Physiological basis for BOLD MR signal changes due to neuronal stimulation: Separation of blood volume and magnetic susceptibility effects

Rp, Kennan; Be, Scanley; Rb, Innis; Jc, Gore

doi:10.1002/mrm.1910400609

Cited by 113 publications

(128 citation statements)

References 33 publications

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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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Section: Discussionmentioning

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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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“…Cerebral blood volume (CBV)-weighted functional magnetic resonance imaging (fMRI) using long blood half-life contrast agents has often been applied in animals due to both high sensitivity and its ability to suppress signals from large vessels (Kennan et al, 1998;Kim and Ugurbil, 2003;Mandeville et al, 1999;Mandeville et al, 1998b;Vanduffel et al, 2001), making CBV an appealing fMRI methodology for animal research. Furthermore, CBVweighted fMRI shows high specificity for neuronally active sites.…”

Section: Introductionmentioning

confidence: 99%

Improved cortical-layer specificity of vascular space occupancy fMRI with slab inversion relative to spin-echo BOLD at 9.4 T

Jin

Kim

2008

NeuroImage

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Cerebral blood volume (CBV)-weighted endogenous functional contrast can be obtained by the vascular space occupancy (VASO) technique. VASO relies on nonselective inversion for nulling blood signals, but the implementation of VASO at magnetic fields higher than 3 T is difficult due to similar T 1 values of tissue and blood water and a stronger counteracting blood oxygen leveldependent (BOLD) effect. To improve functional CBV sensitivity, we proposed to use VASO with slab-selective inversion (SI-VASO). Computer simulations showed that the SI-VASO approach significantly increases functional sensitivity compared to the original VASO in a stronger magnetic field with a shorter repetition time. To examine layer-dependent specificity, SI-VASO and spin-echo BOLD (SE-BOLD) functional magnetic resonance imaging (fMRI) experiments were performed on isoflurane-anesthetized cats during visual stimulation at 9.4 T. Unlike simultaneously acquired SE-BOLD signal, the SI-VASO signal peaked at 0.9 mm from the surface of the cortex and was localized to the middle cortical layer. The full-width at half maximal response across the cortex was narrower for SI-VASO than for SE-BOLD (1.7 mm vs. 2.5 mm, respectively), suggesting that SI-VASO is better localized to neuronally active sites than SE-BOLD fMRI. The magnitude of the SI-VASO change in the middle cortex was −1.45% with our experimental parameters, corresponding to a relative CBV change of ∼8% when baseline CBV was assumed to be 5% in a two-compartment model. The signal response profile across the cortex, the calculated CBV change, and the time course of SI-VASO fMRI were similar to those of previously obtained CBV-weighted fMRI with contrast agent in the same animal model, suggesting that SI-VASO measures predominately functional CBV responses.

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“…Dextran-coated iron oxide nanoparticles have been used as a long half-life intravascular susceptibility contrast agent (Kennan et al, 1998;Mandeville et al, 1998;van Bruggen et al, 1998), similar to endogenous irons in dHb molecules (used for the BOLD contrast). The half-life of the iron oxides in blood is dependent on particle size and species; the typical half-life of 20-30 μm diameter particles is >4 hours in rats (Mandeville et al, 1998), 3-6 hours in cats (in our observation), and >18 hours in non-human primates (Vanduffel et al, 2001).…”

Section: Sensitivity and Specificity Of Hemodynamic-based Fmrimentioning

confidence: 99%

Lessons from fMRI about Mapping Cortical Columns

Kim

Fukuda

2007

Neuroscientist

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Recently-developed functional magnetic resonance imaging (fMRI) can map small functional structures non-invasively and repeatedly without any depth limitation. However, there has been a persistent concern as to whether the high-resolution fMRI signals actually mark the sites of increased neural activity. To examine this outstanding issue, we used iso-orientation columns of isofluraneanestheized cats as a biological model and confirmed the neural correlation of fMRI iso-orientation maps by comparing with intrinsic optical imaging maps. Our results suggest that highest fMRI signals indeed indicate the sites of increased neuronal activity. Now fMRI can be used to determine plastic and/or developmental change of functional columnar structure possibly on a layer to layer basis. In this review we focus mainly on what technical aspects should be considered when mapping functional cortical columns, including imaging techniques and experimental design.

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Physiological basis for BOLD MR signal changes due to neuronal stimulation: Separation of blood volume and magnetic susceptibility effects

Cited by 113 publications

References 33 publications

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

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

Improved cortical-layer specificity of vascular space occupancy fMRI with slab inversion relative to spin-echo BOLD at 9.4 T

Lessons from fMRI about Mapping Cortical Columns

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