Abstract

We demonstrate a 60 mg light video-endomicroscope with a cylindrical shape of the rigid tip of only 1.6 mm diameter and 6.7 mm length. A novel implementation method of the illumination unit in the endomicroscope is presented. It allows for the illumination of the biological sample with fiber-coupled LED light at 455 nm and the imaging of the red-shifted fluorescence light above 500 nm in epi-direction. A large numerical aperture of 0.7 leads to a sub-cellular resolution and yields to high-contrast images within a field of view of 160 μm. A miniaturized chip-on-the-tip CMOS image sensor with more than 150,000 pixels captures the multicolor images at 30 fps. Considering size, plug-and-play capability, optical performance, flexibility and weight, we hence present a probe which sets a new benchmark in the field of epifluorescence endomicroscopes. Several ex-vivo and in-vivo experiments in rodents and humans suggest future application in biomedical fields, especially in the neuroscience community, as well as in medical applications targeting optical biopsies or the detection of cellular anomalies.

© 2017 Optical Society of America

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2017 (4)

E. Segev, J. Reimer, L. C. Moreaux, T. M. Fowler, D. Chi, W. D. Sacher, M. Lo, K. Deisseroth, A. S. Tolias, A. Faraon, and M. L. Roukes, “Patterned photostimulation via visible-wavelength photonic probes for deep brain optogenetics,” Neurophotonics 4, 011002 (2017).
[Crossref]

O. Uckermann, R. Galli, S. Leupold, R. Coras, M. Meinhardt, S. Hallmeyer-Elgner, T. Mayer, A. Storch, G. Schackert, E. Koch, and et al., “Label-free multiphoton microscopy reveals altered tissue architecture in hippocampal sclerosis,” Epilepsia 5813598 (2017).
[Crossref] [PubMed]

Z. Huang, S. Shi, H. Qiu, D. Li, J. Zou, and S. Hu, “Fluorescence-guided resection of brain tumor: review of the significance of intraoperative quantification of protoporphyrin IX fluorescence,” Neurophotonics 4, 011011 (2017).
[Crossref] [PubMed]

A. Lukic, S. Dochow, H. Bae, G. Matz, I. Latka, B. Messerschmidt, M. Schmitt, and J. Popp, “Endoscopic fiber probe for nonlinear spectroscopic imaging,” Optica 4, 496–501 (2017).
[Crossref]

2016 (1)

2015 (2)

M. E. Bocarsly, W.-C. Jiang, C. Wang, J. T. Dudman, N. Ji, and Y. Aponte, “Minimally invasive microendoscopy system for in vivo functional imaging of deep nuclei in the mouse brain,” Biomed. Opt. Express 6, 4546–4556 (2015).
[Crossref] [PubMed]

J. M. Gee, M. B. Gibbons, M. Taheri, S. Palumbos, S. C. Morris, R. M. Smeal, K. F. Flynn, M. N. Economo, C. G. Cizek, M. R. Capecchi, and et al., “Imaging activity in astrocytes and neurons with genetically encoded calcium indicators following in utero electroporation,” Front. Mol. Neurosci. 8, 425 (2015).
[Crossref]

2014 (1)

H. Dana, T.-W. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo,” PLoS One 9, e108697 (2014).
[Crossref] [PubMed]

2013 (3)

C. Laperchia, A. L. A. Mascaro, L. Sacconi, A. Andrioli, A. Matté, L. De Franceschi, G. Grassi-Zucconi, M. Bentivoglio, M. Buffelli, and F. S. Pavone, “Two-photon microscopy imaging of Thy1 GFP-m transgenic mice: A novel animal model to investigate brain dendritic cell subsets in vivo,” PloS one 8, e56144 (2013).
[Crossref]

M. Osanai, T. Suzuki, A. Tamura, T. Yonemura, I. Mori, Y. Yanagawa, H. Yawo, and H. Mushiake, “Development of a micro-imaging probe for functional brain imaging,” Neurosci. Res. 75, 46–52 (2013).
[Crossref]

C. Laperchia, A. L. A. Mascaro, L. Sacconi, A. Andrioli, A. Mattè, L. D. Franceschi, G. Grassi-Zucconi, M. Bentivoglio, M. Buffelli, and F. S. Pavone, “Two-photon microscopy imaging of thy1 GFP-M transgenic mice: A novel animal model to investigate brain dendritic cell subsets in vivo,” PloS one 8, e56144 (2013).
[Crossref]

2011 (3)

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. 108, 17598–17603 (2011).
[Crossref] [PubMed]

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. methods 8, 871–878 (2011).
[Crossref] [PubMed]

R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. med. 17, 223–228 (2011).
[Crossref] [PubMed]

2010 (2)

C. M. Lee, C. J. Engelbrecht, T. D. Soper, F. Helmchen, and E. J. Seibel, “Scanning fiber endoscopy with highly flexible, 1-mm catheterscopes for wide-field, full-color imaging,” J. Biophotonics 3, 385 (2010).
[Crossref] [PubMed]

S. M. Landau, C. Liang, R. T. Kester, T. S. Tkaczyk, and M. R. Descour, “Design and evaluation of an ultra-slim objective for in-vivo deep optical biopsy,” Opt. Express 18, 4758–4775 (2010).
[Crossref] [PubMed]

2009 (7)

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, and W.-C. A. Lee, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 1128–1144 (2009).
[Crossref] [PubMed]

A. C. Kwan, K. Duff, G. K. Gouras, and W. W. Webb, “Optical visualization of Alzheimer‘s pathology via multiphoton-excited intrinsic fluorescence and second harmonic generation,” Opt. Express 17, 3679–3689 (2009).
[Crossref] [PubMed]

G. A. Sonn, S.-N. E. Jones, T. V. Tarin, C. B. Du, K. E. Mach, K. C. Jensen, and J. C. Liao, “Optical biopsy of human bladder neoplasia with in vivo confocal laser endomicroscopy,” J. Urology 182, 1299–1305 (2009).
[Crossref]

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, and et al., “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 1128–1144 (2009).
[Crossref] [PubMed]

S. R. Schultz, K. Kitamura, A. Post-Uiterweer, J. Krupic, and M. Häusser, “Spatial pattern coding of sensory information by climbing fiber-evoked calcium signals in networks of neighboring cerebellar purkinje cells,” J. Neurosci. 29, 8005–8015 (2009).
[Crossref] [PubMed]

J. Sawinski, D. J. Wallace, D. S. Greenberg, S. Grossmann, W. Denk, and J. N. Kerr, “Visually evoked activity in cortical cells imaged in freely moving animals,” Proc. Natl. Acad. Sci. 106, 19557–19562 (2009).
[Crossref] [PubMed]

R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. methods 6, 511–512 (2009).
[Crossref] [PubMed]

2008 (4)

M. E. Llewellyn, R. P. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454, 784–788 (2008).
[PubMed]

P.-L. Hsiung, J. Hardy, S. Friedland, R. Soetikno, C. B. Du, A. P. Wu, P. Sahbaie, J. M. Crawford, A. W. Lowe, C. H. Contag, and et al., “Detection of colonic dysplasia in vivo using a targeted heptapeptide and confocal microendoscopy,” Nat. med. 14, 454–458 (2008).
[Crossref] [PubMed]

K. Bulloch, M. M. Miller, J. Gal-Toth, T. A. Milner, A. Gottfried-Blackmore, E. M. Waters, U.W. Kaunzner, K. Liu, R. Lindquist, and M. C. Nussenzweig, “CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain,” J. Comp. Neurol. 508, 687–710 (2008).
[Crossref] [PubMed]

C. J. Engelbrecht, R. S. Johnston, E. J. Seibel, and F. Helmchen, “Ultra-compact fiber-optic two-photon microscope for functional fluorescence imaging in vivo,” Opt. Express 16, 5556–5564 (2008).
[Crossref] [PubMed]

2007 (4)

S. M. Arribas, C. J. Daly, M. C. Gonzáles, and J. C. McGrath, “Imaging the vascular wall using confocal microscopy,” J. Physiol. 584, 5–9 (2007).
[Crossref] [PubMed]

D. A. Dombeck, A. N. Khabbaz, F. Collman, T. L. Adelman, and D. W. Tank, “Imaging large-scale neural activity with cellular resolution in awake, mobile mice,” Neuron 56, 43–57 (2007).
[Crossref] [PubMed]

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. methods 4, 331–336 (2007).
[Crossref] [PubMed]

L. Thiberville, S. Moreno-Swirc, T. Vercauteren, E. Peltier, C. Cavé, and G. Bourg Heckly, “In vivo imaging of the bronchial wall microstructure using fibered confocal fluorescence microscopy,” Am. J. Respir. Crit. Care Med. 175, 22–31 (2007).
[Crossref]

2005 (4)

B. A. Flusberg, J. C. Jung, E. D. Cocker, E. P. Anderson, and M. J. Schnitzer, “In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope,” Opt. Lett. 30, 2272–2274 (2005).
[Crossref] [PubMed]

F. M. Bareyre, M. Kerschensteiner, T. Misgeld, and J. R. Sanes, “Transgenic labeling of the corticospinal tract for monitoring axonal responses to spinal cord injury,” Nat. med. 11, 1355–1360 (2005).
[Crossref] [PubMed]

K. Ohki, S. Chung, Y. H. Ch’ng, P. Kara, and R. C. Reid, “Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex,” Nature 433, 597–603 (2005).
[Crossref] [PubMed]

A. L. Polglase, W. J. McLaren, S. A. Skinner, R. Kiesslich, M. F. Neurath, and P. M. Delaney, “A fluorescence confocal endomicroscope for in vivo microscopy of the upper-and the lower-GI tract,” Gastrointest. endosc. 62, 686–695 (2005).
[Crossref] [PubMed]

2004 (4)

J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer, “In vivo mammalian brain imaging using one-and two-photon fluorescence microendoscopy,” J. Neurophysiol. 92, 3121–3133 (2004).
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Z. Huang, W. Zheng, S. Xie, R. Chen, H. Zeng, D. I. McLean, and H. Lui, “Laser-induced autofluorescence microscopy of normal and tumor human colonic tissue,” Int. J. Oncol. 24, 59–64 (2004).

W. Göbel, J. N. Kerr, A. Nimmerjahn, and F. Helmchen, “Miniaturized two-photon microscope based on a flexible coherent fiber bundle and a gradient-index lens objective,” Opt. Lett. 29, 2521–2523 (2004).
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E. Laemmel, M. Genet, G. Le Goualher, A. Perchant, J.-F. Le Gargasson, and E. Vicaut, “Fibered confocal fluorescence microscopy (cell-vizio™) facilitates extended imaging in the field of microcirculation,” J. Vasc. Res. 41, 400–411 (2004).
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2003 (1)

C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. 100, 7319–7324 (2003).
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2002 (1)

R. M. Hoffman, “Green fluorescent protein imaging of tumour growth, metastasis, and angiogenesis in mouse models,” Lancet Oncol. 3, 546–556 (2002).
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2001 (3)

D. Frimberger, D. Zaak, H. Stepp, R. Knüchel, R. Baumgartner, P. Schneede, N. Schmeller, and A. Hofstetter, “Autofluorescence imaging to optimize 5-ALA-induced fluorescence endoscopy of bladder carcinoma,” Urology 58, 372–375 (2001).
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F. Helmchen, M. S. Fee, D. W. Tank, and W. Denk, “A miniature head-mounted two-photon microscope: high-resolution brain imaging in freely moving animals,” Neuron 31, 903–912 (2001).
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R. Christie, B. Bacskai, W. Zipfel, R. Williams, S. Kajdasz, W. Webb, and B. Hyman, “Growth arrest of individual senile plaques in a model of alzheimer’s disease observed by in vivo multiphoton microscopy,” J. Neurosci. 21, 858–864 (2001).
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2000 (1)

B. Lendvai, E. A. Stern, B. Chen, and K. Svoboda, “Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo,” Nature 404, 876–881 (2000).
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1999 (2)

A. Miyawaki, O. Griesbeck, R. Heim, and R. Y. Tsien, “Dynamic and quantitative Ca2+ measurements using improved cameleons,” Proc. Natl. Acad. Sci. 96, 2135–2140 (1999).
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1996 (1)

D. Yin, “Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores,” Free Radic. Biol. Med. 21, 871–888 (1996).
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1994 (1)

F. Yuan, H. A. Salehi, Y. Boucher, U. S. Vasthare, R. F. Tuma, and R. K. Jain, “Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows,” Cancer Res. 54, 4564–4568 (1994).
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1991 (1)

J. Hung, S. Lam, J. C. Leriche, and B. Palcic, “Autofluorescence of normal and malignant bronchial tissue,” Lasers Surg. Med. 11, 99–105 (1991).
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1970 (1)

A. N. Siakotos, I. Watanabe, A. Saito, and S. Fleischer, “Procedures for the isolation of two distinct lipopigments from human brain: lipofuscin and ceroid,” Biochem. Med. 4, 361–375 (1970).
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Adelman, T. L.

D. A. Dombeck, A. N. Khabbaz, F. Collman, T. L. Adelman, and D. W. Tank, “Imaging large-scale neural activity with cellular resolution in awake, mobile mice,” Neuron 56, 43–57 (2007).
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Aksay, E.

J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer, “In vivo mammalian brain imaging using one-and two-photon fluorescence microendoscopy,” J. Neurophysiol. 92, 3121–3133 (2004).
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Anderson, E. P.

Andrioli, A.

C. Laperchia, A. L. A. Mascaro, L. Sacconi, A. Andrioli, A. Mattè, L. D. Franceschi, G. Grassi-Zucconi, M. Bentivoglio, M. Buffelli, and F. S. Pavone, “Two-photon microscopy imaging of thy1 GFP-M transgenic mice: A novel animal model to investigate brain dendritic cell subsets in vivo,” PloS one 8, e56144 (2013).
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C. Laperchia, A. L. A. Mascaro, L. Sacconi, A. Andrioli, A. Matté, L. De Franceschi, G. Grassi-Zucconi, M. Bentivoglio, M. Buffelli, and F. S. Pavone, “Two-photon microscopy imaging of Thy1 GFP-m transgenic mice: A novel animal model to investigate brain dendritic cell subsets in vivo,” PloS one 8, e56144 (2013).
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Aponte, Y.

Arribas, S. M.

S. M. Arribas, C. J. Daly, M. C. Gonzáles, and J. C. McGrath, “Imaging the vascular wall using confocal microscopy,” J. Physiol. 584, 5–9 (2007).
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Attardo, A.

R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. med. 17, 223–228 (2011).
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Bacskai, B.

R. Christie, B. Bacskai, W. Zipfel, R. Williams, S. Kajdasz, W. Webb, and B. Hyman, “Growth arrest of individual senile plaques in a model of alzheimer’s disease observed by in vivo multiphoton microscopy,” J. Neurosci. 21, 858–864 (2001).
[PubMed]

Bae, H.

Bareyre, F. M.

F. M. Bareyre, M. Kerschensteiner, T. Misgeld, and J. R. Sanes, “Transgenic labeling of the corticospinal tract for monitoring axonal responses to spinal cord injury,” Nat. med. 11, 1355–1360 (2005).
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Barretto, R. P.

R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. med. 17, 223–228 (2011).
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R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. methods 6, 511–512 (2009).
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M. E. Llewellyn, R. P. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454, 784–788 (2008).
[PubMed]

Baumgartner, R.

D. Frimberger, D. Zaak, H. Stepp, R. Knüchel, R. Baumgartner, P. Schneede, N. Schmeller, and A. Hofstetter, “Autofluorescence imaging to optimize 5-ALA-induced fluorescence endoscopy of bladder carcinoma,” Urology 58, 372–375 (2001).
[Crossref] [PubMed]

C. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25, 323–334 (1999).
[Crossref] [PubMed]

Becker, K.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. methods 4, 331–336 (2007).
[Crossref] [PubMed]

Bentivoglio, M.

C. Laperchia, A. L. A. Mascaro, L. Sacconi, A. Andrioli, A. Matté, L. De Franceschi, G. Grassi-Zucconi, M. Bentivoglio, M. Buffelli, and F. S. Pavone, “Two-photon microscopy imaging of Thy1 GFP-m transgenic mice: A novel animal model to investigate brain dendritic cell subsets in vivo,” PloS one 8, e56144 (2013).
[Crossref]

C. Laperchia, A. L. A. Mascaro, L. Sacconi, A. Andrioli, A. Mattè, L. D. Franceschi, G. Grassi-Zucconi, M. Bentivoglio, M. Buffelli, and F. S. Pavone, “Two-photon microscopy imaging of thy1 GFP-M transgenic mice: A novel animal model to investigate brain dendritic cell subsets in vivo,” PloS one 8, e56144 (2013).
[Crossref]

Betz, C.

C. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25, 323–334 (1999).
[Crossref] [PubMed]

Bocarsly, M. E.

Bonhoeffer, T.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, and et al., “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 1128–1144 (2009).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, and W.-C. A. Lee, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 1128–1144 (2009).
[Crossref] [PubMed]

Boucher, Y.

F. Yuan, H. A. Salehi, Y. Boucher, U. S. Vasthare, R. F. Tuma, and R. K. Jain, “Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows,” Cancer Res. 54, 4564–4568 (1994).
[PubMed]

Bourg Heckly, G.

L. Thiberville, S. Moreno-Swirc, T. Vercauteren, E. Peltier, C. Cavé, and G. Bourg Heckly, “In vivo imaging of the bronchial wall microstructure using fibered confocal fluorescence microscopy,” Am. J. Respir. Crit. Care Med. 175, 22–31 (2007).
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Brown, C. M.

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. 108, 17598–17603 (2011).
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Buffelli, M.

C. Laperchia, A. L. A. Mascaro, L. Sacconi, A. Andrioli, A. Matté, L. De Franceschi, G. Grassi-Zucconi, M. Bentivoglio, M. Buffelli, and F. S. Pavone, “Two-photon microscopy imaging of Thy1 GFP-m transgenic mice: A novel animal model to investigate brain dendritic cell subsets in vivo,” PloS one 8, e56144 (2013).
[Crossref]

C. Laperchia, A. L. A. Mascaro, L. Sacconi, A. Andrioli, A. Mattè, L. D. Franceschi, G. Grassi-Zucconi, M. Bentivoglio, M. Buffelli, and F. S. Pavone, “Two-photon microscopy imaging of thy1 GFP-M transgenic mice: A novel animal model to investigate brain dendritic cell subsets in vivo,” PloS one 8, e56144 (2013).
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Bulloch, K.

K. Bulloch, M. M. Miller, J. Gal-Toth, T. A. Milner, A. Gottfried-Blackmore, E. M. Waters, U.W. Kaunzner, K. Liu, R. Lindquist, and M. C. Nussenzweig, “CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain,” J. Comp. Neurol. 508, 687–710 (2008).
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Burns, L. D.

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. methods 8, 871–878 (2011).
[Crossref] [PubMed]

Capecchi, M. R.

J. M. Gee, M. B. Gibbons, M. Taheri, S. Palumbos, S. C. Morris, R. M. Smeal, K. F. Flynn, M. N. Economo, C. G. Cizek, M. R. Capecchi, and et al., “Imaging activity in astrocytes and neurons with genetically encoded calcium indicators following in utero electroporation,” Front. Mol. Neurosci. 8, 425 (2015).
[Crossref]

Capps, G.

R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. med. 17, 223–228 (2011).
[Crossref] [PubMed]

Cavé, C.

L. Thiberville, S. Moreno-Swirc, T. Vercauteren, E. Peltier, C. Cavé, and G. Bourg Heckly, “In vivo imaging of the bronchial wall microstructure using fibered confocal fluorescence microscopy,” Am. J. Respir. Crit. Care Med. 175, 22–31 (2007).
[Crossref]

Ch’ng, Y. H.

K. Ohki, S. Chung, Y. H. Ch’ng, P. Kara, and R. C. Reid, “Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex,” Nature 433, 597–603 (2005).
[Crossref] [PubMed]

Chen, B.

B. Lendvai, E. A. Stern, B. Chen, and K. Svoboda, “Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo,” Nature 404, 876–881 (2000).
[Crossref] [PubMed]

Chen, R.

Z. Huang, W. Zheng, S. Xie, R. Chen, H. Zeng, D. I. McLean, and H. Lui, “Laser-induced autofluorescence microscopy of normal and tumor human colonic tissue,” Int. J. Oncol. 24, 59–64 (2004).

Chen, T.-W.

H. Dana, T.-W. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo,” PLoS One 9, e108697 (2014).
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Chi, D.

E. Segev, J. Reimer, L. C. Moreaux, T. M. Fowler, D. Chi, W. D. Sacher, M. Lo, K. Deisseroth, A. S. Tolias, A. Faraon, and M. L. Roukes, “Patterned photostimulation via visible-wavelength photonic probes for deep brain optogenetics,” Neurophotonics 4, 011002 (2017).
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Chow, D. K.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, and et al., “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 1128–1144 (2009).
[Crossref] [PubMed]

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, and W.-C. A. Lee, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 1128–1144 (2009).
[Crossref] [PubMed]

Christie, R.

R. Christie, B. Bacskai, W. Zipfel, R. Williams, S. Kajdasz, W. Webb, and B. Hyman, “Growth arrest of individual senile plaques in a model of alzheimer’s disease observed by in vivo multiphoton microscopy,” J. Neurosci. 21, 858–864 (2001).
[PubMed]

Chuckowree, J.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, and W.-C. A. Lee, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 1128–1144 (2009).
[Crossref] [PubMed]

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, and et al., “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 1128–1144 (2009).
[Crossref] [PubMed]

Chung, S.

K. Ohki, S. Chung, Y. H. Ch’ng, P. Kara, and R. C. Reid, “Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex,” Nature 433, 597–603 (2005).
[Crossref] [PubMed]

Cizek, C. G.

J. M. Gee, M. B. Gibbons, M. Taheri, S. Palumbos, S. C. Morris, R. M. Smeal, K. F. Flynn, M. N. Economo, C. G. Cizek, M. R. Capecchi, and et al., “Imaging activity in astrocytes and neurons with genetically encoded calcium indicators following in utero electroporation,” Front. Mol. Neurosci. 8, 425 (2015).
[Crossref]

Cocker, E. D.

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. methods 8, 871–878 (2011).
[Crossref] [PubMed]

B. A. Flusberg, J. C. Jung, E. D. Cocker, E. P. Anderson, and M. J. Schnitzer, “In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope,” Opt. Lett. 30, 2272–2274 (2005).
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Collman, F.

D. A. Dombeck, A. N. Khabbaz, F. Collman, T. L. Adelman, and D. W. Tank, “Imaging large-scale neural activity with cellular resolution in awake, mobile mice,” Neuron 56, 43–57 (2007).
[Crossref] [PubMed]

Contag, C. H.

P.-L. Hsiung, J. Hardy, S. Friedland, R. Soetikno, C. B. Du, A. P. Wu, P. Sahbaie, J. M. Crawford, A. W. Lowe, C. H. Contag, and et al., “Detection of colonic dysplasia in vivo using a targeted heptapeptide and confocal microendoscopy,” Nat. med. 14, 454–458 (2008).
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Coras, R.

O. Uckermann, R. Galli, S. Leupold, R. Coras, M. Meinhardt, S. Hallmeyer-Elgner, T. Mayer, A. Storch, G. Schackert, E. Koch, and et al., “Label-free multiphoton microscopy reveals altered tissue architecture in hippocampal sclerosis,” Epilepsia 5813598 (2017).
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Crawford, J. M.

P.-L. Hsiung, J. Hardy, S. Friedland, R. Soetikno, C. B. Du, A. P. Wu, P. Sahbaie, J. M. Crawford, A. W. Lowe, C. H. Contag, and et al., “Detection of colonic dysplasia in vivo using a targeted heptapeptide and confocal microendoscopy,” Nat. med. 14, 454–458 (2008).
[Crossref] [PubMed]

Daly, C. J.

S. M. Arribas, C. J. Daly, M. C. Gonzáles, and J. C. McGrath, “Imaging the vascular wall using confocal microscopy,” J. Physiol. 584, 5–9 (2007).
[Crossref] [PubMed]

Dana, H.

H. Dana, T.-W. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo,” PLoS One 9, e108697 (2014).
[Crossref] [PubMed]

De Franceschi, L.

C. Laperchia, A. L. A. Mascaro, L. Sacconi, A. Andrioli, A. Matté, L. De Franceschi, G. Grassi-Zucconi, M. Bentivoglio, M. Buffelli, and F. S. Pavone, “Two-photon microscopy imaging of Thy1 GFP-m transgenic mice: A novel animal model to investigate brain dendritic cell subsets in vivo,” PloS one 8, e56144 (2013).
[Crossref]

De Paola, V.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, and et al., “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 1128–1144 (2009).
[Crossref] [PubMed]

Deininger, K.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. methods 4, 331–336 (2007).
[Crossref] [PubMed]

Deisseroth, K.

E. Segev, J. Reimer, L. C. Moreaux, T. M. Fowler, D. Chi, W. D. Sacher, M. Lo, K. Deisseroth, A. S. Tolias, A. Faraon, and M. L. Roukes, “Patterned photostimulation via visible-wavelength photonic probes for deep brain optogenetics,” Neurophotonics 4, 011002 (2017).
[Crossref]

Delaney, P. M.

A. L. Polglase, W. J. McLaren, S. A. Skinner, R. Kiesslich, M. F. Neurath, and P. M. Delaney, “A fluorescence confocal endomicroscope for in vivo microscopy of the upper-and the lower-GI tract,” Gastrointest. endosc. 62, 686–695 (2005).
[Crossref] [PubMed]

Delp, S. L.

M. E. Llewellyn, R. P. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454, 784–788 (2008).
[PubMed]

Denk, W.

J. Sawinski, D. J. Wallace, D. S. Greenberg, S. Grossmann, W. Denk, and J. N. Kerr, “Visually evoked activity in cortical cells imaged in freely moving animals,” Proc. Natl. Acad. Sci. 106, 19557–19562 (2009).
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F. Helmchen, M. S. Fee, D. W. Tank, and W. Denk, “A miniature head-mounted two-photon microscope: high-resolution brain imaging in freely moving animals,” Neuron 31, 903–912 (2001).
[Crossref] [PubMed]

Descour, M. R.

Deussing, J. M.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. methods 4, 331–336 (2007).
[Crossref] [PubMed]

Dochow, S.

Dodt, H.-U.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. methods 4, 331–336 (2007).
[Crossref] [PubMed]

Dombeck, D. A.

D. A. Dombeck, A. N. Khabbaz, F. Collman, T. L. Adelman, and D. W. Tank, “Imaging large-scale neural activity with cellular resolution in awake, mobile mice,” Neuron 56, 43–57 (2007).
[Crossref] [PubMed]

Du, C. B.

G. A. Sonn, S.-N. E. Jones, T. V. Tarin, C. B. Du, K. E. Mach, K. C. Jensen, and J. C. Liao, “Optical biopsy of human bladder neoplasia with in vivo confocal laser endomicroscopy,” J. Urology 182, 1299–1305 (2009).
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P.-L. Hsiung, J. Hardy, S. Friedland, R. Soetikno, C. B. Du, A. P. Wu, P. Sahbaie, J. M. Crawford, A. W. Lowe, C. H. Contag, and et al., “Detection of colonic dysplasia in vivo using a targeted heptapeptide and confocal microendoscopy,” Nat. med. 14, 454–458 (2008).
[Crossref] [PubMed]

Dudman, J. T.

Duff, K.

Economo, M. N.

J. M. Gee, M. B. Gibbons, M. Taheri, S. Palumbos, S. C. Morris, R. M. Smeal, K. F. Flynn, M. N. Economo, C. G. Cizek, M. R. Capecchi, and et al., “Imaging activity in astrocytes and neurons with genetically encoded calcium indicators following in utero electroporation,” Front. Mol. Neurosci. 8, 425 (2015).
[Crossref]

Eder, M.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. methods 4, 331–336 (2007).
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[Crossref] [PubMed]

Schmitt, M.

Schneede, P.

D. Frimberger, D. Zaak, H. Stepp, R. Knüchel, R. Baumgartner, P. Schneede, N. Schmeller, and A. Hofstetter, “Autofluorescence imaging to optimize 5-ALA-induced fluorescence endoscopy of bladder carcinoma,” Urology 58, 372–375 (2001).
[Crossref] [PubMed]

Schnitzer, M. J.

R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. med. 17, 223–228 (2011).
[Crossref] [PubMed]

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. methods 8, 871–878 (2011).
[Crossref] [PubMed]

R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. methods 6, 511–512 (2009).
[Crossref] [PubMed]

M. E. Llewellyn, R. P. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454, 784–788 (2008).
[PubMed]

B. A. Flusberg, J. C. Jung, E. D. Cocker, E. P. Anderson, and M. J. Schnitzer, “In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope,” Opt. Lett. 30, 2272–2274 (2005).
[Crossref] [PubMed]

J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer, “In vivo mammalian brain imaging using one-and two-photon fluorescence microendoscopy,” J. Neurophysiol. 92, 3121–3133 (2004).
[Crossref] [PubMed]

Schultz, S. R.

S. R. Schultz, K. Kitamura, A. Post-Uiterweer, J. Krupic, and M. Häusser, “Spatial pattern coding of sensory information by climbing fiber-evoked calcium signals in networks of neighboring cerebellar purkinje cells,” J. Neurosci. 29, 8005–8015 (2009).
[Crossref] [PubMed]

Segev, E.

E. Segev, J. Reimer, L. C. Moreaux, T. M. Fowler, D. Chi, W. D. Sacher, M. Lo, K. Deisseroth, A. S. Tolias, A. Faraon, and M. L. Roukes, “Patterned photostimulation via visible-wavelength photonic probes for deep brain optogenetics,” Neurophotonics 4, 011002 (2017).
[Crossref]

Seibel, E. J.

C. M. Lee, C. J. Engelbrecht, T. D. Soper, F. Helmchen, and E. J. Seibel, “Scanning fiber endoscopy with highly flexible, 1-mm catheterscopes for wide-field, full-color imaging,” J. Biophotonics 3, 385 (2010).
[Crossref] [PubMed]

C. J. Engelbrecht, R. S. Johnston, E. J. Seibel, and F. Helmchen, “Ultra-compact fiber-optic two-photon microscope for functional fluorescence imaging in vivo,” Opt. Express 16, 5556–5564 (2008).
[Crossref] [PubMed]

Shi, S.

Z. Huang, S. Shi, H. Qiu, D. Li, J. Zou, and S. Hu, “Fluorescence-guided resection of brain tumor: review of the significance of intraoperative quantification of protoporphyrin IX fluorescence,” Neurophotonics 4, 011011 (2017).
[Crossref] [PubMed]

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H. Dana, T.-W. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo,” PLoS One 9, e108697 (2014).
[Crossref] [PubMed]

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A. N. Siakotos, I. Watanabe, A. Saito, and S. Fleischer, “Procedures for the isolation of two distinct lipopigments from human brain: lipofuscin and ceroid,” Biochem. Med. 4, 361–375 (1970).
[Crossref] [PubMed]

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A. L. Polglase, W. J. McLaren, S. A. Skinner, R. Kiesslich, M. F. Neurath, and P. M. Delaney, “A fluorescence confocal endomicroscope for in vivo microscopy of the upper-and the lower-GI tract,” Gastrointest. endosc. 62, 686–695 (2005).
[Crossref] [PubMed]

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J. M. Gee, M. B. Gibbons, M. Taheri, S. Palumbos, S. C. Morris, R. M. Smeal, K. F. Flynn, M. N. Economo, C. G. Cizek, M. R. Capecchi, and et al., “Imaging activity in astrocytes and neurons with genetically encoded calcium indicators following in utero electroporation,” Front. Mol. Neurosci. 8, 425 (2015).
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G. A. Sonn, S.-N. E. Jones, T. V. Tarin, C. B. Du, K. E. Mach, K. C. Jensen, and J. C. Liao, “Optical biopsy of human bladder neoplasia with in vivo confocal laser endomicroscopy,” J. Urology 182, 1299–1305 (2009).
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C. M. Lee, C. J. Engelbrecht, T. D. Soper, F. Helmchen, and E. J. Seibel, “Scanning fiber endoscopy with highly flexible, 1-mm catheterscopes for wide-field, full-color imaging,” J. Biophotonics 3, 385 (2010).
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J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer, “In vivo mammalian brain imaging using one-and two-photon fluorescence microendoscopy,” J. Neurophysiol. 92, 3121–3133 (2004).
[Crossref] [PubMed]

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D. Frimberger, D. Zaak, H. Stepp, R. Knüchel, R. Baumgartner, P. Schneede, N. Schmeller, and A. Hofstetter, “Autofluorescence imaging to optimize 5-ALA-induced fluorescence endoscopy of bladder carcinoma,” Urology 58, 372–375 (2001).
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C. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25, 323–334 (1999).
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H. Dana, T.-W. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo,” PLoS One 9, e108697 (2014).
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B. Lendvai, E. A. Stern, B. Chen, and K. Svoboda, “Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo,” Nature 404, 876–881 (2000).
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J. M. Gee, M. B. Gibbons, M. Taheri, S. Palumbos, S. C. Morris, R. M. Smeal, K. F. Flynn, M. N. Economo, C. G. Cizek, M. R. Capecchi, and et al., “Imaging activity in astrocytes and neurons with genetically encoded calcium indicators following in utero electroporation,” Front. Mol. Neurosci. 8, 425 (2015).
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M. Osanai, T. Suzuki, A. Tamura, T. Yonemura, I. Mori, Y. Yanagawa, H. Yawo, and H. Mushiake, “Development of a micro-imaging probe for functional brain imaging,” Neurosci. Res. 75, 46–52 (2013).
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G. A. Sonn, S.-N. E. Jones, T. V. Tarin, C. B. Du, K. E. Mach, K. C. Jensen, and J. C. Liao, “Optical biopsy of human bladder neoplasia with in vivo confocal laser endomicroscopy,” J. Urology 182, 1299–1305 (2009).
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F. Yuan, H. A. Salehi, Y. Boucher, U. S. Vasthare, R. F. Tuma, and R. K. Jain, “Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows,” Cancer Res. 54, 4564–4568 (1994).
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A. N. Siakotos, I. Watanabe, A. Saito, and S. Fleischer, “Procedures for the isolation of two distinct lipopigments from human brain: lipofuscin and ceroid,” Biochem. Med. 4, 361–375 (1970).
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R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. med. 17, 223–228 (2011).
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K. Bulloch, M. M. Miller, J. Gal-Toth, T. A. Milner, A. Gottfried-Blackmore, E. M. Waters, U.W. Kaunzner, K. Liu, R. Lindquist, and M. C. Nussenzweig, “CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain,” J. Comp. Neurol. 508, 687–710 (2008).
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R. Christie, B. Bacskai, W. Zipfel, R. Williams, S. Kajdasz, W. Webb, and B. Hyman, “Growth arrest of individual senile plaques in a model of alzheimer’s disease observed by in vivo multiphoton microscopy,” J. Neurosci. 21, 858–864 (2001).
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D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. 108, 17598–17603 (2011).
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R. Christie, B. Bacskai, W. Zipfel, R. Williams, S. Kajdasz, W. Webb, and B. Hyman, “Growth arrest of individual senile plaques in a model of alzheimer’s disease observed by in vivo multiphoton microscopy,” J. Neurosci. 21, 858–864 (2001).
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Z. Huang, W. Zheng, S. Xie, R. Chen, H. Zeng, D. I. McLean, and H. Lui, “Laser-induced autofluorescence microscopy of normal and tumor human colonic tissue,” Int. J. Oncol. 24, 59–64 (2004).

Xu, C.

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. 108, 17598–17603 (2011).
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M. Osanai, T. Suzuki, A. Tamura, T. Yonemura, I. Mori, Y. Yanagawa, H. Yawo, and H. Mushiake, “Development of a micro-imaging probe for functional brain imaging,” Neurosci. Res. 75, 46–52 (2013).
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M. Osanai, T. Suzuki, A. Tamura, T. Yonemura, I. Mori, Y. Yanagawa, H. Yawo, and H. Mushiake, “Development of a micro-imaging probe for functional brain imaging,” Neurosci. Res. 75, 46–52 (2013).
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M. Osanai, T. Suzuki, A. Tamura, T. Yonemura, I. Mori, Y. Yanagawa, H. Yawo, and H. Mushiake, “Development of a micro-imaging probe for functional brain imaging,” Neurosci. Res. 75, 46–52 (2013).
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F. Yuan, H. A. Salehi, Y. Boucher, U. S. Vasthare, R. F. Tuma, and R. K. Jain, “Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows,” Cancer Res. 54, 4564–4568 (1994).
[PubMed]

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D. Frimberger, D. Zaak, H. Stepp, R. Knüchel, R. Baumgartner, P. Schneede, N. Schmeller, and A. Hofstetter, “Autofluorescence imaging to optimize 5-ALA-induced fluorescence endoscopy of bladder carcinoma,” Urology 58, 372–375 (2001).
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Z. Huang, W. Zheng, S. Xie, R. Chen, H. Zeng, D. I. McLean, and H. Lui, “Laser-induced autofluorescence microscopy of normal and tumor human colonic tissue,” Int. J. Oncol. 24, 59–64 (2004).

Zheng, W.

Z. Huang, W. Zheng, S. Xie, R. Chen, H. Zeng, D. I. McLean, and H. Lui, “Laser-induced autofluorescence microscopy of normal and tumor human colonic tissue,” Int. J. Oncol. 24, 59–64 (2004).

Zieglgänsberger, W.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. methods 4, 331–336 (2007).
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R. Christie, B. Bacskai, W. Zipfel, R. Williams, S. Kajdasz, W. Webb, and B. Hyman, “Growth arrest of individual senile plaques in a model of alzheimer’s disease observed by in vivo multiphoton microscopy,” J. Neurosci. 21, 858–864 (2001).
[PubMed]

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K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. El Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. methods 8, 871–878 (2011).
[Crossref] [PubMed]

R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. med. 17, 223–228 (2011).
[Crossref] [PubMed]

Zou, J.

Z. Huang, S. Shi, H. Qiu, D. Li, J. Zou, and S. Hu, “Fluorescence-guided resection of brain tumor: review of the significance of intraoperative quantification of protoporphyrin IX fluorescence,” Neurophotonics 4, 011011 (2017).
[Crossref] [PubMed]

Am. J. Respir. Crit. Care Med. (1)

L. Thiberville, S. Moreno-Swirc, T. Vercauteren, E. Peltier, C. Cavé, and G. Bourg Heckly, “In vivo imaging of the bronchial wall microstructure using fibered confocal fluorescence microscopy,” Am. J. Respir. Crit. Care Med. 175, 22–31 (2007).
[Crossref]

Biochem. Med. (1)

A. N. Siakotos, I. Watanabe, A. Saito, and S. Fleischer, “Procedures for the isolation of two distinct lipopigments from human brain: lipofuscin and ceroid,” Biochem. Med. 4, 361–375 (1970).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

Cancer Res. (1)

F. Yuan, H. A. Salehi, Y. Boucher, U. S. Vasthare, R. F. Tuma, and R. K. Jain, “Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows,” Cancer Res. 54, 4564–4568 (1994).
[PubMed]

Epilepsia (1)

O. Uckermann, R. Galli, S. Leupold, R. Coras, M. Meinhardt, S. Hallmeyer-Elgner, T. Mayer, A. Storch, G. Schackert, E. Koch, and et al., “Label-free multiphoton microscopy reveals altered tissue architecture in hippocampal sclerosis,” Epilepsia 5813598 (2017).
[Crossref] [PubMed]

Free Radic. Biol. Med. (1)

D. Yin, “Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores,” Free Radic. Biol. Med. 21, 871–888 (1996).
[Crossref] [PubMed]

Front. Mol. Neurosci. (1)

J. M. Gee, M. B. Gibbons, M. Taheri, S. Palumbos, S. C. Morris, R. M. Smeal, K. F. Flynn, M. N. Economo, C. G. Cizek, M. R. Capecchi, and et al., “Imaging activity in astrocytes and neurons with genetically encoded calcium indicators following in utero electroporation,” Front. Mol. Neurosci. 8, 425 (2015).
[Crossref]

Gastrointest. endosc. (1)

A. L. Polglase, W. J. McLaren, S. A. Skinner, R. Kiesslich, M. F. Neurath, and P. M. Delaney, “A fluorescence confocal endomicroscope for in vivo microscopy of the upper-and the lower-GI tract,” Gastrointest. endosc. 62, 686–695 (2005).
[Crossref] [PubMed]

Int. J. Oncol. (1)

Z. Huang, W. Zheng, S. Xie, R. Chen, H. Zeng, D. I. McLean, and H. Lui, “Laser-induced autofluorescence microscopy of normal and tumor human colonic tissue,” Int. J. Oncol. 24, 59–64 (2004).

J. Biophotonics (1)

C. M. Lee, C. J. Engelbrecht, T. D. Soper, F. Helmchen, and E. J. Seibel, “Scanning fiber endoscopy with highly flexible, 1-mm catheterscopes for wide-field, full-color imaging,” J. Biophotonics 3, 385 (2010).
[Crossref] [PubMed]

J. Comp. Neurol. (1)

K. Bulloch, M. M. Miller, J. Gal-Toth, T. A. Milner, A. Gottfried-Blackmore, E. M. Waters, U.W. Kaunzner, K. Liu, R. Lindquist, and M. C. Nussenzweig, “CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain,” J. Comp. Neurol. 508, 687–710 (2008).
[Crossref] [PubMed]

J. Neurophysiol. (1)

J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer, “In vivo mammalian brain imaging using one-and two-photon fluorescence microendoscopy,” J. Neurophysiol. 92, 3121–3133 (2004).
[Crossref] [PubMed]

J. Neurosci. (2)

S. R. Schultz, K. Kitamura, A. Post-Uiterweer, J. Krupic, and M. Häusser, “Spatial pattern coding of sensory information by climbing fiber-evoked calcium signals in networks of neighboring cerebellar purkinje cells,” J. Neurosci. 29, 8005–8015 (2009).
[Crossref] [PubMed]

R. Christie, B. Bacskai, W. Zipfel, R. Williams, S. Kajdasz, W. Webb, and B. Hyman, “Growth arrest of individual senile plaques in a model of alzheimer’s disease observed by in vivo multiphoton microscopy,” J. Neurosci. 21, 858–864 (2001).
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J. Physiol. (1)

S. M. Arribas, C. J. Daly, M. C. Gonzáles, and J. C. McGrath, “Imaging the vascular wall using confocal microscopy,” J. Physiol. 584, 5–9 (2007).
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J. Urology (1)

G. A. Sonn, S.-N. E. Jones, T. V. Tarin, C. B. Du, K. E. Mach, K. C. Jensen, and J. C. Liao, “Optical biopsy of human bladder neoplasia with in vivo confocal laser endomicroscopy,” J. Urology 182, 1299–1305 (2009).
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J. Vasc. Res. (1)

E. Laemmel, M. Genet, G. Le Goualher, A. Perchant, J.-F. Le Gargasson, and E. Vicaut, “Fibered confocal fluorescence microscopy (cell-vizio™) facilitates extended imaging in the field of microcirculation,” J. Vasc. Res. 41, 400–411 (2004).
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Lasers Surg. Med. (2)

C. Betz, M. Mehlmann, K. Rick, H. Stepp, G. Grevers, R. Baumgartner, and A. Leunig, “Autofluorescence imaging and spectroscopy of normal and malignant mucosa in patients with head and neck cancer,” Lasers Surg. Med. 25, 323–334 (1999).
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Supplementary Material (2)

NameDescription
» Visualization 1: MP4 (4971 KB)      Video captured with the endomicroscopic probe of a thin histological brain slice of a transgenic Thy1-GFP-M
» Visualization 2: MP4 (13420 KB)      Video demonstrates cell flow in blood vessels in real time in the mouth of a human by locally staining the area under observation with fluorescine

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Figures (10)

Fig. 1
Fig. 1 Optical design of the endoscopic probe based on a double deflection approach using a side-fire fiber and a 500 nm longpass filter. Peak emission of the incoherent illumination light source (LED) at 455 nm and imaging of the red shifted fluorescence light on a subcellular level with a numerical aperture of 0.7. Object is magnified by a factor of 4.1 and captured by a miniaturized CMOS image sensor chip with more than 150,000 pixels.
Fig. 2
Fig. 2 a) Monochromatic (@ 532 nm) Strehl ratio indicates a diffraction limited performance (Strehl ratio≥0.8) within the entire field of view. Consideration of a quadratic object with 173 μm side length. b) Monochromatic image simulation (@ 532 nm) of a Siemens-star-type object (left) observed through the endomicroscope (right) confirms the excellent point-to-point image quality but exposes slight vignetting and pincushion distortion effects progressively increasing towards the edge of the field of view. The pixelation of the camera chip is not considered. Scale in object space (Evaluations performed with ZEMAX).
Fig. 3
Fig. 3 a) Oval-shape 500 nm long-pass dichroic beam splitter fixed inside the final mechanical mounting. b) Size comparison of a customary matchstick next to the final probe illustrates the miniature appearance of the device with a spatial extent of only 1.6 mm in diameter, a length of 6.7 mm and a total weight of 60±10 mg excluding the wires. Scale bars 2.0 mm, respectively.
Fig. 4
Fig. 4 a) Image captured with the endomicroscopic probe of a uniform chrome grid with a period of 32 μm placed in front of a homogeneously fluorescent target illuminated in epi-direction. A highly resolving image quality is obtained. Slight pincushion distortion effects are visible and progressively increase towards the edge of the field of view. b) Radial intensity profile obtained within the red rectangle in (a) indicates precise edge response functions as a function of the radial distance from the optical axis. c) The first derivative of the edge response function (b) shows the line spread function. Its full-width-at-half-maximum is a measure for the resolution of the device. Averaged FWHM of 0.74±0.08 μm has been obtained.
Fig. 5
Fig. 5 Pictures of the upper surface of a leaf of Begonia x ricinifolia captured with the endomicroscope at the same lateral position but at different axial distances. Probe has been attached to a five-axis stage and moved mechanically away from the specimen in 20 μm steps (from left to right). The ability to sharply image the different axial tissue layers consisting of different cell sizes with a uniformly high resolution but slight intensity reduction for deeper layers is observed. Scale bars 50 μm, respectively.
Fig. 6
Fig. 6 Pictures captured with the endomicroscopic probe of a thin histological brain slice of a transgenic Thy1-GFP-M mouse expressing enhanced green fluorescent protein in a sparse subset of neuronal populations. Illumination in epi-direction. The submicrometer resolution enables the visualization of cellular compartments like dendrites and somas. Scale bars 50 μm, respectively.
Fig. 7
Fig. 7 Image captured with the endomicroscopic probe in epi-direction a) of a cryosection of 10 μm thickness of an experimental tumor expressing eGFP that was grown in an incubated chicken egg. Morphology of tumor tissue could be visualized (left). Healthy tissue (dark) could be accurately distinguished from malignant lesions (bright) at the boundary of the tumor (right). b) Investigation of a glioblastoma biopsy (volume tissue) surgically removed from the brain of a human. Stained in-vivo with 5-Ala. Four adjacent images 150 ± 20 μm apart from each other (top left to bottom right) demonstrate a diffuse delineation capability of the device between malignant (top left), a transition area and healthy tissue (bottom right). Scale bars 50 μm, respectively.
Fig. 8
Fig. 8 Images captured with the endomicroscope in epi-direction. a) Contours of pyramidal cells (white arrows) and b) Lipofuscin (granular depositions) visualized in autofluorescence mode in a thin unstained section of a human hippocampus. c) Autofluorescence signal of a thin section of unstained human brain tissue illustrates the transverse section of a blood vessel. Scale bars 50 μm, respectively.
Fig. 9
Fig. 9 In-vivo imaging of neuronal cells through a cranial window implanted in the skull of an anesthetized Thy1-GFP-M mouse expressing green fluorescent protein in a sparse subset of neurons. a) Mouse has been placed on a heated stage. The endomicroscopic probe has been moved precisely by a five-axis-stage in lateral and axial direction to sharply image the region of interest. b) Visualization of dendritic cells and blood vessels directly below the cranial window. c) Measurements at up to 60 μm deep inside layer I of the neocortex reveals single dendrites and blood vessels. Scale bars 50 μm, respectively.
Fig. 10
Fig. 10 a) The endomicroscope has been assembled into a provisional metal sleeve with a rigid length/diameter of 14.5 cm / 2.3 mm (1) and an additional movable part with a length/diameter of 47.5 cm / 5.0 mm (2) to improve the handling properties of the probe in the medical environment. Scale bar 3 cm. b) Cell flow in blood vessels can be imaged in real time in the mouth of a human by locally staining the area under observation with fluorescein (ALCON). c) By intraveneous injection of 1 ml 10-percent fluorescein into the volunteer’s arm we could detect the contours of single cells after a slight post-processing local contrast enhancement. Scale bars b) and c) 50 μm, respectively.

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