Arterial versus Total Blood Volume Changes during Neural Activity-Induced Cerebral Blood Flow Change: Implication for BOLD fMRI

Kim, Tae Il; Hendrich, Kristy; Masamoto, Kazuto; Kim, Seong‐Gi

doi:10.1038/sj.jcbfm.9600429

Cited by 172 publications

(228 citation statements)

References 51 publications

(100 reference statements)

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“…In addition, there were remarkably similar and significant aBV GM -CBF relationships in all three conditions, as evidenced by power law analyses. The relatively high a-values of 0.55 to 0.69 are consistent with the few studies showing significant arterial blood volume responses that correlated with flow increases in rodents during hypercapnia (Lee et al, 2001) and sensory stimulation (Kim et al, 2007;Kim and Kim, 2010). These studies also show that most of the total CBV changes during hypercapnia and visual stimulation arise from the arterial component.…”

Section: Vascular Reactions During Functional Challengessupporting

confidence: 88%

Similarities and Differences in Arterial Responses to Hypercapnia and Visual Stimulation

Petersen

Zimine³

et al. 2010

J Cereb Blood Flow Metab

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Despite the different origins of cerebrovascular activity induced by neurogenic and nonneurogenic conditions, a standard assumption in functional studies is that the consequence on the vascular system will be mechanically similar. Using a recently developed arterial spin labeling method, we examined arterial blood volume, arterial-microvascular transit time, and cerebral blood flow (CBF) in the gray matter and in areas with large arterial vessels under hypercapnia, visual stimulation, and a combination of the two. Spatial heterogeneity in arterial reactivity was observed between conditions. During hypercapnia, large arterial volume changes contributed to CBF increase and further downstream, there were reductions in the gray matter transit time. These changes were not significant during visual stimulation, and during the combined condition they were moderated. These findings suggest distinct vascular mechanisms for large and small arterial segments that may be condition specific. However, the power relationships between gray matter arterial blood volume and CBF in hypercapnia (a = 0.69 ± 0.24) and visual stimulation (a = 0.68 ± 0.20) were similar. Assuming consistent capillary and venous volume responses across these conditions, these results offer support for a consistent total CBV-flow relationship typically assumed in blood oxygen-level dependent calibration techniques.

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Section: Vascular Reactions During Functional Challengessupporting

confidence: 88%

Similarities and Differences in Arterial Responses to Hypercapnia and Visual Stimulation

Petersen

Zimine³

et al. 2010

J Cereb Blood Flow Metab

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“…However, as noted by Boas et al (2008) it is not clear whether dominant volume changes occur on the arteriole side Kim et al, 2007;Lee et al, 2001;Vanzetta et al, 2005) or venous side (Buxton et al, 1998;Kong et al, 2004;Mandeville et al, 1999). Our results indicate that the arteriolar blood volume change comprises more than 96%, i.e., the major portion of the blood volume change.…”

Section: Blood Flow Control and Passive Responsesmentioning

confidence: 48%

Simulation study of brain blood flow regulation by intra-cortical arterioles in an anatomically accurate large human vascular network. Part II: Flow variations induced by global or localized modifications of arteriolar diameters

Lorthois¹,

Cassot²,

Lauwers³

2011

NeuroImage

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OATAO is an open access repository that collects the work of Toulouse researchers and makes it freely available over the web where possible. In a companion paper (Lorthois et al., Neuroimage, in press), we perform the first simulations of blood flow in an anatomically accurate large human intra-cortical vascular network (~10000 segments), using a 1D non-linear model taking into account the complex rheological properties of blood flow in microcirculation. This model predicts blood pressure, blood flow and hematocrit distributions, volumes of functional vascular territories, regional flow at voxel and network scales, etc. Using the same approach, we study flow reorganizations induced by global arteriolar vasodilations (an isometabolic global increase in cerebral blood flow). For small to moderate global vasodilations, the relationship between changes in volume and changes in flow is in close agreement with Grubb's law, providing a quantitative tool for studying the variations of its exponent with underlying vascular architecture. A significant correlation between blood flow and vascular structure at the voxel scale, practically unchanged with respect to baseline, is demonstrated. Furthermore, the effects of localized arteriolar vasodilations, representative of a local increase in metabolic demand, are analyzed. In particular, localized vasodilations induce flow changes, including vascular steal, in the neighboring arteriolar trunks at small distances (b 300 μm), while their influence in the neighboring veins is much larger (about 1 mm), which provides an estimate of the vascular point spread function. More generally, for the first time, the hemodynamic component of various functional neuroimaging techniques has been isolated from metabolic and neuronal components, and a direct relationship with several known characteristics of the BOLD signal has been demonstrated. IntroductionThere is increasing recognition that, by its structural implication in neuro-vascular coupling, underlying vascular architecture is a key player in hemodynamically based functional imaging techniques (including fMRI and PET) (Harrison et al., 2002;d'Esposito et al., 2003;Logothetis and Wandell, 2004;Lauwers et al., 2008;Weber et al., 2008). In particular, the spatial resolution and specificity of such techniques are bound to the density of blood capillary vasculature and blood flow regulating structures (Harel et al., 2006). This is especially important in the context of high field fMRI Harel et al., 2006), because, despite a dramatic increase in the theoretical spatial resolution obtained by using higher magnetic fields, associated with other hardware advancements, "the spatial extent of the hemodynamic response ultimately will impose a fundamental limitation on the spatial resolution of fMRI modalities" ).However, little is known about the fundamentals of the relationship between vascular structure and hemodynamic changes induced by brain activation. A growing body of evidence indicates that neurons, glia, and cerebral blood vessels, actin...

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“…This raises the question why opposing results have frequently been reported in animal studies (Kennan et al, 1998;Kida et al, 2007;Kim et al, 2007;Leite et al, 2002;Mandeville et al, 1998Mandeville et al, , 1999a. Previously, we suggested interspecies differences, the need for anesthesia, and the use of long-lasting iron oxide contrast agents as candidates for the discrepant findings (Frahm et al, 2008).…”

Section: Discussionmentioning

confidence: 92%

“…Although CBF and CBV normalize comparably fast in both visual and motor systems, the BOLD undershoot was found to return more quickly to baseline in the motor cortex (Donahue et al, 2009a). In fact, most human studies of the BOLD undershoot used visual stimulation (Blockley et al, 2009;Donahue et al, 2009b;Frahm et al, 1996;Jones et al, 1998;Krü ger et al, 1999aKrü ger et al, , b, 1998Lu et al, 2004;Tuunanen et al, 2006), whereas stimulation of the somatosensory system is preferred in anesthesized animals because of technical reasons (Kennan et al, 1998;Kida et al, 2007;Kim et al, 2007;Mandeville et al, 1998Mandeville et al, , 1999aShen et al, 2008). So far, no definite conclusions can be drawn about respective differences.…”

Section: Discussionmentioning

confidence: 99%

“…Although human studies consistently found normalized CBV values after the end of stimulation (Blockley et al, 2009;Frahm et al, 2008;Jasdzewski et al, 2003;Lu et al, 2004;Poser and Norris, 2007;Schroeter et al, 2006;Toronov et al, 2003;Tuunanen et al, 2006), several animal experiments reported elevated CBV during the BOLD undershoot (Jones et al, 2001(Jones et al, , 2002Kida et al, 2007;Kim et al, 2007;Leite et al, 2002;Mandeville et al, 1998Mandeville et al, , 1999a. One possible reason for these discrepancies is a methodological difference as most of the animal studies are based on blood-pool contrast agents with iron oxide particles (Jin and Kim, 2008;Kennan et al, 1998;Kida et al, 2007;Kim et al, 2007;Mandeville et al, 1998Mandeville et al, , 1999aSmirnakis et al, 2007). Thus, to investigate the impact of the specific contrast agent used for assessing CBV effects, we set up an experiment using dynamic T1-weighted three-dimensional (3D) MRI and the blood-pool contrast agent Vasovist, containing gadofosveset trisodium (Majos et al, 2009;Morton et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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Basal Cerebral Blood Volume during the Poststimulation Undershoot in BOLD MRI of the Human Brain

Dechent

Schütze

Helms

et al. 2010

J Cereb Blood Flow Metab

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One of the characteristics of the blood oxygenation level-dependent (BOLD) magnetic resonance imaging (MRI) response to functional challenges of the brain is the poststimulation undershoot, which has been suggested to originate from a delayed recovery of either cerebral blood volume (CBV) or cerebral metabolic rate of oxygen to baseline. Using bolus-tracking MRI in humans, we recently showed that relative CBV rapidly normalizes after the end of stimulation. As this observation contradicts at least part of the blood-pool contrast agent studies performed in animals, we reinvestigated the CBV contribution by dynamic T1-weighted three-dimensional MRI (8 seconds temporal resolution) and Vasovist at 3 T (12 subjects). Initially, we determined the time constants of individual BOLD responses. After injection of Vasovist, CBV-related T1-weighted signal changes revealed a signal increase during visual stimulation (1.7%±0.4%), but no change relative to baseline in the poststimulation phase (0.2% ± 0.3%). This finding renders the specific nature of the contrast agent unlikely to be responsible for the discrepancy between human and animal studies. With the assumption of normalized cerebral blood flow after stimulus cessation, a normalized CBV lends support to the idea that the BOLD MRI undershoot reflects a prolonged elevation of oxidative metabolism.

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Arterial versus Total Blood Volume Changes during Neural Activity-Induced Cerebral Blood Flow Change: Implication for BOLD fMRI

Cited by 172 publications

References 51 publications

Similarities and Differences in Arterial Responses to Hypercapnia and Visual Stimulation

Similarities and Differences in Arterial Responses to Hypercapnia and Visual Stimulation

Simulation study of brain blood flow regulation by intra-cortical arterioles in an anatomically accurate large human vascular network. Part II: Flow variations induced by global or localized modifications of arteriolar diameters

Basal Cerebral Blood Volume during the Poststimulation Undershoot in BOLD MRI of the Human Brain

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