Interpreting the BOLD signal.

The development of functional magnetic resonance imaging (fMRI) has brought together a broad community of scientists interested in measuring the neural basis of the human mind. Because fMRI signals are an indirect measure of neural activity, interpreting these signals to make deductions about the nervous system requires some understanding of the signaling mechanisms. We describe our current understanding of the causal relationships between neural activity and the blood-oxygen-level-dependent (BOLD) signal, and we review how these analyses have challenged some basic assumptions that have guided neuroscience. We conclude with a discussion of how to use the BOLD signal to make inferences about the neural signal.

[1]  W. H. Vance,et al.  Effects of antidromic stimulation of the ventral root on glucose utilization in the ventral horn of the spinal cord in the rat. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

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

[3]  Cristopher M Niell,et al.  Live optical imaging of nervous system development. , 2004, Annual review of physiology.

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

[5]  H. Said,et al.  Recent advances in carrier-mediated intestinal absorption of water-soluble vitamins. , 2004, Annual review of physiology.

[6]  M. Raichle A Brief History of Human Functional Brain Mapping , 2000 .

[7]  P. Gillespie,et al.  Myosin-1c, the hair cell's adaptation motor. , 2004, Annual review of physiology.

[8]  K. Mosier,et al.  Parallel cortical networks for volitional control of swallowing in humans , 2001, Experimental Brain Research.

[9]  J. Stone,et al.  Sampling properties of microelectrodes assessed in the cat's retina. , 1973, Journal of neurophysiology.

[10]  C. Nicholson,et al.  Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. , 1975, Journal of neurophysiology.

[11]  Benjamin W. Zweifach,et al.  Topography and function of the mesenteric capillary circulation , 1944 .

[12]  G. Fromm,et al.  SLOW CHANGES IN THE ELECTROCORTICOGRAM AND THE ACTIVITY OF CORTICAL NEURONS. , 1964, Electroencephalography and clinical neurophysiology.

[13]  Martin Lauritzen,et al.  Brain Function and Neurophysiological Correlates of Signals Used in Functional Neuroimaging , 2003, The Journal of Neuroscience.

[14]  D L Rothman,et al.  Quantitative multi-modal functional MRI with blood oxygenation level dependent exponential decays adjusted for flow attenuated inversion recovery (BOLDED AFFAIR). , 2000, Magnetic resonance imaging.

[15]  A. Rodríguez-Baeza,et al.  Morphological characteristics and distribution pattern of the arterial vessels in human cerebral cortex: A scanning electron microscope study , 1998, The Anatomical record.

[16]  A. Maggi,et al.  Estrogens in the nervous system: mechanisms and nonreproductive functions. , 2004, Annual review of physiology.

[17]  L. Sokoloff,et al.  RELATION BETWEEN PHYSIOLOGICAL FUNCTION AND ENERGY METABOLISM IN THE CENTRAL NERVOUS SYSTEM , 1977, Journal of neurochemistry.

[18]  A. Crofts,et al.  The cytochrome bc1 complex: function in the context of structure. , 2004, Annual review of physiology.

[19]  G. Yang,et al.  Glutamate microinjections in cerebellar cortex reproduce cerebrovascular effects of parallel fiber stimulation. , 1996, The American journal of physiology.

[20]  J F Toole,et al.  Anastomoses in the vascular bed of the human cerebrum. , 1968, Journal of neuropathology and experimental neurology.

[21]  R. Nudo,et al.  Stimulation‐induced [14C]2‐deoxyglucose labeling of synaptic activity in the central auditory system , 1986, The Journal of comparative neurology.

[22]  A W Toga,et al.  The metabolic consequence of visual deprivation in the rat. , 1987, Brain research.

[23]  H. Liu,et al.  An investigation of the impulse functions for the nonlinear BOLD response in functional MRI. , 2000, Magnetic resonance imaging.

[24]  M. Privalsky,et al.  The role of corepressors in transcriptional regulation by nuclear hormone receptors. , 2004, Annual review of physiology.

[25]  D. Ts'o,et al.  Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Y Harada,et al.  The calcium component of the action potential in spinal motoneurones of the rat. , 1983, The Journal of physiology.

[27]  K. Walton,et al.  Ionic mechanisms underlying the firing properties of rat neonatal motoneurons studied in vitro , 1986, Neuroscience.

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

[29]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[30]  S. Tsai,et al.  Genetically engineered mouse models for lung cancer. , 2004, Annual review of physiology.

[31]  N. Harel,et al.  Blood capillary distribution correlates with hemodynamic-based functional imaging in cerebral cortex. , 2002, Cerebral cortex.

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

[33]  G. Palm,et al.  Density of neurons and synapses in the cerebral cortex of the mouse , 1989, The Journal of comparative neurology.

[34]  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.

[35]  G. H. Bishop,et al.  Factors determining the form of the potential record in the vicinity of the synapses of the dorsal nucleus of the lateral geniculate body , 1942 .

[36]  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.

[37]  R. Buxton,et al.  A Model for the Coupling between Cerebral Blood Flow and Oxygen Metabolism during Neural Stimulation , 1997, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[38]  E. Argandoña,et al.  Visual deprivation effects on the s100beta positive astrocytic population in the developing rat visual cortex: a quantitative study. , 2003, Brain research. Developmental brain research.

[39]  H. D. Morris,et al.  Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat , 2003, Neuroscience.

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

[41]  Marsan Ca ELECTRICAL ACTIVITY OF THE BRAIN: SLOW WAVES AND NEURONAL ACTIVITY. , 1965 .

[42]  P T Fox,et al.  Comparison of the temporal response in perfusion and BOLD‐based event‐related functional MRI , 2000, Magnetic resonance in medicine.

[43]  Keith J. Worsley,et al.  Statistical analysis of activation images , 2001 .

[44]  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.

[45]  JENNIFER S. BUCHWALD,et al.  Comparison of Multiple-unit and Electroencephalogram Activity recorded from the same Brain Sites during Behavioural Conditioning , 1965, Nature.

[46]  R. Turner,et al.  Echo‐planar time course MRI of cat brain oxygenation changes , 1991, Magnetic resonance in medicine.

[47]  A. Araque,et al.  Tripartite synapses: glia, the unacknowledged partner , 1999, Trends in Neurosciences.

[48]  D. Perani,et al.  Interhemispheric transmission of visuomotor information in humans: fMRI evidence. , 2002, Journal of neurophysiology.

[49]  B. Wandell Computational neuroimaging of human visual cortex. , 1999, Annual review of neuroscience.

[50]  Timothy P. L. Roberts,et al.  The use of fMRI for determining the topographic organization of cortical fields in human and nonhuman primates , 1999, Brain Research.

[51]  N. Logothetis The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[52]  D. Humphrey,et al.  Properties of pyramidal tract neuron system within a functionally defined subregion of primate motor cortex. , 1978, Journal of neurophysiology.

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

[54]  M. Raichle,et al.  Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[55]  C. Rovainen,et al.  Journal of Cerebral Blood Flow and Metabolism Localized Dynamic Changes in Cortical Blood Flow with Whisker Stimulation Corresponds to Matched Vascular and Neuronal Architecture of Rat Barrels , 2022 .

[56]  D. G. Albrecht,et al.  Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? , 2000, Nature Neuroscience.

[57]  L. Sokoloff,et al.  Relationships among local functional activity, energy metabolism, and blood flow in the central nervous system. , 1981, Federation proceedings.

[58]  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.

[59]  A. Fergus,et al.  Regulation of cerebral microvessels by glutamatergic mechanisms , 1997, Brain Research.

[60]  W. Greenough,et al.  Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

[62]  Adrian T. Lee,et al.  fMRI of human visual cortex , 1994, Nature.

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

[64]  D. Heeger,et al.  Spatial attention affects brain activity in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[65]  J. Csicsvari,et al.  Intracellular features predicted by extracellular recordings in the hippocampus in vivo. , 2000, Journal of neurophysiology.

[66]  K. Hossmann,et al.  Simultaneous recording of evoked potentials and T  *2 ‐weighted MR images during somatosensory stimulation of rat , 1999, Magnetic resonance in medicine.

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

[68]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[69]  P. Lennie The Cost of Cortical Computation , 2003, Current Biology.

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

[71]  E. Tanaka,et al.  Ionic mechanisms underlying the depolarizing and hyperpolarizing afterpotentials of single spike in guinea-pig cingulate cortical neurons , 1993, Neuroscience.

[72]  Nikos K. Logothetis,et al.  Motion Processing in the Macaque: Revisited with Functional Magnetic Resonance Imaging , 2001, The Journal of Neuroscience.

[73]  N. Logothetis,et al.  Visual competition , 2002, Nature Reviews Neuroscience.

[74]  O Hidaka,et al.  Role of calcium conductances on spike afterpotentials in rat trigeminal motoneurons. , 1997, Journal of neurophysiology.

[75]  H. Duvernoy,et al.  Cortical blood vessels of the human brain , 1981, Brain Research Bulletin.

[76]  W. Rall Electrophysiology of a dendritic neuron model. , 1962, Biophysical journal.

[77]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[78]  N. Logothetis,et al.  Visual Areas in Macaque Cortex Measured Using Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[79]  Rodney A. Brooks,et al.  Nuclear Magnetic Relaxation in Blood , 1975, IEEE Transactions on Biomedical Engineering.

[80]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[81]  A L Towe,et al.  Extracellular microelectrode sampling bias. , 1970, Experimental neurology.

[82]  G L Shulman,et al.  Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[83]  S. Heinemann,et al.  Metabolic regulation of potassium channels. , 2004, Annual review of physiology.

[84]  B. Gustafsson,et al.  Afterpotentials and transduction properties in different types of central neurones. , 1984, Archives italiennes de biologie.

[85]  R E Weller,et al.  Cortical connections of the caudal subdivision of the dorsolateral area (V4) in monkeys , 1991, The Journal of comparative neurology.

[86]  Alex R. Wade,et al.  Functional imaging of the visual pathways. , 2003, Neurologic clinics.

[87]  E. Adrian,et al.  The impulses produced by sensory nerve-endings: Part II. The response of a Single End-Organ. , 2006, The Journal of physiology.

[88]  F. Hyder,et al.  Total neuroenergetics support localized brain activity: Implications for the interpretation of fMRI , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[89]  S. H. Chandler,et al.  Electrophysiological properties of guinea pig trigeminal motoneurons recorded in vitro. , 1994, Journal of neurophysiology.

[90]  Louis Sokoloff,et al.  Activity‐dependent Energy Metabolism in Rat Posterior Pituitary Primarily Reflects Sodium Pump Activity , 1980, Journal of neurochemistry.

[91]  M. Reivich,et al.  THE [14C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT 1 , 1977, Journal of neurochemistry.

[92]  P. G. Nelson Interaction between spinal motoneurons of the cat. , 1966, Journal of neurophysiology.

[93]  R G Shulman,et al.  A model for the regulation of cerebral oxygen delivery. , 1998, Journal of applied physiology.

[94]  S. Shimojyo,et al.  The effects of graded hypoxia upon transient cerebral blood flow and oxygen consumption , 1968, Neurology.

[95]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

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

[97]  T. Ebner,et al.  Local and propagated vascular responses evoked by focal synaptic activity in cerebellar cortex. , 1997, Journal of neurophysiology.

[98]  D. Heeger,et al.  Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry , 2000, Nature Neuroscience.

[99]  J. B. Ranck,et al.  Specific impedance of rabbit cerebral cortex. , 1963, Experimental neurology.

[100]  Alexander Thiele,et al.  Effects of attention on orientation-tuning and contrast response functions in primate V1 , 2005 .

[101]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[102]  C. Mathiesen,et al.  Temporal coupling between neuronal activity and blood flow in rat cerebellar cortex as indicated by field potential analysis , 2000, The Journal of physiology.

[103]  F. Hyder,et al.  Cerebral energetics and spiking frequency: The neurophysiological basis of fMRI , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[104]  C. Iadecola,et al.  Nitric oxide and adenosine mediate vasodilation during functional activation in cerebellar cortex , 1994, Neuropharmacology.

[105]  S. Chiu,et al.  Neurotransmitter‐mediated signaling between axons and glial cells , 1994, Glia.

[106]  B. McNaughton,et al.  Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex , 1995, Journal of Neuroscience Methods.

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

[108]  Wolfgang Engelien,et al.  A CBF-Based Event-Related Brain Activation Paradigm: Characterization of Impulse–Response Function and Comparison to BOLD , 2000, NeuroImage.

[109]  D. Kernell,et al.  Delayed depolarization and the repetitive response to intracellular stimulation of mammalian motoneurones , 1963, The Journal of physiology.

[110]  M. Colonnier,et al.  A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys , 1982, The Journal of comparative neurology.

[111]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

[112]  E. Adrian,et al.  The impulses produced by sensory nerve‐endings , 1926 .

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

[114]  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.

[115]  J Xiong,et al.  Cerebral hemodynamic response in Chinese (first) and English (second) language processing revealed by event-related functional MRI. , 2001, Magnetic resonance imaging.

[116]  M. Jüptner,et al.  Review: Does Measurement of Regional Cerebral Blood Flow Reflect Synaptic Activity?—Implications for PET and fMRI , 1995, NeuroImage.

[117]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

[118]  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.

[119]  R. L. Nó,et al.  Action potential of the motoneurons of the hypoglossus nucleus. , 1947 .

[120]  A. Toga,et al.  5 – Optical Imaging Based on Intrinsic Signals , 2002 .

[121]  B. Siesjö,et al.  Brain energy metabolism , 1978 .

[122]  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.

[123]  H. Pfeifer Principles of Nuclear Magnetic Resonance Microscopy , 1992 .

[124]  T A Woolsey,et al.  Neuronal units linked to microvascular modules in cerebral cortex: response elements for imaging the brain. , 1996, Cerebral cortex.

[125]  F. Grover,et al.  Correlation of cell size with amplitude of background fast activity in specific brain nuclei. , 1970, Journal of neurophysiology.

[126]  T. Bullock,et al.  Signals and signs in the nervous system: the dynamic anatomy of electrical activity is probably information-rich. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[127]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[128]  W. Pitts,et al.  What the Frog's Eye Tells the Frog's Brain , 1959, Proceedings of the IRE.

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

[130]  C. D. Coryell,et al.  The Magnetic Properties and Structure of Hemoglobin, Oxyhemoglobin and Carbonmonoxyhemoglobin , 1936, Proceedings of the National Academy of Sciences.

[131]  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.

[132]  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.

[133]  G. Buzsáki,et al.  Nucleus basalis and thalamic control of neocortical activity in the freely moving rat , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[134]  Carrie J. McAdams,et al.  Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4 , 1999, The Journal of Neuroscience.

[135]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[136]  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.

[137]  Adelbert Ames,et al.  CNS energy metabolism as related to function , 2000, Brain Research Reviews.

[138]  Leslie G. Ungerleider,et al.  Cortical connections of visual area MT in the macaque , 1986, The Journal of comparative neurology.

[139]  S. Ogawa,et al.  An approach to probe some neural systems interaction by functional MRI at neural time scale down to milliseconds. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[140]  J B Ranck,et al.  Electrical impedance in the subicular area of rats during paradoxical sleep. , 1966, Experimental neurology.

[141]  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.

[142]  Prof. Dr. Dr. Valentino Braitenberg,et al.  Cortex: Statistics and Geometry of Neuronal Connectivity , 1998, Springer Berlin Heidelberg.

[143]  P. Magistretti,et al.  Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[144]  C A MARSAN ELECTRICAL ACTIVITY OF THE BRAIN: SLOW WAVES AND NEURONAL ACTIVITY. , 1965, Israel journal of medical sciences.

[145]  G. Radda,et al.  Oxygenation dependence of the transverse relaxation time of water protons in whole blood at high field. , 1982, Biochimica et biophysica acta.

[146]  K. Breese,et al.  Nitric oxide mediates vasodilatation in response to activation of N-methyl-D-aspartate receptors in brain. , 1993, Circulation research.

[147]  F. Grover,et al.  Amplitudes of background fast activity characteristic of specific brain sites. , 1970, Journal of neurophysiology.

[148]  D L Rothman,et al.  High-Resolution CMRO2 Mapping in Rat Cortex: A Multiparametric Approach to Calibration of BOLD Image Contrast at 7 Tesla , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[149]  Elizabeth P Dahlhoff,et al.  Biochemical indicators of stress and metabolism: applications for marine ecological studies. , 2004, Annual review of physiology.

[150]  N. Logothetis The Underpinnings of the BOLD Functional Magnetic Resonance Imaging Signal , 2003, The Journal of Neuroscience.

[151]  R. Desimone,et al.  Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. , 1987, Journal of neurophysiology.

[152]  Ying Zheng,et al.  The Hemodynamic Impulse Response to a Single Neural Event , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[153]  Stephen A. Engel,et al.  Interocular rivalry revealed in the human cortical blind-spot representation , 2001, Nature.

[154]  G. Buzsáki,et al.  Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: Activity‐dependent phase‐precession of action potentials , 1998, Hippocampus.

[155]  C. Sherrington,et al.  On the Regulation of the Blood‐supply of the Brain , 1890, The Journal of physiology.

[156]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[157]  E. Argandoña,et al.  Influence of visual experience deprivation on the postnatal development of the microvascular bed in layer IV of the rat visual cortex , 2000, Brain Research.

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

[159]  E A Disbrow,et al.  Functional MRI at 1.5 tesla: a comparison of the blood oxygenation level-dependent signal and electrophysiology. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[160]  S. Laughlin,et al.  An Energy Budget for Signaling in the Grey Matter of the Brain , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[161]  S. Ogawa,et al.  Oxygenation‐sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields , 1990, Magnetic resonance in medicine.

[162]  Wen‐Hui Wang,et al.  Regulation of renal K transport by dietary K intake. , 2004, Annual review of physiology.

[163]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

[164]  G. Fromm,et al.  The relationship between neuron activity and cortical steady potentials. , 1967, Electroencephalography and clinical neurophysiology.

[165]  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.

[166]  W. Koch,et al.  Viral-based myocardial gene therapy approaches to alter cardiac function. , 2004, Annual review of physiology.

[167]  J. Allman,et al.  Mapping human visual cortex with positron emission tomography , 1986, Nature.

[168]  S. W. Kuffler Discharge patterns and functional organization of mammalian retina. , 1953, Journal of neurophysiology.

[169]  A. Crane,et al.  Differential effects of electrical stimulation of sciatic nerve on metabolic activity in spinal cord and dorsal root ganglion in the rat. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[170]  D. Attwell,et al.  The neural basis of functional brain imaging signals , 2002, Trends in Neurosciences.

[171]  Paul M. Matthews,et al.  Functional magnetic resonance imaging: An introduction to methods , 2001 .

[172]  M. Mintun,et al.  Nonoxidative glucose consumption during focal physiologic neural activity. , 1988, Science.