Abstract

The application of the fluorescence imaging method to living animals, together with the use of genetically engineered animals and synthesized photo-responsive compounds, is a powerful method for investigating brain functions. Here, we report a fluorescence imaging method for the brain surface and deep brain tissue that uses compact and mass-producible semiconductor imaging devices based on complementary metal-oxide semiconductor (CMOS) technology. An image sensor chip was designed to be inserted into brain tissue, and its size was 1500 × 450 μm. Sample illumination is also a key issue for intravital fluorescence imaging. Hence, for the uniform illumination of the imaging area, we propose a new method involving the epi-illumination of living biological tissues, and we performed investigations using optical simulations and experimental evaluation.

© 2015 Optical Society of America

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2014 (2)

H. Takehara, A. Nagaoka, J. Noguchi, T. Akagi, H. Kasai, and T. Ichiki, “Lab-on-a-brain: Implantable micro-optical fluidic devices for neural cell analysis in vivo,” Sci. Rep. 4, 6721 (2014).
[Crossref] [PubMed]

M. Haruta, C. Kitsumoto, Y. Sunaga, H. Takehara, T. Noda, K. Sasagawa, T. Tokuda, and J. Ohta, “An implantable CMOS device for blood-flow imaging during experiments on freely moving rats,” Jpn. J. Appl. Phys. 53(4S), 04EL05 (2014).
[Crossref]

2013 (3)

M. Choi, J. W. Choi, S. Kim, S. Nizamoglu, S. K. Hahn, and S. H. Yun, “Light-guiding hydrogels for cell-based sensing and optogenetic synthesis in vivo,” Nat. Photonics 7(12), 987–994 (2013).
[Crossref] [PubMed]

E. Petryayeva, W. R. Algar, and I. L. Medintz, “Quantum dots in bioanalysis: a review of applications across various platforms for fluorescence spectroscopy and imaging,” Appl. Spectrosc. 67(3), 215–252 (2013).
[Crossref] [PubMed]

S. Sekiya, T. Shimizu, and T. Okano, “Vascularization in 3D tissue using cell sheet technology,” Regen. Med. 8(3), 371–377 (2013).
[Crossref] [PubMed]

2012 (2)

G. Hall, S. L. Jacques, K. W. Eliceiri, and P. J. Campagnola, “Goniometric measurements of thick tissue using Monte Carlo simulations to obtain the single scattering anisotropy coefficient,” Biomed. Opt. Express 3(11), 2707–2719 (2012).
[Crossref] [PubMed]

R. M. Valentine, K. Wood, C. T. Brown, S. H. Ibbotson, and H. Moseley, “Monte Carlo simulations for optimal light delivery in photodynamic therapy of non-melanoma skin cancer,” Phys. Med. Biol. 57(20), 6327–6345 (2012).
[Crossref] [PubMed]

2011 (5)

O. Yizhar, L. E. Fenno, T. J. Davidson, M. Mogri, and K. Deisseroth, “Optogenetics in neural systems,” Neuron 71(1), 9–34 (2011).
[Crossref] [PubMed]

K. K. Ghosh, L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. E. Gamal, and M. J. Schnitzer, “Miniaturized integration of a fluorescence microscope,” Nat. Methods 8(10), 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(2), 223–228 (2011).
[Crossref] [PubMed]

M. J. Pittet and R. Weissleder, “Intravital imaging,” Cell 147(5), 983–991 (2011).
[Crossref] [PubMed]

J. Noguchi, A. Nagaoka, S. Watanabe, G. C. R. Ellis-Davies, K. Kitamura, M. Kano, M. Matsuzaki, and H. Kasai, “In vivo two-photon uncaging of glutamate revealing the structure-function relationships of dendritic spines in the neocortex of adult mice,” J. Physiol. 589(10), 2447–2457 (2011).
[Crossref] [PubMed]

2010 (4)

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

A. Tagawa, H. Minami, M. Mitani, T. Noda, K. Sasagawa, T. Tokuda, H. Tamura, Y. Hatanaka, Y. Ishikawa, S. Shiosaka, and J. Ohta, “Multimodal Complementary Metal–Oxide–Semiconductor Sensor Device for Imaging of Fluorescence and Electrical Potential in Deep Brain of Mouse,” Jpn. J. Appl. Phys. 49(1), 01AG02 (2010).
[Crossref]

A. Tagawa, M. Mitani, H. Minami, T. Noda, K. Sasagawa, T. Tokuda, and J. Ohta, “Complementary Metal Oxide Semiconductor Based Multimodal Sensor for In vivo Brain Function Imaging with a Function for Simultaneous Cell Stimulation,” Jpn. J. Appl. Phys. 49, 04DL02 (2010).

R. G. Aswathy, Y. Yoshida, T. Maekawa, and D. S. Kumar, “Near-infrared quantum dots for deep tissue imaging,” Anal. Bioanal. Chem. 397(4), 1417–1435 (2010).
[Crossref] [PubMed]

2009 (2)

J. Ohta, T. Tokuda, K. Sasagawa, and T. Noda, “Implantable CMOS biomedical devices,” Sensors (Basel) 9(11), 9073–9093 (2009).
[Crossref] [PubMed]

J.-H. Wang, S.-Y. Lien, J.-R. Ho, T.-K. Shih, C.-F. Chen, C.-C. Chen, and W.-T. Whang, “Optical diffusers based on silicone emulsions,” Opt. Mater. 32(2), 374–377 (2009).
[Crossref]

2008 (9)

P. Ruffieux, T. Scharf, I. Philipoussis, H. P. Herzig, R. Voelkel, and K. J. Weible, “Two step process for the fabrication of diffraction limited concave microlens arrays,” Opt. Express 16(24), 19541–19549 (2008).
[Crossref] [PubMed]

C. Y. Wu, T. H. Chiang, and C. C. Hsu, “Fabrication of microlens array diffuser films with controllable haze distribution by combination of breath figures and replica molding methods,” Opt. Express 16(24), 19978–19986 (2008).
[Crossref] [PubMed]

D. Huber, L. Petreanu, N. Ghitani, S. Ranade, T. Hromádka, Z. Mainen, and K. Svoboda, “Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice,” Nature 451(7174), 61–64 (2008).
[Crossref] [PubMed]

B. A. Flusberg, A. Nimmerjahn, E. D. Cocker, E. A. Mukamel, R. P. Barretto, T. H. Ko, L. D. Burns, J. C. Jung, and M. J. Schnitzer, “High-speed, miniaturized fluorescence microscopy in freely moving mice,” Nat. Methods 5(11), 935–938 (2008).
[Crossref] [PubMed]

J. G. Bernstein, X. Han, M. A. Henninger, E. Y. Ko, X. Qian, G. T. Franzesi, J. P. McConnell, P. Stern, R. Desimone, and E. S. Boyden, “Prosthetic systems for therapeutic optical activation and silencing of genetically-targeted neurons,” Proc. Soc. Photo Opt. Instrum. Eng. 6854, 68540H (2008).
[PubMed]

M. Mank, A. F. Santos, S. Direnberger, T. D. Mrsic-Flogel, S. B. Hofer, V. Stein, T. Hendel, D. F. Reiff, C. Levelt, A. Borst, T. Bonhoeffer, M. Hübener, and O. Griesbeck, “A genetically encoded calcium indicator for chronic in vivo two-photon imaging,” Nat. Methods 5(9), 805–811 (2008).
[Crossref] [PubMed]

D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
[Crossref] [PubMed]

P. A. Mayes, D. T. Dicker, Y. Y. Liu, and W. S. El-Deiry, “Noninvasive vascular imaging in fluorescent tumors using multispectral unmixing,” Biotechniques 45(4), 459–464 (2008).
[Crossref] [PubMed]

H. Tamura, D. C. Ng, T. Tokuda, H. Naoki, T. Nakagawa, T. Mizuno, Y. Hatanaka, Y. Ishikawa, J. Ohta, and S. Shiosaka, “One-chip sensing device (biomedical photonic LSI) enabled to assess hippocampal steep and gradual up-regulated proteolytic activities,” J. Neurosci. Methods 173(1), 114–120 (2008).
[Crossref] [PubMed]

2007 (2)

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

A. M. Aravanis, L. P. Wang, F. Zhang, L. A. Meltzer, M. Z. Mogri, M. B. Schneider, and K. Deisseroth, “An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology,” J. Neural Eng. 4(3), S143–S156 (2007).
[Crossref] [PubMed]

2006 (2)

T. Binzoni, T. Leung, A. Gandjbakhche, D. Rüfenacht, and D. Delpy, “The use of the Henyey–Greenstein phase function in Monte Carlo simulations in biomedical optics,” Phys. Med. Biol. 51, N313 (2006).

D. C. Ng, T. Tokuda, A. Yamamoto, M. Matsuo, M. Nunoshita, H. Tamura, Y. Ishikawa, S. Shiosaka, and J. Ohta, “On-chip biofluorescence imaging inside a brain tissue phantom using a CMOS image sensor for in vivo brain imaging verification,” Sens. Actuators B Chem. 119(1), 262–274 (2006).
[Crossref]

2005 (7)

X. Michalet, F. F. Pinaud, L. A. Bentolila, J. M. Tsay, S. Doose, J. J. Li, G. Sundaresan, A. M. Wu, S. S. Gambhir, and S. Weiss, “Quantum dots for live cells, in vivo imaging, and diagnostics,” Science 307(5709), 538–544 (2005).
[Crossref] [PubMed]

Q. T. Le, A. Ohashi, S. Hirose, and N. Katunuma, “Reverse zymography using fluorogenic substrates for protease inhibitor detection,” Electrophoresis 26(6), 1038–1045 (2005).
[Crossref] [PubMed]

D. Sakai, K. Harada, S. Kamemaru, M. A. El-Morsy, M. Itoh, and T. Yatagai, “Direct fabrication of surface relief holographic diffusers in azobenzene polymer films,” Opt. Rev. 12(5), 383–386 (2005).
[Crossref]

G. Kim, “A PMMA composite as an optical diffuser in a liquid crystal display backlighting unit (BLU),” Eur. Polym. J. 41(8), 1729–1737 (2005).
[Crossref]

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(7026), 597–603 (2005).
[Crossref] [PubMed]

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref] [PubMed]

B. A. Flusberg, E. D. Cocker, W. Piyawattanametha, J. C. Jung, E. L. Cheung, and M. J. Schnitzer, “Fiber-optic fluorescence imaging,” Nat. Methods 2(12), 941–950 (2005).
[Crossref] [PubMed]

2003 (1)

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

2001 (1)

M. Matsuzaki, G. C. R. Ellis-Davies, T. Nemoto, Y. Miyashita, M. Iino, and H. Kasai, “Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons,” Nat. Neurosci. 4(11), 1086–1092 (2001).
[Crossref] [PubMed]

1997 (1)

O. Barajas, Å. M. Ballangrud, G. G. Miller, R. B. Moore, and J. Tulip, “Monte Carlo modelling of angular radiance in tissue phantoms and human prostate: PDT light dosimetry,” Phys. Med. Biol. 42(9), 1675–1687 (1997).
[Crossref] [PubMed]

1941 (1)

L. G. Henyey and J. L. Greenstein, “Diffuse radiation in the galaxy,” Astrophys. J. 93, 70–83 (1941).
[Crossref]

1894 (1)

A. Koehler, “New method of illumination for phomicrographical purposes,” J. Roy. Microscop. Soc. 14, 261–262 (1894).

Adamantidis, A.

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

Akagi, T.

H. Takehara, A. Nagaoka, J. Noguchi, T. Akagi, H. Kasai, and T. Ichiki, “Lab-on-a-brain: Implantable micro-optical fluidic devices for neural cell analysis in vivo,” Sci. Rep. 4, 6721 (2014).
[Crossref] [PubMed]

Algar, W. R.

Aravanis, A. M.

A. M. Aravanis, L. P. Wang, F. Zhang, L. A. Meltzer, M. Z. Mogri, M. B. Schneider, and K. Deisseroth, “An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology,” J. Neural Eng. 4(3), S143–S156 (2007).
[Crossref] [PubMed]

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

Astori, S.

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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(7026), 597–603 (2005).
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J. Ohta, T. Tokuda, K. Sasagawa, and T. Noda, “Implantable CMOS biomedical devices,” Sensors (Basel) 9(11), 9073–9093 (2009).
[Crossref] [PubMed]

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Science (1)

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Figures (7)

Fig. 1
Fig. 1

Schematics of epi-illumination and imaging in brain tissues using a light-emitting diode (LED) and a semiconductor imaging device.

Fig. 2
Fig. 2

Schematics and photographs of the implantable semiconductor imaging device. (a) Schematics of the implantable semiconductor imaging device. The device is constructed with a thin-film absorption filter, an imaging sensor chip, and a flexible printed circuit (FPC). (b) Photograph of the implantable semiconductor imaging device. The semiconductor image sensor chip is immobilized onto the FPC, which is connected to the small relay board. (c) Fabrication process of the implantable semiconductor imaging device.

Fig. 3
Fig. 3

Schematics and photographs of fabricated CMOS image-sensor chip. (a) The CMOS imaging-sensor chip has a pixel array and four bonding pads. The imaging sensor chip is 450-μm wide, 1500-μm long, and 150-μm thick. (b) Block diagram of the CMOS image-sensor chip. The chip has three inputs (VDD, GND, and CLK) and one output (Out). Schematics of output circuit was reported in detail elsewhere [44]. (c) Sensitivity of the CMOS image-sensor chip.

Fig. 4
Fig. 4

Performance of thin-film absorption filters and the semiconductor imaging device integrated with the thin-film absorption filter. (a) Transmittance T at 470 nm as a function of film thickness t (μm) of the absorption filter. The film thickness was controlled by the numbers of spin-coated layers. Horizontal error bars show the standard deviations of the thickness. (b) The transmittance spectra of the absorption filters of thickness 0.8 μm and 3.4 μm. (c) Obtained fluorescent image using the image sensor integrated with the thin-film absorption filter. Fluorescent microspheres (ϕ = 15 μm) were placed directly onto the image sensor and illuminated by excitation light using a blue LED. Representative fluorescent intensity profile along x-pixels was shown at the upper-right corner. The experimental data (dots) were fitted by a Gaussian function (line).

Fig. 5
Fig. 5

Numerical analysis of the intensity distribution of excitation light in brain tissues. (a) Cross-sectional image of excitation light intensity in brain tissues. Contours represent the surfaces where the light intensity drops to 10%, 1%, and 0.1%. (b) Normalized excitation light intensity on the surface of the image sensor at various positions (L = 0, 1, and 2 mm). (c) Experimentally measured light intensity profiles (dots) and computationally calculated light intensity profiles (lines) at various positions (L = 0, 1, and 2 mm) as a function of y-pixels.

Fig. 6
Fig. 6

Fluorescence imaging in deep brain tissues using the implantable semiconductor device. (a) Photographs of the exposed brain surface of a mouse and illuminated brain surface using an LED. (b) Obtained images of fluorescent microspheres (ϕ = 15 μm) in deep brain tissue (1–2 mm in depth) by implanted image sensors at various positions (L = 0, 1, and 2 mm). Saturation of fluorescent signal in the top sensor area (y-pixel > 300 μm) was observed with the image sensor at L = 0 mm. Elliptical shadowing in the images was considered to be an artifact caused by a silicone rubber sheet used to attach microspheres on the device. (c) The ratio of the fluorescent intensity of microspheres in the top sensor area (y-pixel > 300 μm) and bottom sensor area (y-pixel < –300 μm). The intensity ratio of the image sensor at L = 2 mm was at the same level as that of a control image obtained under uniform illumination in vitro. Error bars show the standard deviations.

Fig. 7
Fig. 7

Fluorescence imaging of fluorescent substances embedded in brain tissues obtained using the implantable semiconductor device. (a) Obtained images of fluorescent microspheres (ϕ = 15 μm) embedded in a 50-μm-thick brain tissue slice. (b) Representative fluorescent intensity profile along x-pixels of the microsphere embedded in brain tissue slice. The experimental data (dots) were fitted by a Gaussian function (line). (c) Fluorescence signal change of blood vessels embedded in the brain tissue of a living mouse that was labeled with quantum dots.

Tables (1)

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Table 1 Specifications of fabricated CMOS image-sensor chip

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