Oxygen Consumption of Cerebral Cortex Fails to Increase during Continued Vibrotactile Stimulation

Fujita, Hitoshi; Kuwabara, Hiroto; Reutens, David C.; Gjedde, Albert

doi:10.1097/00004647-199903000-00004

Cited by 47 publications

(50 citation statements)

References 28 publications

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“…However, the generated functional images suffer from statistical noise, which is attributed to the need for determination of multiple Rapid quantitative measurement of CMRO 2 and CBF N Kudomi et al parameters from a small amount of time-varying data. Cerebral blood flow images, in particular, suffer significantly from noise; precise determination of CBF often requires another PET scan with H 2 15 O injection (Meyer et al, 1987;Ohta et al, 1999;Fujita et al, 1999;Mintun et al, 2002). In contrast, the present approach can generate images of reasonable quality from a single 6-min PET scan.…”

Section: Discussionmentioning

confidence: 93%

“…The quality of the image suffers, however, from statistical noise because of the lack of predictability of the multiple parameters of CBF, CMRO 2 , and the arterial vascular compartment (V 0 ) and the limited acquisition time (Meyer et al, 1987;Ohta et al, 1992). Therefore, this technique has not been generally applied in clinical settings, but has been used primarily for research purposes (Fujita et al, 1999;Vafaee and Gjedde, 2000;Okazawa et al, 2001a, b;Mintun et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

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Rapid Quantitative Measurement of CMRO₂ and CBF by Dual Administration of ¹⁵O-Labeled Oxygen and Water During a Single PET Scan—a Validation Study and Error Analysis in Anesthetized Monkeys

Kudomi

Hayashi

Teramoto

et al. 2005

J Cereb Blood Flow Metab

101

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Cerebral blood flow (CBF) and rate of oxygen metabolism (CMRO 2 ) may be quantified using positron emission tomography (PET) with 15 O-tracers, but the conventional three-step technique requires a relatively long study period, attributed to the need for separate acquisition for each of 15 O 2 , H 2 15 O, and C 15 O tracers, which makes the multiple measurements at different physiologic conditions difficult. In this study, we present a novel, faster technique that provides a pixel-by-pixel calculation of CBF and CMRO 2 from a single PET acquisition with a sequential administration of 15 O 2 and H 2 15 O. Experiments were performed on six anesthetized monkeys to validate this technique. The global CBF, oxygen extraction fraction (OEF), and CMRO 2 obtained by the present technique at rest were not significantly different from those obtained with three-step method. The global OEF (gOEF) also agreed with that determined by simultaneous arterio-sinus blood sampling (gOEF AÀV ) for a physiologically wide range when changing the arterial PaCO 2 (gOEF ¼ 1.03gOEF AÀV þ 0.01, Po0.001). The regional values, as well as the image quality were identical between the present technique and three-step method for CBF, OEF, and CMRO 2 . In addition, a simulation study showed that error sensitivity of the present technique to delay or dispersion of the input function, and the error in the partition coefficient was equivalent to that observed for three-step method. Error sensitivity to cerebral blood volume (CBV) was also identical to that in the three-step and reasonably small, suggesting that a single CBV assessment is sufficient for repeated measures of CBF/CMRO 2 . These results show that this fast technique has an ability for accurate assessment of CBF/CMRO 2 and also allows multiple assessment at different physiologic conditions.

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Section: Discussionmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Rapid Quantitative Measurement of CMRO₂ and CBF by Dual Administration of ¹⁵O-Labeled Oxygen and Water During a Single PET Scan—a Validation Study and Error Analysis in Anesthetized Monkeys

Kudomi

Hayashi

Teramoto

et al. 2005

J Cereb Blood Flow Metab

101

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“…However, two positron emission tomography (PET) studies conducted by Fox et al (4,5) revealed that in humans large, stimulus-induced increases in CBF (Ϸ30% and 50%) were accompanied by only small increases in CMRO 2 (Ϸ5%). Others using PET and functional MRI confirmed these findings (6)(7)(8)(9)(10). The data indicated that, during short-term functional activation, CBF and CMRO 2 are not directly coupled.…”

mentioning

confidence: 78%

Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data

Mintun

Lundstrom

Snyder

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

328

246

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Coupling of cerebral blood flow (CBF) and cerebral metabolic rate for oxygen (CMRO2) in physiologically activated brain states remains the subject of debates. Recently it was suggested that CBF is tightly coupled to oxidative metabolism in a nonlinear fashion. As part of this hypothesis, mathematical models of oxygen delivery to the brain have been described in which disproportionately large increases in CBF are necessary to sustain even small increases in CMRO2 during activation. We have explored the coupling of CBF and oxygen delivery by using two complementary methods. First, a more complex mathematical model was tested that differs from those recently described in that no assumptions were made regarding tissue oxygen level. Second, [ 15 O] water CBF positron emission tomography (PET) studies in nine healthy subjects were conducted during states of visual activation and hypoxia to examine the relationship of CBF and oxygen delivery. In contrast to previous reports, our model showed adequate tissue levels of oxygen could be maintained without the need for increased CBF or oxygen delivery. Similarly, the PET studies demonstrated that the regional increase in CBF during visual activation was not affected by hypoxia. These findings strongly indicate that the increase in CBF associated with physiological activation is regulated by factors other than local requirements in oxygen. It was long assumed that changes in cerebral blood flow (CBF) and in the cerebral metabolic rate of oxygen (CMRO 2 ) are tightly coupled in both resting and active brain states. This assumption resulted from the premises that the brain needs oxygen, that CBF is a main homeostatic factor for oxygen supply regulation, and that oxygen availability should be adjusted to meet tissue needs (1). It is known that the brain needs an abundant supply of oxygen and that, at rest, 80-92% of its ATP comes from oxidative metabolism of glucose. Early studies by Kety and Schmidt (2) and Cohen et al. (3) demonstrated that resting CBF does change with hypoxia and hyperoxia, thereby suggesting that CBF regulates oxygen delivery, although it was noted that blood oxygen levels but not tissue oxygen levels likely triggered these CBF changes (1). Therefore, if the cerebral oxygen supply was closely regulated to match tissue demands, then functional activation, which implies the need for additional ATP and oxygen, should cause a coupled increase in both CBF and CMRO 2 . However, two positron emission tomography (PET) studies conducted by Fox et al. (4,5) revealed that in humans large, stimulus-induced increases in CBF (Ϸ30% and 50%) were accompanied by only small increases in CMRO 2 (Ϸ5%). Others using PET and functional MRI confirmed these findings (6-10). The data indicated that, during short-term functional activation, CBF and CMRO 2 are not directly coupled.Recently, several reports using theoretical models suggested that the apparent uncoupling of CMRO 2 and CBF might actually be a tight nonlinear coupling. Mathematical models of oxygen delivery to the brai...

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“…However, many studies have reported different results concerning the transient mismatch of ΔCMR Glc , CBF and ΔCMR O2 during functional activity (reviewed in Buxton (2010)). The characterization of these changes has been reported in positron emission tomography (PET) (Fox and Raichle, 1986;Fox et al, 1988;Fujita et al, 1999;Marrett and Gjedde, 1997;Vafaee and Gjedde, 2000) and in MR studies (Chen et al, 1993Davis et al, 1998;Hoge et al, 1999;Kim and Ugurbil, 1997;Kim et al, 1999;Lin et al, 2010;Liu et al, 2004;Vafaee et al, 2012;Wey et al, 2011), and their differences have been attributed to different experimental conditions and the brain region examined (Buxton, 2010;Rothman et al, 2003;Gjedde, 2000, 2004;Zhu et al, 2009). Nevertheless, an energy balance calculation suggests that the energy demands during visual activation are largely met through oxidative metabolism at all times (Mangia et al, 2007a).…”

Section: Introductionmentioning

confidence: 99%

Are glutamate and lactate increases ubiquitous to physiological activation? A 1H functional MR spectroscopy study during motor activation in human brain at 7Tesla

Xin²,

et al. 2014

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a b s t r a c t a r t i c l e i n f oRecent studies at high field (7 Tesla) have reported small metabolite changes, in particular lactate and glutamate (below 0.3 μmol/g) during visual stimulation. These studies have been limited to the visual cortex because of its high energy metabolism and good magnetic resonance spectroscopy (MRS) sensitivity using surface coil. The aim of this study was to extend functional MRS (fMRS) to investigate for the first time the metabolite changes during motor activation at 7 T. Small but sustained increases in lactate (0.17 μmol/g ± 0.05 μmol/g, p b 0.001) and glutamate (0.17 μmol/g ± 0.09 μmol/g, p b 0.005) were detected during motor activation followed by a return to the baseline after the end of activation. The present study demonstrates that increases in lactate and glutamate during motor stimulation are small, but similar to those observed during visual stimulation. From the observed glutamate and lactate increase, we inferred that these metabolite changes may be a general manifestation of the increased neuronal activity. In addition, we propose that the measured metabolite concentration increases imply an increase in ΔCMR O2 that is transiently below that of ΔCMR Glc during the first 1 to 2 min of the stimulation.© 2014 Elsevier Inc. All rights reserved. IntroductionFunctional MR spectroscopy (fMRS) provides direct insights into brain metabolism by investigating the metabolic response of the brain to a physiological stimulus. The high spectral resolution and signal-tonoise ratio (SNR) of fMRS at high field (N3 Tesla) improve the accuracy and precision of the quantification of many brain metabolites (Mekle et al., 2009;Tkac et al., 2001Tkac et al., , 2009. In addition to the increased chemical shift dispersion, a high time resolution is of advantage for the characterization of the small transient changes observed. Recent fMRS studies (Lin et al., 2012;Mangia et al., 2007b;Schaller et al., 2013) at high field (7 Tesla) reported small metabolite concentration changes during visual stimulation (around 0.2 μmol/g). In particular, a very small lactate concentration increase between 10 and 23% has been observed. Recently, functional diffusion-weighted MRS has been used to investigate metabolite ADC changes as a potential consequence of micro structural changes during activation (Branzoli et al., 2013).The lactate increase observed during visual stimulation has been suggested to explain the mismatch of cerebral metabolic rate of change for glucose (ΔCMR Glc ) (or cerebral blood flow, CBF) and cerebral metabolic rate of change for oxygen (ΔCMR O2 ) during brain activation. However, many studies have reported different results concerning the transient mismatch of ΔCMR Glc , CBF and ΔCMR O2 during functional activity (reviewed in Buxton (2010)). The characterization of these changes has been reported in positron emission tomography (PET) (Fox and

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Oxygen Consumption of Cerebral Cortex Fails to Increase during Continued Vibrotactile Stimulation

Cited by 47 publications

References 28 publications

Rapid Quantitative Measurement of CMRO₂ and CBF by Dual Administration of ¹⁵O-Labeled Oxygen and Water During a Single PET Scan—a Validation Study and Error Analysis in Anesthetized Monkeys

Rapid Quantitative Measurement of CMRO₂ and CBF by Dual Administration of ¹⁵O-Labeled Oxygen and Water During a Single PET Scan—a Validation Study and Error Analysis in Anesthetized Monkeys

Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data

Are glutamate and lactate increases ubiquitous to physiological activation? A 1H functional MR spectroscopy study during motor activation in human brain at 7Tesla

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Oxygen Consumption of Cerebral Cortex Fails to Increase during Continued Vibrotactile Stimulation

Cited by 47 publications

References 28 publications

Rapid Quantitative Measurement of CMRO2 and CBF by Dual Administration of 15O-Labeled Oxygen and Water During a Single PET Scan—a Validation Study and Error Analysis in Anesthetized Monkeys

Rapid Quantitative Measurement of CMRO2 and CBF by Dual Administration of 15O-Labeled Oxygen and Water During a Single PET Scan—a Validation Study and Error Analysis in Anesthetized Monkeys

Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data

Are glutamate and lactate increases ubiquitous to physiological activation? A 1H functional MR spectroscopy study during motor activation in human brain at 7Tesla

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Product

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Rapid Quantitative Measurement of CMRO₂ and CBF by Dual Administration of ¹⁵O-Labeled Oxygen and Water During a Single PET Scan—a Validation Study and Error Analysis in Anesthetized Monkeys

Rapid Quantitative Measurement of CMRO₂ and CBF by Dual Administration of ¹⁵O-Labeled Oxygen and Water During a Single PET Scan—a Validation Study and Error Analysis in Anesthetized Monkeys