Exploring the post‐stimulus undershoot with spin‐echo fMRI: Implications for models of neurovascular response

Poser, Benedikt A.; Mierlo, Emily van; Norris, David G.

doi:10.1002/hbm.21003

Cited by 18 publications

(16 citation statements)

References 57 publications

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“…CMRO 2 and OEF were then determined using more complicated multi-compartment modeling of vasculature (arterioles/venules) and tissue, but the overall conclusion was based on simple physiological considerations. Using these same scientific arguments, this conclusion was later substantiated in humans (Dechent et al, 2011; Donahue et al, 2009a; Frahm et al, 2008; Hua et al, 2011a; Poser et al, 2011) and in animals (Jin and Kim, 2008b; Yacoub et al, 2006). Especially the high-resolution animal experiments where BOLD-PSUs were localized in surface pial vessel regions are important, because no delayed CBV effects were measured there during the BOLD-PSU.…”

Section: Have Sustained Post-stimulus Cmro2 Increases Actually Been Mmentioning

confidence: 85%

“…At 1.5T, SE-BOLD is mainly (nearly 100%) intravascular, while this reduces to at most 67% at 3T (Jochimsen et al, 2004). Using a SE sequence without EPI readout (to avoid potential GRE contributions), the Norris group (Poser et al, 2011) recently investigated SE-BOLD effects at 1.5T and 3T and found the same ratio of the positive BOLD effect versus the PSU. In addition, they found no difference in this temporal response positive/negative ratio between SE and GRE effects at 3T.…”

Section: Spin Echo Versus Gradient Echo Bold Undershoots; More Comparmentioning

confidence: 99%

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The BOLD post-stimulus undershoot, one of the most debated issues in fMRI

Zijl

Hua

2012

NeuroImage

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This paper provides a brief overview of how we got involved in fMRI work and of our efforts to elucidate the mechanisms underlying BOLD signal changes. The phenomenon discussed here in particular is the post-stimulus undershoot (PSU), the interpretation of which has captivated many fMRI scientists and is still under debate to date. This controversy is caused both by the convoluted physiological origin of BOLD effect, which allows many possible explanations, and the lack of comprehensive data in the early years. BOLD effects reflect changes in cerebral blood flow (CBF), volume (CBV), metabolic rate of oxygen (CMRO2), and hematocrit fraction (Hct). However, the size of such effects is modulated by vascular origin such as intravascular, extravascular, macro and microvascular, venular and capillary, the relative contributions of which depend not only on the spatial resolution of the measurements, but also on stimulus duration, on magnetic field strength and on whether spin echo (SE) or gradient echo (GRE) detection is used. The two most dominant explanations of the PSU have been delayed vascular compliance (first venular, later arteriolar, and recently capillary) and sustained increases in CMRO2, while post-activation reduction in CBF is a distant third. MRI has the capability to independently measure CBF and arteriolar, venous, and total CBV contributions in humans and animals, which has been of great assistance in improving the understanding of BOLD phenomena. Using currently available MRI and optical data, we conclude that the predominant PSU origin is a sustained increase in CMRO2. However, some contributions from delayed vascular compliance are likely, and small CBF undershoot contributions that are difficult to detect with current arterial spin labeling technology can also not be excluded. The relative contribution of these different processes, which are not mutually exclusive and can act together, is likely to vary with stimulus duration and type.

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Section: Have Sustained Post-stimulus Cmro2 Increases Actually Been Mmentioning

confidence: 85%

Section: Spin Echo Versus Gradient Echo Bold Undershoots; More Comparmentioning

confidence: 99%

The BOLD post-stimulus undershoot, one of the most debated issues in fMRI

Zijl

Hua

2012

NeuroImage

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“…The post-stimulus undershoot often lasts more than 20 s and can persist up to 1 minute after the positive response (Frahm et al, 2008; Chen and Pike, 2009). The mechanisms underlying the phenomenon are not completely understood, and have been attributed to possible undershoot in CBF, persistent elevation of cerebral metabolic rate of oxygen (CMRO 2 ), a delayed recovery of increased CBV, or a combination of these effects (Buxton et al, 1998; Mandeville et al, 1999a; Mandeville et al, 1999b; Lu et al, 2004; Schroeter et al, 2006; Devor et al, 2007; Frahm et al, 2008; Donahue et al, 2008; Harshbarger and Song, 2008; Chen and Pike, 2009; Sadaghiani et al, 2009; Poser et al, 2011). Although the existence of the post-stimulus undershoot for both block-design and ER paradigms is indisputable, it is an open question whether there exists a quantitative relationship between the positive response and the post-stimulus undershoot in an ER paradigm.…”

Section: Introductionmentioning

confidence: 99%

Linear coupling of undershoot with BOLD response in ER-fMRI and nonlinear BOLD response in rapid-presentation ER-fMRI

Zong¹,

Huang²

2011

NeuroImage

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In event-related (ER) BOLD-fMRI brain activation studies, understanding the relationship between the elicited BOLD signal and its underlying neuronal activity is essential for any quantitative interpretation of the neural events from the BOLD measurements. This requires a better understanding of the dynamic BOLD response. Besides the neuronal activity-induced positive BOLD response, the dynamic response is also characterized by a profound post-stimulus undershoot. The relationship between the positive response and the post-stimulus undershoot, however, remains poorly understood. Earlier studies using block-design paradigms with long stimulation durations (>10 s) do not suggest a quantitative relationship. Using an ER paradigm, this study revealed a linear coupling between the positive BOLD response and the post-stimulus undershoot across the human visual cortex. The voxelwise linear coupling across the visual cortex strongly supports a homogeneous hemodynamic response in ER paradigms, though the BOLD response magnitude varies substantially over a wide range across the visual cortex. Although underlying neuronal activity is responsible for a BOLD response, the blood volume fraction affects the magnitude of the BOLD response; the larger the blood volume fraction, the larger the magnitude. This effect needs to be accounted for in any quantitative interpretation of the BOLD measurements. In the absence of nonlinear neuronal activities, the nonlinear vascular response renders the estimated BOLD responses smaller in rapid presentation (RP) ER paradigms compared to that in ER paradigms, and this reduction effect also needs to be considered when interpreting the estimated BOLD responses in RP-ER paradigms. Interestingly, this nonlinear effect might be simply accounted for by a scaling factor across the visual cortex.

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“…The PSU is dependent on both oxidative metabolism and delayed CBV recovery 37,59 and may be biased toward arteriolar-dependent changes in oxyhemoglobin levels. 60 An alteration in the normal relationship between CBF and CBV after TBI could result in a decrease in the amplitude of the PSU. 21 Reductions in CBF as a function of age, however, have not directly translated into a reduction in the BOLD PSU, 61 suggesting that other mechanisms such as a decrease in the number/width of microvessels 40 and/or alterations in vasocompliance after injury may also be contributing factors.…”

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confidence: 99%

Investigating the Properties of the Hemodynamic Response Function after Mild Traumatic Brain Injury

Mayer

Toulouse

Klimaj

et al. 2014

Journal of Neurotrauma

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Although several functional magnetic resonance imaging (fMRI) studies have been conducted in human models of mild traumatic brain injury (mTBI), to date no studies have explicitly examined how injury may differentially affect both the positive phase of the hemodynamic response function (HRF) as well as the post-stimulus undershoot (PSU). Animal models suggest that the acute and semi-acute stages of mTBI are associated with significant disruptions in metabolism and to the microvasculature, both of which could impact on the HRF. Therefore, fMRI data were collected on a cohort of 30 semi-acute patients with mTBI (16 males; 27.83 -9.97 years old; 13.00 -2.18 years of education) and 30 carefully matched healthy controls (HC; 16 males; 27.17 -10.08 years old; 13.37 -2.31 years of education) during a simple sensory-motor task. Patients reported increased cognitive, somatic, and emotional symptoms relative to controls, although no group differences were detected on traditional neuropsychological examination. There were also no differences between patients with mTBI and controls on fMRI data using standard analytic techniques, although mTBI exhibited a greater volume of activation during the task qualitatively. A significant Group · Time interaction was observed in the right supramarginal gyrus, bilateral primary and secondary visual cortex, and the right parahippocampal gyrus. The interaction was the result of an earlier time-to-peak and positive magnitude shift throughout the estimated HRF in patients with mTBI relative to HC. This difference in HRF shape combined with the greater volume of activated tissue may be indicative of a potential compensatory mechanism to injury. The current study demonstrates that direct examination and modeling of HRF characteristics beyond magnitude may provide additional information about underlying neuropathology that is not available with more standard fMRI analyses.

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Exploring the post‐stimulus undershoot with spin‐echo fMRI: Implications for models of neurovascular response

Cited by 18 publications

References 57 publications

The BOLD post-stimulus undershoot, one of the most debated issues in fMRI

The BOLD post-stimulus undershoot, one of the most debated issues in fMRI

Linear coupling of undershoot with BOLD response in ER-fMRI and nonlinear BOLD response in rapid-presentation ER-fMRI

Investigating the Properties of the Hemodynamic Response Function after Mild Traumatic Brain Injury

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