Neurophysiological investigation of the basis of the fMRI signal

Functional magnetic resonance imaging (fMRI) is widely used to study the operational organization of the human brain, but the exact relationship between the measured fMRI signal and the underlying neural activity is unclear. Here we present simultaneous intracortical recordings of neural signals and fMRI responses. We compared local field potentials (LFPs), single- and multi-unit spiking activity with highly spatio-temporally resolved blood-oxygen-level-dependent (BOLD) fMRI responses from the visual cortex of monkeys. The largest magnitude changes were observed in LFPs, which at recording sites characterized by transient responses were the only signal that significantly correlated with the haemodynamic response. Linear systems analysis on a trial-by-trial basis showed that the impulse response of the neurovascular system is both animal- and site-specific, and that LFPs yield a better estimate of BOLD responses than the multi-unit responses. These findings suggest that the BOLD contrast mechanism reflects the input and intracortical processing of a given area rather than its spiking output.

[1]  K Rossmann,et al.  Image Quality , 2018, Definitions.

[2]  Donald O. Walter,et al.  Mass action in the nervous system , 1975 .

[3]  P. Mansfield.  Multi-planar image formation using NMR spin echoes , 1977 .

[4]  H. Vaughan,et al.  Averaged multiple unit activity as an estimate of phasic changes in local neuronal activity: effects of volume-conducted potentials , 1980, Journal of Neuroscience Methods.

[5]  U. Mitzdorf.  Properties of the evoked potential generators: current source-density analysis of visually evoked potentials in the cat cortex. , 1987, The International journal of neuroscience.

[6]  G. Seeley,et al.  Image Quality , 1989, [1989] Proceedings. The First International Conference on Image Management and Communication in Patient Care: Implementation and Impact.

[7]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[8]  S. Ogawa,et al.  Magnetic resonance imaging of blood vessels at high fields: In vivo and in vitro measurements and image simulation , 1990, Magnetic resonance in medicine.

[9]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[10]  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.

[11]  J. Frahm,et al.  Dynamic MR imaging of human brain oxygenation during rest and photic stimulation , 1992, Journal of magnetic resonance imaging : JMRI.

[12]  D. Tank,et al.  Functional Brain Mapping Using Magnetic Resonance Imaging: Signal Changes Accompanying Visual Stimulation , 1992, Investigative radiology.

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

[14]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[15]  R. Eckhorn,et al.  A new method for the insertion of multiple microprobes into neural and muscular tissue, including fiber electrodes, fine wires, needles and microsensors , 1993, Journal of Neuroscience Methods.

[16]  W. Singer.  Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[17]  Ravi S. Menon,et al.  Imaging at high magnetic fields: initial experiences at 4 T. , 1993, Magnetic resonance quarterly.

[18]  R Gruetter,et al.  Automatic, localized in Vivo adjustment of all first‐and second‐order shim coils , 1993, Magnetic resonance in medicine.

[19]  R. Llinás,et al.  Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[20]  P. Magistretti,et al.  Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[21]  L. Sokoloff,et al.  Role of sodium and potassium ions in regulation of glucose metabolism in cultured astroglia. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[22]  A. Kleinschmidt,et al.  Dynamic uncoupling and recoupling of perfusion and oxidative metabolism during focal brain activation in man , 1996, Magnetic resonance in medicine.

[23]  A. Kleinschmidt,et al.  Dynamic MRI sensitized to cerebral blood oxygenation and flow during sustained activation of human visual cortex , 1996, Magnetic resonance in medicine.

[24]  A. Grinvald,et al.  Interactions Between Electrical Activity and Cortical Microcirculation Revealed by Imaging Spectroscopy: Implications for Functional Brain Mapping , 1996, Science.

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

[26]  J. Movshon,et al.  Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex , 1997, The Journal of Neuroscience.

[27]  J. Ford,et al.  Combined event‐related fMRI and EEG evidence for temporal—parietal cortex activation during target detection , 1997, Neuroreport.

[28]  O Bertrand,et al.  Combined EEG and MEG recordings of visual 40 Hz responses to illusory triangles in human , 1997, Neuroreport.

[29]  X. Hu,et al.  Evaluation of the early response in fMRI in individual subjects using short stimulus duration , 1997, Magnetic resonance in medicine.

[30]  P. Bandettini,et al.  Echo-planar imaging : theory, technique and application , 1998 .

[31]  R G Shulman,et al.  Interpreting functional imaging studies in terms of neurotransmitter cycling. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R. Buxton,et al.  Dynamics of blood flow and oxygenation changes during brain activation: The balloon model , 1998, Magnetic resonance in medicine.

[33]  R. Shulman,et al.  Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[35]  N. Logothetis,et al.  Functional imaging of the monkey brain , 1999, Nature Neuroscience.

[36]  Robert G. Shulman,et al.  Energy on Demand , 1999, Science.

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

[38]  R. Eckhorn,et al.  Visual stimulation elicits locked and induced gamma oscillations in monkey intracortical- and EEG-potentials, but not in human EEG , 1999, Experimental Brain Research.

[39]  R G Shulman,et al.  In vivo nuclear magnetic resonance spectroscopy studies of the relationship between the glutamate-glutamine neurotransmitter cycle and functional neuroenergetics. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  J. Anthony Movshon,et al.  Review A Critical Evaluation of the Temporal Binding Hypothesis , 1999 .

[41]  M R Symms,et al.  EEG-triggered functional MRI of interictal epileptiform activity in patients with partial seizures. , 1999, Brain : a journal of neurology.

[42]  Michael N. Shadlen,et al.  Synchrony Unbound A Critical Evaluation of the Temporal Binding Hypothesis , 1999, Neuron.

[43]  J W Belliveau,et al.  Visual evoked potential (VEP) measured by simultaneous 64-channel EEG and 3T fMRI. , 1999, Neuroreport.

[44]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

[45]  O. Josephs,et al.  EEG recording during fMRI experiments: Image quality , 2000, Human brain mapping.

[46]  H. Scheich,et al.  New Insights into the Hemodynamic Blood Oxygenation Level-Dependent Response through Combination of Functional Magnetic Resonance Imaging and Optical Recording in Gerbil Barrel Cortex , 2000, The Journal of Neuroscience.

[47]  G. Shulman,et al.  Spectroscopic imaging of glutamate C4 turnover in human brain , 2000, Magnetic resonance in medicine.

[48]  Nikos K. Logothetis,et al.  Nonmonotonic noise tuning of BOLD fMRI signal to natural images in the visual cortex of the anesthetized monkey , 2001, Current Biology.

[49]  J. Mazziotta,et al.  Brain Mapping: The Methods , 2002 .