Physiologic basis for BOLD MR signal changes due to hypoxia/hyperoxia: Separation of blood volume and magnetic susceptibility effects

Kennan, Richard P.; Scanley, B. Ellen; Gore, John C.

doi:10.1002/mrm.1910370621

Cited by 83 publications

(76 citation statements)

References 21 publications

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“…As well as physiologic effects, the increased PO 2 in blood changes the NMR relaxation properties (Kennan et al, 1997;Tadamura et al, 1997). The change in T 2 * is useful for BOLD contrast, although the T 1 and T 2 also change with FiO 2 affecting the computation of flow using the QUIPSS2 sequence.…”

Section: Resultsmentioning

confidence: 99%

Cerebral Perfusion Response to Hyperoxia

Bulte

Chiarelli

Wise

et al. 2006

J Cereb Blood Flow Metab

166

168

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Graded levels of supplemental inspired oxygen were investigated for their viability as a noninvasive method of obtaining intravascular magnetic resonance image contrast. Administered hyperoxia has been shown to be effective as a blood oxygenation level-dependent contrast agent for magnetic resonance imaging (MRI); however, it is known that high levels of inspired fraction of oxygen result in regionally decreased perfusion in the brain potentially confounding the possibility of using hyperoxia as a means of measuring blood flow and volume. Although the effects of hypoxia on blood flow have been extensively studied, the hyperoxic regime between normoxia and 100% inspired oxygen has been only intermittently studied. Subjects were studied at four levels of hyperoxia induced during a single session while perfusion was measured using arterial spin labelling MRI. Reductions in regional perfusion of grey matter were found to occur even at moderate levels of hyperoxia; however, perfusion changes at all oxygen levels were relatively mild (less than 10%) supporting the viability of hyperoxia-induced contrast.

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Section: Resultsmentioning

confidence: 99%

Cerebral Perfusion Response to Hyperoxia

Bulte

Chiarelli

Wise

et al. 2006

J Cereb Blood Flow Metab

166

168

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“…⌬CBF͞CBF (spin labeling) and ⌬S͞S (gradient and spin echo) were measured in an interleaved manner (17) in both conditions I and II. ⌬CBV͞CBV in condition II was measured by introducing an MRI contrast agent (18), whereas in condition I ⌬CBV͞CBV was established from its relation with ⌬CBF͞CBF (10,12,19). The value of Á (0.4 Ϯ 0.1) was determined from a prior calibration obtained by comparison of measured (by 13 C MRS) and predicted (from Eq.…”

Section: Methodsmentioning

confidence: 99%

“…‡ ⌬CBV͞CBV was calculated from (1⌬CBF͞CBF) Ϫ 1, as described in the literature (10,12,19), where the value of has been determined to be Ϸ0.1 in the same rat brain model (12). § ⌬CBV͞CBV was measured using the MRI contrast agent (AMI-227; see Materials and Methods) as described (10,12,18). ¶ ⌬S͞S measured from spin echo (echo time, 40 ms) contrast (12,17) with sequentially sampled echo-planar data (21).…”

Section: Relationship Between Cortical Energy Metabolism and Spiking mentioning

confidence: 99%

Cerebral energetics and spiking frequency: The neurophysiological basis of fMRI

Smith

Blumenfeld

Behar

et al. 2002

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

323

274

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Functional MRI (fMRI) is widely assumed to measure neuronal activity, but no satisfactory mechanism for this linkage has been identified. Here we derived the changes in the energetic component from the blood oxygenation level-dependent (BOLD) fMRI signal and related it to changes in the neuronal spiking frequency in the activated voxels. Extracellular recordings were used to measure changes in cerebral spiking frequency (⌬ ͞ ) of a neuronal ensemble during forepaw stimulation in the ␣-chloralose anesthetized rat. Under the same conditions localized changes in brain energy metabolism (⌬CMR O2͞CMRO2) were obtained from BOLD fMRI data in conjunction with measured changes in cerebral blood flow (⌬CBF͞CBF), cerebral blood volume (⌬CBV͞CBV), and transverse relaxation rates of tissue water (T 2 * and T2) by MRI methods at 7T. On stimulation from two different depths of anesthesia ⌬CMRO2͞CMRO2 Ϸ ⌬ ͞ . Previous 13 C magnetic resonance spectroscopy studies, under similar conditions, had shown that ⌬CMR O2͞CMRO2 was proportional to changes in glutamatergic neurotransmitter flux (⌬Vcyc͞Vcyc). These combined results show that ⌬CMR O2͞CMRO2 Ϸ ⌬Vcyc͞Vcyc Ϸ ⌬ ͞ , thereby relating the energetic basis of brain activity to neuronal spiking frequency and neurotransmitter flux. Because ⌬CMRO2͞CMRO2 had the same high spatial and temporal resolutions of the fMRI signal, these results show how BOLD imaging, when converted to ⌬CMR O2͞CMRO2, responds to localized changes in neuronal spike frequency.R elations between cerebral energy consumption and neuronal activity have been intensely studied since such a coupling was suggested by Roy and Sherrington (1). Sokoloff and coworkers (2) showed that in peripheral neurons increases in energy consumption associated with electrical activity are localized to the neuropil and are approximately proportional to spiking frequency. This proportionality suggested that quantitation of regional brain energy metabolism may provide a direct measure of cortical activity. Nearly all cerebral energy consumption is derived from glucose oxidation (3). 13 C magnetic resonance spectroscopy (MRS) studies have measured the oxidative rate of [1-13 C]glucose use by the flow of the 13 C label into neuronal glutamate pools (4). The subsequent flow of the 13 C label into astrocytic glutamine pools showed that the rates of neuronal oxidative metabolism (CMR O2 ) and glutamate neurotransmitter release͞cycling (V cyc ) are stoichiometrically related (5). The model of glutamate neurotransmitter cycling (6) supported by the 13 C MRS data provides the hypothesis that V cyc , and consequently CMR O2 , should be proportional to spiking frequency of glutamatergic neurons.In this paper we have measured the relationship between energy metabolism and the neuronal spiking frequency in the ␣-chloralose anesthetized rat during forepaw stimulation (7,8). First, ⌬CMR O2 ͞CMR O2 values were derived from multimodal MRI measurements based on the blood oxygenation leveldependent (BOLD) image-contrast as described (9-12). Second, relative sp...

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“…However, this limited the number of subjects included. Finally, we did not compare OCI results with a 'gold standard'-ideally a further study could be performed using steady-state 15 O-labeled PET, which may provide the definitive diagnosis of CCD, and back-to-back Oxygen Challenge MR imaging.…”

Section: Discussionmentioning

confidence: 99%

“…It was first described by Baron et al 1,2 who, using steady-state 15 O-labeled positron emission technology (PET), showed a matched reduction in blood flow and metabolism, and therefore unaffected oxygen extraction fraction (OEF), in the contralesional cerebellar hemisphere of stroke subjects. The incidence of CCD after stroke is B50%.…”

Section: Introductionmentioning

confidence: 99%

Crossed Cerebellar Diaschisis: Insights into Oxygen Challenge MRI

Dani

Santosh

Brennan

et al. 2012

J Cereb Blood Flow Metab

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Hyperoxia during T2∗-weighted magnetic resonance imaging (oxygen challenge imaging (OCI)) causes T2∗-weighted signal change that is dependent on cerebral blood volume (CBV) and oxygen extraction fraction (OEF). Crossed cerebellar diaschisis (CCD), where CBV is reduced but OEF is maintained, may be used to understand the relative contributions of OEF and CBV to OCI results. In subjects with large hemispheric strokes, OCI showed reduced signal change in the contralesional cerebellum ( P = 0.027, n = 12). This was associated with reduced CBV in contralesional cerebellum ( P = 0.039, n = 9). CCD may be a useful model to determine the relative contribution of CBV to signal change measured by OCI.

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Physiologic basis for BOLD MR signal changes due to hypoxia/hyperoxia: Separation of blood volume and magnetic susceptibility effects

Cited by 83 publications

References 21 publications

Cerebral Perfusion Response to Hyperoxia

Cerebral Perfusion Response to Hyperoxia

Cerebral energetics and spiking frequency: The neurophysiological basis of fMRI

Crossed Cerebellar Diaschisis: Insights into Oxygen Challenge MRI

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