Current Opinion in Solid State and Materials Science 17 (2013) 89–92

Contents lists available at SciVerse ScienceDirect

Current Opinion in Solid State and Materials Science

journal homepage: www.elsevier .com/locate /cossms

Editorial overview

Electron tomography in solid state and materials science – An Introduction

Electron tomography (ET) has become a well-established andimportant technique for the three-dimensional (3D) characteriza-tion of both organic and inorganic materials. The foundation ofthe technique as used today is described in the seminal works ofHart [1], Hoppe [2] and de Rosier and Klug [3]. These three papers,all published in 1968, focussed primarily on how to use bright-field(BF) electron microscopy images in order to determine the 3Dstructure of biological systems such as cells, viruses and bacteria.However, it was a further 20 years or so before ET began to be ap-plied in the materials science field, firstly on polymeric materials,such as block co-polymers [4] and later on porous catalyst struc-tures [5]. The contrast in the image used for such BF tomographyis either ‘mass-absorption contrast’, and in the life sciences heavymetal stains enhance that contrast, or ‘phase contrast’ for whichthe objective lens is defocussed. In materials science, however,samples are often crystalline in nature, and this BF mode (usingphase or mass-absorption contrast) may be problematic. Thecoherence of the beam leads to both Fresnel imaging artefacts, seenpredominantly at the edge of a specimen, and to diffraction con-trast, such as ‘bend contours’ or ‘thickness fringes’, evident in manyBF images. Such contrast does not conform to the ‘projectionrequirement’ [6], used extensively in tomographic reconstructionalgorithms, which states that the image (or projection) signalshould vary monotonically with a physical property, such as thick-ness. Diffraction contrast, for example, is related to the underlyingcrystal potential but, in general, in a complicated (and highly non-monotonic) way.

At the turn of the century, a new imaging mode for tomographywas introduced as a way to overcome (mostly) the problems men-tioned above and thus enable ET to be applied to a much widerrange of materials. High annular dark-field scanning transmissionelectron microscopy (HAADF STEM) imaging [7], in which a fo-cussed STEM probe is rastered across the specimen, is based ondetecting electrons scattered to high angles (>�50 mrad) using alarge annular detector, building up the image pixel by pixel. Theresultant image is one which is highly suited to tomography[8,9]. For the most part, it is free from diffraction and Fresnel con-trast and the intensity varies monotonically over a wide range ofthickness and density. Further, because the scattered intensityvaries approximately as the square of the atomic number, aHAADF-STEM image contains information about changes in thecomposition as well as the morphology (see e.g. [10]). This modeof ET has become adopted by many researchers as a standard toolfor materials science microscopy, although other modes, includingBF, still play an important role in extracting valuable 3Dinformation [11,12].

In this Special Issue, five papers describe recent technical devel-opments in ET and illustrate the application of the technique across

1359-0286/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.cossms.2013.07.006

a variety of materials and structures. The papers give a snap-shotof the state-of-the-art, valuable insights as to how the subjectmay develop in the next few years and illustrate the diversityand richness of the field at the present time.

Many key topics are touched upon by the authors in this SpecialIssue. In general, ET requires many images within a tilt series in or-der to produce a high fidelity reconstruction. Jinnai in his paper[13] shows how by using a needle-shaped sample, it is possibleto acquire data across the whole tilt range, improving the recon-struction quality. For thick specimens, the depth of field is crucialand a new STEM-based method involving very small convergenceangles helps in this regard. Once the data is acquired, alignmentand pre-processing is needed before a reconstruction can takeplace. The choice of reconstruction algorithms has grown in recentyears with an emphasis on reducing reconstruction artefacts fromlimited data sets. Both Fernandez [14] and Zecevic et al. [15] de-scribe the advantages and disadvantages of different reconstruc-tion algorithms with examples of their application. The work ofBals et al. [16] pushes the tomographic spatial resolution to theatomic level and, with only a few projections, a 3D reconstructioncan be made using prior information (such as periodicity con-straints). The paper by Wolf et al. [17] shows how it is possibleto reconstruct electromagnetic potentials in 3D, highlightinghow, combining ET with electron holography, electrostatic poten-tials at junctions, interfaces, and surfaces can be mapped in 3D.

In such a special issue, however, it is never possible to cover alltopics in depth. In the last part of this Introduction we mentionbriefly some other ET modes and their applications which comple-ment those described above and in the papers of this special issue.

Although HAADF-STEM images contain information aboutchanges in composition, for species with similar atomic numberlittle compositional contrast arises. More direct ways to image3D compositional changes are possible using inelastic scatteringand combining spectroscopy and tomography. Some of the earlywork in this area used energy-filtered TEM (EFTEM) to form 2D ele-mental maps across a tilt series [18,9]. 3D composition can bemapped using either core-loss ionization edges or low-loss (plas-mon) features [19]. More recently, STEM EELS has been used to ac-quire similar data sets but with increased spectral informationallowing, for example, different silicon signals (arising from theelement, a silicide and an oxide) to be mapped separately in 3D[20].

Early pioneering work with EDX tomography showed that map-ping 3D composition using X-ray spectra was also possible [18].However, a conventional EDX spectrometer on one side of the col-umn, coupled with limited detector geometry, inhibited its use as aroutine tomography tool [21]. Recently, the introduction of highsolid angle detectors (ca. 1 sr) with symmetrical collection

90 Editorial overview / Current Opinion in Solid State and Materials Science 17 (2013) 89–92

geometry has led to a renaissance in EDX tomography. Recentpapers [22,23] have shown how high quality EDX data sets canbe acquired in a reasonable time (see Fig. 1), and with novel recon-struction algorithms, even limited data sets should produce highfidelity reconstructions showing 3D compositional changes.

ET can also be applied to the study of crystalline defects andespecially dislocations. Whilst stereo-pairs may provide a qualita-tive or, at best, semi-quantitative view of dislocation networks, EToffers a way to reconstruct a 3D picture of a dislocation networkfrom which measurements (e.g. dislocation spacings) can be madeaccurately in any direction. For many years weak-beam DF imaging[24] has been regarded as the standard method to image single dis-locations or dislocation arrays revealing subtle fine-scale defectstructure e.g. partial dislocations, jogs, kinks, etc. It was thereforeperhaps natural for this imaging method to be extended to 3D toprovide the first electron tomographic reconstructions of disloca-tions. Analogous X-ray ‘topo-tomography’ had been introducedsome years previously [25] but with a spatial resolution that is or-ders of magnitude lower. As WBDF imaging relies on diffractioncontrast to form an image of the dislocation, one might thereforeconsider this technique to be invalid for electron tomography.However, if the diffraction conditions are kept constant (or near-constant) over the entire tilt range the reconstruction is still inter-pretable and suffers from relatively few artefacts [26]; for a recentexample of WBDF tomography see Fig. 2 [27].

A little later, ADF-STEM tomography was shown to provide 3Dreconstructions of dislocation networks with less extraneous con-trast compared to WBDF tomography [28]. In each ADF-STEM im-age, the annular detector is set to collect low to medium anglescattered electrons. Each ADF-STEM image can be considered asbeing approximately equivalent to a sum of individual DF-TEMimages each acquired using a reflection seen by the annular detec-tor. Each reflection will have a different excitation error (deviationparameter) and so this summation tends to enhance (and slightlyblur) the dislocation contrast but average out unwanted contrastsuch as that from thickness fringes or bend contours. ComparableBF-STEM images have also been used to reconstruct dislocationnetworks [29]. Very recent work has shown how it is possible toacquire high resolution HAADF-STEM images of dislocation struc-tures in nanoparticles as a function of tilt and to reconstruct a3D image of the dislocation core at atomic resolution [30]. This isa remarkable achievement given the difficulty of the experiment.

Fig. 1. Illustration of STEM-EDX tomography on a 28 nm FDSOI transistor. A rod-shaped sample is prepared with a focused ion beam, and STEM EDX spectrumimages are acquired from �90� to 90� with a 2� increment. 3D voxel renderings ofthe Ni, W and Cu stacks and the superposition of each elemental volume (Ni, Cu, W,Si, Ti, Hf and Ta) are shown. Reprinted from [22], with permission from Elsevier.

Slices through the reconstruction of nanoparticles of platinumindicated the presence of both screw and edge dislocations withimages showing atomic positions around the cores and well-defined Burgers vectors.

The introduction of new imaging modes coupled with novelsample holders and software has increased the versatility of elec-tron tomography not only in materials science but also in the lifesciences, the field where it originated. For example, the HAADF-STEM mode has been used for the study of bio-nano hybrids,showing an enhanced image and reconstruction contrast com-pared to results obtained using a conventional BF-TEM mode[31,32]. By using two different camera lengths, Sousa et al. showedthat with ADF-STEM it is possible to identify structures containingboth light and heavy atoms within biological specimens [33] andEFTEM tomography has been used to estimate quantitatively thephosphorus content in unstained sections of embedded cells[34]. Energy-filtered ADF-STEM would improve the reliability of3D quantification even further since the contribution of inelasti-cally-scattered electrons from the ADF-STEM images would be re-moved. BF-STEM imaging mode has also been investigated as away to image thicker samples. In [35], Sousa et al. showed thathigh-quality ET reconstructions of micron-thick biological samplescould be achieved by combining the BF-STEM mode with a dual-axis acquisition scheme, see Fig. 3. The possibility to image thickersamples enables larger biological structures to be studied with lessdependence on serial sectioning. Over the past few years the trans-fer of knowledge across the biological and materials science com-munities has increased and joint projects, especially in the area ofreconstruction algorithms and the development of segmentationtools [14], have progressed.

In a combined SEM-FIB microscope, so-called ‘slice and view’tomography can be used to reconstruct 3D images of objectsfar too large for (S)TEM analysis [36]. Using the SEM-FIB, slicesof material are removed sequentially revealing a new image ofthe surface below the previous one. By acquiring many suchimages one can build up a 3D reconstruction slice-by-slice. Slicethicknesses of less than 10 nm are now quite common and theoverall spatial resolution is starting to approach that of tomogra-phy in the TEM for certain samples. In addition, with an increasein slice thickness, large volumes (at moderate resolution) can bereconstructed, too large for TEM and too small for many X-raytomography experiments, revealing important structural detailsin this ‘mesoscopic’ regime. Finally, SEM-FIB, a technique de-signed originally for materials science, has recently been appliedto the life sciences, where, for example, stained blocks of ratbrain were sliced and imaged to produce a total volume of sev-eral thousands of lm3 with an isotropic voxel size estimated be-tween 5 and 7.5 nm [37]. Tilt series tomography of thin samplesmay also be undertaken in the SEM. By installing a tilt stage thatallows full rotation about an axis perpendicular to the beam, theSEM can be used as a low voltage STEM using a post-sampleSTEM detector [38].

Lastly, it is possible to acquire 3D crystallographic data in theTEM using a combination of electron diffraction and tomography.By acquiring diffraction patterns (often using precession electrondiffraction (PED)) across a large tilt range, reciprocal space canbe finely sampled and, using standard structure solution rou-tines, a 3D map of the atomic positions can be reconstructed[39,40].

In this short Introduction we have tried to set the scene for thework reported in this Special Issue. These five review papers showhow the field of electron tomography, particularly in the solid stateand materials science arena has grown rapidly and matured into atechnique used across a remarkably wide range of materials. It iscertain that further applications of electron tomography will springforth and ever-more complex devices and structures will demand

Fig. 2. 3D analysis of dislocation-precipitate interactions in an Al–Mg–Sc alloy by weak-beam dark-field electron tomography. (a) and (b) are tomographic reconstructionsviewed from two different angles. (c) and (d) are views extracted from a 3D model produced by tracing the dislocations structures in the tomogram. Reprinted from [27], withpermission from Cambridge University Press.

Fig. 3. (a) Dual-axis BF-STEM tomography of 1 lm thick section of pancreatic beta cells. The resolution and SNR achieved with this technique are comparable to thoseobtained by conventional BF-TEM tomography of 300 nm thick section shown in (b). Reprinted from [35], with permission from Elsevier.

Editorial overview / Current Opinion in Solid State and Materials Science 17 (2013) 89–92 91

more sophisticated 3D imaging. The pioneers of electron tomogra-phy whose work started the topic nearly 5 decades ago would beperhaps both surprised and delighted that their methods havefound such wide-ranging and important application across muchof the physical sciences.

Acknowledgments

The authors acknowledge funding from the European ResearchCouncil under the European Union’s Seventh FrameworkProgramme (FP7/2007-2013)/ERC Grant Agreement 291522-3DIMAGE.

References

[1] Hoppe W, Langer R, Knesch G, Poppe C. Protein-kristallstrukturanalyse mitElektronenstrahlen. Naturwissenschaften 1968;55:333–6.

[2] Hart RG. Electron microscopy of unstained biological material: the polytropicmontage. Science 1968;159:1464–7.

[3] De Rosier DJ, Klug A. Reconstruction of three dimensional structures fromelectron micrographs. Nature 1968;217:130–4.

[4] Spontak RJ, Williams MC, Agard DA. Three-dimensional study of cylindricalmorphology in a styrene–butadiene–styrene block copolymer. Polymer1988;29(3):387–95.

[5] Koster AJ, Ziese U, Verkleij AJ, Janssen AH, de Jong KP. Three-dimensionaltransmission electron microscopy: a novel imaging and characterizationtechnique with nanometer scale resolution for materials science. J PhysChem 2000;104(40):9368–70.

92 Editorial overview / Current Opinion in Solid State and Materials Science 17 (2013) 89–92

[6] Hawkes PW. The electron microscope as a structure projector. In: Frank J,editor. Electron tomography. New York (London): Plenum Press; 1992. p. 17–38.

[7] Howie A. Image contrast and localized signal selection techniques. J Microsc1979;117(1):11–23.

[8] Midgley PA, Weyland M, Thomas JM, Johnson BFG. Z-Contrast tomography: atechnique in three-dimensional nanostructural analysis based on Rutherfordscattering. Chem Commun 2001;10:907–8.

[9] Midgley PA, Weyland M. 3D electron microscopy in the physical sciences: thedevelopment of Z-contrast and EFTEM tomography. Ultramicroscopy2003;96(3–4):413–31.

[10] Macias-Montero M, Borras A, Saghi Z, Romero-Gomez P, Sanchez-Valencia JR,Gonzalez JC, et al. Superhydrophobic supported Ag-NPs@ZnO nanorods withphotoactivity in the visible range. J Mater Chem 2012;22:1341–6.

[11] Prieto G, Zecevic J, Friedrich H, de Jong KP, de Jongh PE. Towards stablecatalysts by controlling collective properties of supported metal nanoparticles.Nat Mater 2013;12:34–9.

[12] Florea I, Demortière A, Petit C, Bulou H, Hirlimann C, Ersen O. 3D quantitativeanalysis of platinum nanocrystal superlattices by electron tomography. ACSNano 2012;6(3):2574–81.

[13] Jinnai H, Jiang X. Electron tomography in soft materials. Curr Opin Solid StateMater Sci 2013; current issue.

[14] Fernandez JJ. Computational methods for materials characterization byelectron tomography. Curr Opin Solid State Mater Sci 2013; current issue.

[15] Zecevic J, de Jong KP, de Jongh PE. Progress in electron tomography to assessthe 3D nanostructure of catalysts. Curr Opin Solid State Mater Sci 2013;current issue.

[16] Bals S, Van Aert S, Van Tendeloo G. High resolution electron tomography. CurrOpin Solid State Mater Sci 2013; current issue.

[17] Wolf D, Lubk A, Röder F, Lichte H. Electron holographic tomography. Curr OpinSolid State Mater Sci 2013; current issue.

[18] Möbus G, Doole RC, Inkson BJ. Spectroscopic electron tomography.Ultramicroscopy 2003;96(3–4):433–51.

[19] Gass MH, Koziol KK, Windle AH, Midgley PA. Four-dimensional spectraltomography of carbonaceous nanocomposites. Nano Lett 2006;6(3):376–9.

[20] Jarausch K, Thomas P, Leonard DN, Twesten R, Booth CR. Four-dimensionalSTEM-EELS: enabling nano-scale chemical tomography. Ultramicroscopy2009;109(4):326–37.

[21] Saghi Z, Xu X, Peng Y, Inkson BJ, Möbus G. Three-dimensional chemicalanalysis of tungsten probes by energy dispersive X-ray nanotomography. ApplPhys Lett 2007;91. 251906-1–3.

[22] Lepinay K, Lorut F, Pantel R, Epicier T. Chemical 3D tomography of 28 nm highK metal gate transistor: STEM XEDS experimental method and results. Micron2013;47:43–9.

[23] Genc A, Kovarik L, Gu M, Cheng H, Plachinda P, Pullan L, et al. XEDS STEMtomography for 3D chemical characterization of nanoscale particles.Ultramicroscopy 2013;131:24–32.

[24] Cockayne DJH, Ray ILF, Whelan MJ. Investigations of dislocation strain fieldsusing weak beams. Phil Mag 1969;20(168). 1265:70.

[25] Ludwig W, Cloetens P, Härtwig J, Baruchel J, Hamelin B, Bastie P. Three-dimensional imaging of crystal defects by ‘topo-tomography’. J ApplCrystallogr 2001;34:602–7.

[26] Barnard JS, Sharp J, Tong JR, Midgley PA. High-resolution three-dimensionalimaging of dislocations. Science 2006;313(5785):319.

[27] Liu GS, Robertson IM. Three-dimensional visualization of dislocation-precipitate interactions in a Al–4Mg–0.3Sc alloy using weak-beam dark-fieldelectron tomography. J Mater Res 2011;26(4):514–22.

[28] Sharp J, Barnard JS, Kaneko K, Higashida K, Midgley PA. Dislocationtomography made easy: a reconstruction from ADF STEM images obtainedusing automated image shift correction. J Phys: Conf Ser 2008;126:012013:1–4.

[29] Hata S, Miyazaki H, Miyazaki S, Mitsuhara M, Tanaka M, Kaneko K, et al. High-angle triple-axis specimen holder for three-dimensional diffraction contrastimaging in transmission electron microscopy. Ultramicroscopy2011;111(8):1168–75.

[30] Chen CC, Zhu C, White ER, Chiu CY, Scott MC, Regan BC, et al. Three-dimensional imaging of dislocations in a nanoparticle at atomic resolution.Nature 2013;496(7443):74–7.

[31] Porter AE, Gass M, Muller K, Skepper JN, Midgley PA, Welland M. Directimaging of single-walled carbon nanotubes in cells. Nat Nanotechnol2007;2(11):713–7.

[32] Wei H, Wang Z, Zhang J, House S, Gao Y, Yang L, et al. Time-dependent,protein-directed growth of gold nanoparticles within a single crystal oflysozyme. Nat Nanotechnol 2011;6:93–7.

[33] Sousa AA, Hohmann-Marriott M, Aronova MA, Zhang G, Leapman RD.Determination of quantitative distributions of heavy-metal stain inbiological specimens by annular dark-field STEM. J Struct Biol2008;162:14–28.

[34] Aronova MA, Kim YC, Harmon R, Sousa AA, Zhang G, Leapman RD. Three-dimensional elemental mapping of phosphorus by quantitative electronspectroscopic tomography (QuEST). J Struct Biol 2007;160(1):35–48.

[35] Sousa AA, Azari AA, Zhang G, Leapman RD. Dual-axis electron tomography ofbiological specimens: extending the limits of specimen thickness with bright-field STEM imaging. J Struct Biol 2011;174(1):107–14.

[36] Inkson BJ, Steer T, Möbus G, Wagner T. Subsurface nanoindentationdeformation of Cu–Al multilayers mapped in 3D by focused ion beammicroscopy. J Microsc 2001;201(2):256–69.

[37] Cantoni M, Genoud C, Hébert C, Knott G. Large volume, isotropic, 3D imagingof cell structure on the nanometer scale. Microsc Anal 2010:13–6.

[38] Jornsanoh P, Thollet G, Ferreira J, Masenelli-Varlot K, Gauthier C, Bogner A.Electron tomography combining ESEM and STEM: a new 3D imagingtechnique. Ultramicroscopy 2011;111:1247–54.

[39] Kolb U, Gorelik T, Kübel C, Otten MT, Hubert D. Towards automated diffractiontomography: Part I—Data acquisition. Ultramicroscopy 2007;107(6–7):507–13.

[40] Kolb U, Mugnaioli E, Gorelik TE. Automated electron diffraction tomography –a new tool for nano crystal structure analysis. Cryst Res Technol2011;46(6):542–54.

Paul A. MidgleyZineb Saghi

Department of Materials Science and Metallurgy,University of Cambridge, Pembroke Street, Cambridge CB2 3QZ, UK

Tel.: +44 1223 334561; fax: +44 1223 334567E-mail address: pam33@cam.ac.uk (P.A. Midgley)

Available online 26 July 2013