Nanoscale NMR spectroscopy and imaging of multiple nuclear species - 248413172444104215_nnano.2014.313

Nuclear magnetic resonance(NMR) spectroscopy and magnetic resonance imaging (MRI) provide non-invasive information about multiple nuclear species in bulk matter, with wideranging applications from basic physics and chemistry to biomedical imaging1. However, the spatial resolution of conventional NMR and MRI is limited2 to several micrometres even at large magnetic fields (>1T), which is inadequate for many frontier scientific applications such as single-molecule NMR spectroscopy and in vivo MRI of individual biological cells. A promising approach for nanoscale NMR and MRI exploits optical measurements of nitrogen–vacancy (NV) colour centres in diamond, which provide a combination of magnetic field sensitivity and nanoscale spatial resolution unmatched by any existing technology, while operating under ambient conditions in a robust, solid-state system3–5. Recently, single, shallow NV centres wereused to demonstrateNMRof nanoscaleensembles of proton spins, consisting of a statistical polarization equivalent to ∼100–1,000 spins in uniform samples covering the surface of a bulk diamond chip6,7. Here, we realize nanoscale NMR spectroscopy and MRI of multiple nuclear species (1H, 19F, 31P) in non-uniform (spatially structured) samples under ambient conditions and at moderate magnetic fields (∼20 mT) using two complementary sensor modalities. We interrogate single shallow NV centres in a diamond chip to perform simultaneous multi-species NMR spectroscopy and one-dimensional MRI on few-nanometre-sized samples placed on the diamond surface, which have a statistical spin polarization equivalent to ~100 polarized nuclei. We also use a diamond chip containing a shallow, high-density NV layer to demonstrate widefield optical NMR spectroscopy and two-dimensional MRI with sub-micrometre resolution of samples containing multiple nuclear species. For all diamond samples exposed to air, we identify a ubiquitous 1H NMR signal, consistent with a ∼1 nm layer of adsorbed hydrocarbons or water on the diamond surface and below any sample placed on the diamond. This work lays the foundation for diverse NMR and MRI applications at the nanoscale, such as determination of the structure and dynamics of single proteins and other biomolecules, identification of transition states in surface chemical reactions, functional biological imaging with subcellular resolution and cellular circuit field of view, and characterization of thin films with sub-nanometre resolution. The spatial resolution of conventional NMR and MRI is limited to macroscopic length scales due to the modest signal-to-noise ratio (SNR) provided by inductively detected thermal spin polarization, even in large (>1 T) magnetic fields, and the finite strength of the externally applied magnetic field gradients used for Fourier k-space imaging2. Other precision magnetic sensors have only macroscopic resolution (for example, semiconductor Hall effect sensors8 and atomic magnetometers9) and/or require operation at cryogenic temperatures or in vacuum (for example, superconducting quantum interference devices (SQUIDs)10 and magnetic resonance force microscopy (MRFM)11,12). Alternatively, NV centres in room-temperature diamond can be brought within a few nanometres of magnetic field sources of interest while maintaining long NV electronic spin coherence times (∼100 μs), a large Zeeman shift of the NV spin states (∼28 MHz mT−1), and optical preparation and readout of the NV spin (Fig. 1a). Highlights of NV-diamond magnetic sensing to date (all performed under ambient conditions) include sensitive spectroscopy13–15 and imaging16–18 of electron and nuclear spin impurities within the diamond sample, single electron spin imaging external to the diamond sensor19, sensing the aforementioned nanoscale NMR of proton spins in samples placed on the diamond surface6,7,20, targeted detection of single paramagnetic molecules attached to the diamond surface21, wide-field magnetic imaging of living magnetotactic bacteria, with sub-micrometre resolution22, and the recent realization of single proton NMR and MRI for very shallow NV centres23. In the first NV-diamond sensor modality used in the present work (Fig. 1b), a scanning confocal microscope interrogates a single NV centre located a few nanometres below the surface of a high-purity diamond chip. In the second sensor modality (Fig. 1c), the fluorescence from a shallow (5–15 nm deep), highdensity (3.5 × 1011 cm−2) NV ensemble layer near the surface of a diamond chip is imaged onto a charge-coupled device (CCD) camera24. The NV ensemble wide-field microscope provides pixel-by-pixel multi-species NMR spectroscopy and twodimensional MRI with sub-micrometre resolution and wide field of view, in a robust device that does not rely on identifying and addressing an optimally chosen NV centre, while the single NV confocal microscope can extract thickness information of layered thin films containing different nuclear species, with sub-nanometre resolution. For both sensor modalities, an NV NMR measurement proceeds in the following way. First, an 8-μs-long 532 nm laser pulse optically pumps the NV electronic spins into the |0〉 state. Resonant microwave pulses are then applied to the NV electronic spins. First, a π/2 pulse prepares a coherent superposition of ground spin states