Deciphering laminar-specific neural inputs with line-scanning fMRI

Yu, Xin; Cui, Qian; Chen, Der Yow; Dodd, Stephen J.; Koretsky, Alan P.

doi:10.1038/nmeth.2730

Cited by 165 publications

(247 citation statements)

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“…For 24 example, Trampel et al, (2012) investigated the increased activity in primary motor cortex 25 (M1) associated with motor imagery as compared with an actual motion task, demonstrating 26 that the layer dependence of the ensuing activation differs strikingly for the two conditions. In 27 another example, layer-dependent fMRI was used to study the input characteristics of sensory 28 cortex, and thus to investigate the restructuring of brain connectivity consequent upon 29 denervation-induced plasticity (Yu et al, 2014). In the visual system, layer-dependent fMRI 30 can help to address questions regarding the feedforward-feedback pathways during excitatory 31 and inhibitory stimuli (Goense et al, 2012).…”

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Cortical lamina-dependent blood volume changes in human brain at 7 T

et al. 2015

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Highlights: 21• A CBV-sensitive fMRI method is developed for high resolution fMRI in humans. 22• Lamina-dependent CBV fMRI responses are shown in humans. 23• VASO cortical profiles are validated with Fe-contrast agent fMRI in animals. 24• Sensitivity to large veins can be minimized using VASO-CBV instead of BOLD fMRI. 25• Ipsilateral fMRI responses to finger-tapping are positive in M1 and negative in S1. 26 27 Abstract 28Cortical layer-dependent high (sub-millimeter) resolution functional magnetic resonance imaging 29 (fMRI) in human or animal brain can be used to address questions regarding the functioning of 30 cortical circuits, such as the effect of different afferent and efferent connectivity on activity in 31 specific cortical layers. The sensitivity of gradient echo (GE) blood oxygenation level dependent 32 (BOLD) responses to large draining veins reduces its local specificity and can render the 33 interpretation of the underlying laminar neural activity impossible. Application of the more spatially 34 specific cerebral blood volume (CBV) based fMRI in humans has been hindered by the low sensitivity 35 of the non-invasive modalities available. Here, a Vascular Space Occupancy (VASO) variant, adapted 36 for use at high field, is further optimized to capture layer-dependent activity changes in human 37 motor cortex at sub-millimeter resolution. Acquired activation maps and cortical profiles show that 38 the VASO signal peaks in grey matter at 0.8 -1.6 mm depth, and deeper compared to the superficial 39 and vein-dominated GE-BOLD responses. Validation of the VASO signal change versus well-40 established iron-oxide contrast agent based fMRI methods in animals showed the same cortical 41 profiles of CBV change, after normalization for lamina-dependent baseline CBV. In order to evaluate 42 its potential of revealing small lamina-dependent signal differences due to modulations of the input-43 output characteristics, layer-dependent VASO responses were investigated in the ipsilateral 44 hemisphere during unilateral finger tapping. Positive activation in ipsilateral primary motor cortex 45 *7. Manuscript Click here to view linked References 2 and negative activation in ipsilateral primary sensory cortex were observed. This feature is only 1 visible in high-resolution fMRI where opposing sides of a sulcus can be investigated independently 2 because of a lack of partial volume effects. Based on the results presented here we conclude that 3 VASO offers good reproducibility, high sensitivity, and lower sensitivity than GE-BOLD to changes in 4 larger vessels, making it a valuable tool for layer-dependent fMRI studies in humans. 5Abbreviations: BOLD = blood oxygenation level dependent; CBV = cerebral blood volume; CNR = 6 contrast-to-noise ratio; CSF = cerebrospinal fluid; ΔCBV = change in CBV; EPI = echo planar imaging; 7 Fe = iron; fMRI = functional magnetic resonance imaging; GE = gradient echo; GM = grey matter; ROI 8 = region of interest; SNR = signal-to-noise ratio; SS-SI-VASO = slice-selective slab-inversion VASO...

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“…Channels with unstable signal or severe aliasing artifacts 42 (between 0 and 8) were excluded from the subsequent sum-of-squares combination (see 43 supplementary Fig. S1 for more details).…”

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Cortical lamina-dependent blood volume changes in human brain at 7 T

et al. 2015

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“…In the present study, T 1 values between segments after the TGN stimulation stage were also well correlated in the range 0.2-1 s with slopes close to 1.0 for all the layers (not shown). Understanding how neural activity is distributed among cortical layers in the barrel cortex is complex (Herman et al 2013;Yu et al 2014). Recently, Yu et al (2014) concluded that the location of BOLD fMRI onset matches well with the input layers across the cortical depth as detected by MEMRI.…”

Section: Discussionmentioning

confidence: 99%

“…Understanding how neural activity is distributed among cortical layers in the barrel cortex is complex (Herman et al 2013;Yu et al 2014). Recently, Yu et al (2014) concluded that the location of BOLD fMRI onset matches well with the input layers across the cortical depth as detected by MEMRI. However, they also mentioned that differences in timing between fMRI and neural events make their results difficult to interpret.…”

Section: Discussionmentioning

confidence: 99%

“…transients due to various mediators that as a consequence induce plastic changes as well as long-term potentiation or depression or adaptation processes. Several recent studies have used high-resolution BOLD fMRI to investigate neurovascular coupling issues in cortical layers of the rat primary somatosensory cortex (Herman et al 2013;Shih et al 2013;Yu et al 2014). Because of the different neuronal populations in these cortical layers, it was expected to obtain an improved interpretation of the underlying neural activity.…”

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Quantitative activity-induced manganese-dependent MRI for characterizing cortical layers in the primary somatosensory cortex of the rat

et al. 2014

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The ability of Mn 2? to follow Ca 2? pathways upon stimulation transform them into remarkable surrogate markers of neuronal activity using activity-induced manganese-dependent MRI (AIM-MRI). In the present study, a precise follow-up of physiological parameters during MnCl 2 and mannitol infusions improved the reproducibility of AIM-MRI allowing in-depth evaluation of the technique. Pixel-by-pixel T 1 data were investigated using histogram distributions in the barrel cortex (BC) and the thalamus before and after Mn 2? infusion, after blood brain barrier opening and after BC activation. Mean BC T 1 values dropped significantly upon trigeminal nerve (TGN) stimulation (-38 %, P = 0.02) in accordance with previous literature findings. T 1 histogram distributions showed that 34 % of T 1s in the range 600-1500 ms after Mn 2? ? mannitol infusions shifted to 50-350 ms after TGN stimulation corresponding to a twofold increase of the percentage of pixels with the lowest T 1s in BC. Moreover, T 1 changes in response to stimulation increased significantly from superficial cortical layers (I-III) to deeper layers (V-VI). Cortical cytoarchitecture detection during a functional paradigm was performed extending the potential of AIM-MRI. Quantitative AIM-MRI could thus offer a means to interpret local neural activity across cortical layers while identification of the role of calcium dynamics in vivo during brain activation could play a key role in resolving neurovascular coupling mechanisms.

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High Spatiotemporal Resolution Radial Encoding Single‐Vessel fMRI

Jiang,

Pais‐Roldán,

Pohmann

et al. 2024

Advanced Science

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High‐field preclinical functional MRI (fMRI) is enabled the high spatial resolution mapping of vessel‐specific hemodynamic responses, that is single‐vessel fMRI. In contrast to investigating the neuronal sources of the fMRI signal, single‐vessel fMRI focuses on elucidating its vascular origin, which can be readily implemented to identify vascular changes relevant to vascular dementia or cognitive impairment. However, the limited spatial and temporal resolution of fMRI is hindered hemodynamic mapping of intracortical microvessels. Here, the radial encoding MRI scheme is implemented to measure BOLD signals of individual vessels penetrating the rat somatosensory cortex. Radial encoding MRI is employed to map cortical activation with a focal field of view (FOV), allowing vessel‐specific functional mapping with 50 × 50 µm2 in‐plane resolution at a 1 to 2 Hz sampling rate. Besides detecting refined hemodynamic responses of intracortical micro‐venules, the radial encoding‐based single‐vessel fMRI enables the distinction of fMRI signals from vessel and peri‐vessel voxels due to the different contribution of intravascular and extravascular effects.

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Deciphering laminar-specific neural inputs with line-scanning fMRI

Cited by 165 publications

References 30 publications

Cortical lamina-dependent blood volume changes in human brain at 7 T

Cortical lamina-dependent blood volume changes in human brain at 7 T

Quantitative activity-induced manganese-dependent MRI for characterizing cortical layers in the primary somatosensory cortex of the rat

High Spatiotemporal Resolution Radial Encoding Single‐Vessel fMRI

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