Magnetic imaging is a powerful tool for probing biological and physical systems. However, existing techniques either have poor spatial resolution compared to optical microscopy and are hence not generally applicable to imaging of sub-cellular structure (e.g., magnetic resonance imaging [MRI]1), or entail operating conditions that preclude application to living biological samples while providing sub-micron resolution (e.g., scanning superconducting quantum interference device [SQUID] microscopy2, electron holography3, and magnetic resonance force microscopy [MRFM]4). Here we demonstrate magnetic imaging of living cells (magnetotactic bacteria) under ambient laboratory conditions and with sub-cellular spatial resolution (400 nm), using an optically-detected magnetic field imaging array consisting of a nanoscale layer of nitrogen-vacancy (NV) colour centres implanted at the surface of a diamond chip. With the bacteria placed on the diamond surface, we optically probe the NV quantum spin states and rapidly reconstruct images of the vector components of the magnetic field created by chains of magnetic nanoparticles (magnetosomes) produced in the bacteria, and spatially correlate these magnetic field maps with optical images acquired in the same apparatus. Wide-field sCMOS acquisition allows parallel optical and magnetic imaging of multiple cells in a population with sub-micron resolution and >100 micron field-of-view. Scanning electron microscope (SEM) images of the bacteria confirm that the correlated optical and magnetic images can be used to locate and characterize the magnetosomes in each bacterium. The results provide a new capability for imaging bio-magnetic structures in living cells under ambient conditions with high spatial resolution, and will enable the mapping of a wide range of magnetic signals within cells and cellular networks5, 6.
Nuclear magnetic resonance (NMR) and magnetic resonance imaging (MRI) are wellestablished techniques that provide valuable information in a diverse set of disciplines but are currently limited to macroscopic sample volumes. Here we demonstrate nanoscale NMR spectroscopy and imaging under ambient conditions of samples containing multiple nuclear species, using nitrogen-vacancy (NV) colour centres in diamond as sensors. With single, shallow NV centres in a diamond chip and samples placed on the diamond surface, we perform NMR spectroscopy and one-dimensional MRI on few-nanometre-sized samples containing 1 H and 19 F nuclei. Alternatively, we employ a high-density NV layer near the surface of a diamond chip to demonstrate wide-field optical NMR spectroscopy of nanoscale samples containing 1 H, 19 F, and 31 P nuclei, as well as multi-species two-dimensional optical MRI with sub-micron resolution. For all diamond samples exposed to air, we identify a ubiquitous 1 H 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 nanoscale NMR and MRI applications such as studies of single proteins and functional biological imaging with subcellular resolution, as well as characterization of thin films with sub-nanometre resolution.
We demonstrate a robust experimental method for determining the depth of individual shallow Nitrogen-Vacancy (NV) centers in diamond with ∼ 1 nm uncertainty. We use a confocal microscope to observe single NV centers and detect the proton nuclear magnetic resonance (NMR) signal produced by objective immersion oil, which has well understood nuclear spin properties, on the diamond surface. We determine the NV center depth by analyzing the NV NMR data using a model that describes the interaction of a single NV center with the statistically-polarized proton spin bath. We repeat this procedure for a large number of individual, shallow NV centers and compare the resulting NV depths to the mean value expected from simulations of the ion implantation process used to create the NV centers, with reasonable agreement.
We introduce a broadly applicable technique to create nuclear spin singlet states in organic molecules and other many-atom systems. We employ a novel pulse sequence to produce a spin-lock induced crossing (SLIC) of the spin singlet and triplet energy levels, which enables triplet/singlet polarization transfer and singlet state preparation. We demonstrate the utility of the SLIC method by producing a long-lived nuclear spin singlet state on two strongly-coupled proton pairs in the tripeptide molecule phenylalanine-glycine-glycine dissolved in D2O, and by using SLIC to measure the J-couplings, chemical shift differences, and singlet lifetimes of the proton pairs. We show that SLIC is more efficient at creating nearly-equivalent nuclear spin singlet states than previous pulse sequence techniques, especially when triplet/singlet polarization transfer occurs on the same timescale as spin-lattice relaxation.There is great current interest in the controlled preparation and coherent manipulation of singlet states for nuclear spin pairs in molecules and other many-atom systems (e.g., spin networks in solids), as spin singlet states are largely decoupled from environmental perturbations that limit the spin state lifetime. For example, in liquid state experiments singlet states in nuclear spin pairs can exhibit lifetimes much longer than the single-spin polarization lifetime (T 1 ) [1][2][3][4][5][6][7][8][9][10][11][12]. In addition, nuclear spin singlet states can be used as a resource for spectroscopic interrogation of couplings within many-spin systems, including J-couplings, dipolar, and hyperfine couplings in both organic molecules and spin networks in solids [13][14][15]. Such singlet states exist naturally when nuclear spins are strongly J-coupled relative to their resonance frequency differences, ∆ν, i.e., J >> ∆ν. However, due to the differences in spin singlet and triplet state symmetries, it is not possible to transfer polarization from the triplet to the singlet state by directly driving a radiofrequency transition, which limits the control of singlet state preparation and manipulation. Tayler and Levitt demonstrated that triplet/singlet polarization transfer can instead be acheived using a series of π-pulse trains in which the pulse timing is synchronized to the J-coupling strength between nuclei [5]. This "M2S" sequence takes advantage of the small amount of mixing between singlet and triplet states that is present when- * devience@fas.harvard.edu † rwalsworth@cfa.harvard.edu ‡ mrosen@cfa.harvard.edu ever ∆ν > 0. Feng and Warren also showed that the M2S sequence can create singlet states in certain heteronuclear systems even when ∆ν = 0 [12]. These results hold promise for creating hyperpolarized singlet states without the need for a symmetry-breaking chemical reaction or continuous spin-locking [11]. However, in all results to date, the polarization transfer to the spin singlet state only occurs during the final third of the M2S sequence time, and before this stage the spin polarization occupies states subj...
Optically-detected magnetic resonance using Nitrogen Vacancy (NV) color centres in diamond is a leading modality for nanoscale magnetic field imaging, 1-3 as it provides single electron spin sensitivity, 4 three-dimensional resolution better than 1 nm, 5 and applicability to a wide range of physical 6-8 and biological 9 samples under ambient conditions. To date, however, NV-diamond magnetic imaging has been performed using "real space" techniques, which are either limited by optical diffraction to ≈250 nm resolution 10 or require slow, point-by-point scanning for nanoscale resolution, e.g., using an atomic force microscope, 11 magnetic tip, 5 or superresolution optical imaging. 12 Here we introduce an alternative technique of Fourier magnetic imaging using NV-diamond. In analogy with conventional magnetic resonance imaging (MRI), we employ pulsed magnetic field gradients to phase-encode spatial information on NV electronic spins in wavenumber or "k-space" 13 followed by a fast Fourier transform to yield real-space images with nanoscale resolution, wide field-of-view (FOV), and compressed sensing speed-up. 2Key advantages of NV-diamond Fourier magnetic imaging, relative to real-space imaging, are: (i) spatially multiplexed detection, 14 which enhances the signal-to-noise ratio (SNR) for typical NV centre densities; (ii) a high data acquisition rate that can be further boosted with compressed sensing; 15,16 and (iii) simultaneous acquisition of signal from all NV centres in the FOV, which allows probing of temporally correlated dynamics and provides isolation from system drift. As described below, we apply the Fourier technique using a relatively simple apparatus, and demonstrate one-dimensional imaging of individual NV centres with <5 nm resolution; two-dimensional imaging of multiple NV centres with ≈30 nm resolution; and two-dimensional imaging of nanoscale magnetic field patterns, with magnetic gradient sensitivity ~14 nT/nm/Hz 1/2 and spatial dynamic range (FOV/resolution) ~500. We also show that compressed sensing can accelerate the image acquisition time by an order-of-magnitude using sparse sampling followed by convex-optimization-based signal recovery. With further improvements, NV Fourier magnetic imaging may enable MRI with atom-scale resolution and centimeter FOV, with applications ranging from mapping the structure of individual biomolecules to functional MRI in living cells to studies of quantum phenomena in magnetic materials. Similar Fourier techniques could also be applied to NV-diamond imaging of nanoscale electric fields, temperature, and pressure, as well as to other optically-addressable solid-state spin systems.Schematic views of the Fourier magnetic microscope are shown in Figs. 1a and 1b.The diamond sample has a thin layer of NV centres at the surface created via ion implantation (see Methods). NV electronic spin states (Fig. 1c) are optically polarized with green illumination (λ=532 nm), coherently manipulated using resonant microwave fields applied by a microwave loop, and detected via sp...
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