Oxygen Level and LFP in Task-Positive and Task-Negative Areas: Bridging BOLD fMRI and Electrophysiology

Cerebral Cortex

Volumn 26, Issue 1, 2016, Pages 346-357

  Bentley, William J ^a   Li, Jingfeng M ^a   Snyder, Abraham Z ^a,b   Raichle, Marcus E ^a,b   Snyder, Lawrence H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

default mode network; neurohemodynamic coupling; oxygen polarography; power spectrum; transfer function

Indexed keywords

OXYGEN;

ARTICLE; BOLD SIGNAL; BRAIN BLOOD FLOW; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; BRAIN METABOLISM; CONTROLLED STUDY; DEFAULT MODE NETWORK; ELECTROPHYSIOLOGICAL PROCEDURES; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LOCAL FIELD POTENTIAL; MACACA; NONHUMAN; OXYGEN CONCENTRATION; POLAROGRAPHY; POSTERIOR CINGULATE; PRIORITY JOURNAL; TASK POSITIVE NETWORK; VISUAL AREA V3; VISUAL STIMULATION; ACTION POTENTIAL; ANIMAL; ATTENTION; BRAIN MAPPING; IMAGE PROCESSING; METABOLISM; NERVE CELL; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; VISION; VISUAL CORTEX; VISUAL EVOKED POTENTIAL;

ACTION POTENTIALS; ANIMALS; ATTENTION; BRAIN MAPPING; EVOKED POTENTIALS, VISUAL; IMAGE PROCESSING, COMPUTER-ASSISTED; MACACA; MAGNETIC RESONANCE IMAGING; NEURONS; OXYGEN; PHOTIC STIMULATION; VISUAL CORTEX; VISUAL PERCEPTION;

EID: 84959925888     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu260     Document Type: Article

References (91)

1. Anticevic A, Cole MW, Murray JD, Corlett PR, Wang XJ, Krystal JH. 2012. The role of default network deactivation in cognition and disease. Trends Cogn Sci. 16: 584-592.
2. Bartolo MJ, Gieselmann MA, Vuksanovic V, Hunter D, Sun L, Chen X, Delicato LS, Thiele A. 2011. Stimulus-induced dissociation of neuronal firing rates and local field potential gamma power and its relationship to the resonance blood oxygen level-dependent signal in macaque primary visual cortex. Eur J Neurosci. 34: 1857-1870.
3. Binder JR, Frost JA, Hammeke TA, Bellgowan PS, Rao SM, Cox RW. 1999. Conceptual processing during the conscious resting state. A functional MRI study. J Cogn Neurosci. 11: 80-95.
4. Birn RM. 2012. The role of physiological noise in resting-state functional connectivity. NeuroImage. 62: 864-870.
5. Boynton GM, Engel SA, Glover GH, Heeger DJ. 1996. Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci. 16: 4207-4221.
6. BronkDW, Larrabee MG, DaviesPW. 1946. The rate of oxygen consumption in localized regions of the nervous system: in presynaptic endings and in cell bodies. Fed Proc. 5: 11.
7. Buckner RL, Andrews-Hanna JR, Schacter DL. 2008. The brain's default network: Anatomy, function, and relevance to disease. Ann N Y Acad Sci. 1124: 1-38.
8. Clark LC Jr, Wolf R, Granger D, Taylor Z. 1953. Continuous recording of blood oxygen tensions by polarography. J Appl Physiol. 6: 189-193.
9. Conner CR, Ellmore TM, Pieters TA, DiSano MA, Tandon N. 2011. Variability of the relationship between electrophysiology and BOLD-fMRI across cortical regions in humans. J Neurosci. 31: 12855-12865.
10. DastjerdiM, Foster BL, NasrullahS, RauscheckerAM, Dougherty RF, Townsend JD, Chang CT, Greicius MD, Menon V, Kennedy DP, et al. 2011. Differential electrophysiological response during rest, self-referential, and non-self-referential tasks in human posteromedial cortex. Proc Natl Acad Sci USA. 108: 3023-3028.
11. Davies PW, Brink F. 1942. Microelectrodes for measuring local oxygen tension in animal tissues. Rev Sci Instrum. 13: 524-533.
12. De Martino F, Zimmermann J, Muckli L, Ugurbil K, Yacoub E, Goebel R. 2013. Cortical depth dependent functional responses in humans at 7T: improved specificity with 3D GRASE. PloS One. 8: e60514.
13. Devor A, Tian PF, Nishimura N, Teng IC, Hillman EMC, Narayanan SN, Ulbert I, Boas DA, Kleinfeld D, Dale AM. 2007. Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation leveldependent signal. J Neurosci. 27: 4452-4459.
14. Dosenbach NUF, Visscher KM, Palmer ED, Miezin FM, Wenger KK, Kang HC, Burgund ED, Grimes AL, Schlaggar BL, Petersen SE. 2006. A core system for the implementation of task sets. Neuron. 50: 799-812.
15. Ekstrom A, Suthana N, Millett D, Fried I, Bookheimer S. 2009. Correlation between BOLD fMRI and theta-band local field potentials in the human hippocampal area. J Neurophysiol. 101: 2668-2678.
16. Fatt I. 1976. Polarographic Oxygen Sensors. Cleveland, Ohio: CRC Press.
17. Foster BL, Dastjerdi M, Parvizi J. 2012. Neural populations in human posteromedial cortex display opposing responses during memory and numerical processing. Proc Natl Acad Sci USA. 109: 15514-15519.
18. Foster BL, Parvizi J. 2012. Resting oscillations and cross-frequency coupling in the human posteromedial cortex. NeuroImage. 60: 384-391.
19. Fox MD, Snyder AZ, Barch DM, Gusnard DA, Raichle ME. 2005. Transient BOLD responses at block transitions. NeuroImage. 28: 956-966.
20. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME. 2005. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA. 102: 9673-9678.
21. Friston KJ, Josephs O, Rees G, Turner R. 1998. Nonlinear event-related responses in fMRI. Magn Reson Med. 39: 41-52.
22. Gabbott PL, Rolls ET. 2013. Increased neuronal firing in resting and sleep in areas of the macaque medial prefrontal cortex. Eur J Neurosci. 37: 1737-1746.
23. Goense JB, Logothetis NK. 2008. Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr Biol. 18: 631-640.
24. Greicius MD, KrasnowB, Reiss AL, Menon V. 2003. Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc Natl Acad Sci USA. 100: 253-258.
25. Griffanti L, Salimi-Khorshidi G, Beckmann CF, Auerbach EJ, Douaud G, Sexton CE, Zsoldos E, Ebmeier KP, Filippini N, Mackay CE, et al. 2014. ICA-based artefact removal and accelerated fMRI acquisition for improved resting state network imaging. NeuroImage. 95C: 232-247.
26. Harvey BM, Vansteensel MJ, Ferrier CH, Petridou N, Zuiderbaan W, Aarnoutse EJ, Bleichner MG, Dijkerman HC, van Zandvoort MJ, Leijten FS, et al. 2013. Frequency specific spatial interactions in human electrocorticography: V1 alpha oscillations reflect surround suppression. NeuroImage. 65: 424-432.
27. Hayden BY, Smith DV, Platt ML. 2009. Electrophysiological correlates of default-mode processing inmacaque posterior cingulate cortex. Proc Natl Acad Sci USA. 106: 5948-5953.
28. Haynes J-D, Lotto RB, Rees G. 2004. Responses of human visual cortex to uniform surfaces. Proc Natl Acad Sci. 101: 4286-4291.
29. He BYJ, Snyder AZ, Zempel JM, Smyth MD, Raichle ME. 2008. Electrophysiological correlates of the brain's intrinsic largescale functional architecture. Proc Natl Acad Sci USA. 105: 16039-16044.
30. Heeger DJ, Ress D. 2002. What does fMRI tell us about neuronal activity? Nat Rev Neurosci. 3: 142-151.
31. Hermes D, Miller KJ, Vansteensel MJ, Aarnoutse EJ, Leijten FS, Ramsey NF. 2012. Neurophysiologic correlates of fMRI in human motor cortex. Hum Brain Mapp. 33: 1689-1699.
32. Horiguchi H, Nakadomari S, Misaki M, Wandell BA. 2009. Two temporal channels in human V1 identified using fMRI. NeuroImage. 47: 273-280.
33. Jerbi 2010. Exploring the electrophysiological correlates of the default-mode network with intracerebral EEG. Front Syst Neurosc. 4: 27.
34. Kayser C. 2004. A comparison of hemodynamic and neural responses in cat visual cortex using complex stimuli. Cereb Cortex. 14: 881-891.
35. Kim DS, Duong TQ, Kim SG. 2000. High-resolutionmapping of isoorientation columns by fMRI. Nat Neurosci. 3: 164-169.
36. Kim R, Hyder F, Blumenfeld H. 2014. Physiological basis of BOLD fMRI decreases. In: Zhao M, Ma H, Schwartz TH, editors. Neurovascular Coupling Methods. New York: Springer. p. 221-236.
37. Kim S-G, Bandettini PA. 2011. Principles of BOLD functional MRI. In: Boston, MA: Springer US. p. 293-303.
38. Kim SG, Ogawa S. 2012. Biophysical and physiological origins of blood oxygenation level-dependent fMRI signals. J Cereb Blood Flow Metab. 32: 1188-1206.
39. Kojima T, Onoe H, Hikosaka K, Tsutsui K, Tsukada H, Watanabe M. 2009. Default mode of brain activity demonstrated by positron emission tomography imaging in awake monkeys: higher rest-related than working memory-related activity in medial cortical areas. J Neurosci. 29: 14463-14471.
40. Konishi S, Donaldson DI, Buckner RL. 2001. Transient activation during block transition. NeuroImage. 13: 364-374.
41. Kwong KK, Belliveau JW, Chesler DA, Goldberg IE, Weisskoff RM, Poncelet BP, Kennedy DN, Hoppel BE, Cohen MS, Turner R, et al. 1992. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci USA. 89: 5675-5679.
42. Lauritzen M, Mathiesen C, Schaefer K, Thomsen KJ. 2012. Neuronal inhibition and excitation, and the dichotomic control of brain hemodynamic and oxygen responses. Neuroimage. 62: 1040-1050.
43. Logothetis NK, Guggenberger H, Peled S, Pauls J. 1999. Functional imaging of the monkey brain. Nat Neurosci. 2: 555-562.
44. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. 2001. Neurophysiological investigation of the basis of the fMRI signal. Nature. 412: 150-157.
45. Lowry JP, Griffin K, McHugh SB, Lowe AS, Tricklebank M, Sibson NR. 2010. Real-time electrochemical monitoring of brain tissue oxygen: A surrogate for functional magnetic resonance imaging in rodents. NeuroImage. 52: 549-555.
46. Lu H, Zuo Y, Gu H, Waltz Ja, Zhan W, Scholl Ca, Rea W, Yang Y, Stein Ea. 2007. Synchronized delta oscillations correlate with the resting-state functional MRI signal. Proc Natl Acad Sci USA. 104: 18265-18269.
47. Lustig C, Snyder AZ, Bhakta M, O'Brien KC, McAvoyM, Raichle ME, Morris JC, Buckner RL. 2003. Functional deactivations: change with age and dementia of the Alzheimer type. Proc Natl Acad Sci USA. 100: 14504-14509.
48. Magri C, Schridde U, Murayama Y, Panzeri S, Logothetis NK. 2012. The amplitude and timing of the BOLD signal reflects the relationship between local field potential power at different frequencies. J Neurosci. 32: 1395-1407.
49. Maier A, Wilke M, Aura C, Zhu C, Ye FQ, Leopold Da. 2008. Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey. Nat Neurosci. 11: 1193-1200.
50. Malonek D, Grinvald A. 1996. Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science. 272: 551-554.
51. Mantini D, Corbetta M, Romani GL, Orban GA, VanduffelW. 2013. Evolutionarily novel functional networks in the human brain? J Neurosci. 33: 3259-3275.
52. Mantini D, Gerits A, Nelissen K, Durand JB, Joly O, Simone L, Sawamura H, Wardak C, Orban GA, Buckner RL, et al. 2011. Default mode of brain function in monkeys. J Neurosci. 31: 12954-12962.
53. Masamoto K, Vazquez A, Wang P, Kim S-G. 2008. Trial-by-trial relationship between neural activity, oxygen consumption, and blood flow responses. NeuroImage. 40: 442-450.
54. Mayhew SD, Macintosh BJ, Dirckx SG, Iannetti GD, Wise RG. 2010. Coupling of simultaneously acquired electrophysiological and haemodynamic responses during visual stimulation. Magn Reson Imag. 28: 1066-1077.
55. Mazoyer B, Zago L, Mellet E, Bricogne S, Etard O, Houdé O, Crivello F, Joliot M, Petit L, Tzourio-Mazoyer N. 2001. Cortical networks for working memory and executive functions sustain the conscious resting state in man. Brain Res Bull. 54: 287-298.
56. Menon RS, Ogawa S, Kim SG, Ellermann JM, Merkle H, Tank DW, Ugurbil K. 1992. Functional brain mapping using magnetic resonance imaging. Signal changes accompanying visual stimulation. Invest Radiol. 27 Suppl 2: S47-S53.
57. Mintun MA, Lundstrom BN, Snyder AZ, Vlassenko AG, Shulman GL, Raichle ME. 2001. Blood flowand oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data. Proc Natl Acad Sci. 98: 6859-6864.
58. Mukamel R. 2005. Coupling between neuronal firing, field potentials, and fMRI in human auditory cortex. Science. 309: 951-954.
59. Murayama Y, Biessmann F, Meinecke FC, Muller KR, Augath M, Oeltermann A, Logothetis NK. 2010. Relationship between neural and hemodynamic signals during spontaneous activity studied with temporal kernel CCA. Magn Reson Imag. 28: 1095-1103.
60. Niessing J. 2005. Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science. 309: 948-951.
61. Ogawa S, Lee TM, Kay aR, Tank DW. 1990. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA. 87: 9868-9872.
62. Ogawa S, Lee TM, Nayak AS, Glynn P. 1990. Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields. Magn Reson Med. 14: 68-78.
63. Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, Ugurbil K. 1992. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA. 89: 5951-5955.
64. Ossandon T, Jerbi K, Vidal JR, Bayle DJ, Henaff MA, Jung J, Minotti L, Bertrand O, Kahane P, Lachaux JP. 2011. Transient suppression of broadband gamma power in the defaultmode network is correlated with task complexity and subject performance. J Neurosci. 31: 14521-14530.
65. Pan W-J, Thompson GJ, Magnuson ME, Jaeger D, Keilholz S. 2013. Infraslow LFP correlates to resting-state fMRI BOLD signals. NeuroImage. 74: 288-297.
66. Press WHT, Saul A, Vetterling William T, Flannery Brain P. 2007. Numerical Recipes: The Art of Scientific Computing Third Edition. New York: Cambridge University Press.
67. Raichle ME, MacLeod aM, Snyder aZ, Powers WJ, Gusnard Da, Shulman GL. 2001. A default mode of brain function. Proc Natl Acad Sci USA. 98: 676-682.
68. Ramot M, Fisch L, Harel M, Kipervasser S, Andelman F, Neufeld MY, Kramer U, Fried I, Malach R. 2012. A widely distributed spectral signature of task-negative electrocorticography responses revealed during a visuomotor task in the human cortex. J Neurosci. 32: 10458-10469.
69. Rosa MJ, Kilner J, Blankenburg F, Josephs O, Penny W. 2010. Estimating the transfer function from neuronal activity to BOLD using simultaneous EEG-fMRI. NeuroImage. 49: 1496-1509.
70. Saleem KS, Logothetis NK. 2007. A Combined MRI and Histology Atlas of the Rhesus Monkey Brain in Stereotaxic Coordinates. San Diego: Elsevier/Academic Press.
71. Sambataro F, Murty VP, Callicott JH, Tan H-Y, Das S, Weinberger DR, Mattay VS. 2010. Age-related alterations in default mode network: impact on working memory performance. Neurobiol Aging. 31: 839-852.
72. Scheeringa R, Fries P, Petersson KM, Oostenveld R, Grothe I, Norris DG, Hagoort P, Bastiaansen MC. 2011. Neuronal dynamics underlying high-and low-frequency EEG oscillations contribute independently to the human BOLD signal. Neuron. 69: 572-583.
73. ShmuelA, AugathM, OeltermannA, LogothetisNK. 2006. Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci. 9: 569-577.
74. Shulman GL, Corbetta M, Buckner RL, Fiez JA, Miezin FM, Raichle ME, Petersen SE. 1997. Common blood flow changes across visual tasks: I. Increases in subcortical structures and cerebellum but not in nonvisual cortex. J Cogn Neurosci. 9: 624-647.
75. Shulman GL, Fiez JA, Corbetta M, Buckner RL, Miezin FM, Raichle ME, Petersen SE. 1997. Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J Cogn Neurosci. 9: 648-663.
76. Siero JC, Hermes D, Hoogduin H, Luijten PR, Petridou N, Ramsey NF. 2013. BOLD consistently matches electrophysiology in human sensorimotor cortex at increasing movement rates: A combined 7T fMRI and ECoG study on neurovascular coupling. J Cereb Blood Flow Metab. 33: 1448-1456.
77. Singh KD. 2012. Which "neural activity" do you mean? fMRI, MEG, oscillations and neurotransmitters. NeuroImage. 62: 1121-1130.
78. Sloan HL, Austin VC, Blamire AM, Schnupp JW, Lowe AS, Allers KA, Matthews PM, Sibson NR. 2010. Regional differences in neurovascular coupling in rat brain as determined by fMRI and electrophysiology. NeuroImage. 53: 399-411.
79. Thompson JK. 2005. Separate spatial scales determine neural activity-dependent changes in tissue oxygen within central visual pathways. J Neurosci. 25: 9046-9058.
80. Thompson JK, Peterson MR, Freeman RD. 2004. High-resolution neurometabolic coupling revealed by focal activation of visual neurons. Nat Neurosci. 7: 919-920.
81. Thompson JK, Peterson MR, Freeman RD. 2003. Single-neuron activity and tissue oxygenation in the cerebral cortex. Science. 299: 1070-1072.
82. Thomsen K, Piilgaard H, Gjedde A, Bonvento G, Lauritzen M. 2009. Principal cell spiking, postsynaptic excitation, and oxygen consumption in the rat cerebellar cortex. J Neurophysiol. 102: 1503-1512.
83. Uludag? K. 2008. Transient and sustained BOLD responses to sustained visual stimulation. Magn Reson Imag. 26: 863-869.
84. van den Heuvel MP, Sporns O. 2013. An anatomical substrate for integration among functional networks in human cortex. J Neurosci. 33: 14489-14500.
85. Vanduffel W, Fize D, Mandeville JB, Nelissen K, Van Hecke P, Rosen BR, Tootell RBH, Orban GA. 2001. Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys. Neuron. 32: 565-577.
86. Vincent JL, Patel GH, Fox MD, Snyder AZ, Baker JT, Van Essen DC, Zempel JM, Snyder LH, Corbetta M, Raichle ME. 2007. Intrinsic functional architecture in the anaesthetized monkey brain. Nature. 447: 83-86.
87. Volkow ND, Rosen B, Farde L. 1997. Imaging the living human brain: magnetic resonance imaging and positron emission tomography. Proc Natl Acad Sci USA. 94: 2787-2788.
88. Worsley KJ, Friston KJ. 1995. Analysis of fMRI time-series revisited-again. NeuroImage. 2: 173-181.
89. Wu L, Eichele T, Calhoun VD. 2010. Reactivity of hemodynamic responses and functional connectivity to different states of alpha synchrony: A concurrent EEG-fMRI study. NeuroImage. 52: 1252-1260.
90. Xu J, Moeller S, Auerbach EJ, Strupp J, Smith SM, Feinberg DA, Yacoub E, Ugurbil K. 2013. Evaluation of slice accelerations using multiband echo planar imaging at 3T. NeuroImage. 83: 991-1001.
91. Yarkoni T, Speer NK, Zacks JM. 2008. Neural substrates of narrative comprehension and memory. NeuroImage. 41: 1408-1425.