SQUID-Detected Magnetic Resonance Imaging in Microtesla Fields (2008)

Magnetic resonance imaging (MRI) has developed into a powerful clinical tool for imaging the human body (1). This technique is based on nuclear magnetic resonance (NMR) of protons (2, 3) in a static magnetic field B{sub 0}. An applied radiofrequency pulse causes the protons to precess about B{sub 0} at their Larmor frequency {nu}{sub 0} = ({gamma}/2{pi})B{sub 0}, where {gamma} is the gyromagnetic ratio; {gamma}/2{pi} = 42.58 MHz/tesla. The precessing protons generate an oscillating magnetic field and hence a voltage in a nearby coil that is amplified and recorded. The application of three-dimensional magnetic field gradients specifies a unique magnetic field and thus an NMR frequency in each voxel of the subject, so that with appropriate encoding of the signals one can acquire a complete image (4). Most clinical MRI systems involve magnetic fields generated by superconducting magnets, and the current trend is to higher magnetic fields than the widely used 1.5-T systems (5). Nonetheless, there is ongoing interest in the development of less expensive imagers operating at lower fields. Commercially available 0.2-T systems based on permanent magnets offer both lower cost and a more open access than their higher-field counterparts, at the expense of signal-to-noise-ratio (SNR) and spatial resolution. At the still lower field of 0.03 mT maintained by a conventional, room-temperature solenoid, Connolly and co-workers (6, 7) obtain good spatial resolution and signal-to-noise ratio (SNR) by prepolarizing the protons in a field B{sub p} of 0.3 T. Prepolarization (8) enhances the magnetic moment of an ensemble of protons over that produced by the lower precession field; after the polarizing field is removed, the higher magnetic moment produces a correspondingly larger signal during its precession in B{sub 0}. Using the same method, Stepisnik et al. (9) obtained MR images in the Earth's magnetic field ({approx} 50 {micro}T). Alternatively, one can enhance the signal amplitude in MRI using laser polarized noble gases such as {sup 3}He or {sup 129}Xe (10-12). Hyperpolarized gases were used successfully to image the human lung in fields on the order of several mT (13-15). To overcome the sensitivity loss of Faraday detection at low frequencies, ultrasensitive magnetometers based on the Superconducting QUantum Interference Device (SQUID) (16) are used to detect NMR and MRI signals (17-24). Recently, SQUID-based MRI systems capable of acquiring in vivo images have appeared. For example, in the 10-mT system of Seton et al. (18) signals are coupled to a SQUID via a superconducting tuned circuit, while Clarke and coworkers (22, 25, 26) developed a system at 132 {micro}T with an untuned input circuit coupled to a SQUID. In a quite different approach, atomic magnetometers have been used recently to detect the magnetization (27) and NMR signal (28) of hyperpolarized gases. This technique could potentially be used for low-field MRI in the future. The goal of this review is to summarize the current state-of-the-art of MRI in microtesla fields detected with SQUIDs. The principles of SQUIDs and NMR are briefly reviewed. We show that very narrow NMR linewidths can be achieved in low magnetic fields that are quite inhomogeneous, with illustrative examples from spectroscopy. After describing our ultralow-field MRI system, we present a variety of images. We demonstrate that in microtesla fields the longitudinal relaxation T{sub 1} is much more material dependent than is the case in high fields; this results in a substantial improvement in 'T{sub 1}-weighted contrast imaging'. After outlining the first attempts to combine microtesla NMR with magnetoencephalography (MEG) (29), we conclude with a discussion of future directions.