Advanced NMR Methods. P NMR in vivo: Perfused Rat Heart. P NMR in vivo: First Observations. Slide copies:
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1 Slide copies: Advanced NMR Methods Lecture 4: NMR and Living Systems Henri Bergson et Harry Potter NMR in vivo 31 P spectroscopy and cellular energetics 1 H spectroscopy and metabolism field gradients and localisation MR imaging methods image contrast and its chemical basis flow and functional imaging 4 NMR in vivo? 31 P NMR in vivo: First Observations 31 P NMR in vivo: Perfused Rat Heart In 1974 a 31 P spectrum was measured of a frog gastrocnemius muscle in a 5 mm NMR tube 10 ppm 10 ppm
2 31 P NMR in vivo: Cellular Energetics in Muscle (i) 31 P NMR in vivo: Cellular Energetics in Muscle (ii) P i (inorganic phosphate) PCr (phosphocreatine) ATP (adenosine triphosphate) Shift difference depends on ph These spectra show the effect of exercise on the 31 P spectrum of muscle in the human arm, measured using a surface coil. ATP is the fuel for muscle contraction: its concentration is kept up by using PCr reserves. Exercising with insufficient oxygen supply forces glucose to be burnt to lactic acid instead of CO 2, lowering ph; this changes the ionisation state of inorganic phosphate and causes the P i peak to shift. 31 P NMR allows the concentrations of PCr, ATP and Pi and the ph to be monitored in real time. Stop exercise and release tourniquet Exercise with tourniquet on Exercising the calf muscle while restricting the blood supply with a tourniquet causes rapid depletion of PCr, increase in P i, and lowering of ph. On stopping exercise and restoring blood flow, PCr recovers and P i drops. 13 C NMR in vivo: Human Muscle 13 C NMR in vivo: Rat Heart Metabolism lipid Diseased 13 C-labelled palmitate is infused into a beating heart, and is gradually metabolised into glutarate and triglycerides Normal creatine glucose 2
3 23 Na NMR in Perfused Rat Heart 1 H NMR of the Brain: Medical Applications 23 Na signals were measured in a heart perfused with a solution containing the shift reagent Dy(PPP 1 ) 2. This causes a difference in chemical shift between intracellular and extracellular Na + ions, allowing the inflow of Na + during hypoxia to be detected. normal 1 H spectra now allow localised measurement of concentrations of metabolites such as N-acetyl aspartate (NAA), phosphocreatine (PCr) and choline (Cho) hypoxic Field Gradients and Localisation: Signal Projections (i) Field Gradients and Localisation: Signal Projections (ii) The Larmor frequency is proportional to magnetic field : ν = γ B 0 /2π. Suppose that we have a sample (e.g. water) which has a single resonance (i.e. only one chemical shift) and that we make B 0 vary linearly along the z axis. If we measure the spectrum of the sample, the signal we see at one end of the spectrum will come from the top of the sample, the signal at the other end from the bottom, and the remainder of the spectrum from all positions in between. The spectrum measured is a projection of the signal distribution along the z direction: Applying gradients along different directions will yield different projections, reflecting the different spin densities along different axes z Higher B 0 x y z x y Lower B 0 RF coil Sample 3
4 Field Gradients and Localisation: Slice Selection A weak radiofrequency pulse will excite only a narrow range of Larmor frequencies. If we apply a weak RF pulse in the presence of a field gradient, only a thin slice of the sample will be excited: slice selection. This allows 2D images to be made of 3D objects. Higher B 0 RF pulse frequency Projection-Reconstruction Imaging The spectrum of an object measured in the presence of a field gradient along a given axis is a projection onto the axis of all the signal at right angles to it. By taking a series of measurements using gradients along different directions it is possible to determine the signal distribution in 2 or 3 dimensions. Consider an object consisting of cylinder and a square prism: if we measure projections at enough angles, we can reconstruct a full 2D image. Lower B 0 slice excited By using a shaped pulse we can arrange that there is close to full excitation (or inversion, or refocusing) over the desired slice, and little excitation outside it. Projection-Reconstruction Imaging A big showcase at the end of the room is a reconstitution of an item of furniture that once belonged to Rodin, containing an accumulation of all that was dear to the artist: Egyptian reliefs mingled with medieval Pietas or Persian vases. As in the lifetime of Rodin, the antiquities are mounted on a sculptor s turntable or a plaster plinth that he also used as stands for his own works. Auguste Rodin ( ) was probably the most famous and controversial sculptor at the turn of the twentieth century. His sculptures were so lifelike that his critics accused him of cheating by taking direct plaster casts of his models. In fact, he had developed a rather original method for converting what he observed into the finished product. The model sat on a rotating turntable with backlighting so that Rodin saw only a twodimensional silhouette. He then rotated the turntable in small angular steps to obtain a set of different views, thereby gathering the information needed to construct a faithful three-dimensional image. A case can be made that Rodin was the true originator of projection reconstruction. (Ray Freeman, in the Encyclopedia of Magnetic Resonance) The Collas machine Revision: Multidimensional NMR One-dimensional NMR Radiofrequency pulse! free induction decay S(t) Fourier transformation with respect to t! spectrum S(f) Two-Dimensional ("2D") NMR Pulse sequence including delay t 1! free induction decay S(t 2) Repeat incrementing t 1! matrix S(t 1,t 2) Fourier transformation with respect to t 2! S(t 1,f 2) Fourier transformation with respect to t 1! S(f 1,f 2) Signal dispersion as a function of f 1 depends on average signal frequency during t 1 Signal dispersion as a function of f 2 depends on frequency during t 2 4
5 Fourier NMR Imaging (i) In 1975, Richard Ernst showed that there was a direct analogy between the very new techniques of 2D NMR and MR imaging. Applying a field gradient during the evolution period of a simple 2D experiment and a second orthogonal gradient during the detection period allows a 2D image to be produced directly by double Fourier transformation. Fourier NMR Imaging (ii) Ernst s method can easily be extended to 3 dimensions; a possible pulse sequence (one of many) is shown below. RF signal acquired G x δ G y δ G z t (NMR imaging lost the N when it began to be used on patients) In this simplified spin warp gradient echo pulse sequence, the read gradient G z gives the signals recorded a frequency that varies linearly with z; the phase encoding gradients G x and G y, which are varied systematically on successive acquisitions like the evolution period t 1 in 2D NMR, make the signal phase vary linearly with x and y. A 3D FT of the whole data set gives a 3D image: The Mathematics of Fourier NMR Imaging (i) If the 3D distribution of proton concentration is P(x,y,z), then in the presence of field gradients g x, g y and g z the Larmor frequency in the rotating frame of reference at position (x,y,z) is γ(x g x + y g y + z g z )/2π Hz. Thus during the first phase-encoding period of a spin warp sequence, when an x gradient is applied, the signal builds up a phase angle γ x g x δ radians, the second (y) period adds a further angle γ y g y δ radians, and then during signal acquisition the phase evolves at a rate γ z g z radians per second. The total signal measured is thus S(g x,g y,t) =!(x, y,z)p(x, y, z)e i" gxx# e i" g yy# $$$ e i" gzzt dxdydz with the signal being recorded as a function of time t for a series of different values of the gradients g x and g y and a proportionality constant α that depends on the details of the experiment used. The Mathematics of Fourier NMR Imaging (ii) Fourier transforming these data with respect to the variables q x = γ g x δ /2π, q x = γ g y δ /2π and q z = γ g z t /2π gives an image I(x i, y i,z i ) $$$ $$$ dxdydze %2&i(q xx i +q y y i +q z z ) i dq x dq y dq z $$$ $$$ dq x dq y dq z dxdydz =!(x, y,z)p(x, y,z)e i" (g xx# +g y y# +g z zt ) =!(x, y,z)p(x, y,z)e 2&i(q xx+q y y+q z z)%2&i(q x x i +q y y i +q z z i ) = $$$!(x, y,z)p(x, y,z)#(x % x i )#(x % y i )#(z % z i )dxdydz =!(x, y,z)p(x i, y i,z i ) where the Dirac delta function δ(q q i ) has unit integral, is infinite where q = q i, and is zero everywhere else. Thus the 3D Fourier transform of the experimental data gives a 3D map of the proton concentration as a function of position. [In practice α depends on the NMR properties of the protons involved, which vary with position; unlike X-ray imaging, MRI allows the experimenter to control what physical properties (e.g. T 1, T 2, diffusion) control the image contrast.] 5
6 Spin Echo Imaging Variations in signal intensities in gradient echo images caused by local variations in B0can be avoided by using a spin echo: RF TR TE MR Imaging Apparatus (i) Whole body imaging instruments typically use horizontal superconducting solenoids with up to 1 m access bore and fields of up to 10 T. G x G y G z In this spin echo pulse sequence, a slice-selective 90 excitation pulse is used to restrict observation to a thin slice in the x direction. Phase encoding in the y direction during the echo evolution time TE and acquisition under a read gradient G z then gives a dataset which Fourier transforms to a 2D image in the yz plane. The echo time TE and the recovery time TR can be varied systematically to control image contrast. RF coils may be whole body, head, surface, extremity or internal. Stringent safety precautions are needed to avoid injury from ferromagnetic objects, RF heating etc. MR Imaging Apparatus (ii) MR Imaging of Fruit Vertical field room temperature solenoids can be used for special purposes, but are limited in field to < 2 T 6
7 Typical MR Images (i) Typical MR Images (ii) High resolution image of the ankle Very high resolution wrist image Image of complete spinal column Typical MR Images (iii) MR Images with Chemical Shift Discrimination High resolution knee image Image of arterial system Lower leg images; (left) normal image, (right) with fat signal suppressed. Blood vessels in subcutaneous fat show up clearly in the fat-suppressed image. 7
8 MRI Contrast T 1 and T 2 Weighted Images of Orange and Kiwi Fruit The contrast in an NMR image - the difference between high and low signal - depends on the concentration of spins in each voxel (at each position), but also on other, more subtle, properties. If the delay between measurements is not long compared to T 1, the magnetization will not recover fully and the signal strength will depend on T 1. Areas with long T 1 will show weak signals, and areas with short T 1, strong: the image is T 1 -weighted. Similarly, if the imaging pulse sequence includes a long spin echo delay, short T 2 signals will suffer more than long T 2 : T2-weighting. We can manipulate relaxation to highlight certain sorts of tissue or pathology by using paramagnetic or ferromagnetic contrast agents, for example injecting a stable gadolinium complex into the bloodstream to follow the circulation of the blood or to detect a breakdown in the blood:brain barrier. If we include strong field gradient pulses and a spin or stimulated echo in the imaging sequence we can produce a diffusion-weighted image, sensitive to tissue damage such as oedema (swelling). We can even use field gradient pulses along different axes to measure diffusion in different directions; 3D diffusion-weighted images can be used to map the way that nerves interconnect different parts of the brain. T 1 -weighted T 2 -weighted The skins of both fruits, and the pip of the orange, have short T 1 and show as bright in the T 1 -weighted image. The orange pip has a short T 2 so shows as dark in the T 2 -weighted image, as do the membranes between the orange segments. MRI Contrast: T 1 Weighting MRI Contrast: T 2 Weighting T 1 -weighting in brain discriminates between white and grey matter. T 2 -weighting in brain highlights liquids such as cerebrospinal fluid. 8
9 MRI Contrast: Magnetization Transfer Contrast MRI Contrast: Magnetization Transfer Contrast Living tissues contain a range of different components with different NMR properties. The exchange of magnetization between water and solid or semi-solid tissue components means that saturating radiofrequency irradiation applied far from the water resonance can lead to a tissue-dependent reduction in the water signal. In imaging this gives rise to magnetization transfer contrast (MTC). Water signal of human cartilage as a function of frequency of radiofrequency presaturation. Human knee images with (right) and without (left) presaturation. The presaturation in the right image reduces the signal from cartilage, improving the discrimination between the different layers of cartilage. Magnetization Transfer Dynamics Measurements of the kinetics of exchange of nuclear magnetization are used in many different applications of magnetic resonance. The same basic phenomena and analyses go under many different names: MR imaging Magnetization Transfer Dynamics: MTC The kinetics of magnetization transfer in MTC can be followed by applying a 180 pulse to the solid tissue components only, and then measuring the signal as a function of time. This is directly analogous to the dynamic NOE experiment in high resolution NMR, where the magnetization exchange is caused by the Overhauser effect; here the main mechanism is the exchange of OH protons. MTC High resolution NMR Solid-state NMR Dynamic NOE NOESY EXSY NOED Hoffman-Forsén experiment Saturation Transfer Difference (STD) Goldman-Shen experiment Water signal Solid signal Water signal of human cartilage as a function of time after selective inversion of the solid component. 9
10 Magnetization Transfer Dynamics: Hoffman-Forsén Experiment This is exactly the same as a dynamic NOE experiment using a selective 180 pulse, except that it is intended for the study of magnetization exchange by chemical reaction rather than by Overhauser effect. Amine proton signals of creatinine in pyridine-d 5 at 44 C as a function of time after the inversion of one signal, showing an exchange rate of 2.2 s 1. Magnetization Transfer Dynamics: STD In saturation transfer difference (STD) experiments, saturating RF irradiation is applied to a sample containing one or more small molecules and a large target molecule or assembly such as a protein. The negative NOE in the large species means that spin diffusion transfers saturation throughout the species by spin diffusion, and also to any small molecules that bind to it, identifying potential inhibitors or agonists. 1 H spectrum of a mixture of small molecules (0.5-6 mm) and 40 nm human rhinovirus 2 STD spectrum of the mixture showing transfer of saturation to the drug Repla394 Magnetization Transfer Dynamics: Goldman-Shen Experiment MRI Contrast: Contrast Agents In solid materials containing mixed crystalline and amorphous domains, the rate of transfer of magnetization through spin diffusion can be used to determine the domain size. The first two pulses saturate the signal of the crystalline component of a polypropylene film; measuring the signal as a function of recovery time t establishes the rate of spin diffusion and hence the domain size, here about 5 nm T 1 -weighted brain images (a) before and (b) after injecting the gadolinium chelate GdDTPA into the bloodstream. 10
11 MRI Angiography (i) MRI Angiography (ii) If we design our MRI experiment to show only signals from moving spins, we can make an angiogram: an image of the blood flow through arteries, veins etc. This image shows the vascular system of the upper torso and head Angiograms can also be made by injecting a contrast agent to lower the blood T 1 and hence increase its signal. The image shows a 2D rendering of the 3D brain angiogram of a stroke patient. The arrow points to a blockage in the left middle cerebral artery. Diffusion MRI Tractography Selective Excitation: the DANTE Sequence MRI experiments that measure the extent to which water molecules can diffuse in different directions allow the paths of fibres in the brain to be traced out τ τ τ 1/τ 1/τ 0 A train of m pulses of flip angle 90 /m spaced τ s apart gives full excitation only on resonance and at offsets of ±n/τ Hz, allowing just one resonance to be excited at a time J.Magn Reson. 23, 177 (1976); 29, 433 (1978) 11
12 DANTE: Delays Alternating with Nutations for Tailored Excitation Heart Imaging with DANTE Labelling Magnetizations alternately are rotated about X by pulses, and rotate about Z during delays, so that only magnetizations close to resonance (or n/τ Hz away) are excited Hyperpolarisation: 3He Imaging of Rat Lung Hyperpolarisation The sensitivity of NMR is in part limited by the low net spin state polarization (~ 1 part in 104) present at thermal equilibrium, determined by the Boltzmann distribution. Much larger polarizations, approaching 100%, are possible through selective optical pumping of hyperfine transitions (for gases such as 3 He, 129Xe), or at low temperature through the electronnuclear Overhauser effect and related mechanisms. 13C spectra of urea 3D MR images Measured in 1 s after 1.2 h of hyperpolarisation at 1.2 K Calculated lung oxygenation images Measured conventionally in 65 h 12
13 Hyperpolarisation: 13 C Imaging of Rat Lung Fast MR Imaging: Echo Planar Imaging RF G x G y G z Acquisition 2D images of hyperpolarised 13 C-labelled pyruvate as a function of time after intravenous injection Rapidly (< 1 ms) alternating the sign of the z gradient allows a long sequence of echoes, each blipped with a short pulse of y gradient, to be acquired, giving a 2D image in a fraction of a second - echo planar imaging (EPI). EPI is used in functional magnetic resonance imaging (fmri), in which changes in brain activity are measured. Functional Magnetic Resonance Imaging (fmri) fmri of Song Recognition in Zebra Finch Brain activity uses oxygen, changing the NMR properties of water. Mapping Blood Oxygen Level Dependent (BOLD) changes in NMR signal shows which areas of the brain are involved in different functions. song silence The sedated bird is placed in B 0 with an RF coil around its head, and the brain oxygen demand is monitored as a function of position to determine the change when it hears a recording of its own song 1 mm 3D brain images of a volunteer asked to think of words containing a given phoneme. The normal brain image is in grey, the activated areas in colour. 13
14 fmri: Real-Life Mind-Reading Slide copies: Advanced NMR Methods Lecture 4: NMR and Living Systems Henri Bergson et Harry Potter NMR in vivo 31 P spectroscopy and cellular energetics 1 H spectroscopy and metabolism 4 H. Bergson (Collège de France, ) Fantômes des vivants et recherche psychique, Society for Psychical Research, Londres, 1913 H. Potter field gradients and localisation MR imaging methods image contrast and its chemical basis flow and functional imaging 14
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