Oxidative neuroenergetics in event-related paradigms

Journal of Neuroscience

Volumn 29, Issue 6, 2009, Pages 1707-1718

  Sanganahalli, Basavaraju G ^a,b   Herman, Peter ^a,b,d   Blumenfeld, Hal ^b   Hyder, Fahmeed ^a,b,c  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Yale University   (United States)

^d SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

fMRI; Glia; Glucose; Glutamate; Mitochondria; Oxygen transport

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BLOOD OXYGENATION; BRAIN BLOOD FLOW; BRAIN BLOOD VOLUME; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; ENERGY CONSUMPTION; EVOKED SOMATOSENSORY RESPONSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; MALE; NERVE CELL; NONHUMAN; OXIDATION; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX;

ANIMALS; BLOOD FLOW VELOCITY; BLOOD VOLUME; ENERGY METABOLISM; EVOKED POTENTIALS; MAGNETIC RESONANCE IMAGING; MALE; NEURONS; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; SOMATOSENSORY CORTEX;

EID: 60849136602     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5549-08.2009     Document Type: Article

References (94)

1. Ances BM (2004) Coupling of changes in cerebral blood flow with neural activity: what must initially dip must come back up. J Cereb Blood Flow Metab 24:1-6.
2. Ances BM, Zarahn E, Greenberg JH, Detre JA (2000) 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 20:921-930.
3. Ances BM, Buerk DG, Greenberg JH, Detre JA (2001) Temporal dynamics of the partial pressure of brain tissue oxygen during functional forepaw stimulation in rats. Neurosci Lett 306:106-110.
4. Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133-1145.
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. *-weighted MR images during somatosensory stimulation of rat. Magn Reson Med 41:469-473.
7. Buracas GT, Boynton GM (2002) Efficient design of event-related fMRI experiments using M-sequences. Neuroimage 16:801-813.
8. Buzsáki G, Kaila K, Raichle M (2007) Inhibition and brain work. Neuron 56:771-783.
9. Caesar K, Hashemi P, Douhou A, Bonvento G, Boutelle MG, Walls AB, Lauritzen M (2008) Glutamate receptor-dependent increments in lactate, glucose and oxygen metabolism evoked in rat cerebellum in vivo. J Physiol 586:1337-1349.
10. Chahboune H, Ment LR, Stewart WB, Ma X, Rothman DL, Hyder F (2007) Neurodevelopment of C57B/L6 mouse brain assessed by in vivo diffusion tensor imaging. NMR Biomed 20:375-382.
11. Chiarelli PA, Bulte DP, Wise R, Gallichan D, Jezzard P (2007) A calibration method for quantitative BOLD fMRI based on hyperoxia. Neuroimage 37:808-820.
12. Davis TL, Kwong KK, Weisskoff RM, Rosen BR (1998) Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc Natl Acad Sci USA 95:1834-1839.
13. Devor A, Dunn AK, Andermann ML, Ulbert I, Boas DA, Dale AM (2003) Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex. Neuron 39:353-359.
14. Dunn AK, Devor A, Dale AM, Boas DA (2005) Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex. Neuroimage 27:279-290.
15. Durduran T, Yu G, Burnett MG, Detre JA, Greenberg JH, Wang J, Zhou C, Yodh AG (2004) Diffuse optical measurement of blood flow, blood oxygenation, and metabolism in a human brain during sensorimotor cortex activation. Opt Lett 29:1766-1768.
16. Englot DJ, Mishra AM, Mansuripur PK, Herman P, Hyder F, Blumenfeld H (2008) Remote effects of focal hippocampal seizures on the rat neocortex. J Neurosci 28:9066-9081.
17. Franceschini MA, Nissilä I, Wu W, Diamond SG, Bonmassar G, Boas DA (2008) Coupling between somatosensory evoked potentials and hemodynamic response in the rat. Neuroimage 41:189-203.
18. Friston KJ, Fletcher P, Josephs O, Holmes A, Rugg MD, Turner R (1998) Event-related fMRI: characterizing differential responses. Neuroimage 7:30-40.
19. Glover GH (1999) Deconvolution of impulse response in event-related BOLD fMRI. Neuroimage 9:416-429.
20. Goense JB, Logothetis NK (2008) Neurophysiologyofthe BOLD fMRI signal in awake monkeys. Curr Biol 18:631-640.
21. 2 on cerebral blood volume, blood flow, and vascular mean transit time. Stroke 5:630-639.
22. Harel N, Lee SP, Nagaoka T, Kim DS, Kim SG (2002) Origin of negative blood oxygenation level-dependent fMRI signals. J Cereb Blood Flow Metab 22:908-917.
23. Hellweg FC, Schultz W, Creutzfeldt OD (1977) Extracellular and intracellular recordings from cat's cortical whisker projection area: thalamocortical response transformation. J Neurophysiol 40:463-479.
24. Herman P, Trübel HK, Hyder F (2006) A multiparametric assessment of oxygen efflux from the brain. J Cereb Blood Flow Metab 26:79-91.
25. Herman P, Sanganahalli BG, Hyder F (2009a) Multimodal measurements ofblood plasma and red blood cell volumes during functional brain activation. J Cereb Blood Flow Metab 29:19-24.
26. Herman P, Sanganahalli BG, Blumenfeld H, Hyder F (2009b) Cerebral oxygen demand for short-lived and steady-state events. J Neurochem, in press.
27. Hoge RD, Pike GB (2001) Oxidative metabolism and the detection of neuronal activation via imaging. J Chem Neuroanat 22:43-52.
28. Hoge RD, Atkinson J, Gill B, Crelier GR, Marrett S, Pike GB (1999) Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. Proc Natl Acad Sci USA 96:9403-9408.
29. Hu X, Le TH, Ugurbil K (1997) Evaluation of the early response in fMRI in individual subjects using short stimulus duration. Magn Reson Med 37:877-884.
30. Huppert TJ, Allen MS, Benav H, Jones PB, Boas DA (2007) A multicom-partment vascular model for inferring baseline and functional changes in cerebral oxygen metabolism and arterial dilation. J Cereb Blood Flow Metab 27:1262-1279.
31. Huttunen JK, Grohn O, Penttonen M (2008) Coupling between simultaneously recorded BOLD response and neuronal activity in the rat somatosensory cortex. Neuroimage 39:775-785.
32. Hyder F, Rothman DL, Blamire AM (1995) Image reconstruction of sequentially sampled echo-planar data. Magn Reson Imaging 13:97-103.
33. Hyder F, Shulman RG, Rothman DL (1998) A model for the regulation of cerebral oxygen delivery. J Appl Physiol 85:554-564.
34. Hyder F, KidaI, BeharKL, KennanRP, Maciejewski PK, Rothman DL (2001) Quantitative functional imaging of the brain: towards mapping neuronal activity by BOLD fMRI. NMR Biomed 14:413-431.
35. Hyder F, Rothman DL, Shulman RG (2002) Total neuroenergetics support localized brain activity: implications for the interpretation of fMRI. Proc Natl Acad Sci USA 99:10771-10776.
36. Hyder F, Patel AB, Gjedde A, Rothman DL, Behar KL, Shulman RG (2006) Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. J Cereb Blood Flow Metab 26:865-877.
37. Ito H, Ibaraki M, Kanno I, Fukuda H, Miura S (2005) Changes in cerebral blood flow and cerebral oxygen metabolism during neural activation measured by positron emission tomography: comparison with blood oxygenation level-dependent contrast measured by functional magnetic resonance imaging. J Cereb Blood Flow Metab 25:371-377.
38. Jezzard P, Rauschecker JP, Malonek D (1997) An in vivo model for functional MRI in cat visual cortex. Magn Reson Med 38:699-705.
39. Jin T, Kim SG (2008) Cortical layer-dependent dynamic blood oxygenation, cerebral blood flow and cerebral blood volume responses during visual stimulation. Neuroimage 43:1-9.
40. Jones M, Berwick J, Johnston D, Mayhew J (2001) Concurrent optical imaging spectroscopy and laser-Doppler flowmetry: the relationship between blood flow, oxygenation, and volume in rodent barrel cortex. Neuroimage 13:1002-1015.
41. Kastrup A, Krülger G, Neumann-Haefelin T, Glover GH, Moseley ME (2002) Changes of cerebral blood flow, oxygenation, and oxidative metabolism during graded motor activation. Neuroimage 15:74-82.
42. Kida I, Hyder F (2006) Physiology of functional magnetic resonance imaging: energetics and function. Methods Mol Med 124:175-195.
43. O2 mapping in rat cortex: a multiparametric approach to calibration of BOLD image contrast at 7 Tesla. J Cereb Blood Flow Metab 20:847-860.
44. Kida I, Maciejewski PK, Hyder F (2004) Dynamic imaging of perfusion and oxygenation by functional magnetic resonance imaging. J Cereb Blood Flow Metab 24:1369-1381.
45. Kida I, Smith AJ, Blumenfeld H, Behar KL, Hyder F (2006) Lamotrigine suppresses neurophysiological responses to somatosensory stimulation in the rodent. Neuroimage 29:216-224.
46. Kida I, Rothman DL, Hyder F (2007) Dynamics of changes in blood flow, volume, and oxygenation: implications for dynamic functional magnetic resonance imaging calibration. J Cereb Blood Flow Metab 27:690-696.
47. Kim DS, Duong TQ, Kim SG (2000) High-resolution mapping of iso-orientation columns by fMRI. Nat Neurosci 3:164-169.
48. Ku H (1966) Notes on the use of propagation of error formulas. J Res Natl Bur Stand C Eng Instrum 70C:263-273.
49. Kudomi N, Watabe H, Hayashi T, Iida H (2007) Separation of input function for rapid measurement of quantitative CMRO2 and CBF in a single PET scan with a dual tracer administration method. Phys Med Biol 52:1893-1908.
50. Lindauer U, Royl G, Leithner C, Kühl M, Gold L, Gethmann J, Kohl-Bareis M, Villringer A, Dirnagl U (2001) No evidence for early decrease in blood oxygenation in rat whisker cortex in response to functional activation. Neuroimage 13:988-1001.
51. Liu ZM, Schmidt KF, Sicard KM, Duong TQ (2004) Imaging oxygen consumption in forepaw somatosensory stimulation in rats under isoflurane anesthesia. Magn Reson Med 52:277-285.
52. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150-157.
53. Lu H, van Zijl PC (2005) Experimental measurement of extravascular parenchymal BOLD effects and tissue oxygen extraction fractions using multi-echo VASO fMRI at 1.5 and 3.0 T. Magn Reson Med 53:808-816.
54. Lu H, Scholl CA, Zuo Y, Stein EA, Yang Y (2007) Quantifying the blood oxygenation level dependent effect in cerebral blood volume-weighted functional MRI at 9.4T. Magn Reson Med 58:616-621.
55. Maandag NJ, Coman D, Sanganahalli BG, Herman P, Smith AJ, Blumenfeld H, Shulman RG, Hyder F (2007) Energetics of neuronal signaling and fMRI activity. Proc Natl Acad Sci USA 104:20546-20551.
56. Madsen M (1992) A simplified formulation of the gamma variate function. Phys Med Biol 37:1597-1600.
57. 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.
58. Martin C, Martindale J, Berwick J, Mayhew J (2006) Investigating neural- hemodynamic coupling and the hemodynamic response function in the awake rat. Neuroimage 32:33-48.
59. Martindale J, Mayhew J, Berwick J, Jones M, Martin C, Johnston D, Redgrave P, Zheng Y (2003) The hemodynamic impulse response to a single neural event. J Cereb Blood Flow Metab 23:546-555.
60. Martindale J, BerwickJ, Martin C, Kong Y, Zheng Y, MayhewJ (2005) Long duration stimuli and nonlinearities in the neural- haemodynamic coupling. J Cereb Blood Flow Metab 25:651-661.
61. Masamoto K, Kim T, Fukuda M, Wang P, Kim SG (2007) Relationship between neural, vascular, and BOLD signals inisoflurane-anesthetized rat somatosensory cortex. Cereb Cortex 17:942-950.
62. Mathiesen C, Caesar K, Lauritzen M (2000) Temporal coupling between neuronal activity and blood flow in rat cerebellar cortex as indicated by field potential analysis. J Physiol 523:235-246.
63. Matsuura T, Kanno I (2001) Quantitative and temporal relationship between local cerebral blood flow and neuronal activation induced by somatosensory stimulation in rats. Neurosci Res 40:281-290.
64. Mayhew J, Johnston D, Martindale J, Jones M, Berwick J, Zheng Y (2001) Increased oxygen consumption following activation of brain: theoretical footnotes using spectroscopic data from barrel cortex. Neuroimage 13:975-987.
65. Menon RS, Ogawa S, Hu X, Strupp JP, Anderson P, Uǧurbil K (1995) 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 33:453-459.
66. Miller KL, Luh WM, Liu TT, Martinez A, Obata T, Wong EC, Frank LR, Buxton RB (2001) Nonlinear temporal dynamics of the cerebral blood flow response. Hum Brain Mapp 13:1-12.
67. Nemoto M, Sheth S, Guiou M, Pouratian N, Chen JW, Toga AW (2004) Functional signal- and paradigm-dependent linear relationships between synaptic activity and hemodynamic responses in rat somatosensory cortex. J Neurosci 24:3850-3861.
68. Norup Nielsen A, Lauritzen M (2001) Coupling and uncoupling of activity-dependent increases of neuronal activity and blood flow in rat somatosensory cortex. J Physiol 533:773-785.
69. Ogawa S, Lee TM, Barrere B (1993) The sensitivity of magnetic resonance image signals of a rat brain to changes in the cerebral venous blood oxygenation. Magn Reson Med 29:205-210.
70. Pfeuffer J, McCullough JC, Van de Moortele PF, Ugurbil K, Hu X (2003) Spatial dependence of the nonlinear BOLD response at short stimulus duration. Neuroimage 18:990-1000.
71. Riera JJ, Schousboe A, Waagepetersen HS, Howarth C, Hyder F (2008) The micro-architecture of the cerebral cortex: functional neuroimaging models and metabolism. Neuroimage 40:1436-1459.
72. Rothman DL, Sibson NR, Hyder F, Shen J, Behar KL, Shulman RG (1999) In vivo nuclear magnetic resonance spectroscopy studies of the relationship between the glutamate-glutamine neurotransmitter cycle and functional neuroenergetics. Philos Trans R Soc Lond B Biol Sci 354:1165-1177.
73. Roy CS, Sherrington CS (1890) On the regulation of the blood supply of the brain. J Physiol 11:85-158.17.
74. Sanganahalli BG, Herman P, Hyder F (2008) Frequency-dependent tactile responses in rat brain measured by functional MRI. NMR Biomed 21:410-416.
75. Schridde U, Khubchandani M, Motelow JE, Sanganahalli BG, Hyder F, Blumenfeld H (2008) Negative BOLD with large increases in neuronal activity. Cereb Cortex 18:1814-1827.
76. Schummers J, Yu H, Sur M (2008) Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320:1638-1643.
77. Shen Q, Ren H, Duong TQ (2008) CBF, BOLD, CBV, and CMRO2 fMRl signal temporal dynamics at 500-msec resolution. J Magn Reson Imaging 27:599-606.
78. Sheth S, Nemoto M, Guiou M, Walker M, Pouratian N, Toga AW (2003) Evaluation of coupling between optical intrinsic signals and neuronal activity in rat somatosensory cortex. Neuroimage 19:884-894.
79. Sheth SA, Nemoto M, Guiou M, Walker M, Pouratian N, Toga AW (2004) Linear and nonlinear relationships between neuronal activity, oxygen metabolism, and hemodynamic responses. Neuron 42:347-355.
80. Shulman RG, Hyder F, Rothman DL (2002) Biophysical basis of brain activity: implications for neuroimaging. Q Rev Biophys 35:287-325.
81. Shulman RG, Rothman DL, Behar KL, Hyder F (2004) Energetic basis of brain activity: implications for neuroimaging. Trends Neurosci 27:489-495.
82. Silva AC, Lee SP, Iadecola C, Kim SG (2000) Early temporal characteristics of cerebral blood flow and deoxyhemoglobin changes during somatosensory stimulation. J Cereb Blood Flow Metab 20:201-206.
83. Silva AC, Koretsky AP, Duyn JH (2007) Functional MRI impulse response for BOLD and CBV contrast in rat somatosensory cortex. Magn Reson Med 57:1110-1118.
84. Simons DJ (1985) Temporal and spatial integration in the rat SI vibrissa cortex. J Neurophysiol 54:615-635.
85. Smith AJ, Blumenfeld H, Behar KL, Rothman DL, Shulman RG, Hyder F (2002) Cerebral energetics and spiking frequency: the neurophysiological basis of fMRI. Proc Natl Acad Sci USA 99:10765-10770.
86. Soltysik DA, Peck KK, White KD, Crosson B, Briggs RW (2004) Comparison of hemodynamic response nonlinearity across primary cortical areas. Neuroimage 22:1117-1127.
87. Stark E, Abeles M (2007) Predicting movement from multiunit activity. J Neurosci 27:8387-8394.
88. 2+ signaling. Physiology (Bethesda) 23:84-94. Thompson JK, Peterson MR, Freeman RD (2003) Single-neuron activity and tissue oxygenation in the cerebral cortex. Science 299:1070-1072.
89. Trübel HK, Sacolick LI, Hyder F (2006) Regional temperature changes in the brain during somatosensory stimulation. J Cereb Blood Flow Metab 26:68-78.
90. Ureshi M, Matsuura T, Kanno I (2004) Stimulus frequency dependence of the linear relationship between local cerebral blood flow and field potential evoked by activation of rat somatosensory cortex. Neurosci Res 48:147-153.
91. Vafaee MS, Gjedde A (2000) Model of blood-brain transfer of oxygen explains nonlinear flow-metabolism coupling during stimulation of visual cortex. J Cereb Blood Flow Metab 20:747-754.
92. Van Camp N, Verhoye M, Van der Linden A (2006) Stimulation of the rat somatosensory cortex at different frequencies and pulse widths. NMR Biomed 19:10-17.
93. Vazquez AL, Noll DC (1998) Nonlinear aspects of the BOLD response in functional MRI. Neuroimage 7:108-118.
94. 17O NMR approaches for brain study at high field. NMR Biomed 18:83-103.