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Quantitative Functional Imaging of the Brain: Towards Mapping Neuronal Activity by BOLD Fmri

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Quantitative Functional Imaging of the Brain: Towards Mapping Neuronal Activity by BOLD Fmri NMR IN BIOMEDICINE NMR Biomed. 2001;14:413–431 DOI:10.1002/nbm.733 Quantitative functional imaging of the brain: towards mapping neuronal activity by BOLD fMRI Fahmeed Hyder,1,2,5* Ikuhiro Kida,1 Kevin L. Behar,3 Richard P. Kennan,6 Paul K. Maciejewski4 and Douglas L. Rothman1,2,5 1Departments of Diagnostic Radiology, Magnetic Resonance Center for Research in Metabolism and Physiology, Yale University, New Haven, CT, USA 2Department of Biomedical Engineering, Yale University, New Haven, CT, USA 3Department of Psychiatry, Yale University, New Haven, CT, USA 4Department of Internal Medicine, Magnetic Resonance Center for Research in Metabolism and Physiology, Yale University, New Haven, CT, USA 5Section of Bioimaging Sciences, Yale University School of Medicine, New Haven, CT, USA 6Department of Diagnostic Radiology, Albert Einstein College of Medicine, Bronx, NY, USA Received 22 February 2001; Revised 22 August 2001; Accepted 22 August 2001 ABSTRACT: Quantitative magnetic resonance imaging (MRI) and spectroscopy (MRS) measurements of energy metabolism (i.e. cerebral metabolic rate of oxygen consumption, CMRO2), blood circulation (i.e. cerebral blood flow, CBF, and volume, CBV), and functional MRI (fMRI) signal over a wide range of neuronal activity and pharmacological treatments are used to interpret the neurophysiologic basis of blood oxygenation level dependent (BOLD) image-contrast at 7 T in glutamatergic neurons of rat cerebral cortex. Multi-modal MRI and MRS measurements of CMRO2, CBF, CBV and BOLD signal (both gradient-echo and spin-echo) are used to interpret the neuroenergetic basis of BOLD image-contrast. Since each parameter that can influence the BOLD image-contrast is measured quantitatively and separately, multi-modal measurements of changes in CMRO2, CBF, CBV, BOLD fMRI signal allow calibration and validation of the BOLD image-contrast. Good agreement between changes in CMRO2 calculated from BOLD theory and measured by 13C MRS, reveals that BOLD fMRI signal-changes at 7 T are closely linked with alterations in neuronal glucose oxidation, both for activation and deactivation paradigms. To determine the neurochemical basis of BOLD, pharmacological treatment with lamotrigine, which is a neuronal voltage- dependent Na channel blocker and neurotransmitter glutamate release inhibitor, is used in a rat forepaw stimulation model. Attenuation of the functional changes in CBF and BOLD with lamotrigine reveals that the fMRI signal is associated with release of glutamate from neurons, which is consistent with a link between neurotransmitter cycling and energy metabolism. Comparisons of CMRO2 and CBF over a wide dynamic range of neuronal activity provide insight into the regulation of energy metabolism and oxygen delivery in the cerebral cortex. The current results reveal the energetic and physiologic components of the BOLD fMRI signal and indicate the required steps towards mapping neuronal activity quantitatively by fMRI at steady-state. Consequences of these results from rat brain for similar calibrated BOLD fMRI studies in the human brain are discussed. Copyright 2001 John Wiley & Sons, Ltd. KEYWORDS: oxygen; glucose; lactate; glutamate; glutamine; glycogen; neuron; astrocyte; cerebral activity; lamotrigine *Correspondence to: F. Hyder, 126 MRC, 330 Cedar Street, Yale INTRODUCTION University, New Haven, CT 06510, USA. Email: [email protected] Functional imaging of mammalian brain with magnetic Abbreviations used: BOLD, blood-oxygenation level dependent; CBF, resonance imaging (MRI) has become a popular modality cerebral blood flow; CBV, cerebral blood volume; CMRglc, cerebral 1 metabolic rate for glucose consumption; CMRglc(ox), cerebral metabolic in neuroscience, but the exact relationship between the rate for glucose oxidation; CMRO2, cerebral metabolic rate for oxygen measured blood-oxygenation level dependent (BOLD) consumption; D, effective mass transfer coefficient for oxygen in the capillary bed; DANTE, delays alternating with nutations for tailored signal and the underlying neurophysiological parameters excitation; EPI, echo planar imaging; FLASH, fast low-angle shot; fMRI, remains unclear. The BOLD functional MRI (fMRI) functional MRI; ICED PEPSI, in vivo carbon edited detection with proton method allows detection of changes in blood oxygenation echo planar spectroscopic imaging; MRI, magnetic resonance imaging; during a physiological stimulation with gradient-echo MRS, magnetic resonance spectroscopy; OEF, oxygen extraction 2 fraction; PET, positron emission tomography; POCE, 1H observed 13C and spin-echo MRI. The BOLD image-contrast relies on editing; R1, longitudinal relaxation rate of tissue water; R2*, apparent physiologically induced changes in the magnetic proper- tissue water relaxation rate; R2, absolute tissue water relaxation rate; TE, ties of blood (oxyhemoglobin is diamagnetic and echo time; TIR, inversion recovery time; TR, recycle time; VTCA, tricarboxylic acid cycle flux; Y, blood oxygenation. deoxyhemoglobin is paramagnetic), where an increase Copyright 2001 John Wiley & Sons, Ltd. NMR Biomed. 2001;14:413–431 414 F. HYDER ET AL. in the fractional BOLD fMRI signal-change (DS/S > 0) is In this paper, we explore the neurophysiological basis consistent with a drop in venous deoxyhemoglobin of BOLD fMRI at 7 T in rat brain for the purpose of concentration.1–5 At steady-state, DS/S is given by neuronal activity mapping at steady-state. We present changes in neurophysiological parameters based on multi-modal measurements of changes in CMRO2, CBF, Fick’s principle3–5 CBV, and BOLD signal in rat cerebral cortex at 7 T over a wide range of neuronal activity and pharmacological ÁS=S A ÁCBF/CBF À ÁCMRO2=CMRO2 treatments. This approach differs from others in the 1 10–12 = 1 ÁCBF/CBFÀÁCBV/CBV field because each parameter in eqn (1) that influences the image-contrast is measured independently where A´ is a measurable physiological and static in rat cerebral cortex. Furthermore this approach allows magnetic field dependent constant and DCMRO2/CMRO2, validation of BOLD image-contrast, because the pre- DCBF/CBF and DCBV/CBV are the changes in cerebral dicted changes in CMRO2 based on BOLD theory metabolic rate of oxygen consumption, cerebral blood [rearrangement of eqn (1)] can be compared with the flow and cerebral blood volume, respectively (see independently measured changes in CMRO2 based on in Appendix A). Of these physiological parameters, vivo 13C MRS.6 The method of indirect 13C MRS 1 13 DCMRO2/CMRO2 is the most relevant for studying detection (i.e. using H instead of C) for CMRglc(ox) and 6,7 functional brain activity, because it is proportional to CMRO2 measurements is discussed. Insights into energy the change in energy consumption associated with metabolism and oxygen delivery of glutamatergic changes in neuronal activity induced by the stimulation. neurons are gained from comparisons of CMRO2 and Methods which provide direct measurement of the rate CBF over a wide range of activity. of cortical energy utilization or production are considered as ‘gold-standards’ for detection of neuronal activity. In the autoradiography method8 a 14C labeled analog of MATERIAL AND METHODS glucose, 2-deoxyglucose, is infused into the blood stream in trace amounts. The radioactive analog crosses the Animal preparation blood–brain barrier and is phosphorylated much like glucose. Since the 14C labeled phosphate cannot be Adult, male, Sprague–Dawley rats (110–280 g; fasted metabolized further, its concentration is proportional to >16 h) were tracheotomized under halothane (0.7–1.2%) the cerebral metabolic rate of glucose consumption anesthesia and artificially ventilated (70% N2O/30% O2). (CMRglc). The positron emission tomography (PET) A femoral artery was cannulated for continuous mean fluoro-deoxyglucose method uses similar principles to arterial blood pressure monitoring and periodic sampling deoxyglucose autoradiography but measures the distribu- for measurement of blood gases, pH, pressure, and tion of fluoro-deoxyglucose-6-phosphate. In vivo 13C glucose. Femoral veins were cannulated for intravenous magnetic resonance spectroscopy (MRS) detection of (i.v.) infusions of nicotine hydrogen tartrate, iron oxide infused 13C labeled glucose, a stable isotope, can provide contrast agent (AMI-227; Advanced Magnetics Inc., 6,7 13 13 important information on brain energy metabolism. Cambridge, MA), and/or D-[1- C] or [1,6- C]glucose The flow of 13C label from glucose to glutamate can be (99 atom %; Cambridge Isotopes, Andover, MA). used to calculate the tri-carboxylic acid cycle flux Intraperitoneal (i.p.) lines were inserted for administra- (VTCA), cerebral metabolic rates of glucose oxidation tion of anesthetic, paralyzing, and/or pharmacological (CMRglc(ox)) which is proportional to CMRO2. Under agents. The scalp was retracted and a layer of Saran Wrap normal physiological conditions, glucose is the major was placed over the skull. The rat was placed prone in a energy substrate in the mammalian cortex and it is cradle and covered with a water blanket to maintain body metabolized9 either in the presence of oxygen (via temperature (37 °C). Halothane was discontinued after glucose oxidation generating 32–34 ATP/glucose, CO2, the positioning and anesthesia was maintained through- and H2O) or absence of oxygen (via glycolysis and/or out with either morphine sulfate or a-chloralose and glycogen shunt generating 1–2 ATP/glucose and lactate). paralyzed with D-tubocurarine chloride (initial 0.5 mg/ BOLD fMRI has become the method
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