Abstract

A major open challenge in neuroscience is the ability to measure and perturb neural activity in vivo from well defined neural sub-populations at cellular resolution anywhere in the brain. However, limitations posed by scattering and absorption prohibit non-invasive multi-photon approaches for deep (>2mm) structures, while gradient refractive index (GRIN) endoscopes are relatively thick and can cause significant damage upon insertion. Here, we present a novel micro-endoscope design to image neural activity at arbitrary depths via an ultra-thin multi-mode optical fiber (MMF) probe that has 5–10X thinner diameter than commercially available micro-endoscopes. We demonstrate micron-scale resolution, multi-spectral and volumetric imaging. In contrast to previous approaches, we show that this method has an improved acquisition speed that is sufficient to capture rapid neuronal dynamics in-vivo in rodents expressing a genetically encoded calcium indicator (GCaMP). Our results emphasize the potential of this technology in neuroscience applications and open up possibilities for cellular resolution imaging in previously unreachable brain regions.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2017 (5)

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14, 388–390 (2017).
[Crossref] [PubMed]

D. G. Tervo, B.-Y. Hwang, S. Viswanathan, T. Gaj, M. Lavzin, K. Ritola, S. Lindo, S. Michael, E. Kuleshova, D. Ojala, C.-C. Huang, C. Gerfen, J. Schiller, J. Dudman, A. Hantman, L. Looger, D. Schaffer, and A. Karpova, “A designer aav variant permits efficient retrograde access to projection neurons,” Neuron 92, 372–382 (2017).
[Crossref]

M. Li, F. Liu, H. Jiang, T. S. Lee, and S. Tang, “Long-Term Two-Photon imaging in awake macaque monkey,” Neuron 93, 1049–1057 (2017).
[Crossref] [PubMed]

A. M. Caravaca-Aguirre and R. Piestun, “Single multimode fiber endoscope,” Opt. Express 25, 1656 (2017).
[Crossref]

M. Sato, Y. Motegi, S. Yagi, K. Gengyo-Ando, M. Ohkura, and J. Nakai, “Fast varifocal two-photon microendoscope for imaging neuronal activity in the deep brain,” Biomed. Opt. Express 8, 4049–4060 (2017).
[Crossref] [PubMed]

2016 (4)

E. Seidemann, Y. Chen, Y. Bai, S. C. Chen, P. Mehta, B. L. Kajs, W. S. Geisler, and B. V. Zemelman, “Calcium imaging with genetically encoded indicators in behaving primates,” Elife 5, e16178 (2016).
[Crossref] [PubMed]

J. Weickenmeier, R. de Rooij, S. Budday, P. Steinmann, T. Ovaert, and E. Kuhl, “Brain stiffness increases with myelin content,” Acta Biomaterialia 42, 265–272 (2016).
[Crossref] [PubMed]

S. P. Mekhail, G. Arbuthnott, and S. N. Chormaic, “Advances in fibre microendoscopy for neuronal imaging,” Optical Data Processing and Storage 2, 30–42 (2016).
[Crossref]

C. K. Kim, S. J. Yang, N. Pichamoorthy, N. P. Young, I. Kauvar, J. H. Jennings, T. N. Lerner, A. Berndt, S. Y. Lee, C. Ramakrishnan, T. J. Davidson, M. Inoue, H. Bito, and K. Deisseroth, “Simultaneous fast measurement of circuit dynamics at multiple sites across the mammalian brain,” Nat. Methods 13, 325–328 (2016).
[Crossref] [PubMed]

2015 (3)

2014 (5)

D. Kim, J. Moon, M. Kim, T. D. Yang, J. Kim, E. Chung, and W. Choi, “Toward a miniature endomicroscope: pixelation-free and diffraction-limited imaging through a fiber bundle,” Opt. Lett. 39, 1921–1924 (2014).
[Crossref] [PubMed]

L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157, 1535–1551 (2014).
[Crossref] [PubMed]

V. Szabo, C. Ventalon, V. De Sars, J. Bradley, and V. Emiliani, “Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope,” Neuron 84, 1157–1169 (2014).
[Crossref] [PubMed]

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K.-S. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11, 338–346 (2014).
[Crossref] [PubMed]

R. Barankov and J. Mertz, “High-throughput imaging of self-luminous objects through a single optical fibre,” Nat. Commun. 5, 5581 (2014).
[Crossref] [PubMed]

2013 (4)

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499, 295–300 (2013).
[Crossref] [PubMed]

S. Ohayon, P. Grimaldi, N. Schweers, and D. Y. Tsao, “Saccade modulation by optical and electrical stimulation in the macaque frontal eye field,” J. Neurosci. 33, 16684–16697 (2013).
[Crossref] [PubMed]

I. N. Papadopoulos, S. Farahi, C. Moser, and D. Psaltis, “High-resolution, lensless endoscope based on digital scanning through a multimode optical fiber,” Biomed. Opt. Express 4, 260–270 (2013).
[Crossref] [PubMed]

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7, 205–209 (2013).
[Crossref]

2012 (4)

D. B. Conkey, A. M. Caravaca-Aguirre, and R. Piestun, “High-speed scattering medium characterization with application to focusing light through turbid media,” Opt. Express 20, 1733–1740 (2012).
[Crossref] [PubMed]

T. Cižmár and K. Dholakia, “Exploiting multimode waveguides for pure fibre-based imaging,” Nat. Commun. 3, 1027 (2012).
[Crossref]

Y. Choi, C. Yoon, M. Kim, T. D. Yang, C. Fang-Yen, R. R. Dasari, K. J. Lee, and W. Choi, “Scanner-free and wide-field endoscopic imaging by using a single multimode optical fiber,” Phys. Rev. Lett. 109, 203901 (2012).
[Crossref] [PubMed]

R. P. J. Barretto and M. J. Schnitzer, “In vivo microendoscopy of the hippocampus,” Cold Spring Harb. Protoc. 2012, 1092–1099 (2012).
[Crossref] [PubMed]

2011 (2)

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, 871–878 (2011).
[Crossref] [PubMed]

T. Čižmár and K. Dholakia, “Shaping the light transmission through a multimode optical fibre: complex transformation analysis and applications in biophotonics,” Opt. Express 19, 18871–18884 (2011).
[Crossref] [PubMed]

2010 (2)

I. M. Vellekoop, A. Lagendijk, and A. P. Mosk, “Exploiting disorder for perfect focusing,” Nat. Photonics 4, 320–322 (2010).
[Crossref]

S. M. Popoff, G. Lerosey, R. Carminati, M. Fink, A. C. Boccara, and S. Gigan, “Measuring the transmission matrix in optics: an approach to the study and control of light propagation in disordered media,” Phys. Rev. Lett. 104, 100601 (2010).
[Crossref] [PubMed]

2005 (1)

V. S. Polikov, P. A. Tresco, and W. M. Reichert, “Response of brain tissue to chronically implanted neural electrodes,” Journal of Neuroscience Methods 148, 1–18 (2005).
[Crossref] [PubMed]

Adhikari, A.

L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157, 1535–1551 (2014).
[Crossref] [PubMed]

Airan, R. D.

L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157, 1535–1551 (2014).
[Crossref] [PubMed]

Anikeeva, P.

L. A. Gunaydin, L. Grosenick, J. C. Finkelstein, I. V. Kauvar, L. E. Fenno, A. Adhikari, S. Lammel, J. J. Mirzabekov, R. D. Airan, K. A. Zalocusky, K. M. Tye, P. Anikeeva, R. C. Malenka, and K. Deisseroth, “Natural neural projection dynamics underlying social behavior,” Cell 157, 1535–1551 (2014).
[Crossref] [PubMed]

Aponte, Y.

Arbuthnott, G.

S. P. Mekhail, G. Arbuthnott, and S. N. Chormaic, “Advances in fibre microendoscopy for neuronal imaging,” Optical Data Processing and Storage 2, 30–42 (2016).
[Crossref]

Bai, Y.

E. Seidemann, Y. Chen, Y. Bai, S. C. Chen, P. Mehta, B. L. Kajs, W. S. Geisler, and B. V. Zemelman, “Calcium imaging with genetically encoded indicators in behaving primates,” Elife 5, e16178 (2016).
[Crossref] [PubMed]

Baohan, A.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499, 295–300 (2013).
[Crossref] [PubMed]

Barankov, R.

R. Barankov and J. Mertz, “High-throughput imaging of self-luminous objects through a single optical fibre,” Nat. Commun. 5, 5581 (2014).
[Crossref] [PubMed]

Barretto, R. P. J.

R. P. J. Barretto and M. J. Schnitzer, “In vivo microendoscopy of the hippocampus,” Cold Spring Harb. Protoc. 2012, 1092–1099 (2012).
[Crossref] [PubMed]

Berndt, A.

C. K. Kim, S. J. Yang, N. Pichamoorthy, N. P. Young, I. Kauvar, J. H. Jennings, T. N. Lerner, A. Berndt, S. Y. Lee, C. Ramakrishnan, T. J. Davidson, M. Inoue, H. Bito, and K. Deisseroth, “Simultaneous fast measurement of circuit dynamics at multiple sites across the mammalian brain,” Nat. Methods 13, 325–328 (2016).
[Crossref] [PubMed]

Birdsey-Benson, A.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K.-S. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11, 338–346 (2014).
[Crossref] [PubMed]

Bito, H.

C. K. Kim, S. J. Yang, N. Pichamoorthy, N. P. Young, I. Kauvar, J. H. Jennings, T. N. Lerner, A. Berndt, S. Y. Lee, C. Ramakrishnan, T. J. Davidson, M. Inoue, H. Bito, and K. Deisseroth, “Simultaneous fast measurement of circuit dynamics at multiple sites across the mammalian brain,” Nat. Methods 13, 325–328 (2016).
[Crossref] [PubMed]

Bocarsly, M. E.

Boccara, A. C.

S. M. Popoff, G. Lerosey, R. Carminati, M. Fink, A. C. Boccara, and S. Gigan, “Measuring the transmission matrix in optics: an approach to the study and control of light propagation in disordered media,” Phys. Rev. Lett. 104, 100601 (2010).
[Crossref] [PubMed]

Boyden, E. S.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K.-S. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11, 338–346 (2014).
[Crossref] [PubMed]

Bradley, J.

V. Szabo, C. Ventalon, V. De Sars, J. Bradley, and V. Emiliani, “Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope,” Neuron 84, 1157–1169 (2014).
[Crossref] [PubMed]

Budday, S.

J. Weickenmeier, R. de Rooij, S. Budday, P. Steinmann, T. Ovaert, and E. Kuhl, “Brain stiffness increases with myelin content,” Acta Biomaterialia 42, 265–272 (2016).
[Crossref] [PubMed]

Burns, L. D.

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, 871–878 (2011).
[Crossref] [PubMed]

Caravaca-Aguirre, A. M.

Carminati, R.

S. M. Popoff, G. Lerosey, R. Carminati, M. Fink, A. C. Boccara, and S. Gigan, “Measuring the transmission matrix in optics: an approach to the study and control of light propagation in disordered media,” Phys. Rev. Lett. 104, 100601 (2010).
[Crossref] [PubMed]

Carpenter, E. J.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K.-S. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11, 338–346 (2014).
[Crossref] [PubMed]

Chen, S. C.

E. Seidemann, Y. Chen, Y. Bai, S. C. Chen, P. Mehta, B. L. Kajs, W. S. Geisler, and B. V. Zemelman, “Calcium imaging with genetically encoded indicators in behaving primates,” Elife 5, e16178 (2016).
[Crossref] [PubMed]

Chen, T.-W.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499, 295–300 (2013).
[Crossref] [PubMed]

Chen, Y.

E. Seidemann, Y. Chen, Y. Bai, S. C. Chen, P. Mehta, B. L. Kajs, W. S. Geisler, and B. V. Zemelman, “Calcium imaging with genetically encoded indicators in behaving primates,” Elife 5, e16178 (2016).
[Crossref] [PubMed]

Cheng, Y.-T.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14, 388–390 (2017).
[Crossref] [PubMed]

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Supplementary Material (1)

NameDescription
» Visualization 1       Example of calibration and imaging with a multi mode fiber microendoscope

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Figures (14)

Fig. 1
Fig. 1 Simulations of expected brain tissue movement and compression. Small platinum beads (0.1–1mm in diameter) were embedded in agarose gel with brain like consistency and imaged with stereo x-ray system (only one view of the stereo pair is shown). Comparison between insertion of 1mm and 0.1mm probes. Dashed red lines denote surface deformation and false color image overlay shows beads movement (red - before insertion, blue - after insertion).
Fig. 2
Fig. 2 Random access sampling with a multi-mode fiber..
Fig. 3
Fig. 3 Optical system design. See section 2 for details.
Fig. 4
Fig. 4 Mechanical system design. See section 2.3 for details. Main components highlighted: (1) SMF entry port for a incoming light, (2) exit port for fluorescence emissions (large diameter MMF fiber), (3) thin (120μm) optical fiber used for imaging, (4) DMD, (5) DMD PCB controller.
Fig. 5
Fig. 5 Enhancement Factor Estimation. a) Images of the fiber taken under increasing levels of ND filters are combined to form HDR image. b) Two examples of observed distribution of enhancement factor values across the core.
Fig. 6
Fig. 6 Reference and modes trade-off. Enhancement factor distribution as a function of number of input modes and number of mirrors assigned per mode.
Fig. 7
Fig. 7 Point Spread Function. The in plane resolution of the system was estimated by imaging 0.99μm fluorescent beads and fitting 2D Gaussian to the data. The distribution of such fits are shown on the right.
Fig. 8
Fig. 8 Volumetric Imaging. a) Measuring transmission matrix (TM) with a camera focused on the tip can be used to generate spots on the tip. Measuring the TM with a camera that is focused at distance z from the tip can be used to generate spots at distance d from the fiber tip. b) Five sections of the same sample obtained at increasing distances from the fiber tip, collected without moving the fiber (i.e., with five different transmission matrices).
Fig. 9
Fig. 9 Multi-spectral imaging. a) Wavelength selection. The two diffracted wavelengths (blue, green) are spatially disjoint at the Fourier plane after being reflected from the DMD. Only one is allowed to pass through the pinhole at the center. Changing the carrier wave frequency and rotation steers either the blue or the green beams into the pinhole. b) Imaging of two different types of fluorescent micro-spheres with different emissions spectra (scale-bar: 10μm). Image depicts overlay of two images obtained from the two PMTs.
Fig. 10
Fig. 10 Static In-vitro Imaging. a) Schematics of experimental setup. A glass side mounted with a sample was placed between the fiber microendoscope (top) and an epi-fluorescence microscope (bottom), where the latter served as ground truth. b) Imaging of baby hamster kidney cells expression eGFP. c) Intensity cross section of the overlay image. (scale-bar: 11μm)
Fig. 11
Fig. 11 Dynamic In-vitro imaging. a) A similar experimental setup to the one shown in 10a was used to image hippocampal neuronal tissue culture expressing GCaMP6f. b) Time profile of two cells (highlighted in (a)).
Fig. 12
Fig. 12 Dynamic in-vivo imaging. a) Imaging in-vivo neurons expressing GCaMP6f. Imaging plane was fixed at ∼100μm away from the fiber tip. The fiber was inserted slowly into the tissue and videos were acquired at multiple depths. Images show the average intensity over time. b) Same location as (a), but showing standard deviation over time, which correlated directly with the amount of neural activity observed. c) Temporal traces from two example neurons after background subtraction.
Fig. 13
Fig. 13 Gradual image deterioration after fiber bending. a) fluorescent micro-spheres were imaged with a long fiber. The middle part of the fiber was precisely translated while images were obtained to assess maximal bending allowed. b) Quantification of foreground (micro-spheres) to background SNR using the d’ measure (estimated at the two red highlighted regions in (a)).
Fig. 14
Fig. 14 Enhancement Factor temperature fluctuations. a) Intensity of generated point spread function at various locations as a function of fiber temperature. Blue: peak intensity at the PSF, black: avg. intensity of background, yellow: approximated fiber temperature. b) Enhancement factor deterioration as a function of temperature. Small inset: image of a fluorescent bead taken at 41C after a calibration at 25C.

Equations (13)

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C ( x , y ) = cos ( θ ) x + sin ( θ ) y
M ( x , y ) = 1 2 ( 1 + cos ( 2 π f C ( x , y ) Φ ( x , y ) ) )
E out = K * E in
E in ( x , y ) = e π j Φ ( x , y )
E in _ calc = K 1 E desired
K = E observed * E basis
E basis ( x , y , i ) = e π j H ( x , y , i ) ,
I α = | E out | 2 = | r + e j α K * E | = | r | 2 + | K * E | 2 + 2 Re ( r ¯ e j α K * E ) ,
Q = [ Re ( P ) Re ( j P ) + j ( Re ( k P ) Re ( P ) ) ]
P = 1 2 ( Re ( Q ) + Im ( Q ) ) + 1 2 j ( Re ( Q ) Im ( Q ) )
HDR ( x , y ) = max n 10 n ( I ( x , y , n ) I dark ( x , y ) )
F ( x , y ) = A e [ ( x x 0 ) 2 2 σ x 2 + ( y y 0 ) 2 2 σ y 2 ]
d = μ Bead μ Background 1 2 ( σ Bead 2 + σ Background 2 )

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