Dynamic perfusion and diffusion MRI of cortical spreading depolarization in photothrombotic ischemia

Yu-Chieh Jill Kao; Wenjing Li; Hsin-Yi Lai; Esteban A. Oyarzabal; Weili Lin; Yen-Yu Shih

doi:10.1016/j.nbd.2014.07.005

Dynamic perfusion and diffusion MRI of cortical spreading depolarization in photothrombotic ischemia

Yu-Chieh Jill Kao, Wenjing Li, Hsin-Yi Lai, Esteban A. Oyarzabal, Weili Lin, Yen-Yu Shih

Research output: Contribution to journal › Article › peer-review

31 Citations (Scopus)

Abstract

Cortical spreading depolarization (CSD) is known to exacerbate ischemic damage, as the number of CSDs correlates with the final infarct volumes and suppressing CSDs improves functional outcomes. To investigate the role of CSD in ischemic damage, we developed a novel rat model of photothrombotic ischemia using a miniature implantable optic fiber that allows lesion induction inside the magnetic resonance imaging (MRI) scanner. We were able to precisely control the location and the size of the ischemic lesion, and continuously monitor dynamic perfusion and diffusion MRI signal changes at high temporal resolution before, during and after the onset of focal ischemia. Our model showed that apparent diffusion coefficient (ADC) and cerebral blood flow (CBF) in the ischemic core dropped immediately after lesion onset by 20. ±. 6 and 41. ±. 23%, respectively, and continually declined over the next 5. h. Meanwhile, CSDs were observed in all animals (n. =. 36) and displayed either a transient decrease of ADC by 17. ±. 3% or an increase of CBF by 104. ±. 15%. All CSDs were initiated from the rim of the ischemic core, propagated outward, and confined to the ipsilesional cortex. Additionally, we demonstrated that by controlling the size of perfusion-diffusion mismatch (which approximates the penumbra) in our model, the number of CSDs correlated with the mismatch area rather than the final infarct volume. This study introduces a novel platform to study CSDs in real-time with high reproducibility using MRI. © 2014 Elsevier Inc.

Original language	English
Pages (from-to)	131-139
Number of pages	9
Journal	Neurobiology of Disease
Volume	71
DOIs	https://doi.org/10.1016/j.nbd.2014.07.005
Publication status	Published - 2014
Externally published	Yes

Keywords

Cortical spreading depolarization
Diffusion MRI
Ischemia
Perfusion MRI
Rat
adult
animal experiment
animal model
article
brain blood flow
brain cortex
brain infarction size
brain ischemia
controlled study
cortical spreading depolarization
depolarization
diffusion weighted imaging
male
neuroimaging
nonhuman
nuclear magnetic resonance scanner
optic nerve fiber
perfusion weighted imaging
priority journal
rat
adverse effects
analysis of variance
animal
brain circulation
cerebral artery disease
complication
diagnostic use
disease model
laser
magnetic resonance angiography
pathophysiology
physiology
Sprague Dawley rat
spreading cortical depression
time
rose bengal
Analysis of Variance
Animals
Brain Ischemia
Cerebral Cortex
Cerebrovascular Circulation
Cortical Spreading Depression
Diffusion Magnetic Resonance Imaging
Disease Models, Animal
Infarction, Middle Cerebral Artery
Lasers
Magnetic Resonance Angiography
Male
Rats
Rats, Sprague-Dawley
Rose Bengal
Time Factors

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Cite this

@article{66de1da8c5fe4714abb13e5d886047d2,

title = "Dynamic perfusion and diffusion MRI of cortical spreading depolarization in photothrombotic ischemia",

abstract = "Cortical spreading depolarization (CSD) is known to exacerbate ischemic damage, as the number of CSDs correlates with the final infarct volumes and suppressing CSDs improves functional outcomes. To investigate the role of CSD in ischemic damage, we developed a novel rat model of photothrombotic ischemia using a miniature implantable optic fiber that allows lesion induction inside the magnetic resonance imaging (MRI) scanner. We were able to precisely control the location and the size of the ischemic lesion, and continuously monitor dynamic perfusion and diffusion MRI signal changes at high temporal resolution before, during and after the onset of focal ischemia. Our model showed that apparent diffusion coefficient (ADC) and cerebral blood flow (CBF) in the ischemic core dropped immediately after lesion onset by 20. ±. 6 and 41. ±. 23%, respectively, and continually declined over the next 5. h. Meanwhile, CSDs were observed in all animals (n. =. 36) and displayed either a transient decrease of ADC by 17. ±. 3% or an increase of CBF by 104. ±. 15%. All CSDs were initiated from the rim of the ischemic core, propagated outward, and confined to the ipsilesional cortex. Additionally, we demonstrated that by controlling the size of perfusion-diffusion mismatch (which approximates the penumbra) in our model, the number of CSDs correlated with the mismatch area rather than the final infarct volume. This study introduces a novel platform to study CSDs in real-time with high reproducibility using MRI. {\textcopyright} 2014 Elsevier Inc.",

keywords = "Cortical spreading depolarization, Diffusion MRI, Ischemia, Perfusion MRI, Rat, adult, animal experiment, animal model, article, brain blood flow, brain cortex, brain infarction size, brain ischemia, controlled study, cortical spreading depolarization, depolarization, diffusion weighted imaging, male, neuroimaging, nonhuman, nuclear magnetic resonance scanner, optic nerve fiber, perfusion weighted imaging, priority journal, rat, adverse effects, analysis of variance, animal, brain circulation, cerebral artery disease, complication, diagnostic use, disease model, laser, magnetic resonance angiography, pathophysiology, physiology, Sprague Dawley rat, spreading cortical depression, time, rose bengal, Analysis of Variance, Animals, Brain Ischemia, Cerebral Cortex, Cerebrovascular Circulation, Cortical Spreading Depression, Diffusion Magnetic Resonance Imaging, Disease Models, Animal, Infarction, Middle Cerebral Artery, Lasers, Magnetic Resonance Angiography, Male, Rats, Rats, Sprague-Dawley, Rose Bengal, Time Factors",

author = "Kao, {Yu-Chieh Jill} and Wenjing Li and Hsin-Yi Lai and Oyarzabal, {Esteban A.} and Weili Lin and Yen-Yu Shih",

note = "被引用次數：3 Export Date: 6 April 2016 CODEN: NUDIE 通訊地址: Shih, Y.Y.I.; Experimental Neuroimaging Laboratory, Departments of Neurology and Biomedical Research Imaging Center, University of North Carolina, 130 Mason Farm Road, CB# 7513, Chapel Hill, NC 27599, United States; 電子郵件： [email protected] 化學物質/CAS: rose bengal, 11121-48-5, 11139-83-6, 632-68-8; Rose Bengal 商標： BioSpec, Bruker 製造商： Bruker 參考文獻: Ackerman, J.J., Neil, J.J., The use of MR-detectable reporter molecules and ions to evaluate diffusion in normal and ischemic brain (2010) NMR Biomed., 23, pp. 725-733; Ayata, C., Spreading depression and neurovascular coupling (2013) Stroke, 44, pp. S87-S89; Bardutzky, J., Differences in ischemic lesion evolution in different rat strains using diffusion and perfusion imaging (2005) Stroke, 36, pp. 2000-2005; Boquillon, M., Photochemically induced, graded cerebral infarction in the mouse by laser irradiation evolution of brain edema (1992) J. Pharmacol. Toxicol. Methods, 27, pp. 1-6; Bouts, M.J., Early identification of potentially salvageable tissue with MRI-based predictive algorithms after experimental ischemic stroke (2013) J. Cereb. Blood Flow Metab., 33, pp. 1075-1082; Bouts, M.J., Lesion development and reperfusion benefit in relation to vascular occlusion patterns after embolic stroke in rats (2014) J. Cereb. Blood Flow Metab., 34, pp. 332-338; Dani, K.A., Computed tomography and magnetic resonance perfusion imaging in ischemic stroke: definitions and thresholds (2011) Ann. Neurol., 70, pp. 384-401; D'Arceuil, H.E., de Crespigny, A., Dynamic diffusion magnetic resonance imaging of infarct formation and peri-infarct spreading depression after middle cerebral artery occlusion (MCAO) in macacca fasicularis (2011) Open Neuroimag. J., 5, pp. 153-159; de Graaf, R.A., High magnetic field water and metabolite proton T1 and T2 relaxation in rat brain in vivo (2006) Magn. Reson. Med., 56, pp. 386-394; Dietrich, W.D., Photothrombotic infarction triggers multiple episodes of cortical spreading depression in distant brain regions (1994) J. Cereb. Blood Flow Metab., 14, pp. 20-28; Dijkhuizen, R.M., Correlation between tissue depolarizations and damage in focal ischemic rat brain (1999) Brain Res., 840, pp. 194-205; Dobkin, J.A., Evidence for transhemispheric diaschisis in unilateral stroke (1989) Arch. Neurol., 46, pp. 1333-1336; Dreier, J.P., The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease (2011) Nat. Med., 17, pp. 439-447; Dreier, J.P., Endothelin-1 potently induces Le{\~a}o's cortical spreading depression in vivo in the rat: a model for an endothelial trigger of migrainous aura? (2002) Brain, 125, pp. 102-112; Enager, P., Pathway-specific variations in neurovascular and neurometabolic coupling in rat primary somatosensory cortex (2009) J. Cereb. Blood Flow Metab., 29, pp. 976-986; Fabricius, M., Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex (2006) Brain, 129, pp. 778-790; Feuerstein, D., Detecting tissue deterioration after brain injury: regional blood flow level versus capacity to raise blood flow (2014) J. Cereb. Blood Flow Metab., 34, pp. 1117-1127; Freiman, M., In vivo assessment of optimal b-value range for perfusion-insensitive apparent diffusion coefficient imaging (2012) Med. Phys., 39, pp. 4832-4839; Gordon, G.R., Brain metabolism dictates the polarity of astrocyte control over arterioles (2008) Nature, 456, pp. 745-749; Gramer, M., Device for simultaneous positron emission tomography, laser speckle imaging and RGB reflectometry: validation and application to cortical spreading depression and brain ischemia in rats (2014) Neuroimage, 94, pp. 250-262; Guiou, M., Cortical spreading depression produces long-term disruption of activity-related changes in cerebral blood volume and neurovascular coupling (2005) J. Biomed. Opt., 10, p. 11004; Heiss, W.D., The concept of the penumbra: can it be translated to stroke management? (2010) Int. J. Stroke, 5, pp. 290-295; Heiss, W.D., The ischemic penumbra: correlates in imaging and implications for treatment of ischemic stroke. The Johann Jacob Wepfer award 2011 (2011) Cerebrovasc. Dis., 32, pp. 307-320; Herscovitch, P., Raichle, M.E., What is the correct value for the brain-blood partition coefficient for water? (1985) J. Cereb. Blood Flow Metab., 5, pp. 65-69; Hoehn-Berlage, M., Diffusion-weighted NMR imaging: application to experimental focal cerebral ischemia (1995) NMR Biomed., 8, pp. 345-358; Hoehn-Berlage, M., Changes of relaxation times (T1, T2) and apparent diffusion coefficient after permanent middle cerebral artery occlusion in the rat: temporal evolution, regional extent, and comparison with histology (1995) Magn. Reson. Med., 34, pp. 824-834; Hoehn-Berlage, M., Evolution of regional changes in apparent diffusion coefficient during focal ischemia of rat brain: the relationship of quantitative diffusion NMR imaging to reduction in cerebral blood flow and metabolic disturbances (1995) J. Cereb. Blood Flow Metab., 15, pp. 1002-1011; Howells, D.W., Different strokes for different folks: the rich diversity of animal models of focal cerebral ischemia (2010) J. Cereb. Blood Flow Metab., 30, pp. 1412-1431; Jones, P.B., Simultaneous multispectral reflectance imaging and laser speckle flowmetry of cerebral blood flow and oxygen metabolism in focal cerebral ischemia (2008) J. Biomed. Opt., 13, p. 044007; Kidwell, C.S., A trial of imaging selection and endovascular treatment for ischemic stroke (2013) N. Engl. J. Med., 368, pp. 914-923; Koh, D.M., Intravoxel incoherent motion in body diffusion-weighted MRI: reality and challenges (2011) AJR Am. J. Roentgenol., 196, pp. 1351-1361; Lai, H.Y., Design, simulation and experimental validation of a novel flexible neural probe for deep brain stimulation and multichannel recording (2012) J. Neural Eng., 9, p. 036001; Lai, H.Y., Robust deep brain stimulation functional MRI procedures in rats and mice using an MR-compatible tungsten microwire electrode (2014) Magn. Reson. Med., , (in press); Lai, H.Y., Functional MRI reveals frequency-dependent responses during deep brain stimulation at the subthalamic nucleus or internal globus pallidus (2014) Neuroimage, 84, pp. 11-18; Latour, L.L., Spreading waves of decreased diffusion coefficient after cortical stimulation in the rat brain (1994) Magn. Reson. Med., 32, pp. 189-198; Li, F., A new method to improve in-bore middle cerebral artery occlusion in rats: demonstration with diffusion- and perfusion-weighted imaging (1998) Stroke, 29, pp. 1715-1719. , [discussion 1719-20]; Moseley, M.E., Anisotropy in diffusion-weighted MRI (1991) Magn. Reson. Med., 19, pp. 321-326; Nakamura, H., Spreading depolarizations cycle around and enlarge focal ischaemic brain lesions (2010) Brain, 133, pp. 1994-2006; Paul, J.S., Imaging the development of an ischemic core following photochemically induced cortical infarction in rats using Laser Speckle Contrast Analysis (LASCA) (2006) Neuroimage, 29, pp. 38-45; Paxinos, G., Watson, C., (2005) The Rat Brain in Stereotaxic Coordinates, , Elsevier Academic Press, Amsterdam; Boston; Piilgaard, H., Lauritzen, M., Persistent increase in oxygen consumption and impaired neurovascular coupling after spreading depression in rat neocortex (2009) J. Cereb. Blood Flow Metab., 29, pp. 1517-1527; Reid, E., Penumbra detection using PWI/DWI mismatch MRI in a rat stroke model with and without comorbidity: comparison of methods (2012) J. Cereb. Blood Flow Metab., 32, pp. 1765-1777; Risher, W.C., Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra (2010) J. Neurosci., 30, pp. 9859-9868; Rother, J., MR detection of cortical spreading depression immediately after focal ischemia in the rat (1996) J. Cereb. Blood Flow Metab., 16, pp. 214-220; Schroeter, M., Astroglial responses in photochemically induced focal ischemia of the rat cortex (1995) Exp. Brain Res., 106, pp. 1-6; Shen, Q., Pixel-by-pixel spatiotemporal progression of focal ischemia derived using quantitative perfusion and diffusion imaging (2003) J. Cereb. Blood Flow Metab., 23, pp. 1479-1488; Shih, Y.Y., Whole-brain functional magnetic resonance imaging mapping of acute nociceptive responses induced by formalin in rats using atlas registration-based event-related analysis (2008) J. Neurosci. Res., 86, pp. 1801-1811; Shih, Y.Y., Striatal and cortical BOLD, blood flow, blood volume, oxygen consumption, and glucose consumption changes in noxious forepaw electrical stimulation (2011) J. Cereb. Blood Flow Metab., 31, pp. 832-841; Shih, Y.Y., Pharmacological MRI of the choroid and retina: blood flow and BOLD responses during nitroprusside infusion (2012) Magn. Reson. Med., 68, pp. 1273-1278; Shih, Y.Y., Ultra high-resolution fMRI and electrophysiology of the rat primary somatosensory cortex (2013) Neuroimage, 73, pp. 113-120; Shih, Y.Y., Comparison of retinal and cerebral blood flow between continuous arterial spin labeling MRI and fluorescent microsphere techniques (2013) J. Magn. Reson. Imaging, , (in press); Shih, Y.Y., Imaging neurovascular function and functional recovery after stroke in the rat striatum using forepaw stimulation (2014) J. Cereb. Blood Flow Metab., , (in press); Shin, H.K., Vasoconstrictive neurovascular coupling during focal ischemic depolarizations (2006) J. Cereb. Blood Flow Metab., 26, pp. 1018-1030; Sparta, D.R., Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits (2012) Nat. Protoc., 7, pp. 12-23; Takano, K., The role of spreading depression in focal ischemia evaluated by diffusion mapping (1996) Ann. Neurol., 39, pp. 308-318; Takano, T., Cortical spreading depression causes and coincides with tissue hypoxia (2007) Nat. Neurosci., 10, pp. 754-762; van Dorsten, F.A., Dynamic changes of ADC, perfusion, and NMR relaxation parameters in transient focal ischemia of rat brain (2002) Magn. Reson. Med., 47, pp. 97-104; Wahl, M., Change of cerebrovascular reactivity after cortical spreading depression in cats and rats (1987) Brain Res., 411, pp. 72-80; Wardlaw, J.M., Neuroimaging in acute ischaemic stroke: insights into unanswered questions of pathophysiology (2010) J. Intern. Med., 267, pp. 172-190; Watson, B.D., Induction of reproducible brain infarction by photochemically initiated thrombosis (1985) Ann. Neurol., 17, pp. 497-504; Wester, P., A photothrombotic 'ring' model of rat stroke-in-evolution displaying putative penumbral inversion (1995) Stroke, 26, pp. 444-450",

year = "2014",

doi = "10.1016/j.nbd.2014.07.005",

language = "English",

volume = "71",

pages = "131--139",

journal = "Neurobiology of Disease",

issn = "0969-9961",

publisher = "Academic Press Inc.",

}

TY - JOUR

T1 - Dynamic perfusion and diffusion MRI of cortical spreading depolarization in photothrombotic ischemia

AU - Kao, Yu-Chieh Jill

AU - Li, Wenjing

AU - Lai, Hsin-Yi

AU - Oyarzabal, Esteban A.

AU - Lin, Weili

AU - Shih, Yen-Yu

N1 - 被引用次數：3 Export Date: 6 April 2016 CODEN: NUDIE 通訊地址: Shih, Y.Y.I.; Experimental Neuroimaging Laboratory, Departments of Neurology and Biomedical Research Imaging Center, University of North Carolina, 130 Mason Farm Road, CB# 7513, Chapel Hill, NC 27599, United States; 電子郵件： [email protected] 化學物質/CAS: rose bengal, 11121-48-5, 11139-83-6, 632-68-8; Rose Bengal 商標： BioSpec, Bruker 製造商： Bruker 參考文獻: Ackerman, J.J., Neil, J.J., The use of MR-detectable reporter molecules and ions to evaluate diffusion in normal and ischemic brain (2010) NMR Biomed., 23, pp. 725-733; Ayata, C., Spreading depression and neurovascular coupling (2013) Stroke, 44, pp. S87-S89; Bardutzky, J., Differences in ischemic lesion evolution in different rat strains using diffusion and perfusion imaging (2005) Stroke, 36, pp. 2000-2005; Boquillon, M., Photochemically induced, graded cerebral infarction in the mouse by laser irradiation evolution of brain edema (1992) J. Pharmacol. Toxicol. Methods, 27, pp. 1-6; Bouts, M.J., Early identification of potentially salvageable tissue with MRI-based predictive algorithms after experimental ischemic stroke (2013) J. Cereb. Blood Flow Metab., 33, pp. 1075-1082; Bouts, M.J., Lesion development and reperfusion benefit in relation to vascular occlusion patterns after embolic stroke in rats (2014) J. Cereb. Blood Flow Metab., 34, pp. 332-338; Dani, K.A., Computed tomography and magnetic resonance perfusion imaging in ischemic stroke: definitions and thresholds (2011) Ann. Neurol., 70, pp. 384-401; D'Arceuil, H.E., de Crespigny, A., Dynamic diffusion magnetic resonance imaging of infarct formation and peri-infarct spreading depression after middle cerebral artery occlusion (MCAO) in macacca fasicularis (2011) Open Neuroimag. J., 5, pp. 153-159; de Graaf, R.A., High magnetic field water and metabolite proton T1 and T2 relaxation in rat brain in vivo (2006) Magn. Reson. Med., 56, pp. 386-394; Dietrich, W.D., Photothrombotic infarction triggers multiple episodes of cortical spreading depression in distant brain regions (1994) J. Cereb. Blood Flow Metab., 14, pp. 20-28; Dijkhuizen, R.M., Correlation between tissue depolarizations and damage in focal ischemic rat brain (1999) Brain Res., 840, pp. 194-205; Dobkin, J.A., Evidence for transhemispheric diaschisis in unilateral stroke (1989) Arch. Neurol., 46, pp. 1333-1336; Dreier, J.P., The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease (2011) Nat. Med., 17, pp. 439-447; Dreier, J.P., Endothelin-1 potently induces Leão's cortical spreading depression in vivo in the rat: a model for an endothelial trigger of migrainous aura? (2002) Brain, 125, pp. 102-112; Enager, P., Pathway-specific variations in neurovascular and neurometabolic coupling in rat primary somatosensory cortex (2009) J. Cereb. Blood Flow Metab., 29, pp. 976-986; Fabricius, M., Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex (2006) Brain, 129, pp. 778-790; Feuerstein, D., Detecting tissue deterioration after brain injury: regional blood flow level versus capacity to raise blood flow (2014) J. Cereb. Blood Flow Metab., 34, pp. 1117-1127; Freiman, M., In vivo assessment of optimal b-value range for perfusion-insensitive apparent diffusion coefficient imaging (2012) Med. Phys., 39, pp. 4832-4839; Gordon, G.R., Brain metabolism dictates the polarity of astrocyte control over arterioles (2008) Nature, 456, pp. 745-749; Gramer, M., Device for simultaneous positron emission tomography, laser speckle imaging and RGB reflectometry: validation and application to cortical spreading depression and brain ischemia in rats (2014) Neuroimage, 94, pp. 250-262; Guiou, M., Cortical spreading depression produces long-term disruption of activity-related changes in cerebral blood volume and neurovascular coupling (2005) J. Biomed. Opt., 10, p. 11004; Heiss, W.D., The concept of the penumbra: can it be translated to stroke management? (2010) Int. J. Stroke, 5, pp. 290-295; Heiss, W.D., The ischemic penumbra: correlates in imaging and implications for treatment of ischemic stroke. The Johann Jacob Wepfer award 2011 (2011) Cerebrovasc. Dis., 32, pp. 307-320; Herscovitch, P., Raichle, M.E., What is the correct value for the brain-blood partition coefficient for water? (1985) J. Cereb. Blood Flow Metab., 5, pp. 65-69; Hoehn-Berlage, M., Diffusion-weighted NMR imaging: application to experimental focal cerebral ischemia (1995) NMR Biomed., 8, pp. 345-358; Hoehn-Berlage, M., Changes of relaxation times (T1, T2) and apparent diffusion coefficient after permanent middle cerebral artery occlusion in the rat: temporal evolution, regional extent, and comparison with histology (1995) Magn. Reson. Med., 34, pp. 824-834; Hoehn-Berlage, M., Evolution of regional changes in apparent diffusion coefficient during focal ischemia of rat brain: the relationship of quantitative diffusion NMR imaging to reduction in cerebral blood flow and metabolic disturbances (1995) J. Cereb. Blood Flow Metab., 15, pp. 1002-1011; Howells, D.W., Different strokes for different folks: the rich diversity of animal models of focal cerebral ischemia (2010) J. Cereb. Blood Flow Metab., 30, pp. 1412-1431; Jones, P.B., Simultaneous multispectral reflectance imaging and laser speckle flowmetry of cerebral blood flow and oxygen metabolism in focal cerebral ischemia (2008) J. Biomed. Opt., 13, p. 044007; Kidwell, C.S., A trial of imaging selection and endovascular treatment for ischemic stroke (2013) N. Engl. J. Med., 368, pp. 914-923; Koh, D.M., Intravoxel incoherent motion in body diffusion-weighted MRI: reality and challenges (2011) AJR Am. J. Roentgenol., 196, pp. 1351-1361; Lai, H.Y., Design, simulation and experimental validation of a novel flexible neural probe for deep brain stimulation and multichannel recording (2012) J. Neural Eng., 9, p. 036001; Lai, H.Y., Robust deep brain stimulation functional MRI procedures in rats and mice using an MR-compatible tungsten microwire electrode (2014) Magn. Reson. Med., , (in press); Lai, H.Y., Functional MRI reveals frequency-dependent responses during deep brain stimulation at the subthalamic nucleus or internal globus pallidus (2014) Neuroimage, 84, pp. 11-18; Latour, L.L., Spreading waves of decreased diffusion coefficient after cortical stimulation in the rat brain (1994) Magn. Reson. Med., 32, pp. 189-198; Li, F., A new method to improve in-bore middle cerebral artery occlusion in rats: demonstration with diffusion- and perfusion-weighted imaging (1998) Stroke, 29, pp. 1715-1719. , [discussion 1719-20]; Moseley, M.E., Anisotropy in diffusion-weighted MRI (1991) Magn. Reson. Med., 19, pp. 321-326; Nakamura, H., Spreading depolarizations cycle around and enlarge focal ischaemic brain lesions (2010) Brain, 133, pp. 1994-2006; Paul, J.S., Imaging the development of an ischemic core following photochemically induced cortical infarction in rats using Laser Speckle Contrast Analysis (LASCA) (2006) Neuroimage, 29, pp. 38-45; Paxinos, G., Watson, C., (2005) The Rat Brain in Stereotaxic Coordinates, , Elsevier Academic Press, Amsterdam; Boston; Piilgaard, H., Lauritzen, M., Persistent increase in oxygen consumption and impaired neurovascular coupling after spreading depression in rat neocortex (2009) J. Cereb. Blood Flow Metab., 29, pp. 1517-1527; Reid, E., Penumbra detection using PWI/DWI mismatch MRI in a rat stroke model with and without comorbidity: comparison of methods (2012) J. Cereb. Blood Flow Metab., 32, pp. 1765-1777; Risher, W.C., Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra (2010) J. Neurosci., 30, pp. 9859-9868; Rother, J., MR detection of cortical spreading depression immediately after focal ischemia in the rat (1996) J. Cereb. Blood Flow Metab., 16, pp. 214-220; Schroeter, M., Astroglial responses in photochemically induced focal ischemia of the rat cortex (1995) Exp. Brain Res., 106, pp. 1-6; Shen, Q., Pixel-by-pixel spatiotemporal progression of focal ischemia derived using quantitative perfusion and diffusion imaging (2003) J. Cereb. Blood Flow Metab., 23, pp. 1479-1488; Shih, Y.Y., Whole-brain functional magnetic resonance imaging mapping of acute nociceptive responses induced by formalin in rats using atlas registration-based event-related analysis (2008) J. Neurosci. Res., 86, pp. 1801-1811; Shih, Y.Y., Striatal and cortical BOLD, blood flow, blood volume, oxygen consumption, and glucose consumption changes in noxious forepaw electrical stimulation (2011) J. Cereb. Blood Flow Metab., 31, pp. 832-841; Shih, Y.Y., Pharmacological MRI of the choroid and retina: blood flow and BOLD responses during nitroprusside infusion (2012) Magn. Reson. Med., 68, pp. 1273-1278; Shih, Y.Y., Ultra high-resolution fMRI and electrophysiology of the rat primary somatosensory cortex (2013) Neuroimage, 73, pp. 113-120; Shih, Y.Y., Comparison of retinal and cerebral blood flow between continuous arterial spin labeling MRI and fluorescent microsphere techniques (2013) J. Magn. Reson. Imaging, , (in press); Shih, Y.Y., Imaging neurovascular function and functional recovery after stroke in the rat striatum using forepaw stimulation (2014) J. Cereb. Blood Flow Metab., , (in press); Shin, H.K., Vasoconstrictive neurovascular coupling during focal ischemic depolarizations (2006) J. Cereb. Blood Flow Metab., 26, pp. 1018-1030; Sparta, D.R., Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits (2012) Nat. Protoc., 7, pp. 12-23; Takano, K., The role of spreading depression in focal ischemia evaluated by diffusion mapping (1996) Ann. Neurol., 39, pp. 308-318; Takano, T., Cortical spreading depression causes and coincides with tissue hypoxia (2007) Nat. Neurosci., 10, pp. 754-762; van Dorsten, F.A., Dynamic changes of ADC, perfusion, and NMR relaxation parameters in transient focal ischemia of rat brain (2002) Magn. Reson. Med., 47, pp. 97-104; Wahl, M., Change of cerebrovascular reactivity after cortical spreading depression in cats and rats (1987) Brain Res., 411, pp. 72-80; Wardlaw, J.M., Neuroimaging in acute ischaemic stroke: insights into unanswered questions of pathophysiology (2010) J. Intern. Med., 267, pp. 172-190; Watson, B.D., Induction of reproducible brain infarction by photochemically initiated thrombosis (1985) Ann. Neurol., 17, pp. 497-504; Wester, P., A photothrombotic 'ring' model of rat stroke-in-evolution displaying putative penumbral inversion (1995) Stroke, 26, pp. 444-450

PY - 2014

Y1 - 2014

N2 - Cortical spreading depolarization (CSD) is known to exacerbate ischemic damage, as the number of CSDs correlates with the final infarct volumes and suppressing CSDs improves functional outcomes. To investigate the role of CSD in ischemic damage, we developed a novel rat model of photothrombotic ischemia using a miniature implantable optic fiber that allows lesion induction inside the magnetic resonance imaging (MRI) scanner. We were able to precisely control the location and the size of the ischemic lesion, and continuously monitor dynamic perfusion and diffusion MRI signal changes at high temporal resolution before, during and after the onset of focal ischemia. Our model showed that apparent diffusion coefficient (ADC) and cerebral blood flow (CBF) in the ischemic core dropped immediately after lesion onset by 20. ±. 6 and 41. ±. 23%, respectively, and continually declined over the next 5. h. Meanwhile, CSDs were observed in all animals (n. =. 36) and displayed either a transient decrease of ADC by 17. ±. 3% or an increase of CBF by 104. ±. 15%. All CSDs were initiated from the rim of the ischemic core, propagated outward, and confined to the ipsilesional cortex. Additionally, we demonstrated that by controlling the size of perfusion-diffusion mismatch (which approximates the penumbra) in our model, the number of CSDs correlated with the mismatch area rather than the final infarct volume. This study introduces a novel platform to study CSDs in real-time with high reproducibility using MRI. © 2014 Elsevier Inc.

AB - Cortical spreading depolarization (CSD) is known to exacerbate ischemic damage, as the number of CSDs correlates with the final infarct volumes and suppressing CSDs improves functional outcomes. To investigate the role of CSD in ischemic damage, we developed a novel rat model of photothrombotic ischemia using a miniature implantable optic fiber that allows lesion induction inside the magnetic resonance imaging (MRI) scanner. We were able to precisely control the location and the size of the ischemic lesion, and continuously monitor dynamic perfusion and diffusion MRI signal changes at high temporal resolution before, during and after the onset of focal ischemia. Our model showed that apparent diffusion coefficient (ADC) and cerebral blood flow (CBF) in the ischemic core dropped immediately after lesion onset by 20. ±. 6 and 41. ±. 23%, respectively, and continually declined over the next 5. h. Meanwhile, CSDs were observed in all animals (n. =. 36) and displayed either a transient decrease of ADC by 17. ±. 3% or an increase of CBF by 104. ±. 15%. All CSDs were initiated from the rim of the ischemic core, propagated outward, and confined to the ipsilesional cortex. Additionally, we demonstrated that by controlling the size of perfusion-diffusion mismatch (which approximates the penumbra) in our model, the number of CSDs correlated with the mismatch area rather than the final infarct volume. This study introduces a novel platform to study CSDs in real-time with high reproducibility using MRI. © 2014 Elsevier Inc.

KW - Cortical spreading depolarization

KW - Diffusion MRI

KW - Ischemia

KW - Perfusion MRI

KW - Rat

KW - adult

KW - animal experiment

KW - animal model

KW - article

KW - brain blood flow

KW - brain cortex

KW - brain infarction size

KW - brain ischemia

KW - controlled study

KW - cortical spreading depolarization

KW - depolarization

KW - diffusion weighted imaging

KW - male

KW - neuroimaging

KW - nonhuman

KW - nuclear magnetic resonance scanner

KW - optic nerve fiber

KW - perfusion weighted imaging

KW - priority journal

KW - rat

KW - adverse effects

KW - analysis of variance

KW - animal

KW - brain circulation

KW - cerebral artery disease

KW - complication

KW - diagnostic use

KW - disease model

KW - laser

KW - magnetic resonance angiography

KW - pathophysiology

KW - physiology

KW - Sprague Dawley rat

KW - spreading cortical depression

KW - time

KW - rose bengal

KW - Analysis of Variance

KW - Animals

KW - Brain Ischemia

KW - Cerebral Cortex

KW - Cerebrovascular Circulation

KW - Cortical Spreading Depression

KW - Diffusion Magnetic Resonance Imaging

KW - Disease Models, Animal

KW - Infarction, Middle Cerebral Artery

KW - Lasers

KW - Magnetic Resonance Angiography

KW - Male

KW - Rats

KW - Rats, Sprague-Dawley

KW - Rose Bengal

KW - Time Factors

U2 - 10.1016/j.nbd.2014.07.005

DO - 10.1016/j.nbd.2014.07.005

M3 - Article

SN - 0969-9961

VL - 71

SP - 131

EP - 139

JO - Neurobiology of Disease

JF - Neurobiology of Disease

ER -

Dynamic perfusion and diffusion MRI of cortical spreading depolarization in photothrombotic ischemia

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