Abstract

A SPAD-based line sensor fabricated in 130 nm CMOS technology capable of acquiring time-resolved fluorescence spectra (TRFS) in 8.3 milliseconds is presented. To the best of our knowledge, this is the fastest time correlated single photon counting (TCSPC) TRFS acquisition reported to date. The line sensor is an upgrade to our prior work and incorporates: i) parallelized interface from sensor to surrounding circuitry enabling high line rate to the PC (19,000 lines/s) and ii) novel time-gating architecture where detected photons in the OFF region are rejected digitally after the output stage of the SPAD. The time-gating architecture was chosen to avoid electrical transients on the SPAD high voltage supplies when gating is achieved by excess bias modulation. The time-gate has an adjustable location and time window width allowing the user to focus on time-events of interest. On-chip integrated center-of-mass (CMM) calculations provide efficient acquisition of photon arrivals and direct lifetime estimation of fluorescence decays. Furthermore, any of the SPC, TCSPC and on-chip CMM modes can be used in conjunction with the time-gating. The higher readout rate and versatile architecture greatly empower the user and will allow widespread applications across many techniques and disciplines. Here we focused on 3 examples of TRFS and time-gated Raman spectroscopy: i) kinetics of chlorophyll A fluorescence from an intact leaf; ii) kinetics of a thrombin biosensor FRET probe from quenched to fluorescence states; iii) ex vivo mouse lung tissue autofluorescence TRFS; iv) time-gated Raman spectroscopy of toluene at 3056 cm−1 peak. To the best of our knowledge, we detect spectrally for the first time the fast rise in fluorescence lifetime of chlorophyll A in a measurement over single fluorescent transient.

© 2017 Optical Society of America

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2017 (1)

K. Ehrlich, A. Kufcsák, N. Krstajić, R. K. Henderson, R. R. Thomson, and M. G. Tanner, “Fibre optic time-resolved spectroscopy using CMOS-SPAD arrays,” Proc. SPIE 1005, 100580H (2017).
[Crossref]

2016 (5)

M. I. Rowley, A. C. C. Coolen, B. Vojnovic, and P. R. Barber, “Robust Bayesian fluorescence lifetime estimation, decay model selection and instrument response determination for low-intensity FLIM imaging,” PLoS One 11(6), e0158404 (2016).
[Crossref] [PubMed]

S. Burri, H. Homulle, C. Bruschini, and E. Charbon, “LinoSPAD: a time-resolved 256×1 CMOS SPAD line sensor system featuring 64 FPGA-based TDC channels running at up to 8.5 giga-events per second,” Proc. SPIE 9899, 98990D (2016).

F. M. Rocca, J. Nedbal, D. Tyndall, N. Krstajić, D. D.-U. Li, S. M. Ameer-Beg, and R. K. Henderson, “Real-time fluorescence lifetime actuation for cell sorting using a CMOS SPAD silicon photomultiplier,” Opt. Lett. 41(4), 673–676 (2016).
[Crossref] [PubMed]

S. P. Poland, A. T. Erdogan, N. Krstajić, J. Levitt, V. Devauges, R. J. Walker, D. D.-U. Li, S. M. Ameer-Beg, and R. K. Henderson, “New high-speed centre of mass method incorporating background subtraction for accurate determination of fluorescence lifetime,” Opt. Express 24(7), 6899–6915 (2016).
[Crossref] [PubMed]

B. Mills, M. Bradley, and K. Dhaliwal, “Optical imaging of bacterial infections,” Clin. Transl. Imaging 4(3), 163–174 (2016).
[Crossref] [PubMed]

2015 (6)

J. M. Pavia, M. Scandini, S. Lindner, M. Wolf, and E. Charbon, “A 1 x 400 backside-illuminated SPAD sensor with 49.7 ps resolution, 30 pJ/sample TDCs fabricated in 3D CMOS technology for near-infrared optical tomography,” IEEE J. Solid-State Circuits 50(10), 2406–2418 (2015).
[Crossref]

I. Nissinen, J. Nissinen, P. Keränen, A. K. Länsman, J. Holma, and J. Kostamovaara, “A 2×(4)×128 Multitime-Gated SPAD Line Detector for Pulsed Raman Spectroscopy,” IEEE Sens. J. 15, 1358–1365 (2015).
[Crossref]

K. Suhling, L. M. Hirvonen, J. A. Levitt, P.-H. Chung, C. Tregidgo, A. Le Marois, D. A. Rusakov, K. Zheng, S. Ameer-Beg, S. Poland, S. Coelho, R. Henderson, and N. Krstajic, “Fluorescence lifetime imaging (FLIM): Basic concepts and some recent developments,” Med. Photonics 27, 3–40 (2015).
[Crossref]

S. P. Poland, N. Krstajić, J. Monypenny, S. Coelho, D. Tyndall, R. J. Walker, V. Devauges, J. Richardson, N. Dutton, P. Barber, D. D.-U. Li, K. Suhling, T. Ng, R. K. Henderson, and S. M. Ameer-Beg, “A high speed multifocal multiphoton fluorescence lifetime imaging microscope for live-cell FRET imaging,” Biomed. Opt. Express 6(2), 277–296 (2015).
[Crossref] [PubMed]

M. Popleteeva, K. T. Haas, D. Stoppa, L. Pancheri, L. Gasparini, C. F. Kaminski, L. D. Cassidy, A. R. Venkitaraman, and A. Esposito, “Fast and simple spectral FLIM for biochemical and medical imaging,” Opt. Express 23(18), 23511–23525 (2015).
[Crossref] [PubMed]

N. Krstajić, J. Levitt, S. Poland, S. Ameer-Beg, and R. Henderson, “256 × 2 SPAD line sensor for time resolved fluorescence spectroscopy,” Opt. Express 23(5), 5653–5669 (2015).
[Crossref] [PubMed]

2014 (7)

S. P. Poland, N. Krstajić, S. Coelho, D. Tyndall, R. J. Walker, V. Devauges, P. E. Morton, N. S. Nicholas, J. Richardson, D. D.-U. Li, K. Suhling, C. M. Wells, M. Parsons, R. K. Henderson, and S. M. Ameer-Beg, “Time-resolved multifocal multiphoton microscope for high speed FRET imaging in vivo,” Opt. Lett. 39(20), 6013–6016 (2014).
[Crossref] [PubMed]

E. Charbon, “Single-photon imaging in complementary metal oxide semiconductor processes,” Philos. Trans. Roy. Soc. London A 372, 1-31 (2014).

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
[Crossref] [PubMed]

W. Becker, V. Shcheslavkiy, S. Frere, and I. Slutsky, “Spatially resolved recording of transient fluorescence-lifetime effects by line-scanning TCSPC,” Microsc. Res. Tech. 77(3), 216–224 (2014).
[Crossref] [PubMed]

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
[Crossref] [PubMed]

Z. Li and M. J. Deen, “Towards a portable Raman spectrometer using a concave grating and a time-gated CMOS SPAD,” Opt. Express 22(15), 18736–18747 (2014).
[Crossref] [PubMed]

Y. Maruyama, J. Blacksberg, and E. Charbon, “A 1024 x 8, 700-ps time-gated SPAD line sensor for planetary surface exploration with laser Raman spectroscopy and LIBS,” IEEE J. Solid-State Circuits 49(1), 179–189 (2014).
[Crossref]

2013 (4)

J. Kostamovaara, J. Tenhunen, M. Kögler, I. Nissinen, J. Nissinen, and P. Keränen, “Fluorescence suppression in Raman spectroscopy using a time-gated CMOS SPAD,” Opt. Express 21(25), 31632–31645 (2013).
[Crossref] [PubMed]

J. Arlt, D. Tyndall, B. R. Rae, D. D.-U. Li, J. A. Richardson, and R. K. Henderson, “A study of pile-up in integrated time-correlated single photon counting systems,” Rev. Sci. Instrum. 84(10), 103105 (2013).
[Crossref] [PubMed]

S. Preus, K. Kilså, F.-A. Miannay, B. Albinsson, and L. M. Wilhelmsson, “FRETmatrix: a general methodology for the simulation and analysis of FRET in nucleic acids,” Nucleic Acids Res. 41(1), e18 (2013).
[Crossref] [PubMed]

T. Terai and T. Nagano, “Small-molecule fluorophores and fluorescent probes for bioimaging,” Pflugers Arch. 465(3), 347–359 (2013).
[Crossref] [PubMed]

2012 (6)

N. Krstajić, C. T. A. Brown, K. Dholakia, and M. E. Giardini, “Tissue surface as the reference arm in Fourier domain optical coherence tomography,” J. Biomed. Opt. 17(7), 071305 (2012).
[Crossref] [PubMed]

S.-S. Kiwanuka, T. K. Laurila, J. H. Frank, A. Esposito, K. Blomberg von der Geest, L. Pancheri, D. Stoppa, and C. F. Kaminski, “Development of broadband cavity ring-down spectroscopy for biomedical diagnostics of liquid analytes,” Anal. Chem. 84(13), 5489–5493 (2012).
[Crossref] [PubMed]

L. Marcu, “Fluorescence lifetime techniques in medical applications,” Ann. Biomed. Eng. 40(2), 304–331 (2012).
[Crossref] [PubMed]

E. B. Ishay, G. Hazan, G. Rahamim, D. Amir, and E. Haas, “An instrument for fast acquisition of fluorescence decay curves at picosecond resolution designed for “double kinetics” experiments: Application to fluorescence resonance excitation energy transfer study of protein folding,” Rev. Sci. Instrum. 83(8), 084301 (2012).
[Crossref] [PubMed]

H. Xie, J. Bec, J. Liu, Y. Sun, M. Lam, D. R. Yankelevich, and L. Marcu, “Multispectral scanning time-resolved fluorescence spectroscopy (TRFS) technique for intravascular diagnosis,” Biomed. Opt. Express 3(7), 1521–1533 (2012).
[Crossref] [PubMed]

D. Tyndall, B. R. Rae, D. D.-U. Li, J. Arlt, A. Johnston, J. A. Richardson, and R. K. Henderson, “A high-throughput time-resolved mini-silicon photomultiplier with embedded fluorescence lifetime estimation in 0.13 μm CMOS,” IEEE Trans. Biomed. Circuits Syst. 6(6), 562–570 (2012).
[Crossref] [PubMed]

2011 (3)

D. McLoskey, D. Campbell, A. Allison, and G. Hungerford, “Fast time-correlated single-photon counting fluorescence lifetime acquisition using a 100 MHz semiconductor excitation source,” Meas. Sci. Technol. 22(6), 67001 (2011).
[Crossref]

J. Blacksberg, Y. Maruyama, E. Charbon, and G. R. Rossman, “Fast single-photon avalanche diode arrays for laser Raman spectroscopy,” Opt. Lett. 36(18), 3672–3674 (2011).
[Crossref] [PubMed]

D. D.-U. Li, J. Arlt, D. Tyndall, R. Walker, J. Richardson, D. Stoppa, E. Charbon, and R. K. Henderson, “Video-rate fluorescence lifetime imaging camera with CMOS single-photon avalanche diode arrays and high-speed imaging algorithm,” J. Biomed. Opt. 16(9), 096012 (2011).
[Crossref] [PubMed]

2010 (1)

D.-U. Li, B. Rae, R. Andrews, J. Arlt, and R. Henderson, “Hardware implementation algorithm and error analysis of high-speed fluorescence lifetime sensing systems using center-of-mass method,” J. Biomed. Opt. 15, 17006 (2010).

2009 (1)

U. Noomnarm and R. M. Clegg, “Fluorescence lifetimes: fundamentals and interpretations,” Photosynth. Res. 101(2-3), 181–194 (2009).
[Crossref] [PubMed]

2007 (1)

O. Holub, M. J. Seufferheld, C. Gohlke, G. J. Heiss, and R. M. Clegg, “Fluorescence lifetime imaging microscopy of Chlamydomonas reinhardtii: non-photochemical quenching mutants and the effect of photosynthetic inhibitors on the slow chlorophyll fluorescence transient,” J. Microsc. 226(2), 90–120 (2007).
[Crossref] [PubMed]

2006 (1)

D. Renker, “Geiger-mode avalanche photodiodes, history, properties and problems,” Nucl. Instrum. Methods Phys. Res. 567(1), 48–56 (2006).
[Crossref]

2005 (1)

F. Franck, D. Dewez, and R. Popovic, “Changes in the room-temperature emission spectrum of chlorophyll during fast and slow phases of the Kautsky effect in intact leaves,” Photochem. Photobiol. 81(2), 431–436 (2005).
[Crossref] [PubMed]

2004 (1)

R. E. Bell, “Exploiting a transmission grating spectrometer,” Rev. Sci. Instrum. 75(10), 4158–4161 (2004).
[Crossref]

2003 (1)

A. Rochas, M. Gosch, A. Serov, P. A. Besse, R. S. Popovic, T. Lasser, and R. Rigler, “First fully integrated 2-D array of single-photon detectors in standard CMOS technology,” IEEE Photonics Technol. Lett. 15(7), 963–965 (2003).
[Crossref]

2000 (2)

K. Maxwell and G. N. Johnson, “Chlorophyll fluorescence-a practical guide,” J. Exp. Bot. 51(345), 659–668 (2000).
[PubMed]

J. Ervin, J. Sabelko, and M. Gruebele, “Submicrosecond real-time fluorescence sampling: application to protein folding,” J. Photochem. Photobiol. B 54(1), 1–15 (2000).
[Crossref] [PubMed]

1999 (1)

R. H. Clarke, S. Londhe, W. R. Premasiri, and M. E. Womble, “Low‐resolution Raman spectroscopy: instrumentation and applications in chemical analysis,” J. Raman Spectrosc. 30(9), 827–832 (1999).
[Crossref]

1997 (1)

J. M. Beechem, “Picosecond fluorescence decay curves collected on millisecond time scale: direct measurement of hydrodynamic radii, local/global mobility, and intramolecular distances during protein-folding reactions,” Methods Enzymol. 278, 24–49 (1997).
[Crossref] [PubMed]

1995 (1)

Govindje, “Sixty-three years since Kautsky: chlorophyll a fluorescence,” Funct. Plant Biol. 22, 131–160 (1995).

1993 (1)

1992 (1)

J. R. Lakowicz, H. Szmacinski, and M. L. Johnson, “Calcium imaging using fluorescence lifetimes and long-wavelength probes,” J. Fluoresc. 2(1), 47–62 (1992).
[Crossref] [PubMed]

1961 (1)

L. M. Bollinger and G. E. Thomas, “Measurement of the time dependence of scintillation intensity by a delayed‐coincidence method,” Rev. Sci. Instrum. 32(9), 1044–1050 (1961).
[Crossref]

Abbas, T. A.

T. A. Abbas, N. A. W. Dutton, O. Almer, S. Pellegrini, Y. Henrion, and R. K. Henderson, “Backside illuminated SPAD image sensor with 7.83μm pitch in 3D-Stacked CMOS technology,” in 62nd International Electronic Devices Meeting (IEEE, 2016).
[Crossref]

Albinsson, B.

S. Preus, K. Kilså, F.-A. Miannay, B. Albinsson, and L. M. Wilhelmsson, “FRETmatrix: a general methodology for the simulation and analysis of FRET in nucleic acids,” Nucleic Acids Res. 41(1), e18 (2013).
[Crossref] [PubMed]

Allakhverdiev, S. I.

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
[Crossref] [PubMed]

Allison, A.

D. McLoskey, D. Campbell, A. Allison, and G. Hungerford, “Fast time-correlated single-photon counting fluorescence lifetime acquisition using a 100 MHz semiconductor excitation source,” Meas. Sci. Technol. 22(6), 67001 (2011).
[Crossref]

Almer, O.

T. A. Abbas, N. A. W. Dutton, O. Almer, S. Pellegrini, Y. Henrion, and R. K. Henderson, “Backside illuminated SPAD image sensor with 7.83μm pitch in 3D-Stacked CMOS technology,” in 62nd International Electronic Devices Meeting (IEEE, 2016).
[Crossref]

Ameer-Beg, S.

N. Krstajić, J. Levitt, S. Poland, S. Ameer-Beg, and R. Henderson, “256 × 2 SPAD line sensor for time resolved fluorescence spectroscopy,” Opt. Express 23(5), 5653–5669 (2015).
[Crossref] [PubMed]

K. Suhling, L. M. Hirvonen, J. A. Levitt, P.-H. Chung, C. Tregidgo, A. Le Marois, D. A. Rusakov, K. Zheng, S. Ameer-Beg, S. Poland, S. Coelho, R. Henderson, and N. Krstajic, “Fluorescence lifetime imaging (FLIM): Basic concepts and some recent developments,” Med. Photonics 27, 3–40 (2015).
[Crossref]

Ameer-Beg, S. M.

Amir, D.

E. B. Ishay, G. Hazan, G. Rahamim, D. Amir, and E. Haas, “An instrument for fast acquisition of fluorescence decay curves at picosecond resolution designed for “double kinetics” experiments: Application to fluorescence resonance excitation energy transfer study of protein folding,” Rev. Sci. Instrum. 83(8), 084301 (2012).
[Crossref] [PubMed]

Andrews, R.

D.-U. Li, B. Rae, R. Andrews, J. Arlt, and R. Henderson, “Hardware implementation algorithm and error analysis of high-speed fluorescence lifetime sensing systems using center-of-mass method,” J. Biomed. Opt. 15, 17006 (2010).

Arlt, J.

J. Arlt, D. Tyndall, B. R. Rae, D. D.-U. Li, J. A. Richardson, and R. K. Henderson, “A study of pile-up in integrated time-correlated single photon counting systems,” Rev. Sci. Instrum. 84(10), 103105 (2013).
[Crossref] [PubMed]

D. Tyndall, B. R. Rae, D. D.-U. Li, J. Arlt, A. Johnston, J. A. Richardson, and R. K. Henderson, “A high-throughput time-resolved mini-silicon photomultiplier with embedded fluorescence lifetime estimation in 0.13 μm CMOS,” IEEE Trans. Biomed. Circuits Syst. 6(6), 562–570 (2012).
[Crossref] [PubMed]

D. D.-U. Li, J. Arlt, D. Tyndall, R. Walker, J. Richardson, D. Stoppa, E. Charbon, and R. K. Henderson, “Video-rate fluorescence lifetime imaging camera with CMOS single-photon avalanche diode arrays and high-speed imaging algorithm,” J. Biomed. Opt. 16(9), 096012 (2011).
[Crossref] [PubMed]

D.-U. Li, B. Rae, R. Andrews, J. Arlt, and R. Henderson, “Hardware implementation algorithm and error analysis of high-speed fluorescence lifetime sensing systems using center-of-mass method,” J. Biomed. Opt. 15, 17006 (2010).

Barber, P.

Barber, P. R.

M. I. Rowley, A. C. C. Coolen, B. Vojnovic, and P. R. Barber, “Robust Bayesian fluorescence lifetime estimation, decay model selection and instrument response determination for low-intensity FLIM imaging,” PLoS One 11(6), e0158404 (2016).
[Crossref] [PubMed]

Battey, D. E.

Bec, J.

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
[Crossref] [PubMed]

H. Xie, J. Bec, J. Liu, Y. Sun, M. Lam, D. R. Yankelevich, and L. Marcu, “Multispectral scanning time-resolved fluorescence spectroscopy (TRFS) technique for intravascular diagnosis,” Biomed. Opt. Express 3(7), 1521–1533 (2012).
[Crossref] [PubMed]

Becker, W.

W. Becker, V. Shcheslavkiy, S. Frere, and I. Slutsky, “Spatially resolved recording of transient fluorescence-lifetime effects by line-scanning TCSPC,” Microsc. Res. Tech. 77(3), 216–224 (2014).
[Crossref] [PubMed]

Beechem, J. M.

J. M. Beechem, “Picosecond fluorescence decay curves collected on millisecond time scale: direct measurement of hydrodynamic radii, local/global mobility, and intramolecular distances during protein-folding reactions,” Methods Enzymol. 278, 24–49 (1997).
[Crossref] [PubMed]

Bell, R. E.

R. E. Bell, “Exploiting a transmission grating spectrometer,” Rev. Sci. Instrum. 75(10), 4158–4161 (2004).
[Crossref]

Besse, P. A.

A. Rochas, M. Gosch, A. Serov, P. A. Besse, R. S. Popovic, T. Lasser, and R. Rigler, “First fully integrated 2-D array of single-photon detectors in standard CMOS technology,” IEEE Photonics Technol. Lett. 15(7), 963–965 (2003).
[Crossref]

Blacksberg, J.

Y. Maruyama, J. Blacksberg, and E. Charbon, “A 1024 x 8, 700-ps time-gated SPAD line sensor for planetary surface exploration with laser Raman spectroscopy and LIBS,” IEEE J. Solid-State Circuits 49(1), 179–189 (2014).
[Crossref]

J. Blacksberg, Y. Maruyama, E. Charbon, and G. R. Rossman, “Fast single-photon avalanche diode arrays for laser Raman spectroscopy,” Opt. Lett. 36(18), 3672–3674 (2011).
[Crossref] [PubMed]

Blomberg von der Geest, K.

S.-S. Kiwanuka, T. K. Laurila, J. H. Frank, A. Esposito, K. Blomberg von der Geest, L. Pancheri, D. Stoppa, and C. F. Kaminski, “Development of broadband cavity ring-down spectroscopy for biomedical diagnostics of liquid analytes,” Anal. Chem. 84(13), 5489–5493 (2012).
[Crossref] [PubMed]

Bollinger, L. M.

L. M. Bollinger and G. E. Thomas, “Measurement of the time dependence of scintillation intensity by a delayed‐coincidence method,” Rev. Sci. Instrum. 32(9), 1044–1050 (1961).
[Crossref]

Borghetti, F.

J. Richardson, R. Walker, L. Grant, D. Stoppa, F. Borghetti, E. Charbon, M. Gersbach, and R. K. Henderson, “A 32 x32 50ps resolution 10 bit time to digital converter array in 130nm CMOS for time correlated imaging,” in IEEE Custom Integrated Circuits Conference, 2009. Cicc ’09 (2009), pp. 77–80.
[Crossref]

Bosa, K.

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
[Crossref] [PubMed]

Bradley, M.

B. Mills, M. Bradley, and K. Dhaliwal, “Optical imaging of bacterial infections,” Clin. Transl. Imaging 4(3), 163–174 (2016).
[Crossref] [PubMed]

Brestic, M.

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
[Crossref] [PubMed]

Brown, C. T. A.

N. Krstajić, C. T. A. Brown, K. Dholakia, and M. E. Giardini, “Tissue surface as the reference arm in Fourier domain optical coherence tomography,” J. Biomed. Opt. 17(7), 071305 (2012).
[Crossref] [PubMed]

Bruschini, C.

S. Burri, H. Homulle, C. Bruschini, and E. Charbon, “LinoSPAD: a time-resolved 256×1 CMOS SPAD line sensor system featuring 64 FPGA-based TDC channels running at up to 8.5 giga-events per second,” Proc. SPIE 9899, 98990D (2016).

Burri, S.

S. Burri, H. Homulle, C. Bruschini, and E. Charbon, “LinoSPAD: a time-resolved 256×1 CMOS SPAD line sensor system featuring 64 FPGA-based TDC channels running at up to 8.5 giga-events per second,” Proc. SPIE 9899, 98990D (2016).

Bussotti, F.

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
[Crossref] [PubMed]

Calatayud, A.

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
[Crossref] [PubMed]

Campbell, D.

D. McLoskey, D. Campbell, A. Allison, and G. Hungerford, “Fast time-correlated single-photon counting fluorescence lifetime acquisition using a 100 MHz semiconductor excitation source,” Meas. Sci. Technol. 22(6), 67001 (2011).
[Crossref]

Cassidy, L. D.

Charbon, E.

S. Burri, H. Homulle, C. Bruschini, and E. Charbon, “LinoSPAD: a time-resolved 256×1 CMOS SPAD line sensor system featuring 64 FPGA-based TDC channels running at up to 8.5 giga-events per second,” Proc. SPIE 9899, 98990D (2016).

J. M. Pavia, M. Scandini, S. Lindner, M. Wolf, and E. Charbon, “A 1 x 400 backside-illuminated SPAD sensor with 49.7 ps resolution, 30 pJ/sample TDCs fabricated in 3D CMOS technology for near-infrared optical tomography,” IEEE J. Solid-State Circuits 50(10), 2406–2418 (2015).
[Crossref]

Y. Maruyama, J. Blacksberg, and E. Charbon, “A 1024 x 8, 700-ps time-gated SPAD line sensor for planetary surface exploration with laser Raman spectroscopy and LIBS,” IEEE J. Solid-State Circuits 49(1), 179–189 (2014).
[Crossref]

E. Charbon, “Single-photon imaging in complementary metal oxide semiconductor processes,” Philos. Trans. Roy. Soc. London A 372, 1-31 (2014).

D. D.-U. Li, J. Arlt, D. Tyndall, R. Walker, J. Richardson, D. Stoppa, E. Charbon, and R. K. Henderson, “Video-rate fluorescence lifetime imaging camera with CMOS single-photon avalanche diode arrays and high-speed imaging algorithm,” J. Biomed. Opt. 16(9), 096012 (2011).
[Crossref] [PubMed]

J. Blacksberg, Y. Maruyama, E. Charbon, and G. R. Rossman, “Fast single-photon avalanche diode arrays for laser Raman spectroscopy,” Opt. Lett. 36(18), 3672–3674 (2011).
[Crossref] [PubMed]

J. Richardson, R. Walker, L. Grant, D. Stoppa, F. Borghetti, E. Charbon, M. Gersbach, and R. K. Henderson, “A 32 x32 50ps resolution 10 bit time to digital converter array in 130nm CMOS for time correlated imaging,” in IEEE Custom Integrated Circuits Conference, 2009. Cicc ’09 (2009), pp. 77–80.
[Crossref]

Chung, P.-H.

K. Suhling, L. M. Hirvonen, J. A. Levitt, P.-H. Chung, C. Tregidgo, A. Le Marois, D. A. Rusakov, K. Zheng, S. Ameer-Beg, S. Poland, S. Coelho, R. Henderson, and N. Krstajic, “Fluorescence lifetime imaging (FLIM): Basic concepts and some recent developments,” Med. Photonics 27, 3–40 (2015).
[Crossref]

Clarke, R. H.

R. H. Clarke, S. Londhe, W. R. Premasiri, and M. E. Womble, “Low‐resolution Raman spectroscopy: instrumentation and applications in chemical analysis,” J. Raman Spectrosc. 30(9), 827–832 (1999).
[Crossref]

Clegg, R. M.

U. Noomnarm and R. M. Clegg, “Fluorescence lifetimes: fundamentals and interpretations,” Photosynth. Res. 101(2-3), 181–194 (2009).
[Crossref] [PubMed]

O. Holub, M. J. Seufferheld, C. Gohlke, G. J. Heiss, and R. M. Clegg, “Fluorescence lifetime imaging microscopy of Chlamydomonas reinhardtii: non-photochemical quenching mutants and the effect of photosynthetic inhibitors on the slow chlorophyll fluorescence transient,” J. Microsc. 226(2), 90–120 (2007).
[Crossref] [PubMed]

Coelho, S.

Coolen, A. C. C.

M. I. Rowley, A. C. C. Coolen, B. Vojnovic, and P. R. Barber, “Robust Bayesian fluorescence lifetime estimation, decay model selection and instrument response determination for low-intensity FLIM imaging,” PLoS One 11(6), e0158404 (2016).
[Crossref] [PubMed]

Dabrowski, P.

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
[Crossref] [PubMed]

Deen, M. J.

Devauges, V.

Dewez, D.

F. Franck, D. Dewez, and R. Popovic, “Changes in the room-temperature emission spectrum of chlorophyll during fast and slow phases of the Kautsky effect in intact leaves,” Photochem. Photobiol. 81(2), 431–436 (2005).
[Crossref] [PubMed]

Dhaliwal, K.

B. Mills, M. Bradley, and K. Dhaliwal, “Optical imaging of bacterial infections,” Clin. Transl. Imaging 4(3), 163–174 (2016).
[Crossref] [PubMed]

Dholakia, K.

N. Krstajić, C. T. A. Brown, K. Dholakia, and M. E. Giardini, “Tissue surface as the reference arm in Fourier domain optical coherence tomography,” J. Biomed. Opt. 17(7), 071305 (2012).
[Crossref] [PubMed]

Dutton, N.

Dutton, N. A. W.

T. A. Abbas, N. A. W. Dutton, O. Almer, S. Pellegrini, Y. Henrion, and R. K. Henderson, “Backside illuminated SPAD image sensor with 7.83μm pitch in 3D-Stacked CMOS technology,” in 62nd International Electronic Devices Meeting (IEEE, 2016).
[Crossref]

Ehrlich, K.

K. Ehrlich, A. Kufcsák, N. Krstajić, R. K. Henderson, R. R. Thomson, and M. G. Tanner, “Fibre optic time-resolved spectroscopy using CMOS-SPAD arrays,” Proc. SPIE 1005, 100580H (2017).
[Crossref]

Elsheery, N. I.

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
[Crossref] [PubMed]

Elson, D. S.

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
[Crossref] [PubMed]

Erdogan, A.

A. Erdogan, R. Walker, N. Finlayson, N. Krstajic, G. Williams, and R. Henderson, “A 16.5 Giga Events/s 1024 × 8 SPAD Line Sensor with per-pixel Zoomable 50ps-6.4ns/bin Histogramming TDC,” in VLSI Symposium (IEEE, 2017).

Erdogan, A. T.

Ervin, J.

J. Ervin, J. Sabelko, and M. Gruebele, “Submicrosecond real-time fluorescence sampling: application to protein folding,” J. Photochem. Photobiol. B 54(1), 1–15 (2000).
[Crossref] [PubMed]

Esposito, A.

M. Popleteeva, K. T. Haas, D. Stoppa, L. Pancheri, L. Gasparini, C. F. Kaminski, L. D. Cassidy, A. R. Venkitaraman, and A. Esposito, “Fast and simple spectral FLIM for biochemical and medical imaging,” Opt. Express 23(18), 23511–23525 (2015).
[Crossref] [PubMed]

S.-S. Kiwanuka, T. K. Laurila, J. H. Frank, A. Esposito, K. Blomberg von der Geest, L. Pancheri, D. Stoppa, and C. F. Kaminski, “Development of broadband cavity ring-down spectroscopy for biomedical diagnostics of liquid analytes,” Anal. Chem. 84(13), 5489–5493 (2012).
[Crossref] [PubMed]

Ferroni, L.

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
[Crossref] [PubMed]

Finlayson, N.

A. Erdogan, R. Walker, N. Finlayson, N. Krstajic, G. Williams, and R. Henderson, “A 16.5 Giga Events/s 1024 × 8 SPAD Line Sensor with per-pixel Zoomable 50ps-6.4ns/bin Histogramming TDC,” in VLSI Symposium (IEEE, 2017).

Franck, F.

F. Franck, D. Dewez, and R. Popovic, “Changes in the room-temperature emission spectrum of chlorophyll during fast and slow phases of the Kautsky effect in intact leaves,” Photochem. Photobiol. 81(2), 431–436 (2005).
[Crossref] [PubMed]

Frank, J. H.

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Hazan, G.

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N. Krstajić, J. Levitt, S. Poland, S. Ameer-Beg, and R. Henderson, “256 × 2 SPAD line sensor for time resolved fluorescence spectroscopy,” Opt. Express 23(5), 5653–5669 (2015).
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A. Erdogan, R. Walker, N. Finlayson, N. Krstajic, G. Williams, and R. Henderson, “A 16.5 Giga Events/s 1024 × 8 SPAD Line Sensor with per-pixel Zoomable 50ps-6.4ns/bin Histogramming TDC,” in VLSI Symposium (IEEE, 2017).

Henderson, R. K.

K. Ehrlich, A. Kufcsák, N. Krstajić, R. K. Henderson, R. R. Thomson, and M. G. Tanner, “Fibre optic time-resolved spectroscopy using CMOS-SPAD arrays,” Proc. SPIE 1005, 100580H (2017).
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Henrion, Y.

T. A. Abbas, N. A. W. Dutton, O. Almer, S. Pellegrini, Y. Henrion, and R. K. Henderson, “Backside illuminated SPAD image sensor with 7.83μm pitch in 3D-Stacked CMOS technology,” in 62nd International Electronic Devices Meeting (IEEE, 2016).
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Hogewoning, S. W.

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
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Holma, J.

I. Nissinen, J. Nissinen, P. Keränen, A. K. Länsman, J. Holma, and J. Kostamovaara, “A 2×(4)×128 Multitime-Gated SPAD Line Detector for Pulsed Raman Spectroscopy,” IEEE Sens. J. 15, 1358–1365 (2015).
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Holub, O.

O. Holub, M. J. Seufferheld, C. Gohlke, G. J. Heiss, and R. M. Clegg, “Fluorescence lifetime imaging microscopy of Chlamydomonas reinhardtii: non-photochemical quenching mutants and the effect of photosynthetic inhibitors on the slow chlorophyll fluorescence transient,” J. Microsc. 226(2), 90–120 (2007).
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H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
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Johnston, A.

D. Tyndall, B. R. Rae, D. D.-U. Li, J. Arlt, A. Johnston, J. A. Richardson, and R. K. Henderson, “A high-throughput time-resolved mini-silicon photomultiplier with embedded fluorescence lifetime estimation in 0.13 μm CMOS,” IEEE Trans. Biomed. Circuits Syst. 6(6), 562–570 (2012).
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Kalaji, H. M.

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
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J. Kostamovaara, J. Tenhunen, M. Kögler, I. Nissinen, J. Nissinen, and P. Keränen, “Fluorescence suppression in Raman spectroscopy using a time-gated CMOS SPAD,” Opt. Express 21(25), 31632–31645 (2013).
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Kögler, M.

Kostamovaara, J.

I. Nissinen, J. Nissinen, P. Keränen, A. K. Länsman, J. Holma, and J. Kostamovaara, “A 2×(4)×128 Multitime-Gated SPAD Line Detector for Pulsed Raman Spectroscopy,” IEEE Sens. J. 15, 1358–1365 (2015).
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I. Nissinen, J. Nissinen, P. Keränen, and J. Kostamovaara, “On the effects of the time gate position and width on the signal-to-noise ratio for detection of Raman spectrum in a time-gated CMOS single-photon avalanche diode based sensor,” Sens. Actuators B Chem. (n.d.).

Krstajic, N.

K. Ehrlich, A. Kufcsák, N. Krstajić, R. K. Henderson, R. R. Thomson, and M. G. Tanner, “Fibre optic time-resolved spectroscopy using CMOS-SPAD arrays,” Proc. SPIE 1005, 100580H (2017).
[Crossref]

F. M. Rocca, J. Nedbal, D. Tyndall, N. Krstajić, D. D.-U. Li, S. M. Ameer-Beg, and R. K. Henderson, “Real-time fluorescence lifetime actuation for cell sorting using a CMOS SPAD silicon photomultiplier,” Opt. Lett. 41(4), 673–676 (2016).
[Crossref] [PubMed]

S. P. Poland, A. T. Erdogan, N. Krstajić, J. Levitt, V. Devauges, R. J. Walker, D. D.-U. Li, S. M. Ameer-Beg, and R. K. Henderson, “New high-speed centre of mass method incorporating background subtraction for accurate determination of fluorescence lifetime,” Opt. Express 24(7), 6899–6915 (2016).
[Crossref] [PubMed]

N. Krstajić, J. Levitt, S. Poland, S. Ameer-Beg, and R. Henderson, “256 × 2 SPAD line sensor for time resolved fluorescence spectroscopy,” Opt. Express 23(5), 5653–5669 (2015).
[Crossref] [PubMed]

S. P. Poland, N. Krstajić, J. Monypenny, S. Coelho, D. Tyndall, R. J. Walker, V. Devauges, J. Richardson, N. Dutton, P. Barber, D. D.-U. Li, K. Suhling, T. Ng, R. K. Henderson, and S. M. Ameer-Beg, “A high speed multifocal multiphoton fluorescence lifetime imaging microscope for live-cell FRET imaging,” Biomed. Opt. Express 6(2), 277–296 (2015).
[Crossref] [PubMed]

K. Suhling, L. M. Hirvonen, J. A. Levitt, P.-H. Chung, C. Tregidgo, A. Le Marois, D. A. Rusakov, K. Zheng, S. Ameer-Beg, S. Poland, S. Coelho, R. Henderson, and N. Krstajic, “Fluorescence lifetime imaging (FLIM): Basic concepts and some recent developments,” Med. Photonics 27, 3–40 (2015).
[Crossref]

S. P. Poland, N. Krstajić, S. Coelho, D. Tyndall, R. J. Walker, V. Devauges, P. E. Morton, N. S. Nicholas, J. Richardson, D. D.-U. Li, K. Suhling, C. M. Wells, M. Parsons, R. K. Henderson, and S. M. Ameer-Beg, “Time-resolved multifocal multiphoton microscope for high speed FRET imaging in vivo,” Opt. Lett. 39(20), 6013–6016 (2014).
[Crossref] [PubMed]

N. Krstajić, C. T. A. Brown, K. Dholakia, and M. E. Giardini, “Tissue surface as the reference arm in Fourier domain optical coherence tomography,” J. Biomed. Opt. 17(7), 071305 (2012).
[Crossref] [PubMed]

A. Erdogan, R. Walker, N. Finlayson, N. Krstajic, G. Williams, and R. Henderson, “A 16.5 Giga Events/s 1024 × 8 SPAD Line Sensor with per-pixel Zoomable 50ps-6.4ns/bin Histogramming TDC,” in VLSI Symposium (IEEE, 2017).

Kufcsák, A.

K. Ehrlich, A. Kufcsák, N. Krstajić, R. K. Henderson, R. R. Thomson, and M. G. Tanner, “Fibre optic time-resolved spectroscopy using CMOS-SPAD arrays,” Proc. SPIE 1005, 100580H (2017).
[Crossref]

Ladle, R. J.

H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
[Crossref] [PubMed]

Lakowicz, J. R.

J. R. Lakowicz, H. Szmacinski, and M. L. Johnson, “Calcium imaging using fluorescence lifetimes and long-wavelength probes,” J. Fluoresc. 2(1), 47–62 (1992).
[Crossref] [PubMed]

Lam, M.

Länsman, A. K.

I. Nissinen, J. Nissinen, P. Keränen, A. K. Länsman, J. Holma, and J. Kostamovaara, “A 2×(4)×128 Multitime-Gated SPAD Line Detector for Pulsed Raman Spectroscopy,” IEEE Sens. J. 15, 1358–1365 (2015).
[Crossref]

Lasser, T.

A. Rochas, M. Gosch, A. Serov, P. A. Besse, R. S. Popovic, T. Lasser, and R. Rigler, “First fully integrated 2-D array of single-photon detectors in standard CMOS technology,” IEEE Photonics Technol. Lett. 15(7), 963–965 (2003).
[Crossref]

Laurila, T. K.

S.-S. Kiwanuka, T. K. Laurila, J. H. Frank, A. Esposito, K. Blomberg von der Geest, L. Pancheri, D. Stoppa, and C. F. Kaminski, “Development of broadband cavity ring-down spectroscopy for biomedical diagnostics of liquid analytes,” Anal. Chem. 84(13), 5489–5493 (2012).
[Crossref] [PubMed]

Le Marois, A.

K. Suhling, L. M. Hirvonen, J. A. Levitt, P.-H. Chung, C. Tregidgo, A. Le Marois, D. A. Rusakov, K. Zheng, S. Ameer-Beg, S. Poland, S. Coelho, R. Henderson, and N. Krstajic, “Fluorescence lifetime imaging (FLIM): Basic concepts and some recent developments,” Med. Photonics 27, 3–40 (2015).
[Crossref]

Levitt, J.

Levitt, J. A.

K. Suhling, L. M. Hirvonen, J. A. Levitt, P.-H. Chung, C. Tregidgo, A. Le Marois, D. A. Rusakov, K. Zheng, S. Ameer-Beg, S. Poland, S. Coelho, R. Henderson, and N. Krstajic, “Fluorescence lifetime imaging (FLIM): Basic concepts and some recent developments,” Med. Photonics 27, 3–40 (2015).
[Crossref]

Li, D. D.-U.

F. M. Rocca, J. Nedbal, D. Tyndall, N. Krstajić, D. D.-U. Li, S. M. Ameer-Beg, and R. K. Henderson, “Real-time fluorescence lifetime actuation for cell sorting using a CMOS SPAD silicon photomultiplier,” Opt. Lett. 41(4), 673–676 (2016).
[Crossref] [PubMed]

S. P. Poland, A. T. Erdogan, N. Krstajić, J. Levitt, V. Devauges, R. J. Walker, D. D.-U. Li, S. M. Ameer-Beg, and R. K. Henderson, “New high-speed centre of mass method incorporating background subtraction for accurate determination of fluorescence lifetime,” Opt. Express 24(7), 6899–6915 (2016).
[Crossref] [PubMed]

S. P. Poland, N. Krstajić, J. Monypenny, S. Coelho, D. Tyndall, R. J. Walker, V. Devauges, J. Richardson, N. Dutton, P. Barber, D. D.-U. Li, K. Suhling, T. Ng, R. K. Henderson, and S. M. Ameer-Beg, “A high speed multifocal multiphoton fluorescence lifetime imaging microscope for live-cell FRET imaging,” Biomed. Opt. Express 6(2), 277–296 (2015).
[Crossref] [PubMed]

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S.-S. Kiwanuka, T. K. Laurila, J. H. Frank, A. Esposito, K. Blomberg von der Geest, L. Pancheri, D. Stoppa, and C. F. Kaminski, “Development of broadband cavity ring-down spectroscopy for biomedical diagnostics of liquid analytes,” Anal. Chem. 84(13), 5489–5493 (2012).
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D. D.-U. Li, J. Arlt, D. Tyndall, R. Walker, J. Richardson, D. Stoppa, E. Charbon, and R. K. Henderson, “Video-rate fluorescence lifetime imaging camera with CMOS single-photon avalanche diode arrays and high-speed imaging algorithm,” J. Biomed. Opt. 16(9), 096012 (2011).
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J. Richardson, R. Walker, L. Grant, D. Stoppa, F. Borghetti, E. Charbon, M. Gersbach, and R. K. Henderson, “A 32 x32 50ps resolution 10 bit time to digital converter array in 130nm CMOS for time correlated imaging,” in IEEE Custom Integrated Circuits Conference, 2009. Cicc ’09 (2009), pp. 77–80.
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Sun, Y.

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
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D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instrum. 85(3), 034303 (2014).
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H. Xie, J. Bec, J. Liu, Y. Sun, M. Lam, D. R. Yankelevich, and L. Marcu, “Multispectral scanning time-resolved fluorescence spectroscopy (TRFS) technique for intravascular diagnosis,” Biomed. Opt. Express 3(7), 1521–1533 (2012).
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H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
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J. R. Lakowicz, H. Szmacinski, and M. L. Johnson, “Calcium imaging using fluorescence lifetimes and long-wavelength probes,” J. Fluoresc. 2(1), 47–62 (1992).
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H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
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L. M. Bollinger and G. E. Thomas, “Measurement of the time dependence of scintillation intensity by a delayed‐coincidence method,” Rev. Sci. Instrum. 32(9), 1044–1050 (1961).
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K. Ehrlich, A. Kufcsák, N. Krstajić, R. K. Henderson, R. R. Thomson, and M. G. Tanner, “Fibre optic time-resolved spectroscopy using CMOS-SPAD arrays,” Proc. SPIE 1005, 100580H (2017).
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Vojnovic, B.

M. I. Rowley, A. C. C. Coolen, B. Vojnovic, and P. R. Barber, “Robust Bayesian fluorescence lifetime estimation, decay model selection and instrument response determination for low-intensity FLIM imaging,” PLoS One 11(6), e0158404 (2016).
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D. D.-U. Li, J. Arlt, D. Tyndall, R. Walker, J. Richardson, D. Stoppa, E. Charbon, and R. K. Henderson, “Video-rate fluorescence lifetime imaging camera with CMOS single-photon avalanche diode arrays and high-speed imaging algorithm,” J. Biomed. Opt. 16(9), 096012 (2011).
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A. Erdogan, R. Walker, N. Finlayson, N. Krstajic, G. Williams, and R. Henderson, “A 16.5 Giga Events/s 1024 × 8 SPAD Line Sensor with per-pixel Zoomable 50ps-6.4ns/bin Histogramming TDC,” in VLSI Symposium (IEEE, 2017).

J. Richardson, R. Walker, L. Grant, D. Stoppa, F. Borghetti, E. Charbon, M. Gersbach, and R. K. Henderson, “A 32 x32 50ps resolution 10 bit time to digital converter array in 130nm CMOS for time correlated imaging,” in IEEE Custom Integrated Circuits Conference, 2009. Cicc ’09 (2009), pp. 77–80.
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H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
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H. M. Kalaji, G. Schansker, R. J. Ladle, V. Goltsev, K. Bosa, S. I. Allakhverdiev, M. Brestic, F. Bussotti, A. Calatayud, P. Dąbrowski, N. I. Elsheery, L. Ferroni, L. Guidi, S. W. Hogewoning, A. Jajoo, A. N. Misra, S. G. Nebauer, S. Pancaldi, C. Penella, D. Poli, M. Pollastrini, Z. B. Romanowska-Duda, B. Rutkowska, J. Serôdio, K. Suresh, W. Szulc, E. Tambussi, M. Yanniccari, and M. Zivcak, “Frequently asked questions about in vivo chlorophyll fluorescence: practical issues,” Photosynth. Res. 122(2), 121–158 (2014).
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Opt. Express (5)

Opt. Lett. (3)

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Proc. SPIE (2)

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K. Ehrlich, A. Kufcsák, N. Krstajić, R. K. Henderson, R. R. Thomson, and M. G. Tanner, “Fibre optic time-resolved spectroscopy using CMOS-SPAD arrays,” Proc. SPIE 1005, 100580H (2017).
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A. Erdogan, R. Walker, N. Finlayson, N. Krstajic, G. Williams, and R. Henderson, “A 16.5 Giga Events/s 1024 × 8 SPAD Line Sensor with per-pixel Zoomable 50ps-6.4ns/bin Histogramming TDC,” in VLSI Symposium (IEEE, 2017).

A. Le Marois, S. Labouesse, K. Suhling, and R. Heintzmann, “Noise-corrected principal component analysis of fluorescence lifetime imaging data,” J. Biophoton. (2016).

L. Pancheri and D. Stoppa, “A SPAD-based pixel linear array for high-speed time-gated fluorescence lifetime imaging,” in Proceedings of ESSCIRC, 2009. ESSCIRC ’09 (2009), pp. 428–431.
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C. Veerappan, J. Richardson, R. Walker, D.-U. Li, M. W. Fishburn, Y. Maruyama, D. Stoppa, F. Borghetti, M. Gersbach, R. K. Henderson, and E. Charbon, “A 160 x 128 single-photon image sensor with on-pixel 55 ps 10 bit time-to-digital converter,” in Solid-State Circuits Conference Digest of Technical Papers (ISSCC), 2011 IEEE International (2011), pp. 312–314.

R. J. Strasser, M. Tsimilli-Michael, and A. Srivastava, “Analysis of the Chlorophyll a Fluorescence Transient,” in Chlorophyll a Fluorescence, G. C. Papageorgiou and Govindjee, eds. (Springer Netherlands, 2004), pp. 321–362.

D. R. Yankelevich, D. Elson, and L. Marcu, “Pulse sampling technique,” in Fluorescence Lifetime Spectroscopy and Imaging (CRC, 2014), pp. 87–102.

S. V. Kathuria and O. Bilsel, “Probing microsecond reactions with microfluidic mixers and TCSPC,” in Advanced Time-Correlated Single Photon Counting Applications, W. Becker, ed., Springer Series in Chemical Physics No. 111 (Springer International Publishing, 2015), pp. 357–384.

Supplementary Material (2)

NameDescription
» Visualization 1: AVI (2880 KB)      Chlorophyll A fluorescence rise TRFS
» Visualization 2: AVI (3266 KB)      Chlorophyll A fluorescence fall TRFS

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Figures (19)

Fig. 1
Fig. 1

Fluorescence transients can easily be measured using a photodiode in the microsecond to millisecond regime (top graph (I)). Recent developments in compact spectrometers have advanced this further allowing a spectral view into fluorescence transient evolution (middle graph (II)). In this paper we are able to show spectral “double kinetics” in nanosecond and millisecond regime whereby the transient is induced only once. For each time point (t1, t2, ...) a TRFS data cube is acquired during the single transient.

Fig. 2
Fig. 2

Demonstration of spectral decays in two simulated scenarios. The first scenario is photon rich: (a) defined here as most pixels having more than 2000 counts in decay. Plot (b) shows the difference between the decay in single pixel and binning 80 pixels which results in a better looking decay. The second scenario is photon starved: (c) where the decay derived from a single pixel in (d) is too noisy. However, the decay from 80 binned pixels is good enough to allow the user to manipulate the data cube in an optimal way given the amount of light detected. Spectral decays were simulated in Matlab 2014a (Mathworks, USA), shot noise limited, visible to near-infrared TRFS data cubes. Spectral decays have 0.4 ns time resolution and 1.6 nm spectral resolution. Representing broadly the properties of the CMOS SPAD line sensor presented here.

Fig. 3
Fig. 3

Time-gated region is defined for each pixel by two global, pre-defined signals TIME_GATE_START and TIME_GATE_STOP. They define the time during which the TDC counter is enabled. TDC counter acts as TCSPC TDC counter in TCSPC mode, but in SPC mode it acts as a photon counter. Therefore the same circuit controls the time-gating behavior in both modes.

Fig. 4
Fig. 4

Time-gated region (blue) is defined by TIME-GATE-START and TIME-GATE-STOP settings with respect to delayed STOP signal. As opposed to previous designs [12] the SPAD is always on. The TDC conversion only happens if photon arrival time takes place within the time-gated region. Photon arrivals outside the time-gated region do not result in TDC conversion, but they are electrically detected by the SPAD and hence there is a dead-time effect for subsequent detections.

Fig. 5
Fig. 5

Setup comprising epi-fluorescence light collection (right) and the spectrograph (left). The CMOS SPAD line sensor is placed in the focus of the spectrograph optics. Volume phase holographic grating is used to optimize light throughput. See Methods section for details.

Fig. 6
Fig. 6

FRET biosensor works by thrombin cleaving the peptide sequence separating the methyl red and 5-carboxyfluorescein (FAM) thus allowing FAM to fluoresce.

Fig. 7
Fig. 7

Time-gated TCSPC histograms of photon arrival times in ambient light. Time-gates were positioned with an on-chip, 128 step delay line with respect to the STOP signal. The width of each time-gate was 1 step of the delay line. The average FWHM for a short delay (10 steps) ON time-gate was 1.44 ns (a). For the OFF time-gate it was 1.56 ns (b).

Fig. 8
Fig. 8

Sweeping an external delay generator over a fixed time-gate window covering a laser pulse generates a more detailed picture of the time-gate (a) convolved with the asymmetric shapes of the laser pulse and red SPAD IRF (b). Blue SPADs were time-gated in (a) as its IRF does not have the diffuse tail present in red SPADs (b) (see supplementary notes [44]).

Fig. 9
Fig. 9

Chlorophyll A transient curve from SPC acquisition over 120 s.

Fig. 10
Fig. 10

Fluorescent transient of the leaf during fast rise and slow fall. Three TRFS time points at: (a). 0.03 s; (b). 2.04 s; and 120.04 s (c). See Visualization 1 and Visualization 2 for fast rise and slow fall videos respectively. 10 pixels were binned for each 3D plot in (a-b) resulting in 5 nm spectral coverage.

Fig. 11
Fig. 11

Fluorescence decays extracted from TRFS data cubes taken during the fast rise (a,c) and the slow fall (b,d). Increase in lifetime on (a) is more obvious with decays fitted for 26.275 ms and 130.188 ms time points (c). Fluorescence quenching is indicative by reduction of lifetime in (b,d) as expected for the chlorophyll A transient. The decays in (a,b) were taken from single pixel (0.5 nm spectral coverage) and from 1 TRFS data cube (8.3 ms exposure time over 51.25 ms) at each time point during fast rise (a), 3 TRFS data cubes (25 ms exposure time over 153.75 ms) around each time point during slow fall (b).

Fig. 12
Fig. 12

Fluorescence decays during the fast rise (a). Lifetime change is more obvious when binning timestamps of all pixels, but no spectral information is available from decays in (a). The decays were created by binning 150 lines of TCSPC time-events of 1.3 ms total exposure time over 7.7 ms around each time point. The decay fits are shown in (b) for two time points.

Fig. 13
Fig. 13

Increasing fluorescence lifetime over the first 40 ms of fast rise on the 680 nm and 740 m peaks. CMM estimates of single pixel with photons captured over 166.6 µs shown on (a) broadly match lifetimes calculated by fitting decays to TCSPC data. Photons captured over 1.67 ms and 30 pixels result in smoother transients.

Fig. 14
Fig. 14

Enzyme kinetics curve of a thrombin FRET biosensor. At 8 s thrombin was pipetted into a cuvette initiating a rise in fluorescence intensity. TRFS was acquired in 8.3 ms every 50 ms during the first 50 s (every 150 ms after 50s) and the kinetics curve was derived from underlying spectral double kinetics data.

Fig. 15
Fig. 15

Sample TRFS from the time point at 130 s. Spectral resolution is 0.4 nm and no binning was applied in the spectral domain.

Fig. 16
Fig. 16

Decays extracted from the fluorescence peak before enzyme activation (2 s time point) and after enzyme activation (130 s time point). 20 pixels were binned for both decays covering 520-528 nm.

Fig. 17
Fig. 17

TRFS of ex vivo lung acquired in 258 ms. 10 pixels were binned to obtain spectral resolution of 6 nm. Autofluorescence did not vary over 50 s measurements so no transient was observable.

Fig. 18
Fig. 18

Decays (from ex vivo lung tissue) with fits for green band (524 nm) and red band (697 nm) (a). Lifetime reduction in red band is shown in (b), top curve. Lifetime reduction is due to red Inspeck beads. Spectral resolution of each decay was 6 nm.

Fig. 19
Fig. 19

Plot of non-time-gated (blue) spectrum and 5.6 ns time-gated Raman spectrum (red) of toluene. Exposure time was 5s and the acquisition was done in time-gated SPC mode.

Tables (1)

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Table 1 Abbreviations used in the article

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