Abstract

Imaging neural activities at the cellular level in the deep brain is essential to understand the structure and functions of nervous systems. Recently developed fully implantable optical sensors have the capability to capture fluorescence signals within the deep tissue; however, their potential for high-quality imaging is not clear. In this paper, we develop a simplified model to analytically study the photon transport in the biological tissue, and utilize it to understand the optical performance of an implantable fluorescence imager. Spatial resolution of the implanted imager is calculated, and imaging qualities for groups of neurons in two- and three-dimensional configurations are evaluated. The results here establish feasible solutions to design implantable optical sensors and predict their performance for biomedical applications.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2019 (1)

G. K. Anumanchipalli, J. Chartier, and E. F. Chang, “Speech synthesis from neural decoding of spoken sentences,” Nature 568(7753), 493–498 (2019).
[Crossref]

2018 (4)

F. Sun, J. Zeng, M. Jing, J. Zhou, J. Feng, S. F. Owen, Y. Luo, F. Li, H. Wang, T. Yamaguchi, Z. Yong, Y. Gao, W. Peng, L. Wang, S. Zhang, J. Du, D. Lin, M. Xu, A. C. Kreitzer, G. Gui, and Y. Li, “A Genetically Encoded Fluorescent Sensor Enables Rapid and Specific Detection of Dopamine in Flies, Fish, and Mice,” Cell 174(2), 481–496.e19 (2018).
[Crossref]

H. Xu, L. Yin, C. Liu, X. Sheng, and N. Zhao, “Recent Advances in Biointegrated Optoelectronic Devices,” Adv. Mater. 30(33), 1800156 (2018).
[Crossref]

R. Fu, W. Luo, R. Nazempour, D. Tan, H. Ding, K. Zhang, L. Yin, J. Guan, and X. Sheng, “Implantable and Biodegradable Poly(l-lactic acid) Fibers for Optical Neural Interfaces,” Adv. Opt. Mater. 6(3), 1700941 (2018).
[Crossref]

L. Lu, P. Gutruf, L. Xia, D. L. Bhatti, X. Wang, A. Vazquez-Guardado, X. Ning, X. Sheng, T. Sang, R. Ma, G. Pakeltis, G. Sobczak, H. Zhang, D. O. Seo, M. Xue, L. D. Chanda, X. Sheng, M. R. Bruchas, and J. A. Rogers, “Wireless optoelectronic photometers for monitoring neuronal dynamics in the deep brain,” Proc. Natl. Acad. Sci. U. S. A. 115(7), E1374–E1383 (2018).
[Crossref]

2017 (6)

M. Khorasaninejad and F. Capasso, “Metalenses: Versatile multifunctional photonic components,” Science 358(6367), eaam8100 (2017).
[Crossref]

J. Ohta, Y. Ohta, H. Takehara, T. Noda, K. Sasagawa, T. Tokuda, M. Haruta, T. Kobayashi, Y. M. Akay, and M. Akay, “Implantable Microimaging Device for Observing Brain Activities of Rodents,” Proc. IEEE 105(1), 158–166 (2017).
[Crossref]

W. Zong, R. Wu, Y. Hu, Y. Li, J. Li, H. Rong, H. Wu, Y. Xu, Y. Lu, M. Fan, Z. Zhou, A. Wang, H. Cheng, and L. Chen, “Fast High-resolution Miniature Two-photon Microscopy for Brain Imaging in Freely-behaving Mice at the Single-spine Level,” Nat. Methods 14(7), 713–719 (2017).
[Crossref]

J. J. Jun, N. A. Steinmetz, J. H. Siegle, D. J. Denman, M. Bauza, B. Barbarits, A. K. Lee, C. A. Anastassiou, A. Andrei, C. Aydın, M. Barbic, T. J. Blanche, V. Bonin, J. Couto, B. Dutta, S. L. Gratiy, D. A. Gutnisky, M. Hausser, B. Karsh, P. Leochwitsch, C. M. Lopez, C. Mitelut, S. Musa, M. Okun, M. Pachitariu, J. Putzeyes, P. D. Rich, C. Rossant, W. L. Sun, K. Svoboda, M. Crandini, K. D. Harris, C. Koch, J. O’Keefe, and T. D. Harris, “Fully integrated silicon probes for high-density recording of neural activity,” Nature 551(7679), 232–236 (2017).
[Crossref]

R. Chen, A. Canales, and P. Anikeeva, “Neural recording and modulation technologies,” Nat. Rev. Mater. 2(2), 16093 (2017).
[Crossref]

X. Zhu, Y. Xia, X. Wang, K. Si, and W. Gong, “Optical Brain Imaging: A Powerful Tool for Neuroscience,” Neurosci. Bull. 33(1), 1–16 (2017).
[Crossref]

2016 (2)

M. M. Poo, J. L. Du, N. Ip, Z. Q. Xiong, B. Xu, and T. Tan, “China Brain Project: Basic Neuroscience, Brain Diseases, and Brain-Inspired Computing,” Neuron 92(3), 591–596 (2016).
[Crossref]

H. Dana, B. Mohar, Y. Sun, S. Narayan, A. Gordus, J. P. Hasseman, G. Tsegaye, G. T. Holt, A. Hu, D. Walpita, R. Patel, J. J. Macklin, C. I. Bargmann, M. B. Ahrens, E. R. Schreiter, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Sensitive red protein calcium indicators for imaging neural activity,” eLife 5, e12727 (2016).
[Crossref]

2015 (1)

F. Chen, P. W. Tillberg, and E. S. Boyden, “Expansion Microscopy,” Science 347(6221), 543–548 (2015).
[Crossref]

2014 (2)

M. R. Warden, J. A. Cardin, and K. Deisseroth, “Optical Neural Interfaces,” Annu. Rev. Biomed. Eng. 16(1), 103–129 (2014).
[Crossref]

F. St-Pierre, J. D. Marshall, Y. Ying, G. Yiyang, M. J. Schnitzer, and M. Z. Lin, “High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor,” Nat. Neurosci. 17(6), 884–889 (2014).
[Crossref]

2013 (2)

K. Chung, J. Wallace, S. Kim, S. Kalyanasundaram, A. S. Andalman, T. J. Davidson, J. J. Mirzabekov, K. A. Zalocusky, J. Mattis, A. K. Denisin, S. Pak, H. Bernstein, C. Ramakrishnan, L. Grosenick, V. Gradinaru, and K. Deisseroth, “Structural and molecular interrogation of intact biological systems,” Nature 497(7449), 332–337 (2013).
[Crossref]

T. 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(7458), 295–300 (2013).
[Crossref]

2012 (1)

C. Grienberger and A. Konnerth, “Imaging Calcium in Neurons,” Neuron 73(5), 862–885 (2012).
[Crossref]

2011 (3)

H. S. Meyer, D. Schwarz, V. C. Wimmer, A. C. Schmitt, J. N. D. Kerr, B. Sakmann, and M. Helmstaedter, “Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A,” Proc. Natl. Acad. Sci. U. S. A. 108(40), 16807–16812 (2011).
[Crossref]

K. M. Tye, R. Prakash, S. Y. Kim, L. E. Fenno, L. Grosenick, H. Zarrabi, K. R. Thompson, V. Gradinaru, C. Ramakrishnan, and K. Deisseroth, “Amygdala circuitry mediating reversible and bidirectional control of anxiety,” Nature 471(7338), 358–362 (2011).
[Crossref]

J. Viventi, D. H. Kim, L. Vigeland, E. S. Frechette, J. A. Blanco, Y. S. Kim, A. E. Avrin, V. R. Tiruvadi, S. W. Hwang, A. C. Vanleer, D. F. Wulsin, K. Davis, C. E. Gelber, L. Palmer, J. Van der Spiegel, J. Wu, J. Xiao, Y. Huang, D. Cntreras, J. A. Rogers, and B. Litt, “Flexible, foldable, actively multiplexed, high-density electrode array for mapping brain activity in vivo,” Nat. Neurosci. 14(12), 1599–1605 (2011).
[Crossref]

2010 (3)

R. Bhandari, S. Negi, and F. Solzbacher, “Wafer-scale fabrication of penetrating neural microelectrode arrays,” Biomed. Microdevices 12(5), 797–807 (2010).
[Crossref]

A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain,” Science 330(6009), 1404–1408 (2010).
[Crossref]

M. J. Nasse and J. R. C. Woehl, “Realistic modeling of the illumination point spread function in confocal scanning optical microscopy,” J. Opt. Soc. Am. A 27(2), 295 (2010).
[Crossref]

2009 (2)

S. Herculano-Houzel, “The human brain in numbers: a linearly scaled-up primate brain,” Front. Hum. Neurosci. 3, 31 (2009).
[Crossref]

C. D. Harvey, C. Forrest, D. A. Dombeck, and D. W. Tank, “Intracellular dynamics of hippocampal place cells during virtual navigation,” Nature 461(7266), 941–946 (2009).
[Crossref]

2008 (1)

L. V. Wang, H. I. Wu, and B. R. Masters, “Biomedical Optics, Principles and Imaging,” J. Biomed. Opt. 13(4), 049902 (2008).
[Crossref]

2007 (3)

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(1), 43–57 (2007).
[Crossref]

J. M. Wilson, D. A. Dombeck, D. R. Manuel, R. M. Harris-Warrick, and R. M. Brownstone, “Two-photon calcium imaging of network activity in XFP-expressing neurons in the mouse,” J. Neurophysiol. 97(4), 3118–3125 (2007).
[Crossref]

E. M. C. Hillman, “Optical brain imaging in vivo: techniques and applications from animal to man,” J. Biomed. Opt. 12(5), 051402 (2007).
[Crossref]

2006 (1)

S. C. Gebhart, W. C. Lin, and A. Mahadevan-Jansen, “In vitro determination of normal and neoplastic human brain tissue optical properties using inverse adding-doubling,” Phys. Med. Biol. 51(8), 2011–2027 (2006).
[Crossref]

2005 (1)

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

2004 (1)

A. D. Mehta, J. C. Jung, B. A. Flusberg, and M. J. Schnitzer, “Fiber optic in vivo imaging in the mammalian nervous system,” Curr. Opin. Neurobiol. 14(5), 617–628 (2004).
[Crossref]

2002 (1)

E. J. Yoder and D. Kleinfeld, “Cortical imaging through the intact mouse skull using two-photon excitation laser scanning microscopy,” Microsc. Res. Tech. 56(4), 304–305 (2002).
[Crossref]

1995 (1)

L. Wang, S. L. Jacques, and L. Zheng, “MCML—Monte Carlo modeling of light transport in multi-layered tissues,” Comput. Meth. Programs Biomed. 47(2), 131–146 (1995).
[Crossref]

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(1), 43–57 (2007).
[Crossref]

Ahrens, M. B.

H. Dana, B. Mohar, Y. Sun, S. Narayan, A. Gordus, J. P. Hasseman, G. Tsegaye, G. T. Holt, A. Hu, D. Walpita, R. Patel, J. J. Macklin, C. I. Bargmann, M. B. Ahrens, E. R. Schreiter, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Sensitive red protein calcium indicators for imaging neural activity,” eLife 5, e12727 (2016).
[Crossref]

Akay, M.

J. Ohta, Y. Ohta, H. Takehara, T. Noda, K. Sasagawa, T. Tokuda, M. Haruta, T. Kobayashi, Y. M. Akay, and M. Akay, “Implantable Microimaging Device for Observing Brain Activities of Rodents,” Proc. IEEE 105(1), 158–166 (2017).
[Crossref]

Akay, Y. M.

J. Ohta, Y. Ohta, H. Takehara, T. Noda, K. Sasagawa, T. Tokuda, M. Haruta, T. Kobayashi, Y. M. Akay, and M. Akay, “Implantable Microimaging Device for Observing Brain Activities of Rodents,” Proc. IEEE 105(1), 158–166 (2017).
[Crossref]

Anastassiou, C. A.

J. J. Jun, N. A. Steinmetz, J. H. Siegle, D. J. Denman, M. Bauza, B. Barbarits, A. K. Lee, C. A. Anastassiou, A. Andrei, C. Aydın, M. Barbic, T. J. Blanche, V. Bonin, J. Couto, B. Dutta, S. L. Gratiy, D. A. Gutnisky, M. Hausser, B. Karsh, P. Leochwitsch, C. M. Lopez, C. Mitelut, S. Musa, M. Okun, M. Pachitariu, J. Putzeyes, P. D. Rich, C. Rossant, W. L. Sun, K. Svoboda, M. Crandini, K. D. Harris, C. Koch, J. O’Keefe, and T. D. Harris, “Fully integrated silicon probes for high-density recording of neural activity,” Nature 551(7679), 232–236 (2017).
[Crossref]

Andalman, A. S.

K. Chung, J. Wallace, S. Kim, S. Kalyanasundaram, A. S. Andalman, T. J. Davidson, J. J. Mirzabekov, K. A. Zalocusky, J. Mattis, A. K. Denisin, S. Pak, H. Bernstein, C. Ramakrishnan, L. Grosenick, V. Gradinaru, and K. Deisseroth, “Structural and molecular interrogation of intact biological systems,” Nature 497(7449), 332–337 (2013).
[Crossref]

Andrei, A.

J. J. Jun, N. A. Steinmetz, J. H. Siegle, D. J. Denman, M. Bauza, B. Barbarits, A. K. Lee, C. A. Anastassiou, A. Andrei, C. Aydın, M. Barbic, T. J. Blanche, V. Bonin, J. Couto, B. Dutta, S. L. Gratiy, D. A. Gutnisky, M. Hausser, B. Karsh, P. Leochwitsch, C. M. Lopez, C. Mitelut, S. Musa, M. Okun, M. Pachitariu, J. Putzeyes, P. D. Rich, C. Rossant, W. L. Sun, K. Svoboda, M. Crandini, K. D. Harris, C. Koch, J. O’Keefe, and T. D. Harris, “Fully integrated silicon probes for high-density recording of neural activity,” Nature 551(7679), 232–236 (2017).
[Crossref]

Anikeeva, P.

R. Chen, A. Canales, and P. Anikeeva, “Neural recording and modulation technologies,” Nat. Rev. Mater. 2(2), 16093 (2017).
[Crossref]

Anumanchipalli, G. K.

G. K. Anumanchipalli, J. Chartier, and E. F. Chang, “Speech synthesis from neural decoding of spoken sentences,” Nature 568(7753), 493–498 (2019).
[Crossref]

Avrin, A. E.

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Figures (5)

Fig. 1.
Fig. 1. (a) Schematic illustration of an implantable image sensor for fluorescence mapping in the deep brain. (b) Zoomed-in view of the sensor on a thin-film probe, capturing the fluorescence signals of neurons in the brain tissue.
Fig. 2.
Fig. 2. (a) Schematic illustration of the optical model showing one fluorescent neuron on top of the imager, with a distance d from the imager. (b, c) Normalized fluorescence intensity profiles of the neuron detected by the imager at various distances (d = 100, 50, 20, 10 and 5 µm), based on: (b) our analytical model and (c) numerical (Monte Carlo ray tracing) simulation, respectively.
Fig. 3.
Fig. 3. (a) Schematic illustration of the optical model showing two fluorescent neurons on top of the imager, with the same distance d from the imager and a varied spacing Δx between each other. (b–e) Normalized fluorescence intensity profiles detected by the imager at various Δx (150, 90, 38, and 25 µm) and a fixed d (20 µm). (f) Calculated resolution limits R as a function of d.
Fig. 4.
Fig. 4. (a) Schematic illustration of the optical model showing a group of fluorescent neurons on top of the imager, with the same distance d from the imager. The neurons are randomly distributed, with an areal density of ∼1200 /mm2. (b–f) Normalized fluorescence intensity profiles detected by the imager at various distances (d = 5, 10, 20, 50 and 100 µm).
Fig. 5.
Fig. 5. (a–c) Schematic illustrations of the optical models, showing a group of fluorescent neurons in 3D space on top of the imager. The neurons are randomly distributed, with a volumetric density of ∼70000 /mm3. The fluorescence intensities for all the neurons are uniform in (a) and non-uniform in (b) and (c), depending on the positions of excitation sources. (d–f) Normalized fluorescence intensity profiles detected by the imager.

Equations (9)

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I ( x ) = I 0 exp ( μ eff L ) L n
L = x 2 + d 2
μ eff = 3 μ a ( μ a + μ s )
μ s = μ s ( 1 g )
n = 2 for d 1 μ s
n = 1  for d 1 μ s
n = 2 exp ( μ s d )
I ( x ) = I 0 exp ( μ eff L ) L n exp ( μ eff - ex d )
I ( x ) = I 0 exp ( μ eff L ) L n exp ( + μ eff - ex d )

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