Polarographic electrode measures of cerebral tissue oxygenation: implications for functional brain imaging

Sensors

Volumn 8, Issue 12, 2008, Pages 7649-7670

  Bartlett, Kate ^a   Saka, Mohamad ^a   Jones, Myles ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Brain tissue; Neuroimaging; Polarographic oxygen electrode

Indexed keywords

BLOOD OXYGEN LEVEL DEPENDENTS; BRAIN TISSUE; COGNITIVE NEUROSCIENCES; FUNCTIONAL BRAIN IMAGING; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMIC RESPONSE; NEUROIMAGING TECHNIQUES; OXYGEN ELECTRODE;

BLOOD; BRAIN; DATA PROCESSING; FUNCTIONAL NEUROIMAGING; HEMODYNAMICS; MAGNETIC RESONANCE IMAGING; NEUROIMAGING; NEURONS; OXYGENATION; POLAROGRAPHS;

TISSUE;

EID: 58149185323     PISSN: 14248220     EISSN: None     Source Type: Journal    
DOI: 10.3390/s8127649     Document Type: Review

References (91)

1. Clark, L.C.; Misrahy, G.; Fox, R.P. Chronically implanted polarographic electrodes. J. Appl. Physiol. 1958, 13, 85-91.
2. Clark, L.C.; Wolf, R.; Granger, D.; Taylor, Z. Continuous recording of blood oxygen tensions by polarography. J. Appl. Physiol. 1953, 6, 189-193.
3. Gijsbers, K.J.; Melzack, R. Oxygen tension changes evoked in the brain by visual stimulation. Science 1967, 156, 1392-1393.
4. Sick, T.J.; Kreisman, N.R. Local tissue oxygen tension as an index of changes in oxidative metabolism in the bullfrog optic tectum. Brain Res. 1979, 169, 575-579.
5. Travis, R.P., Jr.; Clark, L.C., Jr. Changes in evoked brain oxygen during sensory stimulation and conditioning. Electroencephalogr. Clin. Neurophysiol. 1965, 19, 484-491.
6. Li, B.; Freeman, R.D., High-resolution neurometabolic coupling in the lateral geniculate nucleus. J. Neurosci. 2007, 27, 10223-10229.
7. Thompson, J.K.; Peterson, M.R.; Freeman, R.D. Single-neuron activity and tissue oxygenation in the cerebral cortex. Science 2003, 299, 1070-1072.
8. Thompson, J.K.; Peterson, M.R.; Freeman, R.D. High-resolution neurometabolic coupling revealed by focal activation of visual neurons. Nat. Neurosci. 2004, 7, 919-920.
9. Thompson, J.K.; Peterson, M.R.; Freeman, R.D. Separate spatial scales determine neural activity-dependent changes in tissue oxygen within central visual pathways. J. Neurosci. 2005, 25, 9046-9058.
10. Raichle, M.E.; Herscovitch, P.; Mintun, M.A.; Martin, W.R.; Powers, W. Dynamic measurements of local blood flow and metabolism in the study of higher cortical function in humans with positron emission tomography. Ann. Neurol. 1984, 15, S48-S49.
11. Kwong, K.K.; Belliveau, J.W.; Chesler, D.A.; Goldberg, I.E.; Weisskoff, R.M.; Poncelet, B.P.; Kennedy, D.N.; Hoppel, B.E.; Cohen, M.S.; Turner, R. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc. Natl. Acad. Sci. USA 1992, 89, 5675-5679.
12. Ogawa, S.; Tank, D.W.; Menon, R.; Ellermann, J.M.; Kim, S.G.; Merkle, H.; Ugurbil, K. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc. Natl. Acad. Sci. USA 1992, 89, 5951-5955.
13. Iadecola, C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 2004, 5, 347-360.
14. Zacchigna, S.; Lambrechts, D.; Carmeliet, P. Neurovascular signalling defects in neurodegeneration. Nat. Rev. Neurosci. 2008, 9, 169-181.
15. Rolfe, D.F.; Brown, G.C. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 1997, 77, 731-758.
16. Mintun, M.A.; Raichle, M.E.; Martin, W.R.; Herscovitch, P., Brain oxygen utilization measured with O-15 radiotracers and positron emission tomography. J. Nucl. Med. 1984, 25, 177-187.
17. Kim, S.G.; Richter, W.; Ugurbil, K. Limitations of temporal resolution in functional MRI. Magn. Reson. Med. 1997, 37, 631-636.
18. Thulborn, K.R.; Waterton, J.C.; Matthews, P.M.; Radda, G.K. Oxygenation dependence of the transverse relaxation time of water protons in whole blood at high field. Biochim. Biophys. Acta. 1982, 714, 265-270.
19. Buxton, R.B. Introduction to Functional Magnetic Resonance Imaging: Principles and Techniques. Cambridge University Press: New York, USA, 2001.
20. Hoge, R.D.; Atkinson, J.; Gill, B.; Crelier, G.R.; Marrett, S.; Pike, G.B. Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: the deoxyhemoglobin dilution model. Magn. Reson. Med. 1999, 42, 849-863.
21. Fox, P.T.; Raichle, M.E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl. Acad. Sci. USA 1986, 83, 1140-1144.
22. Raichle, M.E.; Grubb, R.L., Jr.; Gado, M.H.; Eichling, J.O.; Ter-Pogossian, M.M. Correlation between regional cerebral blood flow and oxidative metabolism. In vivo studies in man. Arch. Neurol. 1976, 33, 523-526.
23. Roland, P.E.; Eriksson, L.; Stone-Elander, S.; Widen, L. Does mental activity change the oxidative metabolism of the brain? J. Neurosci. 1987, 7, 2373-2389.
24. Fox, P.T.; Raichle, M.E.; Mintun, M.A.; Dence, C. Nonoxidative glucose consumption during focal physiologic neural activity. Science 1988, 241, 462-464.
25. Vafaee, M.S.; Gjedde, A. Model of blood-brain transfer of oxygen explains nonlinear flowmetabolism coupling during stimulation of visual cortex. J. Cereb. Blood Flow Metab. 2000, 20, 141-154.
26. Vafaee, M.S.; Marrett, S.; Meyer, E.; Evans, A.C.; Gjedde, A. Increased oxygen consumption in human visual cortex: response to visual stimulation. Acta. Neurol. Scand. 1998, 98, 85-89.
27. Vafaee, M.S.; Meyer, E.; Marrett, S.; Paus, T.; Evans, A.C.; Gjedde, A. Frequency-dependent changes in cerebral metabolic rate of oxygen during activation of human visual cortex. J. Cereb. Blood Flow Metab. 1999, 19, 272-277.
28. Calamante, F.; Thomas, D.L.; Pell, G.S.; Wiersma, J.; Turner, R. Measuring cerebral blood flow using magnetic resonance imaging techniques. J. Cereb. Blood Flow Metab. 1999, 19, 701-735.
29. Davis, T.L.; Kwong, K.K.; Weisskoff, R.M.; Rosen, B.R. Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc. Natl. Acad. Sci. USA 1998, 95, 1834-1839.
30. Kim, S.G.; Rostrup, E.; Larsson, H.B.; Ogawa, S.; Paulson, O.B. Determination of relative CMRO2 from CBF and BOLD changes: significant increase of oxygen consumption rate during visual stimulation. Magn. Reson. Med. 1999, 41, 1152-1161.
31. Hoge, R.D.; Atkinson, J.; Gill, B.; Crelier, G.R.; Marrett, S.; Pike, G.B. Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. Proc. Natl. Acad. Sci. USA 1999, 96, 9403-9408.
32. Cohen, L.B. Changes in neuron structure during action potential propagation and synaptic transmission. Physiol. Rev. 1973, 53, 373-418.
33. Grinvald, A.; Lieke, E.; Frostig, R.D.; Gilbert, C.D.; Wiesel, T.N. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 1986, 324, 361-364.
34. Horecker, B. L., the absorption spectra of hemoglobin and itsderivatives in the visible and nearinfra-red regions. J. Biol. Chem. 1943, 148, 173-183.
35. Frostig, R.D.; Lieke, E.E.; Ts'o, D.Y.; Grinvald, A. Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc. Natl. Acad. Sci. USA 1990, 87, 6082-6086.
36. Sheth, S.A.; Nemoto, M.; Guiou, M.; Walker, M.; Pouratian, N.; Hageman, N.; Toga, A.W. Columnar specificity of microvascular oxygenation and volume responses: implications for functional brain mapping. J. Neurosci. 2004, 24, 634-641.
37. Malonek, D.; Grinvald, A. Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science 1996, 272, 551-554.
38. Mayhew, J.; Johnston, D.; Berwick, J.; Jones, M.; Coffey, P.; Zheng, Y. Spectroscopic analysis of neural activity in brain: increased oxygen consumption following activation of barrel cortex. Neuroimage 2000, 12, 664-675.
39. Jones, M.; Berwick, J.; Johnston, D.; Mayhew, J. Concurrent optical imaging spectroscopy and laser-Doppler flowmetry: the relationship between blood flow, oxygenation, and volume in rodent barrel cortex. Neuroimage 2001, 13, 1002-1015.
40. Malonek, D.; Dirnagl, U.; Lindauer, U.; Yamada, K.; Kanno, I.; Grinvald, A. Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc. Natl. Acad. Sci. USA 1997, 94, 14826-14831.
41. Duong, T.Q.; Kim, D.S.; Ugurbil, K.; Kim, S.G. Spatiotemporal dynamics of the BOLD fMRI signals: toward mapping submillimeter cortical columns using the early negative response. Magn. Reson. Med. 2000, 44, 231-242.
42. Kim, D.S.; Duong, T.Q.; Kim, S.G. High-resolution mapping of iso-orientation columns by fMRI. Nat. Neurosci. 2000, 3, 164-169.
43. Logothetis, N.K.; Guggenberger, H.; Peled, S.; Pauls, J. Functional imaging of the monkey brain. Nat. Neurosci. 1999, 2, 555-562.
44. Yacoub, E.; Shmuel, A.; Pfeuffer, J.; Van De Moortele, P.F.; Adriany, G.; Ugurbil, K.; Hu, X. Investigation of the initial dip in fMRI at 7 Tesla. NMR Biomed. 2001, 14, 408-412.
45. Buxton, R.B. The elusive initial dip. Neuroimage 2001, 13, 953-958.
46. Lindauer, U.; Royl, G.; Leithner, C.; Kuhl, M.; Gold, L.; Gethmann, J.; Kohl-Bareis, M.; Villringer, A.; Dirnagl, U. No evidence for early decrease in blood oxygenation in rat whisker cortex in response to functional activation. Neuroimage 2001, 13, 988-1001.
47. Ernst, T.; Hennig, J. Observation of a fast response in functional MR. Magn. Reson. Med. 1994, 32, 146-149.
48. Hu, X.; Le, T.H.; Ugurbil, K. Evaluation of the early response in fMRI in individual subjects using short stimulus duration. Magn. Reson. Med. 1997, 37, 877-884.
49. Menon, R.S.; Ogawa, S.; Hu, X.; Strupp, J.P.; Anderson, P.; Ugurbil, K. BOLD based functional MRI at 4 Tesla includes a capillary bed contribution: echo-planar imaging correlates with previous optical imaging using intrinsic signals. Magn. Reson. Med. 1995, 33, 453-459.
50. Silva, A.C.; Lee, S.P.; Iadecola, C.; Kim, S.G. Early temporal characteristics of cerebral blood flow and deoxyhemoglobin changes during somatosensory stimulation. J. Cereb. Blood Flow Metab. 2000, 20, 201-206.
51. Hathout, G.M.; Varjavand, B.; Gopi, R.K. The early response in fMRI: a modeling approach. Magn. Reson. Med. 1999, 41, 550-554.
52. Devor, A.; Dunn, A.K.; Andermann, M.L.; Ulbert, I.; Boas, D.A.; Dale, A.M. Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex. Neuron 2003, 39, 353-359.
53. Logothetis, N.K. The ins and outs of fMRI signals. Nat. Neurosci. 2007, 10, 1230-1232.
54. Metzger, H.; Erdmann, W.; Thews, G. Effect of short periods of hypoxia, hyperoxia, and hypercapnia on brain O 2 supply. J. Appl. Physiol. 1971, 31, 751-759.
55. Buerk, D. G.; Atochin, D. N.; Riva, C. E., Simultaneous tissue PO02, nitric oxide, and laser Doppler blood flow measurements during neuronal activation of optic nerve. Adv Exp Med Biol 1998, 454, 159-164.
56. Metzger, H. Effects of direct stimulation on cerebral cortex oxygen tension level. Microvasc. Res. 1979, 17, 80-89.
57. Silver, I.A. Cellular microenvironment in relation to local blood flow. Ciba. Found Symp. 1978, 56, 49-67.
58. Lowry, J.P.; Boutelle, M.G.; O'Neill, R.D.; Fillenz, M. Characterization of carbon paste electrodes in vitro for simultaneous amperometric measurement of changes in oxygen and ascorbic acid concentrations in vivo. Analyst 1996, 121, 761-766.
59. Lowry, J.P.; Fillenz, M. Evidence for uncoupling of oxygen and glucose utilization during neuronal activation in rat striatum. J. Physiol. 1997, 498, 497-501.
60. Anees, B.M.; Buerk, D.G.; Greenberg, J.H.; Detre, J.A. Temporal dynamics of the partial pressure of brain tissue oxygen during functional forepaw stimulation in rats. Neurosci. Lett. 2001, 306, 106-110.
61. Masamoto, K.; Omura, T.; Takizawa, N.; Kobayashi, H.; Katura, T.; Maki, A.; Kawaguchi, H.; Tanishita, K., Biphasic changes in tissue partial pressure of oxygen closely related to localized neural activity in guinea pig auditory cortex. J. Cereb. Blood Flow Metab. 2003, 23, 1075-1084.
62. Offenhauser, N.; Thomsen, K.; Caesar, K.; Lauritzen, M. Activity-induced tissue oxygenation changes in rat cerebellar cortex: interplay of postsynaptic activation and blood flow. J. Physiol. 2005, 565, 279-294.
63. Masamoto, K.; Vazquez, A.; Wang, P.; Kim, S.G. Trial-by-trial relationship between neural activity, oxygen consumption, and blood flow responses. Neuroimage 2008, 1, 442-450.
64. Vazquez, A.L.; Masamoto, K.; Kim, S.G. Dynamics of oxygen delivery and consumption during evoked neural stimulation using a compartment model and CBF and tissue P(O2) measurements. Neuroimage 2008, 42, 49-59.
65. Shmuel, A.; Yacoub, E.; Chaimow, D.; Logothetis, N.K.; Ugurbil, K. Spatio-temporal pointspread function of fMRI signal in human gray matter at 7 Tesla. Neuroimage 2007, 35, 539-552.
66. Martindale, J.; Mayhew, J.; Berwick, J.; Jones, M.; Martin, C.; Johnston, D.; Redgrave, P.; Zheng, Y. The hemodynamic impulse response to a single neural event. J. Cereb. Blood Flow Metab. 2003, 23, 546-555.
67. Jones, M.; Hewson-Stoate, N.; Martindale, J.; Redgrave, P.; Mayhew, J. Nonlinear coupling of neural activity and CBF in rodent barrel cortex. Neuroimage 2004, 22, 956-965.
68. Hewson-Stoate, N.; Jones, M.; Martindale, J.; Berwick, J.; Mayhew, J. Further nonlinearities in neurovascular coupling in rodent barrel cortex. Neuroimage 2005, 24, 565-574.
69. Sheth, S.A.; Nemoto, M.; Guiou, M.; Walker, M.; Pouratian, N.; Toga, A.W. Linear and nonlinear relationships between neuronal activity, oxygen metabolism, and hemodynamic responses. Neuron 2004, 42, 347-355.
70. Heckman, G.M.; Bouvier, S.E.; Carr, V.A.; Harley, E.M.; Cardinal, K.S.; Engel, S.A. Nonlinearities in rapid event-related fMRI explained by stimulus scaling. Neuroimage 2007, 34, 651-660.
71. Wan, X.; Riera, J.; Iwata, K.; Takahashi, M.; Wakabayashi, T.; Kawashima, R. The neural basis of the hemodynamic response nonlinearity in human primary visual cortex: Implications for neurovascular coupling mechanism. Neuroimage 2006, 32, 616-625.
72. Martindale, J.; Berwick, J.; Martin, C.; Kong, Y.; Zheng, Y.; Mayhew, J. Long duration stimuli and nonlinearities in the neural-haemodynamic coupling. J. Cereb. Blood Flow Metab. 2005, 25, 651-661.
73. Anees, B.M.; Zarahn, E.; Greenberg, J.H.; Detre, J.A. Coupling of neural activation to blood flow in the somatosensory cortex of rats is time-intensity separable, but not linear. J. Cereb. Blood Flow Metab. 2000, 20, 921-930.
74. Logothetis, N.K.; Wandell, B.A. Interpreting the BOLD signal. Annu. Rev. Physiol. 2004, 66, 735-769.
75. Monosov, I.E.; Trageser, J.C.; Thompson, K.G. Measurements of simultaneously recorded spiking activity and local field potentials suggest that spatial selection emerges in the frontal eye field. Neuron 2008, 57, 614-625.
76. Belitski, A.; Gretton, A.; Magri, C.; Murayama, Y.; Montemurro, M.A.; Logothetis, N.K.; Panzeri, S. Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information. J. Neurosci. 2008, 28, 5696-5709.
77. Viswanathan, A.; Freeman, R.D. Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity. Nat. Neurosci. 2007, 10, 1308-1312.
78. Nir, Y.; Dinstein, I.; Malach, R.; Heeger, D.J. BOLD and spiking activity. Nat. Neurosci. 2008, 11, 523-524.
79. Logothetis, N.K.; Pauls, J.; Augath, M.; Trinath, T.; Oeltermann, A., Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412, 150-157.
80. Goense, J.B.; Logothetis, N.K. Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr. Biol. 2008, 18, 631-640.
81. Rauch, A.; Rainer, G.; Logothetis, N.K. The effect of a serotonin-induced dissociation between spiking and perisynaptic activity on BOLD functional MRI. Proc. Natl. Acad. Sci. USA 2008, 105, 6759-6764.
82. Caesar, K.; Gold, L.; Lauritzen, M. Context sensitivity of activity-dependent increases in cerebral blood flow. Proc. Natl. Acad. Sci. USA 2003, 100, 4239-4244.
83. Lund, J.S. Anatomical organization of macaque monkey striate visual cortex. Annu. Rev. Neurosci. 1988, 11, 253-288.
84. Alonso Bde, C.; Lowe, A.S.; Dear, J.P.; Lee, K.C.; Williams, S.C.; Finnerty, G.T. Sensory inputs from whisking movements modify cortical whisker maps visualized with functional magnetic resonance imaging. Cereb. Cortex. 2008, 18, 1314-1325.
85. Feng, Z.C.; Roberts, E.L., Jr.; Sick, T.J.; Rosenthal, M. Depth profile of local oxygen tension and blood flow in rat cerebral cortex, white matter and hippocampus. Brain Res. 1988, 445, 280-288.
86. Metzger, H.; Heuber, S. Local oxygen tension and spike activity of the cerebral grey matter of the rat and its response to short intervals of O2 deficiency or CO2 excess. Pflugers Arch. 1977, 370, 201-209.
87. LaManna, J.C.; McCracken, K.A.; Patil, M.; Prohaska, O.J. Stimulus-activated changes in brain tissue temperature in the anesthetized rat. Metab. Brain Dis. 1989, 4, 225-237.
88. Lecoq, J.; Tiret, P.; Charpak, S. Analysis of the spatio-temporal relationship between neuronal activity, local blood flow and oxygen partial pressure in the rat olfactory bulb. SFN Conf., San Diego, Nov. 3-7, 2007; 301, p.10.
89. Woolsey, T.A.; Van der Loos, H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 1970, 17, 205-242.
90. Li, J.; Gilmour, G.; Bannerman, D.; De Flippi, G.; Mchugh, S.; Lowry, J. P.; Tricklebank, M. Establishing a controlled whisker-barrel evoked potential model of neural activation to be used in combination with real-time oxygen voltammetry in the anaesthetised rat. SFN Conf., San Diego, Nov. 3-7, 2007; 401, p. 27.
91. Friston, K. Neurophysiology: the brain at work. Curr. Biol. 2008, 18, R418-R420.