Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Nanoscale X-ray imaging

Abstract

Recent years have seen significant progress in the field of soft- and hard-X-ray microscopy, both technically, through developments in source, optics and imaging methodologies, and also scientifically, through a wide range of applications. While an ever-growing community is pursuing the extensive applications of today's available X-ray tools, other groups are investigating improvements in techniques, including new optics, higher spatial resolutions, brighter compact sources and shorter-duration X-ray pulses. This Review covers recent work in the development of direct image-forming X-ray microscopy techniques and the relevant applications, including three-dimensional biological tomography, dynamical processes in magnetic nanostructures, chemical speciation studies, industrial applications related to solar cells and batteries, and studies of archaeological materials and historical works of art.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Four common X-ray microscopy optics (a–d) and three common image-forming systems (e–g).
Figure 2: Materials science applications of nanoscale X-ray imaging.
Figure 3: Biological applications of nanoscale X-ray imaging.
Figure 4: Environmental applications of nanoscale X-ray imaging.
Figure 5: Archaeological and paleontological applications of microscale X-ray imaging.
Figure 6: 3D rendered images of a mouse bone.

References

  1. Attwood, D. T. Soft X-rays and extreme ultraviolet radiation: Principles and applications Ch. 1–9 (Cambridge Univ., 1999).

    Google Scholar 

  2. Kirkpatrick, P. & Baez, A. V. Formation of optical images by X-rays. J. Opt. Soc. Am. 38, 766–773 (1948).

    ADS  Google Scholar 

  3. Baez, A. V. Fresnel zone plate for optical image formation using extreme ultraviolet and soft X radiation. J. Opt. Soc. Am. 51, 405–412 (1961).

    ADS  Google Scholar 

  4. Schmahl, G. (ed.) X-ray microscopy. Proc. Int. Symp. (Springer, 1983).

  5. Sayre, D., Howells, M., Kirz, J. & Rarback, H. (eds) X-ray Microscopy II. Proc. Int. Symp. (Upton, 1987).

  6. Kirz, J., Jacobsen, C. & Howells, M. Soft X-ray microscopes and their biological applications. Q. Rev. Biophys. 28, 33–130 (1995).

    Google Scholar 

  7. Aoki, S. (ed.) Proc. 8th Int. Conf. X-ray Microscopy (IPAP, 2005).

    Google Scholar 

  8. Eichert, D. et al. Imaging with spectroscopic micro-analysis using synchrotron radiation. Anal. Bioanal. Chem. 389, 1121–1132 (2007).

    Google Scholar 

  9. David, C. (ed.) Proc. 9th Int. Conf. X-ray Microscopy (IOP, 2008).

    Google Scholar 

  10. Schmahl, G. & Rudolph, D. Lichtstarke zonenplatten als abbildende systeme für weiche Röntgenstrahlung. Optik 29, 577–585 (1969).

    ADS  Google Scholar 

  11. Niemann, B., Rudolph, D. & Schmahl, G. X-ray microscopy with synchrotron radiation. Appl. Opt. 15, 1883–1884 (1976).

    ADS  Google Scholar 

  12. Rarback, H. et al. Scanning X-ray microscope with 75-nm resolution. Rev. Sci. Instrum. 59, 52–59 (1988).

    ADS  Google Scholar 

  13. Kirz, J. et al. X-ray microscopy with the NSLS soft X-ray undulator. Phys. Scripta T31, 12–17 (1990).

    ADS  Google Scholar 

  14. Ojeda-Castañeda, J. & Gomez-Reino, C. (eds.) Selected papers on zone plates (SPIE, 1996).

    Google Scholar 

  15. Vila-Comamala, J. et al. Advanced thin film technology for ultrahigh resolution X-ray microscopy. Ultramicroscopy 109, 1360–1364 (2009).

    Google Scholar 

  16. Chao, W., Kim, J., Rekawa, S., Fischer, P. & Anderson, E. H. Demonstration of 12 nm resolution Fresnel zone plate lens based soft X-ray microscopy. Opt. Express 17, 17669–17677 (2009).

    ADS  Google Scholar 

  17. Schwarzschild, K. Untersuchungen zur geometrischen optic II. Astronomische Mitteilungen der Kniglichen Sternwarte zu Göttingen. 10, 4–28 (1905).

  18. Cerrina, F. et al. Maximum: A scanning photoelectron microscope at Aladdin. Nucl. Instrum. Meth. A 266, 303–307 (1988).

    ADS  Google Scholar 

  19. Wolter, H. Spiegelsystems streifenden einfalls als abbildende optiken für Röntgenstralen. Ann. Physik 10, 94–114 (1952).

    ADS  MATH  Google Scholar 

  20. Aoki, S. in X-ray Microscopy II (ed. Sayre, D.) 102 (Springer, 1988).

    Google Scholar 

  21. Mimura, H. et al. Breaking the 10 nm barrier in hard-X-ray focusing. Nature Phys. 6, 122–125 (2010).

    ADS  Google Scholar 

  22. Snigirev, A., Kohn, V., Snigireva, I. & Lengeler, B. A compound refractive lens for focusing high energy X-rays. Nature 384, 49–51 (1996).

    ADS  Google Scholar 

  23. Snigirev, A., Kohn, V., Snigireva, I., Souvorov, A. & Lengeler, B. Focusing high-energy X-rays by compound refractive lenses. Appl. Opt. 37, 653–662 (1998).

    ADS  Google Scholar 

  24. Bosak, A., Snigireva, I., Napolskii, K. S. & Snigirev, A. High-resolution transmission X-ray microscopy: A new tool for mesoscopic naterials. Adv. Mater. 22, 3256–3259 (2010).

    Google Scholar 

  25. Yin, G.-C. et al. Sub-30 nm resolution X-ray imaging at 8 keV using third order diffraction of a zone plate lens objective in a transmission microscope. Appl. Phys. Lett. 89, 221122 (2006).

    ADS  Google Scholar 

  26. Chapman, H. N. & Nugent, K. A. Coherent lensless X-ray imaging. Nature Photon. 4, 833–839 (2010).

    ADS  Google Scholar 

  27. Vila-Comamala, J. et al. Dense high aspect ratio hydrogen silsesquioxane nanostructures by 100 keV electron beam lithography. Nanotechnology 21, 285305 (2010).

    Google Scholar 

  28. Maser, J. et al. Near-field stacking of zone plates for hard X-ray range. Proc. SPIE 4783, 74–81 (2002).

    ADS  Google Scholar 

  29. Chao, W., Harteneck, B. D., Liddle, J. A., Anderson, E. H. & Attwood, D. T. Soft X-ray microscopy at a spatial resolution better than 15 nm. Nature 435, 1210–1213 (2005).

    ADS  Article  Google Scholar 

  30. Kang, H. C. et al. Focusing of hard X-rays to 16 nanometers with a multilayer Laue lens. Appl. Phys. Lett. 92, 221114 (2008).

    ADS  Google Scholar 

  31. Yan, H. X-ray nanofocusing by kinoform lenses: A comparative study using different modeling approaches. Phys. Rev. B. 81, 075402 (2010).

    ADS  Google Scholar 

  32. Matsuyama, S. et al. Development of scanning X-ray fluorescence microscope with spatial resolution of 30 nm using Kirkpatrick–Baez mirror optics. Rev. Sci. Instrum. 77, 103102 (2006).

    ADS  Google Scholar 

  33. Zeng, X. et al. Ellipsoidal and parabolic glass capillaries as condensers for X-ray microscopes. Appl. Opt. 47, 2376–2381 (2008).

    ADS  Google Scholar 

  34. Born, M. & Wolf, E. Principles of Optics (Cambridge Univ., 1999).

    Google Scholar 

  35. Jochum, L. & Meyer-Ilse, W. Partially coherent image formation with X-ray microscopes. Appl. Opt. 34, 4944–4950 (1995).

    ADS  Google Scholar 

  36. Yin, G. C. et al. Energy-tunable transmission X-ray microscope for differential contrast imaging with near 60 nm resolution tomography. Appl. Phys. Lett. 88, 241115 (2006).

    ADS  Google Scholar 

  37. von Hofsten, O. et al. Sub-25 nm laboratory X-ray microscopy using a compound Fresnel zone plate. Opt. Lett. 34, 2631–2633 (2009).

    ADS  Google Scholar 

  38. Schmahl, G., Rudolph, D., Schneider, G., Guttmann, P. & Niemann, B. Phase contrast X-ray microscopy studies. Optik 97, 181–182 (1994).

    Google Scholar 

  39. Schmahl, G. et al. Phase contrast studies of biological specimens with the X-ray microscope at BESSY. Rev. Sci. Instrum. 66, 1282–1286 (1995).

    ADS  Google Scholar 

  40. Yokosuka, H. et al. Zernike-type phase-contrast hard X-ray microscope with a zone plate at the Photon Factory. J. Synchrotron Rad. 9, 179–181 (2002).

    Google Scholar 

  41. Youn, H. S. & Jung, S.-W. Hard X-ray microscopy with Zernike phase contrast. J. Microsc. 223, 53–56 (2006).

    MathSciNet  Google Scholar 

  42. Sakdinawat, A. & Liu, Y. Phase contrast soft X-ray microscopy using Zernike zone plates. Opt. Express 16, 1559–1564 (2008).

    ADS  Google Scholar 

  43. Wilhein, T., Kaulich, B., Di Fabrizio, E. & Romanato, F. Differential interference contrast X-ray microscopy with submicron resolution. Appl. Phys. Lett. 78, 2082–2084 (2001).

    ADS  Google Scholar 

  44. Kaulich, B. et al. Differential interference contrast X-ray microscopy with twin zone plates. J. Opt. Soc. Am. A 19, 797–806 (2002).

    ADS  Google Scholar 

  45. Di Fabrizio, E. et al. Diffractive optical elements for differential interference contrast X-ray microscopy. Opt. Express 11, 2278–2288 (2003).

    ADS  Google Scholar 

  46. Chang, C., Sakdinawat, A., Fischer, P., Anderson, E. H. & Attwood, D. T. Single-element objective lens for soft X-ray differential interference contrast microscopy. Opt. Lett. 31, 1564–1566 (2006).

    ADS  Google Scholar 

  47. Sakdinawat, A. & Liu, Y. Soft-X-ray microscopy using spiral zone plates. Opt. Lett. 32, 2635–2637 (2007).

    ADS  Google Scholar 

  48. Attwood, D., Kim, K.-J. & Halback, K. Tunable Coherent Radiation. Science 228, 1265–1272 (1985).

    ADS  Google Scholar 

  49. Tyliszczak, T., Kilcoyne, A., Warwick, A., Liddle, A. & Shuh, D. High spatial resolution scanning transmission X-ray microscope at the Advanced Light Source. Proc. 8th Int. X-ray Microscopy Conf. 88 (IPAP, 2006).

  50. Barinov, A. et al. Synchrotron-based photoelectron microscopy. Nucl. Instrum. Meth. A 601, 195–202 (2009).

    ADS  Google Scholar 

  51. Thompson, A. & Underwood, J. H. in Soft X-rays and Extreme Ultraviolet Radiation 117 (Cambridge Univ., 1999).

    Google Scholar 

  52. Stampononi, M. et al. Trends in synchrotron-based tomographic imaging: the SLS experience. Proc. SPIE 6318, 63180M (2006).

    Google Scholar 

  53. Requena, G. et al. Sub-micrometer synchrotron tomography of multiphase metals using Kirkpatrick-Baez optics. Scripta Mater. 61, 760–763 (2009).

    Google Scholar 

  54. Stampanoni, M. et al. Phase-contrast tomography at the nanoscale using hard X-rays. Phys. Rev. B. 81, 140105 (2010).

    ADS  Google Scholar 

  55. Thole, B. T., Carra, P., Sette, F. & van der Laan, G. X-ray circular dichroism as a probe of orbital magnetization. Phys. Rev. Lett. 68, 1943–1946 (1992).

    ADS  Google Scholar 

  56. Stöhr, J. & Siegmann, H. C. Magnetism: from Fundamentals to Nanoscale Dynamics (Springer, 2006).

    Google Scholar 

  57. Schutz, G., Goerning, E. & Stoll, H. in Handbook of Magnetism and Advanced Magnetic Materials (eds. Kronmueller, H. & Parkin, S.) 1309–1363 (Wiley, 2007).

    Google Scholar 

  58. Kim, K.-J. Polarization characteristics of synchrotron radiation sources and a new two undulator system. Nucl. Instrum. Meth. 222, 11–13 (1984).

    Google Scholar 

  59. Hofmann, A. The Physics of Synchrotron Radiation (Cambridge Univ., 2007).

    Google Scholar 

  60. Pfau, B. et al. Magnetic imaging at linearly polarized X-ray sources. Opt. Express 18, 13608–13615 (2010).

    ADS  Google Scholar 

  61. Mesler, B. L., Fischer, P., Chao, W., Anderson, E. H. & Kim, D.-H. Soft X-ray imaging of spin dynamics at high spatial and temporal resolution. J. Vac. Sci. Technol. B 25, 2598–2602 (2007).

    Google Scholar 

  62. Underwood, J. H., Thompson, A., Wu, Y. & Giauque, R. D. X-ray microprobe using multilayer mirrors. Nucl. Instrum. Meth. A 266, 296–303 (1988).

    ADS  Google Scholar 

  63. Buonassisi, T. et al. Synchrotron-based investigations of the nature and impact of iron contamination in multicrystalline silicon solar cells. J. Appl. Phys. 97, 074901 (2005).

    ADS  Google Scholar 

  64. Buonassisi, T. et al. Engineering metal-impurity nanodefects for low-cost solar cells. Nature Mater. 4, 676–679 (2005).

    ADS  Google Scholar 

  65. Liu, Y. et al. Applications of hard X-ray full-field transmission X-ray microscopy at SSRL. Proc. 10th Int. Conf. X-ray Microscopy (ed. McNulty, I.) (American Institute of Physics Conference Proceedings, in the press).

  66. Gustafsson, M. G. L. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J. Microsc. 198, 82–87 (2000).

    Google Scholar 

  67. Hell, S. W. & Kruog, M. Ground-state depletion fluorescence microscopy, a concept for breaking the diffraction resolution limit. Appl. Phys. B 60, 495–497 (1995).

    ADS  Google Scholar 

  68. Beetz, T. & Jacobsen, C. Soft X-ray radiation damage studies in PMMA using a cryo-STXM. J. Synchrotron Rad. 10, 280–283 (2003).

    Google Scholar 

  69. Weiss, D. et al. Computed tomography of cryogenic biological specimens based on X-ray microscopic images. Ultramicroscopy 84, 185–197 (2000).

    Google Scholar 

  70. McDermott, G., Le Gros, M. A., Knoechel, C., Uchida, M. & Larabell, C. A. Soft X-ray tomography and cryogenic light microscopy: The cool combination in cellular imaging. Trends Cell Biol. 19, 587–595 (2009).

    Google Scholar 

  71. Schneider, G. et al. 3D cellular ultrastructure resolved by a partially-coherent X-ray microscope. Nat. Methods (in the press).

  72. Larabell, C. A. & Le Gros, M. A. X-ray tomography generates 3-D reconstructions of the yeast, Saccharomyces cerevisiae, at 60 nm resolution. Mol. Biol. Cell 15, 957–962 (2004).

    Google Scholar 

  73. Le Gros, M. A., McDermott, G. & Larabell, C. A. X-ray tomography of whole cells. Curr. Opin. Struc. Biol. 15, 593–600 (2005).

    Google Scholar 

  74. Meyer-Ilse, W. et al. High resolution protein localization using soft X-ray microscopy. J. Microsc. 201, 395–403 (2001).

    MathSciNet  Google Scholar 

  75. Stampanoni, M. et al. in Advancements in Neurological Research (ed. Zhang, J. H.) 315–335 (Research Signpost, 2008).

    Google Scholar 

  76. Brown, G. E. & Sturchio, N. C. An overview of synchrotron radiation applications to low temperature geochemistry and environmental science. Rev. Mineral. Geochem. 49, 1–115 (2002).

    Google Scholar 

  77. Skinner, L. B., Chae, S. R., Benmore, C. J., Wenk, H. R. & Monteiro, P. J. M. Nanostructure of calcium silicate hydrates in cements. Phys. Rev. Lett. 104, 195502 (2010).

    ADS  Google Scholar 

  78. Kurtis, K. E., Monteiro, P. J. M., Brown, J. T. & Meyer-Ilse, W. Imaging of ASR gel by soft X-ray microscopy. Cement Concrete Res. 28, 411–421 (1998).

    Google Scholar 

  79. Monteiro, P. J. M. et al. Characterizing the nano and micro structure of concrete to improve its durability. Cement Concrete Comp. 31, 577–584 (2009).

    Google Scholar 

  80. Kaulich, B. et al. Low-energy X-ray fluorescence microscopy opening new opportunities for bio-related research. J. Res. Soc. Interface 6, 641–647 (2009).

    Google Scholar 

  81. Tolra, R. et al. Localization of aluminium in tea (Camellia sinensis) leaves using low energy X-ray fluorescence spectro-microscopy. J. Plant Res. doi:10.1007/s10265-010-0344-3 (2010).

  82. Obst, M. et al. Precipitation of amorphous CaCO3 (aragonite-like) by cyanobacteria: A STXM study of the influence of EPS on the nucleation process. Geochim. Cosmochim. Ac. 73, 4180–4198 (2009).

    ADS  Google Scholar 

  83. Obst, M., Wang, J. & Hitchcock, A. P. Soft X-ray spectro-tomography study of cyanobacterial biomineral nucleation. Geobiology 7, 577–591 (2009).

    Google Scholar 

  84. Dynes, J. et al. Speciation and quantitative mapping of metal species in microbial biofilms using scanning transmission X-ray microscopy. Environ. Sci. Technol. 40, 1556–1565 (2006).

    ADS  Google Scholar 

  85. Cotte, M. Synchrotron-based X-ray spectromicroscopy used for the study of an atypical micrometric pigment in 16th century paintings. Anal. Chem. 79, 6988–6994 (2007).

    Google Scholar 

  86. Cotte, M., Susini, J., Dik, J. & Janssens, K. Synchrotron-based X-ray absorption spectroscopy for art conservation: looking back and looking forward. Accounts Chem. Res. 43, 705–714 (2010).

    Google Scholar 

  87. Janssens, K., Dik, J., Cotte, M. & Susini, J. Photon-based techniques for nondestructive subsurface analysis of painted cultural heritage artifacts. Accounts Chem. Res. 43, 814–825 (2010).

    Google Scholar 

  88. Lahlil, S., Biron, I., Cotte, M., Susini, J. & Menguy, N. Synthesis of calcium antimonite nano-crystals by the 18th dynasty Egyptian glassmakers. Appl. Phys. A 98, 1–8 (2010).

    ADS  Google Scholar 

  89. Donaghue, P. et al. Synchrotron X-ray tomographic microscopy of fossil embryos. Nature 442, 680–683 (2006).

    ADS  Google Scholar 

  90. Bergmann, U. et al. Archaeopteryx feathers and bone chemistry fully revealed via synchrotron imaging. Proc. Natl Acad. Sci. USA 107, 9060–9065 (2010).

    ADS  Google Scholar 

  91. Bergmann, U. Archimedes brought to light. Phys. World 39–42 (November 2007).

    Google Scholar 

  92. Takman, P. A. C. et al. High-resolution compact X-ray microscopy. J. Microsc. 226, 175–181 (2007).

    MathSciNet  Google Scholar 

  93. Bertilson, M., von Hofsten, O., Vogt, U., Holmberg, A. & Hertz, H. M. High-resolution computed tomography with a compact soft X-ray microscope. Opt. Express 17, 11057–11065 (2009).

    ADS  Google Scholar 

  94. Berglund, M., Rymell, L., Hertz, H. M. & Wilhein, T. Cryogenic liquid-jet target for debris-free laser-plasma soft X-ray generation. Rev. Sci. Instrum. 69, 2362–2364 (1998).

    ADS  Google Scholar 

  95. Hemberg, O., Otendal, M. & Hertz, H. M. Liquid-metal-jet anode electron-impact X-ray source. Appl. Phys. Lett. 83, 1483–1485 (2003).

    ADS  Google Scholar 

  96. Emma, P. et al. First lasing and operation of an angstrom-wavelength free-electron laser. Nature Photon. 4, 641–647 (2010).

    ADS  Google Scholar 

  97. Parkinson, D. Y., McDermott, G., Etkin, L. D., Le Gros, M. A. & Larabell, C. A. Quantitative 3-D imaging of eukaryotic cells using soft X-ray tomography. J. Struct. Biol. 162, 380–386 (2008).

    Google Scholar 

Download references

Acknowledgements

The authors acknowledge support from the US National Science Foundation, the Engineering Research Center for EUV Science and Technology, and the King Abdullah University of Science and Technology.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anne Sakdinawat.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sakdinawat, A., Attwood, D. Nanoscale X-ray imaging. Nature Photon 4, 840–848 (2010). https://doi.org/10.1038/nphoton.2010.267

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nphoton.2010.267

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing