Time-dependent effects of hyperoxia on the BOLD fMRI signal in primate visual cortex and LGN

NeuroImage

Volumn 35, Issue 3, 2007, Pages 1044-1063

  Wibral, Michael ^a,b   Muckli, Lars ^a,b   Melnikovic, Katharina ^a,b   Scheller, Bertram ^c   Alink, Arjen ^a,b   Singer, Wolf ^a,b   Munk, Matthias H ^a,b  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b Brain Imaging Center Frankfurt   (Germany)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

Anaesthetized; BOLD; Deoxyhemoglobin dilution model; fMRI; Hyperoxia

Indexed keywords

CARBON DIOXIDE; CONTRAST MEDIUM; DEOXYHEMOGLOBIN; MONOCRYSTALLINE IRON OXIDE NANOPARTICLE; OXYGEN;

ANESTHESIA; ANIMAL EXPERIMENT; ARTICLE; BLOOD OXYGEN LEVEL DEPENDENT; BLOOD OXYGENATION; BLOOD VESSEL REACTIVITY; BODY TEMPERATURE; BRAIN BLOOD FLOW; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HYPEROXIA; LATERAL GENICULATE NUCLEUS; MALE; MONKEY; NEUROIMAGING; NONHUMAN; PRIMATE; PRIORITY JOURNAL; TIME; VISUAL CORTEX; VISUAL STIMULATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; EVOKED POTENTIALS, VISUAL; GENICULATE BODIES; HYPEROXIA; MACACA; MAGNETIC RESONANCE IMAGING; OXYGEN; OXYGEN CONSUMPTION; PHOTIC STIMULATION; TIME FACTORS; VISUAL CORTEX;

EID: 33947725294     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2006.12.039     Document Type: Article

References (68)

1. Adachi Y.U., Watanabe K., Higuchi H., Satoh T., and Vizi E.S. Oxygen inhalation enhances striatal dopamine metabolism and monoamineoxidase enzyme inhibition prevents it: a microdialysis study. Eur. J. Pharmacol. 422 (2001) 61-68
2. Aghakhani Y., Kobayashi E., Bagshaw A.P., Hawco C., Benar C.G., Dubeau F., and Gotman J. Cortical and thalamic fMRI responses in partial epilepsy with focal and bilateral synchronous spikes. Clin. Neurophysiol. 117 (2006) 177-191
3. Atochin D.N., Demchenko I.T., Astern J., Boso A.E., Piantadosi C.A., and Huang P.L. Contributions of endothelial and neuronal nitric oxide synthases to cerebrovascular responses to hyperoxia. J. Cereb. Blood Flow Metab. 23 (2003) 1219-1226
4. Bickford P.C., Chadman K., Williams B., Shukitt-Hale B., Holmes D., Taglialatela G., and Joseph J. Effect of normobaric hyperoxia on two indexes of synaptic function in Fisher 344 rats. Free Radical Biol. Med. 26 (1999) 817-824
5. Boakye M., Krauss B.R., Huckins S.C., Zhang L., Szeverenyi N.M., and Hodge Jr. C.J. Effects of hyperoxia on human sensorimotor cortex activity produced by electrical stimulation of the median nerve: a functional magnetic resonance imaging study. Neurosci. Lett. 321 (2002) 5-8
6. Boxerman J.L., Bandettini P.A., Kwong K.K., Baker J.R., Davis T.L., Rosen B.R., and Weisskoff R.M. The intravascular contribution to fMRI signal change: Monte Carlo modeling and diffusion-weighted studies in vivo. Magn. Reson. Med. 34 (1995) 4-10
7. Boynton G.M., Engel S.A., Glover G.H., and Heeger D.J. Linear systems analysis of functional magnetic resonance imaging in human V1. J. Neurosci. 16 (1996) 4207-4221
8. 2 during neuronal activity. In: Tomita M., Kanno I., and Hamel E. (Eds). Brain Activation and CBF Control (2002), Elsevier Science, The Netherlands 23-32
9. Carvalho C.R., Paula Pinto S.G., Maranhao B., and Bethlem E.P. Hyperoxia and lung disease. Curr. Opin. Pulm. Med. 4 (1998) 300-304
10. Chino Y.M., Kaas J.H., Smith III E.L., Langston A.L., and Cheng H. Rapid reorganization of cortical maps in adult cats following restricted deafferentation in retina. Vision Res. 32 (1992) 789-796
11. Christiansen J., Douglas C.G., and Haldane J.S. The absorption and dissociation of carbon dioxide by human blood. J. Physiol. 48 (1914) 244-271
12. Cohen E.R., Ugurbil K., and Kim S.G. Effect of basal conditions on the magnitude and dynamics of the blood oxygenation level-dependent fMRI response. J. Cereb. Blood Flow Metab. 22 (2002) 1042-1053
13. Davis T.L., Kwong K.K., Weisskoff R.M., and Rosen B.R. Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 1834-1839
14. Demchenko I.T., and Piantadosi C.A. Nitric oxide amplifies the excitatory to inhibitory neurotransmitter imbalance accelerating oxygen seizures. Undersea Hyperbaric Med. 33 (2006) 169-174
15. Demchenko I.T., Luchakov Y.I., Moskvin A.N., Gutsaeva D.R., Allen B.W., Thalmann E.D., and Piantadosi C.A. Cerebral blood flow and brain oxygenation in rats breathing oxygen under pressure. J. Cereb. Blood Flow Metab. 25 (2005) 1288-1300
16. Devor A., Ulbert I., Dunn A.K., Narayanan S.N., Jones S.R., Andermann M.L., Boas D.A., and Dale A.M. Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 3822-3827
17. Dirnagl U., Lindauer U., and Villringer A. Role of nitric oxide in the coupling of cerebral blood flow to neuronal activation in rats. Neurosci. Lett. 149 (1993) 43-46
18. Douglas R.J., Koch C., Mahowald M., Martin K.A., and Suarez H.H. Recurrent excitation in neocortical circuits. Science 269 (1995) 981-985
19. Duong T.Q., Iadecola C., and Kim S.G. Effect of hyperoxia, hypercapnia, and hypoxia on cerebral interstitial oxygen tension and cerebral blood flow. Magn. Reson. Med. 45 (2001) 61-70
20. Eysel U.T., Gonzalez-Aguilar F., and Mayer U. Time-dependent decrease in the extent of visual deafferentation in the lateral geniculate nucleus of adult cats with small retinal lesions. Exp. Brain Res. 41 (1981) 256-263
21. Floyd T.F., Clark J.M., Gelfand R., Detre J.A., Ratcliffe S., Guvakov D., Lambertsen C.J., and Eckenhoff R.G. Independent cerebral vasoconstrictive effects of hyperoxia and accompanying arterial hypocapnia at 1 ATA. J. Appl. Physiol. 95 (2003) 2453-2461
22. Formisano E., Esposito F., Di Salle F., and Goebel R. Cortex-based independent component analysis of fMRI time series. Magn. Reson. Imaging 22 (2004) 1493-1504
23. Fox P.T., and Raichle M.E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl. Acad. Sci. U. S. A. 83 (1986) 1140-1144
24. Govindaiah G., and Cox C.L. Depression of retinogeniculate synaptic transmission by presynaptic D-2-like dopamine receptors in rat lateral geniculate nucleus. Eur. J. Neurosci. 23 (2006) 423-434
25. 2 on cerebral blood volume, blood flow, and vascular mean transit time. Stroke 5 (1974) 630-639
26. Gutsche B.B., and Stephen C.R. Responses of dogs to hyperoxic-, pentylenetetrazol-, and electroshock-induced convulsions. J. Appl. Physiol. 22 (1967) 321-326
27. Harrison N.L., and Sear W.S. Intravenous anaesthetics-Barbiturates, etomidate, propofol, ketamine, and steroids. In: Evers A.S., and Maze M. (Eds). Anesthetic Pharmacology: Physiologic Principles and Clinical Practice (2003), Churchill Livingston, Philadelphia, PA 395-416
28. Hendrich K.S., Kochanek P.M., Melick J.A., Schiding J.K., Statler K.D., Williams D.S., Marion D.W., and Ho C. Cerebral perfusion during anesthesia with fentanyl, isoflurane, or pentobarbital in normal rats studied by arterial spin-labeled MRI. Magn. Reson. Med. 46 (2001) 202-206
29. A receptor-mediated inhibition. Eur. J. Neurosci. 21 (2005) 93-102
30. Hoge R.D., Atkinson J., Gill B., Crelier G.R., Marrett S., and Pike G.B. Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: the deoxyhemoglobin dilution model. Magn. Reson. Med. 42 (1999) 849-863
31. Hoge R.D., Atkinson J., Gill B., Crelier G.R., Marrett S., and Pike G.B. Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 9403-9408
32. Huang Y.C., Caminiti S.P., Fawcett T.A., Moon R.E., Fracica P.J., Miller F.J., Young S.L., and Piantadosi C.A. Natural surfactant and hyperoxic lung injury in primates: I. Physiology and biochemistry. J. Appl. Physiol. 76 (1994) 991-1001
33. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev., Neurosci. 5 (2004) 347-360
34. 2 transport. Acta Physiol. Scand. 182 (2004) 215-227
35. Kalisch R., Elbel G.K., Gossl C., Czisch M., and Auer D.P. Blood pressure changes induced by arterial blood withdrawal influence bold signal in anesthesized rats at 7 Tesla: implications for pharmacologic MRI. NeuroImage 14 (2001) 891-898
36. Kashikura K., Kershaw J., Kashikura A., Matsuura T., and Kanno I. Hyperoxia-enhanced activation-induced hemodynamic response in human VI: an fMRI study. NeuroReport 11 (2000) 903-906
37. Kashikura K., Kershaw J., Kashikura A., Zhang X.J., Matsuura T., and Kanno I. Hyperoxia modified activation-induced blood oxygenation level-dependent response of human visual cortex (V1): an event-related functional magnetic resonance imaging study. Neurosci. Lett. 299 (2001) 53-56
38. Kety S.S., and Schmidt C.F. The effects of altered arterial tensions of carbon dioxide and oxygen on cerebral blood flow and oxygen consumption of normal young men. J. Clin. Invest. 27 (1948) 487-492
39. Kim D.S., Duong T.Q., and Kim S.G. High-resolution mapping of iso-orientation columns by fMRI. Nat. Neurosci. 3 (2000) 164-169
40. Kolbitsch C., Lorenz I.H., Hormann C., Kremser C., Schocke M., Felber S., Moser P.L., Hinteregger M., Pfeiffer K.P., and Benzer A. Sevoflurane and nitrous oxide increase regional cerebral blood flow (rCBF) and regional cerebral blood volume (rCBV) in a drug-specific manner in human volunteers. Magn. Reson. Imaging 19 (2001) 1253-1260
41. Lee S.P., Duong T.Q., Yang G., Iadecola C., and Kim S.G. Relative changes of cerebral arterial and venous blood volumes during increased cerebral blood flow: implications for BOLD fMRI. Magn. Reson. Med. 45 (2001) 791-800
42. Leite F.P., Tsao D., Vanduffel W., Fize D., Sasaki Y., Wald L.L., Dale A.M., Kwong K.K., Orban G.A., Rosen B.R., Tootell R.B., and Mandeville J.B. Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3 Tesla. NeuroImage 16 (2002) 283-294
43. Lindauer U., Gethmann J., Kuhl M., Kohl-Bareis M., and Dirnagl U. Neuronal activity-induced changes of local cerebral microvascular blood oxygenation in the rat: effect of systemic hyperoxia or hypoxia. Brain Res. 975 (2003) 135-140
44. Logothetis N.K., Guggenberger H., Peled S., and Pauls J. Functional imaging of the monkey brain. Nat. Neurosci. 2 (1999) 555-562
45. Logothetis N.K., Pauls J., Augath M., Trinath T., and Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 412 (2001) 150-157
46. Matsuura T., Kashikura K., and Kanno I. Hemodynamics of local cerebral blood flow induced by somatosensory stimulation under normoxia and hyperoxia in rats. Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 129 (2001) 363-372
47. Matta B.F., Heath K.J., Tipping K., and Summors A.C. Direct cerebral vasodilatory effects of sevoflurane and isoflurane. Anesthesiology 91 (1999) 677-680
48. Mcewan A.I., Smith C., Dyar O., Goodman D., Smith L.R., and Glass P.S. Isoflurane minimum alveolar concentration reduction by fentanyl. Anesthesiology 78 (1993) 864-869
49. McMahon T.J., Moon R.E., Luschinger B.P., Carraway M.S., Stone A.E., Stolp B.W., Gow A.J., Pawloski J.R., Watke P., Singel D.J., Piantadosi C.A., and Stamler J.S. Nitric oxide in the human respiratory cycle. Nat. Med. 8 (2002) 711-717
50. Mialon P., and Barthelemy L. Effect of hyperbaric oxygen on prostaglandin and thromboxane synthesis in the cortex and the striatum of rat brain. Mol. Chem. Neuropathol. 20 (1993) 181-189
51. Niessing J., Ebisch B., Schmidt K.E., Niessing M., Singer W., and Galuske R.A. Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309 (2005) 948-951
52. Ogawa S., Lee T.M., Kay A.R., and Tank D.W. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 9868-9872
53. Omae T., Ibayashi S., Kusuda K., Nakamura H., Yagi H., and Fujishima M. Effects of high atmospheric pressure and oxygen on middle cerebral blood flow velocity in humans measured by transcranial Doppler. Stroke 29 (1998) 94-97
54. Pape H.C., and Mager R. Nitric oxide controls oscillatory activity in thalamocortical neurons. Neuron 9 (1992) 441-448
55. Piantadosi C.A. Physiology of hyperbaric hyperoxia. Respir. Care Clin. N. Am. 5 (1999) 7-19
56. Sato T., Takeda Y., Hagioka S., Zhang S., and Hirakawa M. Changes in nitric oxide production and cerebral blood flow before development of hyperbaric oxygen-induced seizures in rats. Brain Res. 918 (2001) 131-140
57. Sicard K.M., and Duong T.Q. Effects of hypoxia, hyperoxia, and hypercapnia on baseline and stimulus-evoked BOLD, CBF, and CMRO(2) in spontaneously breathing animals. NeuroImage 25 (2005) 850-858
58. Singer W., Tretter F., and Cynader M. Organization of cat striate cortex: a correlation of receptive-field properties with afferent and efferent connections. J. Neurophysiol. 38 (1975) 1080-1098
59. Stamler J.S., Jia L., Eu J.P., McMahon T.J., Demchenko I.T., Bonaventura J., Gernert K., and Piantadosi C.A. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276 (1997) 2034-2037
60. Uludag K. Basic principles of functional MRI. In: Edelman R.R., Hesselink J.R., Zlatkin M.B., and Crues J.V. (Eds). Clinical Magnetic Resonance Imaging (2005), Saunders (W.B.) Co Ltd.
61. Uludag K., Dubowitz D.J., Yoder E.J., Restom K., Liu T.T., and Buxton R.B. Coupling of cerebral blood flow and oxygen consumption during physiological activation and deactivation measured with fMRI. NeuroImage 23 (2004) 148-155
62. Wang W.J., Ho X.P., Yan Y.L., Yan T.H., and Li C.L. Intrasynaptosomal free calcium and nitric oxide metabolism in central nervous system oxygen toxicity. Aviat. Space Environ. Med. 69 (1998) 551-555
63. Wang L., Osborne P.G., Yu X., Shangguan D., Zhao R., Han H.W., and Liu G.Q. Hyperoxia caused by microdialysis perfusion decreased striatal monoamines: involvement of oxidative stress. Neurochem. Int. 42 (2003) 465-470
64. Watson N.A., Beards S.C., Altaf N., Kassner A., and Jackson A. The effect of hyperoxia on cerebral blood flow: a study in healthy volunteers using magnetic resonance phase-contrast angiography. Eur. J. Anaesthesiol. 17 (2000) 152-159
65. Weiskopf N., Mathiak K., Bock S.W., Scharnowski F., Veit R., Grodd W., Goebel R., and Birbaumer N. Principles of a brain-computer interface (BCI) based on real-time functional magnetic resonance imaging (fMRI). IEEE Trans. Biomed. Eng. 51 (2004) 966-970
66. Weiskopf N., Klose U., Birbaumer N., and Mathiak K. Single-shot compensation of image distortions and BOLD contrast optimization using multi-echo EPI for real-time fMRI. NeuroImage 24 (2005) 1068-1079
67. Weissleder R., Elizondo G., Wittenberg J., Rabito C.A., Bengele H.H., and Josephson L. Ultrasmall superparamagnetic iron-oxide-characterization of a new class of contrast agents for MR imaging. Radiology 175 (1990) 489-493
68. Wolf T., Lindauer U., Villringer A., and Dirnagl U. Excessive oxygen or glucose supply does not alter the blood flow response to somatosensory stimulation or spreading depression in rats. Brain Res. 761 (1997) 290-299