical intrinsic signals and neuronal activity in rat somatosensory cortex , 2003, NeuroImage.

[50]  Martin Lauritzen,et al.  Dissociation of spikes, synaptic activity, and activity-dependent increments in rat cerebellar blood flow by tonic synaptic inhibition , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[51]  David A Boas,et al.  A haemodynamic response function model in spatio-temporal diffuse optical tomography , 2005, Physics in medicine and biology.

[52]  Anders M. Dale,et al.  Dynamic Statistical Parametric Neurotechnique Mapping: Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000 .

[53]  D. Boas,et al.  Hemodynamic evoked response of the sensorimotor cortex measured noninvasively with near-infrared optical imaging. , 2003, Psychophysiology.

[54]  P. Tueting,et al.  Event-related brain potentials in man , 1978 .

[55]  John A. Nelder,et al.  A Simplex Method for Function Minimization , 1965, Comput. J..

[56]  A Maki,et al.  Wavelength dependence of the precision of noninvasive optical measurement of oxy-, deoxy-, and total-hemoglobin concentration. , 2001, Medical physics.

[57]  Nikos K Logothetis,et al.  Simultaneous EEG and fMRI in the macaque monkey at 4.7 Tesla. , 2005, Magnetic resonance imaging.

[58]  Michiro Negishi,et al.  Removal of time-varying gradient artifacts from EEG data acquired during continuous fMRI , 2004, Clinical Neurophysiology.

[59]  Hiroki Sato,et al.  Practicality of Wavelength Selection to Improve Signal-to-noise Ratio in Near-infrared Spectroscopy , 2003 .

[60]  Heidrun Wabnitz,et al.  Dynamics of cortical neurovascular coupling analyzed by simultaneous DC-magnetoencephalography and time-resolved near-infrared spectroscopy , 2008, NeuroImage.

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

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

[63]  S. Cerutti,et al.  Multimodal analysis of a sustained attention protocol: Continuous Performance Test assessed with Near Infrared Spectroscopy and EEG , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

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

[65]  A. Ngai,et al.  Frequency-dependent changes in cerebral blood flow and evoked potentials during somatosensory stimulation in the rat , 1999, Brain Research.

[66]  J. Mayhew,et al.  Concurrent Optical Imaging Spectroscopy and Laser-Doppler Flowmetry: The Relationship between Blood Flow, Oxygenation, and Volume in Rodent Barrel Cortex , 2001, NeuroImage.

[67]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[68]  L. Trahms,et al.  DC-magnetoencephalography and time-resolved near-infrared spectroscopy combined to study neuronal and vascular brain responses , 2007, Physiological measurement.