Abstract

Multi-photon microscopy (MPM) is a powerful tool for biomedical imaging, enabling molecular contrast and integrated structural and functional imaging on the cellular and subcellular level. However, the cost and complexity of femtosecond laser sources that are required in MPM are significant hurdles to widespread adoption of this important imaging modality. In this work, we describe femtosecond diode pumped Cr:LiCAF laser technology as a low cost alternative to femtosecond Ti:Sapphire lasers for MPM. Using single mode pump diodes which cost only $150 each, a diode pumped Cr:LiCAF laser generates ~70-fs duration, 1.8-nJ pulses at ~800 nm wavelengths, with a repetition rate of 100 MHz and average output power of 180 mW. Representative examples of MPM imaging in neuroscience, immunology, endocrinology and cancer research using Cr:LiCAF laser technology are presented. These studies demonstrate the potential of this laser source for use in a broad range of MPM applications.

© 2008 Optical Society of America

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2008

J. N. Kerr and W. Denk, "Imaging in vivo: watching the brain in action," Nat. Rev. Neurosci. 9, 195-205 (2008).
[CrossRef] [PubMed]

P. Xi, Y. Andegeko, L. R. Weisel, V. V. Lozovoy, and M. Dantus, "Greater signal, increased depth, and less photobleaching in two-photon microscopy with 10 fs pulses," Opt. Commun. 281, 1841-1849 (2008).
[CrossRef]

J. Schummers, H. Yu, and M. Sur, "Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex," Science 320, 1638-1643 (2008).
[CrossRef] [PubMed]

M. J. Pittet and T. R. Mempel, "Regulation of T-cell migration and effector functions: insights from in vivo imaging studies," Immunol. Rev. 221, 107-129 (2008).
[CrossRef] [PubMed]

N. S. Makarov, M. Drobizhev, and A. Rebane, "Two-photon absorption standards in the 550-1600 nm excitation wavelength range," Opt. Express 16, 4029-4047 (2008).
[CrossRef] [PubMed]

U. Demirbas, A. Sennaroglu, F. X. Kartner, and J. G. Fujimoto, "Highly efficient, low-cost femtosecond Cr3+:LiCAF laser pumped by single-mode diodes," Opt. Lett. 33, 590-592 (2008).
[CrossRef] [PubMed]

2007

K. Taira, T. Hashimoto, and H. Yokoyama, "Two-photon fluorescence imaging with a pulse source based on a 980-nm gain-switched laser diode," Opt. Express 15, 2454-2458 (2007).
[CrossRef] [PubMed]

M. Kuramoto, N. Kitajima, H. C. Guo, Y. Furushima, M. Ikeda, and H. Yokoyama, "Two-photon fluorescence bioimaging with an all-semiconductor laser picosecond pulse source," Opt. Lett. 32, 2726-2728 (2007).
[CrossRef] [PubMed]

U. Demirbas, A. Sennaroglu, A. Benedick, A. Siddiqui, F. X. Kartner, and J. G. Fujimoto, "Diode-pumped, high-average power femtosecond Cr+3:LiCAF laser," Opt. Lett. 32, 3309-3311 (2007).
[CrossRef] [PubMed]

P. S. Tsai, B. Migliori, K. Campbell, T. N. Kim, Z. Kam, A. Groisman, and D. Kleinfeld, "Spherical aberration correction in nonlinear microscopy and optical ablation using a transparent deformable membrane," Appl. Phys. Lett. 91, 3 (2007).
[CrossRef]

P. Verant, R. Serduc, B. Van Der Sanden, C. Remy, and J. C. Vial, "A direct method for measuring mouse capillary cortical blood volume using multiphoton laser scanning microscopy," J. Cereb. Blood Flow Metab. 27, 1072-1081 (2007).

G. McConnell, "Nonlinear optical microscopy at wavelengths exceeding 1.4 µm using a synchronously pumped femtosecond-pulsed optical parametric oscillator," Phys. Med. Biol. 52, 717-724 (2007).
[CrossRef] [PubMed]

2006

K. Svoboda and R. Yasuda, "Principles of two-photon excitation microscopy and its applications to neuroscience," Neuron 50, 823-839 (2006).
[CrossRef] [PubMed]

D. Debarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Methods 3, 47-53 (2006).
[CrossRef]

A. Diaspro, P. Bianchini, G. Vicidomini, M. Faretta, P. Ramoino, and C. Usai, "Multi-photon excitation microscopy," Biomed. Eng. Online 5, 1-14 (2006).
[CrossRef]

M. Rueckel, J. A. Mack-Bucher, and W. Denk, "Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing," Proc. Natl. Acad. Sci. USA 103, 17137-17142 (2006).
[CrossRef] [PubMed]

H. Yokoyama, H. C. Guo, T. Yoda, K. Takashima, K. Sato, H. Taniguchi, and H. Ito, "Two-photon bioimaging with picosecond optical pulses from a semiconductor laser," Opt. Express 14, 3467-3471 (2006).
[CrossRef] [PubMed]

P. Theer and W. Denk, "On the fundamental imaging-depth limit in two-photon microscopy," J. Opt. Soc. Am. A 23, 3139-3149 (2006).
[CrossRef]

2005

F. Helmchen and W. Denk, "Deep tissue two-photon microscopy," Nat. Methods 2, 932-940 (2005).
[CrossRef] [PubMed]

J. M. Girkin and G. McConnell, "Advances in laser sources for confocal and multiphoton microscopy," Microsc. Res. Tech. 67, 8-14 (2005).
[CrossRef] [PubMed]

A. Diaspro, G. Chirico, and M. Collini, "Two-photon fluorescence excitation and related techniques in biological microscopy," Q. Rev. Biophys. 38, 97-166 (2005).
[CrossRef]

2004

G. McConnell and E. Riis, "Photonic crystal fibre enables short-wavelength two-photon laser scanning fluorescence microscopy with fura-2," Phys. Med. Biol. 49, 4757-4763 (2004).
[CrossRef] [PubMed]

S. N. Tandon, J. T. Gopinath, A. A. Erchak, G. S. Petrich, L. A. Kolodziejski, and E. P. Ippen, "Large-area oxidation of AlAs layers for dielectric stacks and thick buried oxides," J. Electron. Mater. 33, 774-779 (2004).
[CrossRef]

A. Nimmerjahn, F. Kirchhoff, J. N. Kerr, and F. Helmchen, "Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo," Nat. Methods 1, 31-37 (2004).
[CrossRef]

T. R. Mempel, S. E. Henrickson, and U. H. von Andrian, "T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases," Nature 427, 154-159 (2004).
[CrossRef] [PubMed]

S. N. Tandon, J. T. Gopinath, H. M. Shen, G. S. Petrich, L. A. Kolodziejski, F. X. Kartner, and E. P. Ippen, "Large-area broadband saturable Bragg reflectors by use of oxidized AlAs," Opt. Lett. 29, 2551-2553 (2004).
[CrossRef] [PubMed]

2003

A. Isemann and C. Fallnich, "High-power Colquiriite lasers with high slope efficiencies pumped by broad-area laser diodes," Opt. Express 11, 259-264 (2003).
[CrossRef] [PubMed]

P. Theer, M. T. Hasan, and W. Denk, "Two-photon imaging to a depth of 1000 µm in living brains by use of a Ti:Al2O3 regenerative amplifier," Opt. Lett. 28, 1022-1024 (2003).
[CrossRef] [PubMed]

G. McConnell, G. L. Smith, J. M. Girkin, A. M. Gurney, and A. I. Ferguson, "Two-photon microscopy of fura-2-loaded cardiac myocytes with an all-solid-state tunable and visible femtosecond laser source," Opt. Lett. 28, 1742-1744 (2003).
[CrossRef] [PubMed]

U. H. von Andrian and T. R. Mempel, "Homing and cellular traffic in lymph nodes," Nat. Rev. Immunol. 3, 867-878 (2003).
[CrossRef] [PubMed]

M. E. Dickinson, E. Simbuerger, B. Zimmermann, C. W. Waters, and S. E. Fraser, "Multiphoton excitation spectra in biological samples," J. Biomed. Opt. 8, 329-338 (2003).
[CrossRef] [PubMed]

D. R. Larson, W. R. Zipfel, R. M. Williams, S. W. Clark, M. P. Bruchez, F. W. Wise, and W. W. Webb, "Water-soluble quantum dots for multiphoton fluorescence imaging in vivo," Science 300, 1434-1436 (2003).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, "Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation," Proc. Natl. Acad. Sci. USA 100, 7075-7080 (2003).
[CrossRef] [PubMed]

J. M. Girkin, "Optical physics enables advances in multiphoton imaging," J. Phys. D 36, R250-R258 (2003).
[CrossRef]

D. A. Dombeck, K. A. Kasischke, H. D. Vishwasrao, M. Ingelsson, B. T. Hyman, and W. W. Webb, "Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy," Proc. Natl. Acad. Sci. USA 100, 7081-7086 (2003).
[CrossRef] [PubMed]

W. R. Zipfel, R. M. Williams, and W. W. Webb, "Nonlinear magic: multiphoton microscopy in the biosciences," Nat. Biotechnol. 21, 1368-1376 (2003).
[CrossRef]

2002

A. Zoumi, A. Yeh, and B. J. Tromberg, "Imaging cells and extracellular matrix in vivo by using second-harmonic generation and two-photon excited fluorescence," Proc. Natl. Acad. Sci. USA 99, 11014-11019 (2002).
[CrossRef] [PubMed]

F. Bestvater, E. Spiess, G. Stobrawa, M. Hacker, T. Feurer, T. Porwol, U. Berchner-Pfannschmidt, C. Wotzlaw, and H. Acker, "Two-photon fluorescence absorption and emission spectra of dyes relevant for cell imaging," J. Microsc. 208, 108-115 (2002).
[CrossRef] [PubMed]

B. Agate, B. Stormont, A. J. Kemp, C. T. A. Brown, U. Keller, and W. Sibbett, "Simplified cavity designs for efficient and compact femtosecond Cr:LiSAF lasers," Opt. Commun. 205, 207-213 (2002).
[CrossRef]

J. M. Hopkins, G. J. Valentine, B. Agate, A. J. Kemp, U. Keller, and W. Sibbett, "Highly compact and efficient femtosecond Cr:LiSAF lasers," IEEE J. Quantum Electron. 38, 360-368 (2002).
[CrossRef]

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, "Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror," J. Microsc. 206, 65-71 (2002).
[CrossRef] [PubMed]

E. J. Yoder and D. Kleinfeld, "Cortical imaging through the intact mouse skull using two-photon excitation laser scanning microscopy," Microsc. Res. Tech. 56, 304-305 (2002).
[CrossRef] [PubMed]

F. Helmchen and W. Denk, "New developments in multiphoton microscopy," Curr. Opin. Neurobiol. 12, 593-601 (2002).
[CrossRef] [PubMed]

P. Wagenblast, U. Morgner, F. Grawert, V. Scheuer, G. Angelow, M. J. Lederer, and F. X. Kärtner, "Generation of sub-10-fs pulses from a Kerr-lens modelocked Cr3+:LiCAF laser oscillator using third order dispersion compensating double chirped mirrors," Opt. Lett. 27, 1726-1729 (2002).
[CrossRef]

2001

L. Canioni, S. Rivet, L. Sarger, R. Barille, P. Vacher, and P. Voisin, "Imaging of Ca2+ intracellular dynamics with a third-harmonic generation microscope," Opt. Lett. 26, 515-517 (2001).
[CrossRef]

M. Oheim, E. Beaurepaire, E. Chaigneau, J. Mertz, and S. Charpak, "Two-photon microscopy in brain tissue: parameters influencing the imaging depth," J. Neurosci. Methods 111, 29-37 (2001).
[CrossRef] [PubMed]

E. Beaurepaire, M. Oheim, and J. Mertz, "Ultra-deep two-photon fluorescence excitation in turbid media," Opt. Commun. 188, 25-29 (2001).
[CrossRef]

2000

A. Moore, E. Marecos, A. Bogdanov, and R. Weissleder, "Tumoral distribution of long-circulating dextran-coated iron oxide nanoparticles in a rodent model," Radiology 214, 568-574 (2000).
[PubMed]

M. A. Neil, R. Juskaitis, M. J. Booth, T. Wilson, T. Tanaka, and S. Kawata, "Adaptive aberration correction in a two-photon microscope," J. Microsc. 200, 105-108 (2000).
[CrossRef] [PubMed]

L. Moreaux, O. Sandre, M. Blanchard-Desce, and J. Mertz, "Membrane imaging by simultaneous second-harmonic generation and two-photon microscopy," Opt. Lett. 25, 320-322 (2000).
[CrossRef]

P. T. C. So, C. Y. Dong, B. R. Masters, and K. M. Berland, "Two-photon excitation fluorescence microscopy," Annu. Rev. Biomed. Eng. 2, 399-429 (2000).
[CrossRef]

1999

A. Zumbusch, G. R. Holtom, and X. S. Xie, "Three-dimensional vibrational imaging by coherent anti-Stokes Raman scattering," Phys. Rev. Lett. 82, 4142-4145 (1999).
[CrossRef]

J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, "Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability," Nat. Biotechnol. 17, 763-767 (1999).
[CrossRef] [PubMed]

P. J. Campagnola, M. D. Wei, A. Lewis, and L. M. Loew, "High-resolution nonlinear optical imaging of live cells by second harmonic generation," Biophys. J. 77, 3341-3349 (1999).
[CrossRef] [PubMed]

C. Hönninger, R. Paschotta, F. Morier-Genoud, M. Moser, and U. Keller, "Q-switching stability limits of continuous-wave passive mode locking," J. Opt. Soc. Am. A 16, 46-56 (1999).
[CrossRef]

D. Yelin and Y. Silberberg, "Laser scanning third-harmonic-generation microscopy in biology," Opt. Express 5, 169-175 (1999).
[CrossRef] [PubMed]

1998

M. A. Albota, C. Xu, and W. W. Webb, "Two-photon fluorescence excitation cross sections of biomolecular probes from 690 to 960 nm," Appl. Opt. 37, 7352-7356 (1998).
[CrossRef]

R. A. Warnock, S. Askari, E. C. Butcher, and U. H. von Andrian, "Molecular mechanisms of lymphocyte homing to peripheral lymph nodes," J. Exp. Med. 187, 205-216 (1998).
[CrossRef] [PubMed]

J. M. Hopkins, G. J. Valentine, W. Sibbett, J. A. der Au, F. Morier-Genoud, U. Keller, and A. Valster, "Efficient, low-noise, SESAM-based femtosecond Cr3+:LiSrAlF6 laser," Opt. Commun. 154, 54-58 (1998).
[CrossRef]

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," Proc. Natl. Acad. Sci. USA 95, 15741-15746 (1998).
[CrossRef] [PubMed]

M. Muller, J. Squier, K. R. Wilson, and G. J. Brakenhoff, "3D microscopy of transparent objects using third-harmonic generation," J. Microsc. 191, 266-274 (1998).
[CrossRef] [PubMed]

1997

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, "Nonlinear scanning laser microscopy by third harmonic generation," Appl. Phys. Lett. 70, 922-924 (1997).
[CrossRef]

W. Denk and K. Svoboda, "Photon upmanship: Why multiphoton imaging is more than a gimmick," Neuron 18, 351-357 (1997).
[CrossRef] [PubMed]

J. R. Lakowicz, I. Gryczynski, H. Malak, M. Schrader, P. Engelhardt, H. Kano, and S. W. Hell, "Time-resolved fluorescence spectroscopy and imaging of DNA labeled with DAPI and hoechst 33342 using three-photon excitation," Biophys. J. 72, 567-578 (1997).
[CrossRef] [PubMed]

S. Maiti, J. B. Shear, R. M. Williams, W. R. Zipfel, and W. W. Webb, "Measuring serotonin distribution in live cells with three-photon excitation," Science 275, 530-532 (1997).
[CrossRef] [PubMed]

G. J. Valentine, J. M. Hopkins, P. LozaAlvarez, G. T. Kennedy, W. Sibbett, D. Burns, and A. Valster, "Ultralow-pump-threshold, femtosecond Cr3+:LiSrAlF6 laser pumped by a single narrow-stripe AlGaInP laser diode," Opt. Lett. 22, 1639-1641 (1997).
[CrossRef]

G. Robertson, D. Armstrong, M. J. P. Dymott, A. I. Ferguson, and G. L. Hogg, "Two-photon fluorescence microscopy with a diode-pumped Cr:LiSAF laser," Appl. Opt. 36, 2481-2483 (1997).
[CrossRef] [PubMed]

K. Svoboda, W. Denk, D. Kleinfeld, and D. W. Tank, "In vivo dendritic calcium dynamics in neocortical pyramidal neurons," Nature 385, 161-165 (1997).
[CrossRef] [PubMed]

1996

Q3. U. Keller, K. J. Weingarten, F. X. Kartner, D. kopf, B. Braun, I. D. Jung, R. Fluck, C. Hönninger, N. Matuschek, and J. A. d. Au, "Semiconductor saturable absorber mirrors (SESAM's) for femtosecond to nanosecond pulse generation in solid-state lasers," IEEE Sel. Top. Quantum Electron. 2, 435-453 (1996).
[CrossRef]

Q4. S. Tsuda, W. H. Knox, S. T. Cundiff, W. Y. Jan, and J. E. Cunningham, "Mode-locking ultrafast solid-state lasers with saturable Bragg reflectors," IEEE Sel. Top. Quantum Electron. 2, 454-464 (1996).
[CrossRef]

C. Xu and W. W. Webb, "Measurement of two-photon excitation cross sections of molecular fluorophores with data from 690 to 1050 nm," J. Opt. Soc. Am. B 13, 481-491 (1996).
[CrossRef]

K. Svoboda, W. Denk, W. H. Knox, and S. Tsuda, "Two-photon-excitation scanning microscopy of living neurons with a saturable Bragg reflector mode-locked diode-pumped Cr:LiSrAlFl laser," Opt. Lett. 21, 1411-1413 (1996).
[CrossRef] [PubMed]

G. Peleg, A. Lewis, O. Bouevitch, L. Loew, D. Parnas, and M. Linial, "Gigantic optical non-linearities from nanoparticle-enhanced molecular probes with potential for selectively imaging the structure and physiology of nanometric regions in cellular systems," Bioimaging 4, 215-224 (1996).
[CrossRef]

D. L. Wokosin, V. Centonze, J. G. White, D. Armstrong, G. Robertson, and A. I. Ferguson, "All-solid-state ultrafast lasers facilitate multiphoton excitation fluorescence imaging," IEEE Sel. Top. Quantum Electron. 2, 1051-1065 (1996).
[CrossRef]

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, "Multiphoton fluorescence excitation: New spectral windows for biological nonlinear microscopy," Proc. Natl. Acad. Sci. USA 93, 10763-10768 (1996).
[CrossRef] [PubMed]

C. Xu, R. M. Williams, W. Zipfel, and W. W. Webb, "Multiphoton excitation cross-sections of molecular fluorophores," Bioimaging 4, 198-207 (1996).
[CrossRef]

1995

I. Gryczynski, H. Szmacinski, and J. R. Lakowicz, "On the possibility of calcium imaging using Indo-1 with 3-photon excitation," Photochem. Photobiol. 62, 804-808 (1995).
[CrossRef] [PubMed]

F. X. Kärtner, L. R. Brovelli, D. Kopf, M. Kamp, I. Calasso, and U. Keller, "Control of solid-state laser dynamics by semiconductor devices," Opt. Eng. 34, 2024-2036 (1995).
[CrossRef]

1994

W. Denk, K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge, D. W. Tank, and R. Yuste, "Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy," J. Neurosci. Methods 54, 151-162 (1994).
[CrossRef] [PubMed]

1993

1992

L. K. Smith, S. A. Payne, W. L. Kway, L. L. Chase, and B. H. T. Chai, "Investigation of the laser properties of Cr3+:LiSrGaF6," IEEE J. Quantum Electron. 28, 2612-2618 (1992).
[CrossRef]

P. F. Curley, A. I. Ferguson, J. G. White, and W. B. Amos, "Application of a femtosecond self-sustaining mode-locked Ti-Sapphire laser to the field of laser scanning confocal microscopy," Opt. Quantum Electron. 24, 851-859 (1992).
[CrossRef]

1990

W. Denk, J. H. Strickler, and W. W. Webb, "2-photon laser scanning fluorescence microscopy," Science 248, 73-76 (1990).
[CrossRef] [PubMed]

1989

S. A. Payne, L. L. Chase, L. K. Smith, W. L. Kway, and H. W. Newkirk, "Laser performance of LiSAIF6:Cr3+," J. Appl. Phys. 66, 1051-1056 (1989).
[CrossRef]

1988

S. A. Payne, L. L. Chase, H. W. Newkirk, L. K. Smith, and W. F. Krupke, "LiCaAlF6:Cr3+: a promising new solid-state laser material," IEEE J. Quantum Electron. 24, 2243-2252 (1988).
[CrossRef]

1986

1978

J. N. Gannaway and C. J. R. Sheppard, "2nd-harmonic imaging in scanning optical microscope," Opt. Quantum Electron. 10, 435-439 (1978).
[CrossRef]

Acker, H.

F. Bestvater, E. Spiess, G. Stobrawa, M. Hacker, T. Feurer, T. Porwol, U. Berchner-Pfannschmidt, C. Wotzlaw, and H. Acker, "Two-photon fluorescence absorption and emission spectra of dyes relevant for cell imaging," J. Microsc. 208, 108-115 (2002).
[CrossRef] [PubMed]

Agate, B.

B. Agate, B. Stormont, A. J. Kemp, C. T. A. Brown, U. Keller, and W. Sibbett, "Simplified cavity designs for efficient and compact femtosecond Cr:LiSAF lasers," Opt. Commun. 205, 207-213 (2002).
[CrossRef]

J. M. Hopkins, G. J. Valentine, B. Agate, A. J. Kemp, U. Keller, and W. Sibbett, "Highly compact and efficient femtosecond Cr:LiSAF lasers," IEEE J. Quantum Electron. 38, 360-368 (2002).
[CrossRef]

Albert, O.

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, "Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror," J. Microsc. 206, 65-71 (2002).
[CrossRef] [PubMed]

Albota, M. A.

Amos, W. B.

P. F. Curley, A. I. Ferguson, J. G. White, and W. B. Amos, "Application of a femtosecond self-sustaining mode-locked Ti-Sapphire laser to the field of laser scanning confocal microscopy," Opt. Quantum Electron. 24, 851-859 (1992).
[CrossRef]

Andegeko, Y.

P. Xi, Y. Andegeko, L. R. Weisel, V. V. Lozovoy, and M. Dantus, "Greater signal, increased depth, and less photobleaching in two-photon microscopy with 10 fs pulses," Opt. Commun. 281, 1841-1849 (2008).
[CrossRef]

Angelow, G.

Armstrong, D.

G. Robertson, D. Armstrong, M. J. P. Dymott, A. I. Ferguson, and G. L. Hogg, "Two-photon fluorescence microscopy with a diode-pumped Cr:LiSAF laser," Appl. Opt. 36, 2481-2483 (1997).
[CrossRef] [PubMed]

D. L. Wokosin, V. Centonze, J. G. White, D. Armstrong, G. Robertson, and A. I. Ferguson, "All-solid-state ultrafast lasers facilitate multiphoton excitation fluorescence imaging," IEEE Sel. Top. Quantum Electron. 2, 1051-1065 (1996).
[CrossRef]

Askari, S.

R. A. Warnock, S. Askari, E. C. Butcher, and U. H. von Andrian, "Molecular mechanisms of lymphocyte homing to peripheral lymph nodes," J. Exp. Med. 187, 205-216 (1998).
[CrossRef] [PubMed]

Barad, Y.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, "Nonlinear scanning laser microscopy by third harmonic generation," Appl. Phys. Lett. 70, 922-924 (1997).
[CrossRef]

Barille, R.

Bavister, B. D.

J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, "Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability," Nat. Biotechnol. 17, 763-767 (1999).
[CrossRef] [PubMed]

Beaurepaire, E.

D. Debarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Methods 3, 47-53 (2006).
[CrossRef]

E. Beaurepaire, M. Oheim, and J. Mertz, "Ultra-deep two-photon fluorescence excitation in turbid media," Opt. Commun. 188, 25-29 (2001).
[CrossRef]

M. Oheim, E. Beaurepaire, E. Chaigneau, J. Mertz, and S. Charpak, "Two-photon microscopy in brain tissue: parameters influencing the imaging depth," J. Neurosci. Methods 111, 29-37 (2001).
[CrossRef] [PubMed]

Benedick, A.

Berchner-Pfannschmidt, U.

F. Bestvater, E. Spiess, G. Stobrawa, M. Hacker, T. Feurer, T. Porwol, U. Berchner-Pfannschmidt, C. Wotzlaw, and H. Acker, "Two-photon fluorescence absorption and emission spectra of dyes relevant for cell imaging," J. Microsc. 208, 108-115 (2002).
[CrossRef] [PubMed]

Berland, K. M.

P. T. C. So, C. Y. Dong, B. R. Masters, and K. M. Berland, "Two-photon excitation fluorescence microscopy," Annu. Rev. Biomed. Eng. 2, 399-429 (2000).
[CrossRef]

Bestvater, F.

F. Bestvater, E. Spiess, G. Stobrawa, M. Hacker, T. Feurer, T. Porwol, U. Berchner-Pfannschmidt, C. Wotzlaw, and H. Acker, "Two-photon fluorescence absorption and emission spectra of dyes relevant for cell imaging," J. Microsc. 208, 108-115 (2002).
[CrossRef] [PubMed]

Bianchini, P.

A. Diaspro, P. Bianchini, G. Vicidomini, M. Faretta, P. Ramoino, and C. Usai, "Multi-photon excitation microscopy," Biomed. Eng. Online 5, 1-14 (2006).
[CrossRef]

Blanchard-Desce, M.

Bogdanov, A.

A. Moore, E. Marecos, A. Bogdanov, and R. Weissleder, "Tumoral distribution of long-circulating dextran-coated iron oxide nanoparticles in a rodent model," Radiology 214, 568-574 (2000).
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B. Agate, B. Stormont, A. J. Kemp, C. T. A. Brown, U. Keller, and W. Sibbett, "Simplified cavity designs for efficient and compact femtosecond Cr:LiSAF lasers," Opt. Commun. 205, 207-213 (2002).
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P. S. Tsai, B. Migliori, K. Campbell, T. N. Kim, Z. Kam, A. Groisman, and D. Kleinfeld, "Spherical aberration correction in nonlinear microscopy and optical ablation using a transparent deformable membrane," Appl. Phys. Lett. 91, 3 (2007).
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A. Nimmerjahn, F. Kirchhoff, J. N. Kerr, and F. Helmchen, "Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo," Nat. Methods 1, 31-37 (2004).
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F. X. Kärtner, L. R. Brovelli, D. Kopf, M. Kamp, I. Calasso, and U. Keller, "Control of solid-state laser dynamics by semiconductor devices," Opt. Eng. 34, 2024-2036 (1995).
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S. A. Payne, L. L. Chase, H. W. Newkirk, L. K. Smith, and W. F. Krupke, "LiCaAlF6:Cr3+: a promising new solid-state laser material," IEEE J. Quantum Electron. 24, 2243-2252 (1988).
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G. Peleg, A. Lewis, O. Bouevitch, L. Loew, D. Parnas, and M. Linial, "Gigantic optical non-linearities from nanoparticle-enhanced molecular probes with potential for selectively imaging the structure and physiology of nanometric regions in cellular systems," Bioimaging 4, 215-224 (1996).
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M. Rueckel, J. A. Mack-Bucher, and W. Denk, "Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing," Proc. Natl. Acad. Sci. USA 103, 17137-17142 (2006).
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S. Maiti, J. B. Shear, R. M. Williams, W. R. Zipfel, and W. W. Webb, "Measuring serotonin distribution in live cells with three-photon excitation," Science 275, 530-532 (1997).
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Malak, H.

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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," Proc. Natl. Acad. Sci. USA 95, 15741-15746 (1998).
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A. Moore, E. Marecos, A. Bogdanov, and R. Weissleder, "Tumoral distribution of long-circulating dextran-coated iron oxide nanoparticles in a rodent model," Radiology 214, 568-574 (2000).
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C. Hönninger, R. Paschotta, F. Morier-Genoud, M. Moser, and U. Keller, "Q-switching stability limits of continuous-wave passive mode locking," J. Opt. Soc. Am. A 16, 46-56 (1999).
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C. Hönninger, R. Paschotta, F. Morier-Genoud, M. Moser, and U. Keller, "Q-switching stability limits of continuous-wave passive mode locking," J. Opt. Soc. Am. A 16, 46-56 (1999).
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S. A. Payne, L. L. Chase, L. K. Smith, W. L. Kway, and H. W. Newkirk, "Laser performance of LiSAIF6:Cr3+," J. Appl. Phys. 66, 1051-1056 (1989).
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A. Nimmerjahn, F. Kirchhoff, J. N. Kerr, and F. Helmchen, "Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo," Nat. Methods 1, 31-37 (2004).
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L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, "Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror," J. Microsc. 206, 65-71 (2002).
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M. Oheim, E. Beaurepaire, E. Chaigneau, J. Mertz, and S. Charpak, "Two-photon microscopy in brain tissue: parameters influencing the imaging depth," J. Neurosci. Methods 111, 29-37 (2001).
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G. Peleg, A. Lewis, O. Bouevitch, L. Loew, D. Parnas, and M. Linial, "Gigantic optical non-linearities from nanoparticle-enhanced molecular probes with potential for selectively imaging the structure and physiology of nanometric regions in cellular systems," Bioimaging 4, 215-224 (1996).
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C. Hönninger, R. Paschotta, F. Morier-Genoud, M. Moser, and U. Keller, "Q-switching stability limits of continuous-wave passive mode locking," J. Opt. Soc. Am. A 16, 46-56 (1999).
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L. K. Smith, S. A. Payne, W. L. Kway, L. L. Chase, and B. H. T. Chai, "Investigation of the laser properties of Cr3+:LiSrGaF6," IEEE J. Quantum Electron. 28, 2612-2618 (1992).
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G. Peleg, A. Lewis, O. Bouevitch, L. Loew, D. Parnas, and M. Linial, "Gigantic optical non-linearities from nanoparticle-enhanced molecular probes with potential for selectively imaging the structure and physiology of nanometric regions in cellular systems," Bioimaging 4, 215-224 (1996).
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D. Debarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, "Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy," Nat. Methods 3, 47-53 (2006).
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S. N. Tandon, J. T. Gopinath, H. M. Shen, G. S. Petrich, L. A. Kolodziejski, F. X. Kartner, and E. P. Ippen, "Large-area broadband saturable Bragg reflectors by use of oxidized AlAs," Opt. Lett. 29, 2551-2553 (2004).
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M. J. Pittet and T. R. Mempel, "Regulation of T-cell migration and effector functions: insights from in vivo imaging studies," Immunol. Rev. 221, 107-129 (2008).
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M. Rueckel, J. A. Mack-Bucher, and W. Denk, "Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing," Proc. Natl. Acad. Sci. USA 103, 17137-17142 (2006).
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S. Maiti, J. B. Shear, R. M. Williams, W. R. Zipfel, and W. W. Webb, "Measuring serotonin distribution in live cells with three-photon excitation," Science 275, 530-532 (1997).
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Supplementary Material (5)

» Media 1: MOV (3026 KB)     
» Media 2: MOV (675 KB)     
» Media 3: MOV (2832 KB)     
» Media 4: MOV (3192 KB)     
» Media 5: MOV (1639 KB)     

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Figures (7)

Fig. 1.
Fig. 1.

Schematic of the single-mode diode-pumped Cr3+:LiCAF laser used in multi-photon microscopy experiments. D1-D4: Single-mode pump diodes at 660 nm, HR: 45° high reflectors at 660 nm, f: visible achromatic doublets with a focal length of 65 mm, PBS: polarizing beam splitter cube, M1-M2: pump mirrors with R=75 mm, M3: flat high reflector, M4: curved high reflector with R=150 mm, OC: 2% output coupler, DCM1-DCM3: flat double-chirped mirrors with ~-50 fs2 dispersion per bounce, SESAM/SBR: semiconductor saturable absorber mirror/saturable Bragg reflector. Dashed lines indicate the mode-locked laser cavity.

Fig. 2.
Fig. 2.

Measured spectrum and second harmonic autocorrelation taken with the single-mode diode-pumped mode locked Cr3+:LiCAF laser using the 2% output coupler at an absorbed pump power of ~600 mW. The FWHM of the autocorrelation is 108 fs, corresponding to a ~70-fs pulse duration (assuming sech2 pulse shape). The average output power is 180 mW, corresponding to a pulse energy of 1.8 nJ for the 100-MHz repetition rate cavity. The spectrum has a bandwidth of 10.2 nm (FWHM) centered around ~800 nm. The corresponding time bandwidth product is ~0.335.

Fig. 3.
Fig. 3.

Images of cortical vasculature stained with FITC. (a) MIP along the z direction of a 250-µm-thick 3D stack with a 932×932 µm2 FOV. The data set consists of 26 frames acquired at 10-µm increments. (b) MIP along the z direction of a 400-µm-thick 3D stack with a 233×233 µm2 FOV. The lateral (x, y) position of the image is marked with the window in (a). The data set consists of 400 frames acquired at 1-µm increments. The same data set is presented as a volumetric image in (c) and two MIPs along the z direction of 50-µm-thick regions are presented at depths of 200 µm and 350 µm in (d) and (e), respectively (Media 1). Scale bar is 100 µm.

Fig. 4.
Fig. 4.

Measurement of the RBC flow. (a) Two-dimensional image of cortical vasculature labeled with FITC, with the white arrow marking the line scan position. The scale bar is 50 µm. (b) The intensity plot of 1000 line scans taken along the axis of the blood vessel during 1.49 s. The length of the individual line scan is 18.69 µm. The estimated RBC velocity is 0.6 mm/s.

Fig. 5.
Fig. 5.

MIP of a 20-µm-thick 3D stack image of the neocortex with astrocytes labeled with SR101 (red) and cortical vasculature stained with FITC (green). The data set has a FOV of 233×233 µm2 and it consists of 20 frames acquired at 1-µm increments (Media 2). The imaging depth is 200 µm below the cortical surface. Scale bar is 100 µm.

Fig. 6.
Fig. 6.

Intravital micrographs of a mouse popliteal lymph node. The image (a) was obtained after intravital staining of mitochondria in lymph node cells though i.v.-injection of Rhodamine 6G (red) and labeling of the blood plasma with FITC (green). SHG signals from reticular collagen fibers are shown in blue (Media 3). Media 4 represents MIPs of five optical sections spaced 2.5 µm apart. This time-lapse recording highlights the cellular dynamics within the lymph node in relation to the structural components, such as collagen fibers and blood vessels. The image (b) shows the lymph node conduit system filled through subcutaneous injection of the low-molecular-weight protein lysozyme tagged with Alexa Fluor 633 (red) into the footpad drained by this lymph node (Media 5). The conduits accompany the collagen network (blue). Scale bars are 50 µm. The imaging depths are 100×150 µm (a) and 30×75 µm (b).

Fig. 7.
Fig. 7.

Imaging of the histological specimen. (a) GFP-expressing 9L fliosarcoma tumor. Green color depicts cell cytoplasm stained with GFP. (b) Pancreatic islets with insulin-producing beta cells. Green color represents FITC staining of insulin granules. In both images cell nuclei were stained with DAPI (blue color). Scale bars are 50 µm.

Tables (1)

Tables Icon

Table 1. Representative list of laser sources that have been used for multi-photon microscopy. OPO: Optical parametric oscillators, PCF: Photonic crystal fiber, SHG: Second harmonic generation. * Denotes the Cr:LiCAF laser that will be described in this work.

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