Abstract

Nature has a large repertoire of animals that take advantage of naturally abundant polarization phenomena. Among them, the mantis shrimp possesses one of the most advanced and elegant visual systems nature has developed, capable of high polarization sensitivity and hyperspectral imaging. Here, we demonstrate that by shifting the design paradigm away from the conventional paths adopted in the imaging and vision sensor fields and instead functionally mimicking the visual system of the mantis shrimp, we have developed a single-chip, low-power, high-resolution color-polarization imaging system. Our bio-inspired imager captures co-registered color and polarization information in real time with high resolution by monolithically integrating nanowire polarization filters with vertically stacked photodetectors. These photodetectors capture three different spectral channels per pixel by exploiting wavelength-dependent depth absorption of photons. Our bio-inspired imager comprises 1280 by 720 pixels with a dynamic range of 62 dB and a maximum signal-to-noise ratio of 48 dB. The quantum efficiency is above 30% over the entire visible spectrum, while achieving high polarization extinction ratios of 40 on each spectral channel. This technology is enabling underwater imaging studies of marine species, which exploit both color and polarization information, as well as applications in biomedical fields.

© 2017 Optical Society of America

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References

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2017 (1)

R. Marinov, N. Cui, M. Garcia, S. B. Powell, and V. Gruev, “A 4-megapixel cooled CCD division of focal plane polarimeter for celestial imaging,” IEEE Sens. J. 17, 2725–2733 (2017).
[Crossref]

2016 (5)

I. M. Daly, M. J. How, J. C. Partridge, S. E. Temple, N. J. Marshall, T. W. Cronin, and N. W. Roberts, “Dynamic polarization vision in mantis shrimps,” Nat. Commun. 7, 12140 (2016).
[Crossref]

L. Gao and L. V. Wang, “A review of snapshot multidimensional optical imaging: measuring photon tags in parallel,” Phys. Rep. 616, 1–37 (2016).
[Crossref]

H. Liu, Y. Huang, and H. Jiang, “Artificial eye for scotopic vision with bioinspired all-optical photosensitivity enhancer,” Proc. Natl. Acad. Sci. USA 113, 3982–3985 (2016).
[Crossref]

J. A. Leñero-Bardallo, M. Delgado-Restituto, R. Carmona-Galán, and Á. Rodríguez-Vázquez, “Enhanced sensitivity of CMOS image sensors by stacked diodes,” IEEE Sens. J. 16, 8448–8455 (2016).
[Crossref]

Z. Wang, J. Chu, Q. Wang, and R. Zhang, “Single-layer nanowire polarizer integrated with photodetector and its application for polarization navigation,” IEEE Sens. J. 16, 6579–6585 (2016).
[Crossref]

2015 (8)

J. Ma and E. R. Fossum, “Quanta image sensor jot with sub 0.3  e-rms read noise and photon counting capability,” IEEE Electron Device Lett. 36, 926–928 (2015).
[Crossref]

T.-H. Tsai, X. Yuan, and D. J. Brady, “Spatial light modulator based color polarization imaging,” Opt. Express 23, 11912–11926 (2015).
[Crossref]

C. Fu, H. Arguello, B. M. Sadler, and G. R. Arce, “Compressive spectral polarization imaging by a pixelized polarizer and colored patterned detector,” J. Opt. Soc. Am. A 32, 2178–2188 (2015).
[Crossref]

B. Kunnen, C. Macdonald, A. Doronin, S. Jacques, M. Eccles, and I. Meglinski, “Application of circularly polarized light for non‐invasive diagnosis of cancerous tissues and turbid tissue‐like scattering media,” J. Biophoton. 8, 317–323 (2015).
[Crossref]

S. B. Mondal, S. Gao, N. Zhu, G. P. Sudlow, K. Liang, A. Som, W. J. Akers, R. C. Fields, J. Margenthaler, and R. Liang, “Binocular Goggle Augmented Imaging and Navigation System provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

M. J. Bok, M. L. Porter, and T. W. Cronin, “Ultraviolet filters in stomatopod crustaceans: diversity, ecology and evolution,” J. Exp. Biol. 218, 2055–2066 (2015).
[Crossref]

N. M. Garcia, I. de Erausquin, C. Edmiston, and V. Gruev, “Surface normal reconstruction using circularly polarized light,” Opt. Express 23, 14391–14406 (2015).
[Crossref]

P. C. Brady, A. A. Gilerson, G. W. Kattawar, J. M. Sullivan, M. S. Twardowski, H. M. Dierssen, M. Gao, K. Travis, R. I. Etheredge, A. Tonizzo, A. Ibrahim, C. Carrizo, Y. Gu, B. Russell, K. Mislinski, S. Zhao, and M. Cummings, “Open-ocean fish reveal an omnidirectional solution to camouflage in polarized environments,” Science 350, 965–969 (2015).
[Crossref]

2014 (11)

M. J. Bok, M. L. Porter, A. R. Place, and T. W. Cronin, “Biological sunscreens tune polychromatic ultraviolet vision in mantis shrimp,” Curr. Biol. 24, 1636–1642 (2014).
[Crossref]

H. H. Thoen, M. J. How, T.-H. Chiou, and J. Marshall, “A different form of color vision in mantis shrimp,” Science 343, 411–413 (2014).
[Crossref]

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

T. Charanya, T. York, S. Bloch, G. Sudlow, K. Liang, M. Garcia, W. J. Akers, D. Rubin, V. Gruev, and S. Achilefu, “Trimodal color-fluorescence-polarization endoscopy aided by a tumor selective molecular probe accurately detects flat lesions in colitis-associated cancer,” J. Biomed. Opt. 19, 126002 (2014).
[Crossref]

T. York, L. Kahan, S. P. Lake, and V. Gruev, “Real-time high-resolution measurement of collagen alignment in dynamically loaded soft tissue,” J. Biomed. Opt. 19, 066011 (2014).
[Crossref]

G. M. Calabrese, P. C. Brady, V. Gruev, and M. E. Cummings, “Polarization signaling in swordtails alters female mate preference,” Proc. Natl. Acad. Sci. USA 111, 13397–13402 (2014).
[Crossref]

W.-L. Hsu, G. Myhre, K. Balakrishnan, N. Brock, M. Ibn-Elhaj, and S. Pau, “Full-Stokes imaging polarimeter using an array of elliptical polarizer,” Opt. Express 22, 3063–3074 (2014).
[Crossref]

C. Posch, T. Serrano-Gotarredona, B. Linares-Barranco, and T. Delbruck, “Retinomorphic event-based vision sensors: bioinspired cameras with spiking output,” Proc. IEEE 102, 1470–1484 (2014).
[Crossref]

J. A. Lenero-Bardallo, D. H. Bryn, and P. Hafliger, “Bio-inspired asynchronous pixel event tricolor vision sensor,” IEEE Trans. Biomed. Circuits Syst. 8, 345–357 (2014).
[Crossref]

G. England, M. Kolle, P. Kim, M. Khan, P. Muñoz, E. Mazur, and J. Aizenberg, “Bioinspired micrograting arrays mimicking the reverse color diffraction elements evolved by the butterfly Pierella luna,” Proc. Natl. Acad. Sci. USA 111, 15630–15634 (2014).
[Crossref]

C.-C. Huang, X. Wu, H. Liu, B. Aldalali, J. A. Rogers, and H. Jiang, “Large-field-of-view wide-spectrum artificial reflecting superposition compound eyes,” Small 10, 3050–3057 (2014).
[Crossref]

2013 (2)

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

S. B. Powell and V. Gruev, “Calibration methods for division-of-focal-plane polarimeters,” Opt. Express 21, 21039–21055 (2013).
[Crossref]

2012 (2)

T. York and V. Gruev, “Characterization of a visible spectrum division-of-focal-plane polarimeter,” Appl. Opt. 51, 5392–5400 (2012).
[Crossref]

Y. Zhao, M. A. Belkin, and A. Alù, “Twisted optical metamaterials for planarized ultrathin broadband circular polarizers,” Nat. Commun. 3, 870 (2012).
[Crossref]

2011 (5)

C. Mora, D. P. Tittensor, S. Adl, A. G. Simpson, and B. Worm, “How many species are there on Earth and in the ocean?” PLoS Biol. 9, e1001127 (2011).
[Crossref]

Y.-J. Jen, A. Lakhtakia, C.-W. Yu, C.-F. Lin, M.-J. Lin, S.-H. Wang, and J.-R. Lai, “Biologically inspired achromatic waveplates for visible light,” Nat. Commun. 2, 363 (2011).
[Crossref]

C.-C. Chiao, J. K. Wickiser, J. J. Allen, B. Genter, and R. T. Hanlon, “Hyperspectral imaging of cuttlefish camouflage indicates good color match in the eyes of fish predators,” Proc. Natl. Acad. Sci. USA 108, 9148–9153 (2011).
[Crossref]

S. Gao and V. Gruev, “Bilinear and bicubic interpolation methods for division of focal plane polarimeters,” Opt. Express 19, 26161–26173 (2011).
[Crossref]

R. Berner and T. Delbruck, “Event-based pixel sensitive to changes of color and brightness,” IEEE Trans. Circuits Syst. I 58, 1581–1590 (2011).
[Crossref]

2010 (2)

2009 (1)

E. Salomatina-Motts, V. Neel, and A. Yaroslavskaya, “Multimodal polarization system for imaging skin cancer,” Opt. Spectrosc. 107, 884–890 (2009).
[Crossref]

2008 (1)

S. Tominaga and A. Kimachi, “Polarization imaging for material classification,” Opt. Eng. 47, 123201 (2008).
[Crossref]

2007 (2)

R. Hanlon, “Cephalopod dynamic camouflage,” Curr. Biol. 17, R400–R404 (2007).
[Crossref]

T.-H. Chiou, L. M. Mäthger, R. T. Hanlon, and T. W. Cronin, “Spectral and spatial properties of polarized light reflections from the arms of squid (Loligo pealeii) and cuttlefish (Sepia officinalis L.),” J. Exp. Biol. 210, 3624–3635 (2007).
[Crossref]

2006 (2)

2005 (1)

T.-H. Chiou, T. W. Cronin, R. L. Caldwell, and J. Marshall, “Biological polarized light reflectors in stomatopod crustaceans,” Proc. SPIE 5888, 380–388 (2005).
[Crossref]

2003 (2)

T. W. Cronin, N. Shashar, R. L. Caldwell, J. Marshall, A. G. Cheroske, and T.-H. Chiou, “Polarization signals in the marine environment,” Proc. SPIE 5158, 85–92 (2003).
[Crossref]

G. Biener, A. Niv, V. Kleiner, and E. Hasman, “Near-field Fourier transform polarimetry by use of a discrete space-variant subwavelength grating,” J. Opt. Soc. Am. A 20, 1940–1948 (2003).
[Crossref]

2002 (1)

J. F. De Boer and T. E. Milner, “Review of polarization sensitive optical coherence tomography and Stokes vector determination,” J. Biomed. Opt. 7, 359–371 (2002).
[Crossref]

1999 (1)

J. Marshall and J. Oberwinkler, “Ultraviolet vision: the colourful world of the mantis shrimp,” Nature 401, 873–874 (1999).
[Crossref]

1996 (1)

N. Shashar, P. Rutledge, and T. Cronin, “Polarization vision in cuttlefish in a concealed communication channel?” J. Exp. Biol. 199, 2077–2084 (1996).

1995 (1)

M. A. Green and M. J. Keevers, “Optical properties of intrinsic silicon at 300 K,” Prog. Photovoltaics 3, 189–192 (1995).
[Crossref]

1991 (1)

N. Marshall, M. Land, C. King, and T. Cronin, “The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). I. Compound eye structure: the detection of polarized light,” Philos. Trans. R. Soc. London B 334, 33–56 (1991).
[Crossref]

1989 (1)

T. W. Cronin and N. J. Marshall, “A retina with at least ten spectral types of photoreceptors in a mantis shrimp,” Nature 339, 137–140 (1989).
[Crossref]

Achilefu, S.

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

T. Charanya, T. York, S. Bloch, G. Sudlow, K. Liang, M. Garcia, W. J. Akers, D. Rubin, V. Gruev, and S. Achilefu, “Trimodal color-fluorescence-polarization endoscopy aided by a tumor selective molecular probe accurately detects flat lesions in colitis-associated cancer,” J. Biomed. Opt. 19, 126002 (2014).
[Crossref]

Adl, S.

C. Mora, D. P. Tittensor, S. Adl, A. G. Simpson, and B. Worm, “How many species are there on Earth and in the ocean?” PLoS Biol. 9, e1001127 (2011).
[Crossref]

Aizenberg, J.

G. England, M. Kolle, P. Kim, M. Khan, P. Muñoz, E. Mazur, and J. Aizenberg, “Bioinspired micrograting arrays mimicking the reverse color diffraction elements evolved by the butterfly Pierella luna,” Proc. Natl. Acad. Sci. USA 111, 15630–15634 (2014).
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Supplementary Material (2)

NameDescription
» Visualization 1       Real-time video captured from four marine animals underwater. Left: color image. Right: DoLP image in a false-color map, where red and blue indicate highly polarized and unpolarized light, respectively (see scales at right).
» Visualization 2       Real-time video captured from cuttlefish (S. latimanus) as captured by our bio-inspired sensor. Left panel shows the color image and right panel shows difference in degree of polarization between the green and red channels.

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Figures (6)

Fig. 1.
Fig. 1.

Mantis shrimp’s compound eye (left) is divided into three morphological parts: two hemispheres and a midband section. The rhabdoms in the peripheral hemispheres are sensitive to two orthogonal orientations of linearly polarized light by alternating stacks of bidirectional microvilli, while the midband section utilizes vertically stacked photosensitive cells for spectral discrimination. Similar to its biological counterpart, our bio-inspired imaging sensor (right) utilizes a combination of vertically stacked photodetectors for spectral sensitivity and pixelated metallic nanowire for polarization sensitivity. (a) The stomatopod crustacean Odontodactylus latirostris. (b) Close up view of the ommatidia [inset in (a)]. The following abbreviations are used: midband (MB), dorsal hemisphere (DH), and ventral hemisphere (VH). (c) Diagrammatic representation of a sagittal section [line in (b)] of a generalized stomatopod ommatidia. (d) Photograph of our bio-inspired color-polarization imager. (e) Diagrammatic representation of (d). (a) and (b) Photographs by Michael Bok.

Fig. 2.
Fig. 2.

Cross-sectional diagram of the pixel’s circuitry with its vertically stacked photodiodes. Three transistors per photodiode are utilized in the pixel. The first positively doped epitaxial layer is grown on top of the silicon wafer with 1.5 μm thickness, followed by selective negative doping to realize the red photodiode. The second epitaxial layer is grown on top of the first epitaxial layer with a thickness of 2 μm to realize the green photodiode, and the third epitaxial layer for the blue photodiode, with 0.8  μm thickness, is grown last.

Fig. 3.
Fig. 3.

Optical and spectral characteristics of our bio-inspired color-polarization imaging system. (a) Sinusoidal response of nanowire polarization filters to Malus’s law, with fixed-pattern noise histograms at data points close to full pixel well-depth capacity. (b) Quantum efficiency over the visible spectrum. (c) Scanning electron micrograph of the aluminum nanowires deposited on top of the imager. (d) Scanning electron micrograph showing the four pixelated filter orientations (scale bar, 2 μm). The high overall QE is due to the combination of both shallow and deep photodetectors, which are individually optimized for maximum conversion rate at different wavelengths across the visible spectrum.

Fig. 4.
Fig. 4.

Optoelectronic characterization of the imaging system per color channel. (a) AoP and (b) DoLP errors as a function of the fully polarized input light’s AoP. (c) DoLP error as a function of the partially polarized input light’s DoLP. (d) Diattenuation ratio as a function of the input light’s wavelength over the visible spectrum. This high polarization sensitivity of our bio-inspired sensor is a result of the high aspect ratio of the aluminum nanowires and high QE of the vertically stacked detectors.

Fig. 5.
Fig. 5.

Sample image showing the co-registered color and polarization information. The scene includes a Macbeth color chart, an orange toy race car, a silicon conical ingot, a polarization target, a black plastic horse, and a few beach rocks. (a) Color image. (b) DoLP represented in a false-color map, where red and blue indicate fully polarized and unpolarized light, respectively. (c) AoP represented in a false-color map, where red and light blue indicate horizontally and vertically polarized light, respectively.

Fig. 6.
Fig. 6.

Still frames captured from video of four marine animals underwater. Left: color images. Right: DoLP represented in a false-color maps, where red and blue indicate highly polarized and unpolarized light, respectively (see scales at right). (a) O. scyllarus, with polarized antenna scales. (b) H. trispinosa, with polarized blue maxillipeds. (c) S. latimanus, swimming away from the diver, with polarized stripes. (d) S. latimanus, in a stationary state with polarized stripes [same specimen as in (c)]. (e) S. lessoniana, with polarized stripes.