High b -value diffusion-weighted fMRI in a rat forepaw electrostimulation model at 7 T

Autio, Joonas; Kershaw, Jeff; Shibata, Sayaka; Obata, Takayuki; Kanno, Iwao; Aoki, Ichio

doi:10.1016/j.neuroimage.2011.04.006

Cited by 18 publications

(23 citation statements)

References 57 publications

(84 reference statements)

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“…The link of the diffusion component with neuronal activation has been suggested in the past (12,13) and demonstrated in isolated brain slices (15). Several groups have argued that the relaxivity component, which results from local variations in local susceptibility induced by variations in vascular deoxyhemoglobin content (at the origin of the BOLD response) may completely obscure the diffusion component in vivo (16,17,29). Although this hypothesis is verified with b = 250 s/mm 2 , our results clearly establish this is not the case when the DfMRI signal is acquired at a high level of diffusion weighting (high b values).…”

Section: Discussionmentioning

confidence: 96%

“…Dynamic changes in the tridimensional neuronal tissue microstructure induced by neuronal activation have been observed for several decades in individual cells (9), brain slices (10), and in vivo, mainly using various types of optical measurements, and there is now growing evidence that neuronal swelling occurs during activation. It has been well established that MRI can be made sensitive to tissue microstructure through the measurement of water molecular diffusion (11) and preliminary attempts have been made that suggest that diffusion MRI (DfMRI) could have the potential to monitor such activation-induced tissue changes (12)(13)(14)(15), although residual effects from the hemodynamic changes underlying the BOLD mechanism could interfere with the diffusion measurements (16,17).…”

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confidence: 99%

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Water diffusion in brain cortex closely tracks underlying neuronal activity

Tsurugizawa

Ciobanu

Bihan

2013

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

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Neuronal activity results in a local increase in blood flow. This concept serves as the basis for functional MRI. Still, this approach remains indirect and may fail in situations interfering with the neurovascular coupling mechanisms (drugs, anesthesia). Here we establish that water molecular diffusion is directly modulated by underlying neuronal activity using a rat forepaw stimulation model under different conditions of neuronal stimulation and neurovascular coupling. Under nitroprusside infusion, a neurovascular-coupling inhibitor, the diffusion response and local field potentials were maintained, whereas the hemodynamic response was abolished. As diffusion MRI reflects interactions of water molecules with obstacles (e.g., cell membranes), the observed changes point to a dynamic modulation of the neural tissue structure upon activation, which remains to be investigated. These findings represent a significant shift in concept from the current electrochemical and neurovascular coupling principles used for brain imaging, and open unique avenues to investigate mechanisms underlying brain function.

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Section: Discussionmentioning

confidence: 96%

mentioning

confidence: 99%

Water diffusion in brain cortex closely tracks underlying neuronal activity

Tsurugizawa

Ciobanu

Bihan

2013

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

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“…The debate about whether diffusion MRI can detect neuronal activity more directly and accurately than conventional hemodynamicbased fMRI methods has never stopped since it was proposed (10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20). Our hybrid test bed, which allows for simultaneous monitoring of neuronal activity via intracellular calcium fluorescence imaging during MR acquisition on the organotypic cortical cultures, provides a unique opportunity for direct, time-dependent comparisons of the diffusion MR signals with neuronal activity without any hemodynamic or other physiologic confounds.…”

Section: Discussionmentioning

confidence: 99%

“…Two major reasons for this may be a dearth of experiments that convincingly establish its neurophysiological basis and the poor reproducibility of the originally reported changes in diffusion MRI signals by different laboratories. The inability to detect the predicted changes using fDMRI and the possible confounds of hemodynamic contributions in fDMRI measurements in vivo do not argue for a robust connection between changes in diffusion MRI and underlying neuronal activity (17)(18)(19)(20). Thus, "ground-truth" experiments, potentially establishing a connection between the changes in diffusion MRI and underlying neuronal activity, are needed, particularly to shed light on the possible biophysical basis of the fDMRI signal.…”

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confidence: 99%

Assessing the sensitivity of diffusion MRI to detect neuronal activity directly

Bai

Stewart

Plenz

et al. 2016

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

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Functional MRI (fMRI) is widely used to study brain function in the neurosciences. Unfortunately, conventional fMRI only indirectly assesses neuronal activity via hemodynamic coupling. Diffusion fMRI was proposed as a more direct and accurate fMRI method to detect neuronal activity, yet confirmative findings have proven difficult to obtain. Given that the underlying relation between tissue water diffusion changes and neuronal activity remains unclear, the rationale for using diffusion MRI to monitor neuronal activity has yet to be clearly established. Here, we studied the correlation between water diffusion and neuronal activity in vitro by simultaneous calcium fluorescence imaging and diffusion MR acquisition. We used organotypic cortical cultures from rat brains as a biological model system, in which spontaneous neuronal activity robustly emerges free of hemodynamic and other artifacts. Simultaneous fluorescent calcium images of neuronal activity are then directly correlated with diffusion MR signals now free of confounds typically encountered in vivo. Although a simultaneous increase of diffusion-weighted MR signals was observed together with the prolonged depolarization of neurons induced by pharmacological manipulations (in which cell swelling was demonstrated to play an important role), no evidence was found that diffusion MR signals directly correlate with normal spontaneous neuronal activity. These results suggest that, whereas current diffusion MR methods could monitor pathological conditions such as hyperexcitability, e.g., those seen in epilepsy, they do not appear to be sensitive or specific enough to detect or follow normal neuronal activity.D eveloping a direct MRI method to detect neuronal activity in vivo and noninvasively is a major focus in neuroscience. Progress in this area is required to improve our understanding of normal brain function, and in a clinical setting, to develop new tools for studying normal and abnormal development to diagnose diseases and disorders of the brain. Functional MRI (fMRI) has been widely used in the cognitive neurosciences since its invention in the 1990s (1-3). The most widely used fMRI method, blood-oxygenation-level-dependent (BOLD) MRI, detects hemodynamic changes in the brain, which only indirectly reflects neuronal activity. Moreover, its hemodynamic origin limits both its spatial and temporal resolution and its interpretation as a direct proxy for neuronal activity (4, 5).More recently, several MRI methods were proposed to provide more direct measures of neuronal excitation (6). In particular, diffusion MRI, a method to measure the apparent diffusivity of water within tissues (7-9), has been suggested as a direct functional imaging method to detect neuronal activity (10-13). Early in vivo experiments in both humans and animals reported small but significant increases in highly diffusion-weighted MRI signals, which were ascribed to changes directly induced by the underlying neuronal activity rather than indirect hemodynamic changes (10-13).In vitro experimen...

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“…Indeed, effects of USPIOs are much larger than those of endogenous deoxyhemoglobin. Iron contrast agent injection is becoming a standard over BOLD for fMRI experiments performed in animals, especially non-human primates (Leite et al, 2002;Zhao et al, 2009;Autio et al, 2011;Mandeville, 2012) The present approach has the potential to detect and quantify variations in blood volume in the cortex upon brain activation status, through variations in ξ [Fe] reflecting variations in USPIO concentration.…”

Section: Sn Gp Th Cortexmentioning

confidence: 99%

Quantification of iron in the non-human primate brain with diffusion-weighted magnetic resonance imaging

et al. 2014

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Pathological iron deposits in the brain, especially within basal ganglia, are linked to severe neurodegenerative disorders like Parkinson's disease. As iron induces local changes in magnetic susceptibility, its presence can be visualized with magnetic resonance imaging (MRI). The usual approach, based on iron induced changes in magnetic relaxation (T2/T2'), is often prone, however, to confounding artifacts and lacks specificity. Here, we propose a new method to quantify and map iron deposits using water diffusion MRI. This method is based on the differential sensitivity of two image acquisition schemes to the local magnetic field gradients induced by iron deposits and their cross-term with gradient pulses used for diffusion encoding. Iron concentration could be imaged and estimated with high accuracy in the brain cortex, the thalamus, the substantia nigra and the globus pallidus of macaques, showing iron distributions in agreement with literature. Additionally, iron maps could clearly show a dramatic increase in iron content upon injection of an UltraSmall Particle Iron Oxide (USPIO) contrast agent, notably in the cortex and the thalamus, reflecting regional differences in blood volume. The method will benefit clinical investigations on the effect of iron deposits in the brain or other organs, as iron deposits are increasingly seen as a biomarker for a wide range of diseases, notably, neurodegenerative diseases in the pre-symptomatic stage. It also has the potential for quantifying variations in blood volume induced by brain activation in fMRI studies using USPIOs.

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High b -value diffusion-weighted fMRI in a rat forepaw electrostimulation model at 7 T

Cited by 18 publications

References 57 publications

Water diffusion in brain cortex closely tracks underlying neuronal activity

Water diffusion in brain cortex closely tracks underlying neuronal activity

Assessing the sensitivity of diffusion MRI to detect neuronal activity directly

Quantification of iron in the non-human primate brain with diffusion-weighted magnetic resonance imaging

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