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BioMed Research International
Volume 2015, Article ID 154272, 8 pages
http://dx.doi.org/10.1155/2015/154272
Research Article

Two-Photon Microscopy Allows Imaging and Characterization of Cochlear Microvasculature In Vivo

1Department of Otorhinolaryngology, University of Göttingen Medical Center, Georg-August-Universität Göttingen, Robert-Koch-Strasse 40, 37099 Göttingen, Germany
2Walter-Brendel-Zentrum für Experimentelle Medizin (WBex), Ludwig-Maximilians-Universität München, Marchioninistrasse 15, 81377 München, Germany

Received 1 December 2014; Revised 26 February 2015; Accepted 2 March 2015

Academic Editor: Peter S. Roland

Copyright © 2015 Friedrich Ihler et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. M. Byl Jr., “Sudden hearing loss: eight years' experience and suggested prognostic table,” Laryngoscope, vol. 94, no. 5, part 1, pp. 647–661, 1984. View at Google Scholar · View at Scopus
  2. X. Shi, “Physiopathology of the cochlear microcirculation,” Hearing Research, vol. 282, no. 1-2, pp. 10–24, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Axelsson, “The vascular anatomy of the cochlea in the guinea pig and in man,” Acta Oto-Laryngologica, vol. 66, supplement 243, pp. 3–134, 1968. View at Google Scholar
  4. A. Johnson, M. Hawke, and G. Berger, “Sudden deafness and vertigo due to inner ear hemorrhage—a temporal bone case report,” Journal of Otolaryngology, vol. 13, no. 4, pp. 201–207, 1984. View at Google Scholar · View at Scopus
  5. J. M. Miller and H. Dengerink, “Control of inner ear blood flow,” American Journal of Otolaryngology: Head and Neck Medicine and Surgery, vol. 9, no. 6, pp. 302–316, 1988. View at Google Scholar · View at Scopus
  6. J. M. Miller, T.-Y. Ren, and A. L. Nuttall, “Studies of inner ear blood flow in animals and human beings,” Otolaryngology—Head and Neck Surgery, vol. 112, no. 1, pp. 101–113, 1995. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Nakashima, S. Naganawa, M. Sone et al., “Disorders of cochlear blood flow,” Brain Research Reviews, vol. 43, no. 1, pp. 17–28, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Glacet-Bernard, W. Roquet, A. Coste, R. Peynègre, G. Coscas, and G. Soubrane, “Central retinal vein occlusion and sudden deafness: a possible common pathogenesis,” European Journal of Ophthalmology, vol. 11, no. 2, pp. 197–199, 2001. View at Google Scholar · View at Scopus
  9. J. Thornton, Q. Bashir, V. A. Aletich, G. M. Debrun, F. Charbel, and M. F. Mafee, “Role of magnetic resonance imaging and diagnostic and interventional angiography in vascular and neoplastic diseases of the skull base associated with vestibulocochlear symptoms,” Topics in Magnetic Resonance Imaging, vol. 11, no. 2, pp. 123–137, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Koyuncu, A. R. Elhami, H. Akan, M. Sahin, T. Basoglu, and M. Simsek, “Investigation of the vertebrobasilar arterial system in vertigo by vestibulocochlear test, SPECT and angiography,” Auris Nasus Larynx, vol. 28, no. 1, pp. 23–28, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. L. Carlisle and A. Forge, “The vessels of the stria vascularis: quantitative comparison of three rodent species,” Hearing Research, vol. 38, no. 1-2, pp. 111–117, 1989. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Moriguchi, H. Masutani, M. Sugita, K. Matsunaga, J. Okamoto, and Y. Nakai, “Measurement of inner ear vessel diameters with casting method,” Acta Oto-Laryngologica, Supplement, vol. 486, pp. 39–44, 1991. View at Google Scholar · View at Scopus
  13. L. Fechter and L. Carlisle, “Auditory dysfunction and cochlear vascular injury following trimethyltin exposure in the guinea pig,” Toxicology and Applied Pharmacology, vol. 105, no. 1, pp. 133–143, 1990. View at Publisher · View at Google Scholar · View at Scopus
  14. A. L. Nuttall, “Techniques for the observation and measurement of red blood cell velocity in vessels of the guinea pig cochlea,” Hearing Research, vol. 27, no. 2, pp. 111–119, 1987. View at Publisher · View at Google Scholar · View at Scopus
  15. F. P. Miles and A. L. Nuttall, “In vivo capillary diameters in the stria vascularis and spiral ligament of the guinea pig cochlea,” Hearing Research, vol. 33, no. 2, pp. 191–200, 1988. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Ren, P. B. Brechtelsbauer, J. M. Miller, and A. L. Nuttall, “Cochlear blood flow measured by averaged laser Doppler flowmetry (ALDF),” Hearing Research, vol. 77, no. 1-2, pp. 200–206, 1994. View at Publisher · View at Google Scholar · View at Scopus
  17. P. C. Goodwin, J. M. Miller, H. A. Dengerink, J. W. Wright, and A. Axelsson, “The laser Doppler: a non-invasive measure of cochlear blood flow,” Acta Oto-Laryngologica, vol. 98, no. 5-6, pp. 403–412, 1984. View at Publisher · View at Google Scholar · View at Scopus
  18. A. L. Nuttall, E. Hultcrantz, and M. Lawrence, “Does loud sound influence the intracochlear oxygen tension?” Hearing Research, vol. 5, no. 2-3, pp. 285–293, 1981. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Hultcrantz and C. Angelborg, “Cochlear blood circulation studied with microspheres,” ORL, vol. 40, no. 2, pp. 65–76, 1978. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Prazma, S. G. Vance, and G. Rodgers, “Measurement of cochlear blood flow—new technique,” Hearing Research, vol. 14, no. 1, pp. 21–28, 1984. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Reif, J. Qin, L. Shi et al., “Monitoring hypoxia induced changes in cochlear blood flow and hemoglobin concentration using a combined dual-wavelength laser speckle contrast imaging and Doppler optical microangiography system,” PLoS ONE, vol. 7, no. 12, Article ID e52041, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Canis, W. Arpornchayanon, C. Messmer, M. Suckfuell, B. Olzowy, and S. Strieth, “An animal model for the analysis of cochlear blood flood disturbance and hearing threshold in vivo,” European Archives of Oto-Rhino-Laryngology, vol. 267, no. 2, pp. 197–203, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Axelsson, A. L. Nuttall, and J. M. Miller, “Observations of cochlear microcirculation using intravital microscopy,” Acta Oto-Laryngologica, vol. 109, no. 3-4, pp. 263–270, 1990. View at Publisher · View at Google Scholar · View at Scopus
  24. A. L. Nuttall, “Velocity of red blood cell flow in capillaries of the guinea pig cochlea,” Hearing Research, vol. 27, no. 2, pp. 121–128, 1987. View at Publisher · View at Google Scholar · View at Scopus
  25. J. E. Hawkins Jr., “Microcirculation in the labyrinth,” Archives of Oto-Rhino-Laryngology, vol. 212, no. 4, pp. 241–251, 1976. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Hu and L. V. Wang, “Photoacoustic imaging and characterization of the microvasculature,” Journal of Biomedical Optics, vol. 15, no. 1, Article ID 011101, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science, vol. 248, no. 4951, pp. 73–76, 1990. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Konig, “Multiphoton microscopy in life sciences,” Journal of Microscopy, vol. 200, no. 2, pp. 83–104, 2000. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Ishii and M. Ishii, “Intravital two-photon imaging: a versatile tool for dissecting the immune system,” Annals of the Rheumatic Diseases, vol. 70, supplement 1, pp. i113–i115, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nature Methods, vol. 2, no. 12, pp. 932–940, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron, vol. 50, no. 6, pp. 823–839, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. B.-G. Wang, K. Konig, and K. J. Halbhuber, “Two-photon microscopy of deep intravital tissues and its merits in clinical research,” Journal of Microscopy, vol. 238, no. 1, pp. 1–20, 2010. View at Publisher · View at Google Scholar · View at MathSciNet · View at Scopus
  33. P. Pantazis and W. Supatto, “Advances in whole-embryo imaging: a quantitative transition is underway,” Nature Reviews Molecular Cell Biology, vol. 15, no. 5, pp. 327–339, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. D. M. Small, W. Y. Sanchez, S. Roy, M. J. Hickey, and G. C. Gobe, “Multiphoton fluorescence microscopy of the live kidney in health and disease,” Journal of Biomedical Optics, vol. 19, no. 2, Article ID 020901, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Rehberg, F. Krombach, U. Pohl, and S. Dietzel, “Signal improvement in multiphoton microscopy by reflection with simple mirrors near the sample,” Journal of Biomedical Optics, vol. 15, no. 2, Article ID 026017, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Rehberg, F. Krombach, U. Pohl, and S. Dietzel, “Label-free 3D visualization of cellular and tissue structures in intact muscle with second and third harmonic generation microscopy,” PLoS ONE, vol. 6, no. 11, Article ID e28237, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nature Methods, vol. 9, no. 7, pp. 671–675, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Schindelin, I. Arganda-Carreras, E. Frise et al., “Fiji: an open-source platform for biological-image analysis,” Nature Methods, vol. 9, no. 7, pp. 676–682, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Preibisch, S. Saalfeld, and P. Tomancak, “Globally optimal stitching of tiled 3D microscopic image acquisitions,” Bioinformatics, vol. 25, no. 11, pp. 1463–1465, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. J. J. Vaquero, S. Redondo, E. Lage et al., “Assessment of a new high-performance a small-animal X-ray tomograph,” IEEE Transactions on Nuclear Science, vol. 55, no. 3, pp. 898–905, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. X. Yang, H. Gong, G. Quan, Y. Deng, and Q. Luo, “Combined system of fluorescence diffuse optical tomography and microcomputed tomography for small animal imaging,” Review of Scientific Instruments, vol. 81, no. 5, Article ID 054304, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. D. O. Schwenke and P. A. Cragg, “Comparison of the depressive effects of four anesthetic regimens on ventilatory and cardiovascular variables in the Guinea pig,” Comparative Medicine, vol. 54, no. 1, pp. 77–85, 2004. View at Google Scholar · View at Scopus
  43. Z. L. S. Brookes, N. J. Brown, and C. S. Reilly, “Intravenous anaesthesia and the rat microcirculation: the Dorsal Microcirculatory Chamber,” British Journal of Anaesthesia, vol. 85, no. 6, pp. 901–903, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. R. C. Sloan, M. Rosenbaum, D. O'Rourke et al., “High doses of ketamine-xylazine anesthesia reduce cardiac ischemia-reperfusion injury in guinea pigs,” Journal of the American Association for Laboratory Animal Science, vol. 50, no. 3, pp. 349–354, 2011. View at Google Scholar · View at Scopus
  45. W. Arpornchayanon, M. Canis, F. Ihler, C. Settevendemie, and S. Strieth, “TNF-alpha inhibition using etanercept prevents noise-induced hearing loss by improvement of cochlear blood flow in vivo,” International Journal of Audiology, vol. 52, no. 8, pp. 545–552, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. W. Arpornchayanon, M. Canis, M. Suckfuell, F. Ihler, B. Olzowy, and S. Strieth, “Modeling the measurements of cochlear microcirculation and hearing function after loud noise,” Otolaryngology—Head and Neck Surgery, vol. 145, no. 3, pp. 463–469, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Bertlich, F. Ihler, K. Sharaf, B. G. Weiss, M. Strupp, and M. Canis, “Betahistine metabolites, aminoethylpyridine, and hydroxyethylpyridine increase cochlear blood flow in guinea pigs in vivo,” International Journal of Audiology, vol. 53, no. 10, pp. 753–759, 2014. View at Publisher · View at Google Scholar
  48. F. Ihler, M. Bertlich, K. Sharaf, S. Strieth, M. Strupp, and M. Canis, “Betahistine exerts a dose-dependent effect on cochlear stria vascularis blood flow in guinea pigs in vivo,” PLoS ONE, vol. 7, no. 6, Article ID e39086, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Ihler, K. Sharaf, M. Bertlich et al., “Etanercept prevents decrease of cochlear blood flow dose-dependently caused by tumor necrosis factor alpha,” Annals of Otology, Rhinology & Laryngology, vol. 122, no. 7, pp. 468–473, 2013. View at Google Scholar · View at Scopus
  50. F. Ihler, S. Strieth, N. Pieri, P. Göhring, and M. Canis, “Acute hyperfibrinogenemia impairs cochlear blood flow and hearing function in guinea pigs in vivo,” International Journal of Audiology, vol. 51, no. 3, pp. 210–215, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. W. S. Quirk, G. Avinash, A. L. Nuttall, and J. M. Miller, “The influence of loud sound on red blood cell velocity and blood vessel diameter in the cochlea,” Hearing Research, vol. 63, no. 1-2, pp. 102–107, 1992. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Lawrence, “Control mechanisms of inner ear microcirculation,” The American Journal of Otolaryngology, vol. 1, no. 4, pp. 324–333, 1980. View at Google Scholar · View at Scopus
  53. D. Kepshire, S. C. Davis, H. Dehghani, K. D. Paulsen, and B. W. Pogue, “Fluorescence tomography characterization for sub-surface imaging with protoporphyrin IX,” Optics Express, vol. 16, no. 12, pp. 8581–8593, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Dai, A. Nuttall, Y. Yang, and X. Shi, “Visualization and contractile activity of cochlear pericytes in the capillaries of the spiral ligament,” Hearing Research, vol. 254, no. 1-2, pp. 100–107, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Dai and X. Shi, “Fibro-vascular coupling in the control of cochlear blood flow,” PLoS ONE, vol. 6, no. 6, Article ID e20652, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, “Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 26, pp. 15741–15746, 1998. View at Publisher · View at Google Scholar · View at Scopus
  57. E. Chaigneau, M. Oheim, E. Audinat, and S. Charpak, “Two-photon imaging of capillary blood flow in olfactory bulb glomeruli,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 22, pp. 13081–13086, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. F. Helmchen and D. Kleinfeld, “In vivo measurements of blood flow and glial cell function with two-photon laser-scanning microscopy,” in Angiogenesis: In Vivo Systems, Part A, D. A. Cheresh, Ed., pp. 231–254, Elsevier, 2008. View at Google Scholar
  59. W. S. Kamoun, S.-S. Chae, D. A. Lacorre et al., “Simultaneous measurement of RBC velocity, flux, hematocrit and shear rate in vascular networks,” Nature Methods, vol. 7, no. 8, pp. 655–660, 2010. View at Publisher · View at Google Scholar · View at Scopus