Comparison of BOLD and CBV using 3D EPI and 3D GRASE for cortical layer fMRI at 7T

Purpose Functional MRI (fMRI) at the mesoscale of cortical layers and columns requires both sensitivity and specificity, which can be compromised if the imaging method is affected by vascular artifacts, particularly cortical draining veins at the pial surface. Recent studies have shown that cerebral blood volume (CBV) imaging is more specific to the actual laminar locus of neural activity than BOLD imaging when using standard gradient-echo (GE) EPI sequences. Gradient and Spin Echo (GRASE) BOLD imaging has also shown greater specificity when compared with GE-BOLD. Methods Here we directly compare CBV and BOLD contrasts in high-resolution imaging of the primary motor cortex for laminar fMRI in four combinations of signal labeling, VASO (CBV) and BOLD with 3D GE-EPI and zoomed 3D GRASE image readouts. Results We find that both CBV imaging using EPI-VASO and BOLD imaging using GRASE-BOLD, show similar specificity and sensitivity and are thus useful tools for mesoscopic fMRI in the human cortex. Conclusion These techniques demonstrate sufficient sensitivity and specificity to allow layer-fMRI to be used by neuroscientists in a wide range of investigations of depth-dependent neural circuitry in the human brain.

[1]  P T Fox,et al.  Quantitative assessment of blood inflow effects in functional MRI signals , 1996, Magnetic resonance in medicine.

[2]  N. Shah,et al.  Comparison of Resting-State Brain Activation Detected by BOLD, Blood Volume and Blood Flow , 2018, Front. Hum. Neurosci..

[3]  Jun Hua,et al.  Implementation of vascular‐space‐occupancy MRI at 7T , 2013, Magnetic resonance in medicine.

[4]  David G Norris,et al.  3D single‐shot VASO using a maxwell gradient compensated GRASE sequence , 2009, Magnetic resonance in medicine.

[5]  Ravi S. Menon,et al.  Brief visual stimulation allows mapping of ocular dominance in visual cortex using fMRI , 2001, Human brain mapping.

[6]  V. Mountcastle,et al.  Response properties of neurons of cat's somatic sensory cortex to peripheral stimuli. , 1957, Journal of neurophysiology.

[7]  Essa Yacoub,et al.  High-field fMRI unveils orientation columns in humans , 2008, Proceedings of the National Academy of Sciences.

[8]  Samuel J. D. Lawrence,et al.  Laminar Organization of Working Memory Signals in Human Visual Cortex , 2018, Current Biology.

[9]  P Jezzard,et al.  Functional changes in CSF volume estimated using measurement of water T2 relaxation , 2009, Magnetic resonance in medicine.

[10]  R. Goebel,et al.  Frequency preference and attention effects across cortical depths in the human primary auditory cortex , 2015, Proceedings of the National Academy of Sciences.

[11]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[12]  F. D. Lange,et al.  Selective Activation of the Deep Layers of the Human Primary Visual Cortex by Top-Down Feedback , 2016, Current Biology.

[13]  S.N. Sotiropoulos,et al.  High resolution whole brain diffusion imaging at 7T for the Human Connectome Project , 2015, NeuroImage.

[14]  Lawrence L. Wald,et al.  Three dimensional echo-planar imaging at 7 Tesla , 2010, NeuroImage.

[15]  Essa Yacoub,et al.  Sensitivity and specificity considerations for fMRI encoding, decoding, and mapping of auditory cortex at ultra-high field , 2018, NeuroImage.

[16]  J H Duyn,et al.  Inflow versus deoxyhemoglobin effects in bold functional MRI using gradient echoes at 1.5 T , 1994, NMR in biomedicine.

[17]  David G Norris,et al.  Application of whole‐brain CBV‐weighted fMRI to a cognitive stimulation paradigm: Robust activation detection in a stroop task experiment using 3D GRASE VASO , 2011, Human brain mapping.

[18]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[19]  J. Gray,et al.  PsychoPy2: Experiments in behavior made easy , 2019, Behavior Research Methods.

[20]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[21]  R. Goebel,et al.  Cortical Depth Dependent Functional Responses in Humans at 7T: Improved Specificity with 3D GRASE , 2013, PloS one.

[22]  D. Feinberg,et al.  GRASE (Gradient‐and Spin‐Echo) imaging: A novel fast MRI technique , 1991, Magnetic resonance in medicine.

[23]  Anna Devor,et al.  First principle modeling of simultaneous VASO and BOLD fMRI with two-photon microscopy for optimal quantification of CBV changes in humans , 2019, BiOS.

[24]  K. Uğurbil,et al.  Spin‐echo fMRI in humans using high spatial resolutions and high magnetic fields , 2003, Magnetic resonance in medicine.

[25]  X. Zhang,et al.  In vivo blood T1 measurements at 1.5 T, 3 T, and 7 T , 2013, Magnetic resonance in medicine.

[26]  D. Norris,et al.  Layer‐specific BOLD activation in human V1 , 2010, Human brain mapping.

[27]  Laurentius Huber,et al.  High-Resolution CBV-fMRI Allows Mapping of Laminar Activity and Connectivity of Cortical Input and Output in Human M1 , 2017, Neuron.

[28]  Robert Turner,et al.  How Much Cortex Can a Vein Drain? Downstream Dilution of Activation-Related Cerebral Blood Oxygenation Changes , 2002, NeuroImage.

[29]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Lawrence L. Wald,et al.  Automatic cortical surface reconstruction of high-resolution T 1 echo planar imaging data , 2016, NeuroImage.

[31]  L Kaufman,et al.  Inner volume MR imaging: technical concepts and their application. , 1985, Radiology.

[32]  M. Garwood,et al.  A new localization method using an adiabatic pulse, BIR-4. , 1995, Journal of magnetic resonance. Series B.

[33]  P. Strick,et al.  Subdivisions of primary motor cortex based on cortico-motoneuronal cells , 2009, Proceedings of the National Academy of Sciences.

[34]  David C. Jangraw,et al.  Ultra-high resolution blood volume fMRI and BOLD fMRI in humans at 9.4 T: Capabilities and challenges , 2017, NeuroImage.

[35]  Jun Hua,et al.  Noninvasive functional imaging of cerebral blood volume with vascular‐space‐occupancy (VASO) MRI , 2013, NMR in biomedicine.

[36]  Essa Yacoub,et al.  High resolution data analysis strategies for mesoscale human functional MRI at 7 and 9.4 T , 2018, NeuroImage.

[37]  Essa Yacoub,et al.  Robust detection of ocular dominance columns in humans using Hahn Spin Echo BOLD functional MRI at 7 Tesla , 2007, NeuroImage.

[38]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[39]  Ravi S. Menon,et al.  Ocular dominance in human V1 demonstrated by functional magnetic resonance imaging. , 1997, Journal of neurophysiology.

[40]  Laurentius Huber,et al.  Which fMRI contrast is most specific for high resolution layer-dependent fMRI? Comparison study of GE-BOLD, SE-BOLD, T2-prep BOLD and blood volume fMRI , 2017 .

[41]  Uwe Aickelin,et al.  Tailored RF pulse for magnetization inversion at ultrahigh field , 2010, Magnetic resonance in medicine.

[42]  Claudine Joëlle Gauthier,et al.  Cortical lamina-dependent blood volume changes in human brain at 7T , 2015, NeuroImage.

[43]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[44]  Steen Moeller,et al.  Combined imaging–histological study of cortical laminar specificity of fMRI signals , 2006, NeuroImage.

[45]  Ping Wang,et al.  Cortical layer-dependent BOLD and CBV responses measured by spin-echo and gradient-echo fMRI: Insights into hemodynamic regulation , 2006, NeuroImage.

[46]  J. Mayhew,et al.  Concurrent fMRI and optical measures for the investigation of the hemodynamic response function , 2005, Magnetic resonance in medicine.

[47]  Tao Jin,et al.  Change of the cerebrospinal fluid volume during brain activation investigated by T1ρ-weighted fMRI , 2010, NeuroImage.

[48]  J. Butman,et al.  Whole‐brain cerebral blood flow mapping using 3D echo planar imaging and pulsed arterial tagging , 2011, Journal of magnetic resonance imaging : JMRI.

[49]  Leif Østergaard,et al.  Cerebral Blood Flow, Blood Volume, and Oxygen Metabolism Dynamics in Human Visual and Motor Cortex as Measured by Whole-Brain Multi-Modal Magnetic Resonance Imaging , 2009, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[50]  K. Uğurbil,et al.  Layer-Specific fMRI Reflects Different Neuronal Computations at Different Depths in Human V1 , 2012, PloS one.

[51]  Jyh-Horng Chen,et al.  Effects of CBV, CBF, and blood‐brain barrier permeability on accuracy of PASL and VASO measurement , 2010, Magnetic resonance in medicine.

[52]  Nikos K. Logothetis,et al.  fMRI at High Spatial Resolution: Implications for BOLD-Models , 2016, Front. Comput. Neurosci..

[53]  Tao Jin,et al.  Cortical layer-dependent dynamic blood oxygenation, cerebral blood flow and cerebral blood volume responses during visual stimulation , 2008, NeuroImage.

[54]  R. Goebel,et al.  Mapping the Organization of Axis of Motion Selective Features in Human Area MT Using High-Field fMRI , 2011, PloS one.

[55]  Robert Turner,et al.  Micro- and macrovascular contributions to layer-dependent blood volume fMRI: A multi-modal, multi-species comparison , 2015 .

[56]  Essa Yacoub,et al.  Sub-millimeter T2 weighted fMRI at 7 T: comparison of 3D-GRASE and 2D SE-EPI , 2015, Front. Neurosci..

[57]  Robert Turner,et al.  Slab‐selective, BOLD‐corrected VASO at 7 Tesla provides measures of cerebral blood volume reactivity with high signal‐to‐noise ratio , 2014, Magnetic resonance in medicine.

[58]  J. Pekar,et al.  Functional magnetic resonance imaging based on changes in vascular space occupancy , 2003, Magnetic resonance in medicine.

[59]  Laurentius Huber,et al.  Techniques for blood volume fMRI with VASO: From low-resolution mapping towards sub-millimeter layer-dependent applications , 2018, NeuroImage.

[60]  Nikos K Logothetis,et al.  Laminar specificity in monkey V1 using high-resolution SE-fMRI. , 2006, Magnetic resonance imaging.

[61]  Klaus Scheffler,et al.  Functional MRI in human subjects with gradient‐echo and spin‐echo EPI at 9.4 T , 2014, Magnetic resonance in medicine.

[62]  Lirong Yan,et al.  Detecting resting-state brain activity by spontaneous cerebral blood volume fluctuations using whole brain vascular space occupancy imaging , 2014, NeuroImage.

[63]  Keiji Tanaka,et al.  Human Ocular Dominance Columns as Revealed by High-Field Functional Magnetic Resonance Imaging , 2001, Neuron.

[64]  Essa Yacoub,et al.  Variable flip angle 3D‐GRASE for high resolution fMRI at 7 tesla , 2016, Magnetic resonance in medicine.

[65]  Kamil Ugurbil,et al.  An integrative model for neuronal activity-induced signal changes for gradient and spin echo functional imaging , 2009, NeuroImage.

[66]  Lucy S. Petro,et al.  Contextual Feedback to Superficial Layers of V1 , 2015, Current Biology.

[67]  K. Uğurbil,et al.  Microvascular BOLD contribution at 4 and 7 T in the human brain: Gradient‐echo and spin‐echo fMRI with suppression of blood effects , 2003, Magnetic resonance in medicine.

[68]  Lawrence L. Wald,et al.  Laminar analysis of 7T BOLD using an imposed spatial activation pattern in human V1 , 2010, NeuroImage.

[69]  David G. Norris,et al.  Spin-echo fMRI: The poor relation? , 2012, NeuroImage.

[70]  Peter C M van Zijl,et al.  Theoretical and experimental investigation of the VASO contrast mechanism , 2006, Magnetic resonance in medicine.