On the nature of the BOLD fMRI contrast mechanism

Magnetic Resonance Imaging

Volumn 22, Issue 10 SPEC. ISS., 2004, Pages 1517-1531

  Logothetis, Nikos K ^a   Pfeuffer, Josef ^a  

^a MAX PLANCK INSTITUTE FOR BIOLOGICAL CYBERNETICS   (Germany)

Author keywords

Functional magnetic resonance imaging; Local field potentials; Monkey brain; Multiple unit activity; Synaptic activity

Indexed keywords

OXYGEN;

BLOOD FLOW; BRAIN FUNCTION; BRAIN MAPPING; BRAIN METABOLISM; CONFERENCE PAPER; ELECTROENCEPHALOGRAM; ELECTROSTIMULATION; ENERGY METABOLISM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; IMAGE QUALITY; IMAGING SYSTEM; NERVE CONDUCTION; NONHUMAN; OXYGEN BLOOD LEVEL; OXYGENATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 13544260698     PISSN: 0730725X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mri.2004.10.018     Document Type: Conference Paper

References (125)

1. J.M. Allman Maps in context: some analogies between visual cortical and gentic maps L.M. Vaina Matters of intelligence 1987 D. Reidel Publishing Company Dordrecht (NL) 369 393
2. J.B. Levitt, and J.S. Lund Contrast dependence of contextual effects in primate visual cortex Nature 387 1997 73 76
3. K. Zipser, V.A.F. Lamme, and P.H. Schiller Contextual modulation in primary visual cortex J. Neurosci. 16 22 1996 7376 7389
4. V.A.F. Lamme The neurophysiology of figure-ground segregation in primary visual cortex J. Neurosci. 15 1995 1605 1615
5. V.A. Lamme, H. Super, and H. Spekreijse Feedforward, horizontal, and feedback processing in the visual cortex [83 refs] Curr. Opin. Neurobiol. 8 4 1998 529 535
6. D.L. Ringach, M.J. Hawken, and R. Shapley Dynamics of orientation tuning in macaque primary visual cortex Nature 387 1997 281 284
7. C.D. Gilbert Plasticity in visual perception and physiology [44 refs] Curr. Opin. Neurobiol. 6 2 1996 269 274
8. Y. Trotter, S. Celebrini, B. Stricanne, S. Thorpe, and M. Imbert Modulation of neural stereoscopic processing in primate area V1 by the viewing distance Science 257 1992 1279 1281
9. M.K. Kapadia, G. Westheimer, and C.D. Gilbert Dynamics of spatial summation in primary visual cortex of alert monkeys Proc. Natl. Acad. Sci. U. S. A. 96 1999 12073 12078
10. G. Gratton Attention and probability effects in the human occipital cortex: an optical imaging study Neuroreport 8 7 1997 1749 1753
11. J. McLean, and L.A. Palmer Contrast adaptation and excitatory amino acid receptors in cat striate cortex Vis. Neurosci. 13 1996 1069 1087
12. M. Carandini, H.B. Barlow, L.P. O'Keefe, A.B. Poirson, and J.A. Movshon Adaptation to contingencies in macaque primary visual cortex. Philos. Trans. R. Soc. Lond., B Biol. Sci. 352 1358 1997 1149 1154
13. S.M. Zeki The functional organization of projections from striate to prestriate visual cortex in the rhesus monkey Cold Spring Harb. Symp. Quant. Biol. 40 1976 591 600
14. D.C. Van Essen Functional organization of primate visual cortex A.J. Peters Cerebral cortex 1985 Plenum Publishing New York 259 329
15. K.S. Rockland, and D.N. Pandya Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey Brain Res. 179 1979 3 20
16. D. Boussaoud, L.G. Ungerleider, and R. Desimone Pathways for motion analysis: cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque J. Comp. Neurol. 296 1990 462 495
17. D.J. Felleman, and D.C. Van Essen Distributed hierarchical processing in primate cerebral cortex Cereb. Cortex 1 1991 1 47
18. A. Morel, and J. Bullier Anatomical segregation of two cortical visual pathways in the macaque monkey Vis. Neurosci. 4 1990 555 578
19. L.G. Ungerleider, and M. Mishkin Two cortical visual systems D.J. Ingle Analysis of visual behavior 1982 M.I.T. Press Cambridge 549 586
20. J.P. Rauschecker Parallel processing in the auditory cortex of primates Audiol. Neurootol. 3 2-3 1998 86 103
21. J. Pfeuffer, H. Merkle, M. Beyerlein, T. Steudel, and N.K. Logothetis Anatomical and functional MR imaging in the macaque monkey using a vertical large-bore 7 Tesla setup Magn. Reson. Imaging 22 2004 1343 1359
22. 1H NMR spectroscopy in the anaesthetized and in the awake monkey Magn. Reson. Imaging 22 2004 1361 1372
23. 1H 2D MR chemical shift imaging in the monkey brain at 7T Magn. Reson. Imaging 22 2004 1373 1383
24. K.D. Harris, D.A. Henze, J. Csicsvari, H. Hirase, and G. Buzsaki Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements J. Neurophysiol. 84 1 2000 401 414
25. D.A. Henze, Z. Borhegyi, J. Csicsvari, A. Mamiya, K.D. Harris, and G. Buzsaki Intracellular features predicted by extracellular recordings in the hippocampus in vivo J. Neurophysiol. 84 1 2000 390 400
26. J. Stone Sampling properties of microelectrodes assessed in the cat's retina J. Neurophysiol. 36 1973 1071 1079
27. A.L. Towe, and G.W. Harding Extracellular microelectrode sampling bias Exp. Neurol. 29 2 1970 366 381
28. W. Rall Electrophysiology of a dendritic neuron Biophys. J. 2 1962 145 167
29. D.R. Humphrey, and W.S. Corrie Properties of pyramidal tract neuron system within a functionally defined subregion of primate motor cortex J. Neurophysiol. 41 1 1978 216 243
30. G.H. Bishop, and J.L. O'Leary Factors determining the form of the potential record in the vicinity of the synapses of the dorsal nucleus of the lateral geniculate body J. Cell. Comp. Physiol. 19 1942 315 331
31. R. Lorente de Nó Action potentials of the motorneurones of the hypoglossus nucleus J. Cell. Comp. Physiol. 29 1947 207 288
32. J.S. Buchwald, and F.S. Grover Amplitudes of background fast activity characteristic of specific brain sites J. Neurophysiol. 33 1 1970 148 159
33. P.G. Nelson Interaction between spinal motoneurons of the cat J. Neurophysiol. 29 2 1966 275 287
34. F.S. Grover, and J.S. Buchwald Correlation of cell size with amplitude of background fast activity in specific brain nuclei J. Neurophysiol. 33 1 1970 160 171
35. C. Hunt The reflex activity of mammalian small-nerve fibers J. Physiol. (Lond.) 115 1951 456 469
36. H.S. Gasser, and H. Grundfest Axon diameters in relation to the spike dimensions and the conduction velocity in mammalian A fibers Am. J. Physiol. 127 1939 393 414
37. A.D. Legatt, J. Arezzo, and H.G.J. Vaughan Averaged multiple unit activity as an estimate of phasic changes in local neuronal activity: effects of volume-conducted potentials J. Neurosci. Methods 2 2 1980 203 217
38. C.M. Gray, P.E. Maldonado, M. Wilson, and B. McNaughton Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex J. Neurosci. Methods 63 1995 43 54
39. C. Nicholson, and R. Llinas Field potentials in the alligator cerebellum and theory of their relationship to Purkinje cell dendritic spikes J. Neurophysiol. 34 4 1971 509 531
40. J. Arezzo, A.D. Legatt, and H.G.J. Vaughan Topography and intracranial sources of somatosensory evoked potentials in the monkey: I. Early components Electroencephalogr. Clin. Neurophysiol. 46 2 1979 155 172
41. C.M. Huang, and J.S. Buchwald Interpretation of the vertex short-latency acoustic response: a study of single neurons in the brain stem Brain Res. 137 2 1977 291 303
42. G.H. Fromm, and H.W. Bond Slow changes in the electrocorticogram and the activity of cortical neurons Electroencephalogr. Clin. Neurophysiol. 17 1964 520 523
43. G.H. Fromm, and H.W. Bond The relationship between neuron activity and cortical steady potentials Electroencephalogr. Clin. Neurophysiol. 22 2 1967 159 166
44. C. Ajmone-Marsan Electrical activity of the brain: slow waves and neuronal activity Isr. J. Med. Sci. 1 1965 104 117
45. J.S. Buchwald, E.S. Hala, and S. Schramm A comparison of multi-unit activity and EEG activity recorded from the same brain site in chronic cats during behavioral conditioning Nature 205 1965 1012 1014
46. U. Mitzdorf Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena [324 refs] Physiol. Rev. 65 1 1985 37 100
47. Z. Nadasdy, J. Csicsvari, M. Penttonen, J. Hetke, K. Wise, and G. Buzsaki Extracellular recording and analysis of neuronal activity: from single cells to ensembles H. Eichenbaum J.L. Davis Neuronal ensembles: strategies from recording and decoding 1998 Wiley-Liss New York 17 55
48. U. Mitzdorf Properties of the evoked potential generators: current source-density analysis of visually evoked potentials in the cat cortex Int. J. Neurosci. 33 1-2 1987 33 59
49. E. Juergens, A. Guettler, and R. Eckhorn Visual stimulation elicits locked and induced gamma oscillations in monkey intracortical- and EEG-potentials, but not in human EEG Exp. Brain Res. 129 2 1999 247 259
50. E. Juergens, R. Eckhorn, A. Frien, and T. Woelbern Restricted coupling range of fast oscillations in striate cortex of awake monkey N. Elsner H.-U. Schnitzer Brain and evolution 1996 Thieme Berlin 418
51. A. Kamondi, L. Acsady, and G. Buzsaki Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus J. Neurosci. 18 10 1998 3919 3928
52. R. Granit, D. Kernell, and R.S. Smith Delayed depolarization and the repetitive response to intracellular stimulation of mammalian motoneurones J. Physiol. (Lond.) 168 1963 890 910
53. Y. Harada, and T. Takahashi The calcium component of the action potential in spinal motoneurones of the rat J. Physiol. 335 1983 89 100
54. B. Gustafsson Afterpotentials and transduction properties in different types of central neurones Arch. Ital. Biol. 122 1 1984 17 30
55. S.H. Chandler, C.F. Hsaio, T. Inoue, and L.J. Goldberg Electrophysiological properties of guinea pig trigeminal motoneurons recorded in vitro J. Neurophysiol. 71 1 1994 129 145
56. K. Walton, and B.P. Fulton Ionic mechanisms underlying the firing properties of rat neonatal motoneurons studied in vitro Neuroscience 19 3 1986 669 683
57. H. Higashi, E. Tanaka, H. Inokuchi, and S. Nishi Ionic mechanisms underlying the depolarizing and hyperpolarizing afterpotentials of single spike in guinea-pig cingulate cortical neurons Neuroscience 55 1 1993 129 138
58. M. Kobayashi, T. Inoue, R. Matsuo, Y. Masuda, O. Hidaka, and Y. Kang Role of calcium conductances on spike afterpotentials in rat trigeminal motoneurons J. Neurophysiol. 77 6 1997 3273 3283
59. G. Buzsaki Theta oscillations in the hippocampus Neuron 33 3 1931 325 340
60. G. Buzsaki, and F.H. Gage Mechanisms of action of neural grafts in the limbic system [53 refs] Can. J. Neurol. Sci. 15 2 1988 99 105
61. C.S. Roy, and C.S. Sherrington On the regulation of the blood supply of the brain J. Physiol. (Lond.) 11 1890 85 108
62. S.S. Kety, and C.F. Schmidt Nitrous oxide method for the quantitative determination of cerebral blood flow in man: theory, procedure, and normal values J. Clin. Invest. 27 1948 475 483
63. L. Sokoloff The metabolism of the central nervous system in vivo J. Field H.W. Magoun V.E. Hall Handbook of physiology-neurophysiology 1960 American Physiological Society Washington (DC) 1843 1864
64. L. Sokoloff Relationships among local functional activity, energy metabolism, and blood flow in the central nervous system Fed. Proc. 40 8 1981 2311 2316
65. L. Sokoloff, M. Reivich, C. Kennedy, M.H. DesRosiers, C.S. Patlak, and K.D. Pettigrew The [C14]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure and normal values in the conscious and anesthetized albino rat J. Neurochem. 28 1977 897 916
66. L. Sokoloff Relation between physiological function and energy metabolism in the central nervous system [34 refs] J. Neurochem. 29 1 1977 13 26
67. H.G. Wolff The cerebral blood vessels: anatomical principles The circulation of the brain and spinal cord 1938 Williams and Wilkins Baltimore 29 67
68. R. Lorente de Nó Ein Beitrag zur Kenntnis der Gefaessverteilung in der Hirnrinde J. Psychol. Neurol. 35 1928 19 31
69. H.S. Dunning, and H.G. Wolff The relative vascularity of various parts of the central and peripheral nervous system of the cat and its relation to function J. Comp. Neurol. 67 1937 433 450
70. E.H. Craigie The architecture of the cerebral capillary bed Biol. Rev. 20 1945 133 146
71. E.H. Craigie The vascularity of the cerebral cortex of the albino rat J. Comp. Neurol. 33 1921 193 212
72. H.M. Duvernoy, S. Delon, and J.L. Vannson Cortical blood vessels of the human brain Brain Res. Bull. 7 5 1981 519 579
73. K. Brodmann Beitrage zur histologischen Lokalisation der Grosshirnride. IIIte Mitteilung: Die Rinderfelder der Niederen Affen J. Psychol. Neurol. 4 1905 177 226
74. A. Schuz, and G. Palm Density of neurons and synapses in the cerebral cortex of the mouse J. Comp. Neurol. 286 4 1989 442 455
75. J. O'Kusky, and M. Colonnier A laminar analysis of the number of neurons, glia, and synapses in the adult cortex (area 17) of adult macaque monkeys J. Comp. Neurol. 210 3 1982 278 290
76. D. Zheng, A.-S. LaMantia, and D. Purves Specialized vascularization of the primate visual cortex J. Neurosci. 11 1991 2622 2629
77. M.T.T. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry Brain Res. 171 1979 11 28
78. J.C. Horton, and D.H. Hubel Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey Nature 292 1981 762 764
79. S.B. Cox, T.A. Woolsey, and C.M. Rovainen Localized dynamic changes in cortical blood flow with whisker stimulation corresponds to matched vascular and neuronal architecture of rat barrels J. Cereb. Blood Flow Metab. 13 6 1993 899 913
80. T.A. Woolsey, C.M. Rovainen, S.B. Cox, M.H. Henegar, G.E. Liang, and D. Liu Neuronal units linked to microvascular modules in cerebral cortex: response elements for imaging the brain [Review, 126 refs] Cereb. Cortex 6 5 1996 647 660
81. R.V. Harrison, N. Harel, J. Panesar, and R.J. Mount Blood capillary distribution correlates with hemodynamic-based functional imaging in cerebral cortex Cereb. Cortex 12 3 2002 225 233 [see comments]
82. A. Grinvald, E. Lieke, R.D. Frostig, C.D. Gilbert, and T.N. Wiesel Functional architecture of cortex revealed by optical imaging of intrinsic signals Nature 324 6095 1986 361 364
83. T. Bonhoeffer, and A. Grinvald Optical imaging based on intrinsic signals A.W. Toga J.C. Mazziotta Brain mapping, the methods 1996 Academic Press New York 55 97
84. BoK Siesjo Brain energy metabolism 1978 John Wiley & Sons New York
85. A. Ames CNS energy metabolism as related to function [258 refs] Brain Res. Brain Res. Rev. 34 1-2 2000 42 68
86. A. Volterra, P.J. Magistretti, and P.G. Haydon The tripartite synapse: glia in synaptic transmission 2002 Oxford University Press Oxford (NY)
87. M. Kadekaro, A.M. Crane, and L. Sokoloff Differential effects of electrical stimulation of sciatic nerve on metabolic activity in spinal cord and dorsal root ganglion in the rat Proc. Natl. Acad. Sci. U. S. A. 82 17 1985 6010 6013
88. M. Kadekaro, W.H. Vance, M.L. Terrell, H.J. Gary, H.M. Eisenberg, and L. Sokoloff Effects of antidromic stimulation of the ventral root on glucose utilization in the ventral horn of the spinal cord in the rat Proc. Natl. Acad. Sci. U. S. A. 84 15 1987 5492 5495
89. R.J. Nudo, and R.B. Masterton Stimulation-induced [14]C2-deoxyglucose labeling of synaptic activity in the central auditory system J. Comp. Neurol. 245 4 1986 553 565
90. M. Jueptner, and C. Weiller Review: does measurement of regional cerebral blood flow reflect synaptic activity? Implications for PET and fMRI [60 refs] Neuroimage 2 1995 148 156
91. D. Attwell, and S.B. Laughlin An energy budget for signaling in the grey matter of the brain [70 refs] J. Cereb. Blood Flow Metab. 21 10 2001 1133 1145
92. D. Attwell, and C. Iadecola The neural basis of functional brain imaging signals [Review, 66 refs] Trends Neurosci. 25 12 2002 621 625
93. J. Li, and C. Iadecola Nitric oxide and adenosine mediate vasodilation during functional activation in cerebellar cortex Neuropharmacology 33 11 1994 1453 1461
94. G. Yang, and C. Iadecola Glutamate microinjections in cerebellar cortex reproduce cerebrovascular effects of parallel fiber stimulation Am. J. Physiol. 271 6 Pt. 2 1996 R1568 R1575
95. F.M. Faraci, and K.R. Breese Nitric oxide mediates vasodilatation in response to activation of N-methyl-d-aspartate receptors in brain Circ. Res. 72 2 1993 476 480
96. A. Fergus, and K.S. Lee Regulation of cerebral microvessels by glutamatergic mechanisms Brain Res. 754 1-2 1997 35 45
97. N.K. Logothetis, H. Merkle, M. Augath, T. Trinath, and K. Ugurbil Ultra-high resolution fMRI in monkeys with implanted RF coils Neuron 35 2 2002 227 242
98. K. Ugurbil, G. Adriany, P. Andersen, W. Chen, R. Gruetter, and X.P. Hu Magnetic resonance studies of brain function and neurochemistry Annu. Rev. Biomed. Eng. 2 2000 633 660
99. K. Ugurbil, G. Adriany, P. Andersen, W. Chen, M. Garwood, and R. Gruetter Ultrahigh field magnetic resonance imaging and spectroscopy Magn. Reson. Imaging 21 10 2003 1263 1281
100. K. Ugurbil, M. Garwood, J. Ellermann, K. Hendrich, R. Hinke, and X. Hu Imaging at high magnetic fields: initial experiences at 4 T Magn. Reson. Q. 9 4 1993 259 277
101. N.K. Logothetis, and B.A. Wandell Interpreting the BOLD signal [Review] Annu. Rev. Physiol. 66 2004 735 769
102. S. Ogawa, T.M. Lee, A.S. Nayak, and P. Glynn Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields Magn. Reson. Med. 14 1 1990 68 78
103. S. Ogawa, T.M. Lee, A.R. Kay, and D.W. Tank Brain magnetic resonance imaging with contrast dependent on blood oxygenation Proc. Natl. Acad. Sci. U. S. A. 87 24 1990 9868 9872
104. P.T. Fox, and M.E. Raichle Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects Proc. Natl. Acad. Sci. U. S. A. 83 4 1986 1140 1144
105. P.T. Fox, M.E. Raichle, M.A. Mintun, and C. Dence Nonoxidative glucose consumption during focal physiologic neural activity Science 241 4864 1988 462 464
106. P.A. Bandettini, E.C. Wong, R.S. Hinks, R.S. Tikofsky, and J.S. Hyde Time course EPI of human brain function during task activation Magn. Reson. Med. 25 2 1992 390 397
107. K.K. Kwong, J.W. Belliveau, D.A. Chesler, I.E. Goldberg, R.M. Weisskoff, and B.P. Poncelet Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation Proc. Natl. Acad. Sci. U. S. A. 89 12 1992 5675 5679
108. S. Ogawa, D.W. Tank, R. Menon, J.M. Ellermann, S.G. Kim, and H. Merkle Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging Proc. Natl. Acad. Sci. U. S. A. 89 13 1992 5951 5955
109. C.T. Moonen, P.A. Bandettini, and A.L. Baert Functional MRI 1999 Springer Verlag Berlin
110. Buxton, R. An introduction to functional magnetic resonance imaging: principles and techniques. Cambridge (UK): Cambridge University Press.
111. P. Jezzard, P.M. Matthews, and S.M. Smith Functional magnetic resonance imaging: an introduction to methods 2002 Oxford University Press Oxford (NY)
112. S.G. Kim, and K. Ugurbil Comparison of blood oxygenation and cerebral blood flow effects in fMRI: estimation of relative oxygen consumption change Magn. Reson. Med. 38 1 1997 59 65
113. N.K. Logothetis On the neural basis of the BOLD fMRI signal Philos. Trans. R. Soc. Lond. Biol. 357 2002 1003 1037
114. N.K. Logothetis The underpinnings of the BOLD functional magnetic resonance imaging signal [Review] J. Neurosci. 23 10 2003 3963 3971
115. N.K. Logothetis, H. Guggenberger, S. Peled, and J. Pauls Functional imaging of the monkey brain Nat. Neurosci. 2 6 1999 555 562
116. N.K. Logothetis, J. Pauls, M. Augath, T. Trinath, and A. Oeltermann Neurophysiological investigation of the basis of the fMRI signal Nature 412 6843 2001 150 157
117. C. Mathiesen, K. Caesar, N. Akgoren, and M. Lauritzen Modification of activity-dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex J. Physiol. 512 Pt. 2 1998 555 566
118. J.A. Saint-Cyr, L.G. Ungerleider, and R. Desimone Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido-nigral complex in the monkey J. Comp. Neurol. 298 2 1990 129 156
119. D.J. Felleman, and D.C. Van Essen Distributed hierarchical processing in the primate cerebral cortex Cereb. Cortex 1 1 1991 1 47
120. W.N. Sloot, and J.B. Gramsbergen Axonal transport of manganese and its relevance to selective neurotoxicity in the rat basal ganglia Brain Res. 19 1-2 1994 124 132
121. A. Takeda, Y. Kodama, S. Ishiwatari, and S. Okada Manganese transport in the neural circuit of rat CNS Brain Res. Bull. 45 2 1998 149 152
122. R.G. Pautler, A.C. Silva, and A.P. Koretsky In vivo neuronal tract tracing using manganese-enhanced magnetic resonance imaging Magn. Reson. Med. 40 5 1998 740 748
123. 2+-induced contrast Magn. Reson. Med. 46 3 2001 424 429
124. K.S. Saleem, J. Pauls, M. Augath, T. Trinath, B.A. Prause, and N.K. Logothetis Magnetic resonance imaging of neuronal connections in the macaque monkey Neuron 34 2002 685 700
125. N.K. Logothetis, J. Pauls, A. Oeltermann, M. Augath, and T. Trinath Studying connectivity with electrical microstimulation & fMRI Soc. Neurosci. Abstr. 27 2001 821