Abstract

A method of controllable light delivery to retinal rod cells using an optical fiber is described. Photo-induced current of the living rod cells was measured with the suction electrode technique. The approach was tested with measurements relating the spatial distribution of the light intensity to photo-induced current. In addition, the ion current responses of rod cells to polarized light at two different orientation geometries of the cells were studied.

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References

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  1. J. E. Dowling, The Retina (Harvard University Press, Cambridge, Massachusetts, 1987).
  2. F. Rieke and D. A. Baylor, “Single-photon detection by rod cells of the retina,” Rev. Mod. Phys.70(3), 1027–1036 (1998).
    [CrossRef]
  3. S. Hecht, S. Shlaer, and M. H. Pirenne, “Energy, quanta and vision,” J. Gen. Physiol.25(6), 819–840 (1942).
    [CrossRef] [PubMed]
  4. D. A. Baylor, T. D. Lamb, and K.-W. Yau, “The membrane current of single rod outer segments,” J. Physiol.288, 589–611 (1979).
    [PubMed]
  5. D. A. Baylor, T. D. Lamb, and K.-W. Yau, “Responses of retinal rods to single photons,” J. Physiol.288, 613–634 (1979).
    [PubMed]
  6. P. B. Detwiler, J. D. Conner, and R. D. Bodoia, “Gigaseal patch clamp recordings from outer segments of intact retinal rods,” Nature300(5887), 59–61 (1982).
    [CrossRef] [PubMed]
  7. A. L. Hodgkin, P. A. McNaughton, B. J. Nunn, and K. W. Yau, “Effect of ions on retinal rods from Bufo marinus,” J. Physiol.350, 649–680 (1984).
    [PubMed]
  8. E. N. Pugh, Jr. and T. D. Lamb, “Phototransduction in vertebrate rods and cones: molecular mechanisms of amplification, recovery and light adaptation,” in Molecular Mechanisms of Visual Transduction, Vol. 3. of Handbook of Biological Physics, D. G. Stavenga, W. J. de Grip, and E. N. Pugh, Jr., eds. (Elsevier science, 2000), Chap. 5, pp. 183–255.
  9. W. H. Xiong and K.-W. Yau, “Rod sensitivity during Xenopus development,” J. Gen. Physiol.120(6), 817–827 (2002).
    [CrossRef] [PubMed]
  10. J. L. Schnapf, “Dependence of the single photon response on longitudinal position of absorption in toad rod outer segments,” J. Physiol.343, 147–159 (1983).
    [PubMed]
  11. V. I. Govardovskii, D. A. Korenyak, S. A. Shukolyukov, and L. V. Zueva, “Lateral diffusion of rhodopsin in photoreceptor membrane: a reappraisal,” Mol. Vis.15, 1717–1729 (2009).
    [PubMed]
  12. D. A. Baylor and R. Fettiplace, “Light path and photon capture in turtle photoreceptors,” J. Physiol.248(2), 433–464 (1975).
    [PubMed]
  13. F. I. Hárosi, “Absorption spectra and linear dichroism of some amphibian photoreceptors,” J. Gen. Physiol.66(3), 357–382 (1975).
    [CrossRef] [PubMed]
  14. D. A. Baylor, B. J. Nunn, and J. L. Schnapf, “The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis,” J. Physiol.357, 575–607 (1984).
    [PubMed]
  15. G. Horvath and D. Varju, Polarized Light in Animal Vision (Springer-Verlag, Berlin, 2004).
  16. N. W. Roberts and M. G. Needham, “A mechanism of polarized light sensitivity in cone photoreceptors of the goldfish Carassius auratus,” Biophys. J.93(9), 3241–3248 (2007).
    [CrossRef] [PubMed]
  17. F. L. Tobey and J. M. Enoch, “Directionality and waveguide properties of optically isolated rat rods,” Invest. Ophthalmol.12(12), 873–880 (1973).
    [PubMed]
  18. A. Koskelainen, K. Donner, G. Kalamkarov, and S. Hemilä, “Changes in the light-sensitive current of salamander rods upon manipulation of putative pH-regulating mechanisms in the inner and outer segment,” Vision Res.34(8), 983–994 (1994).
    [CrossRef] [PubMed]
  19. W. A. Shurkliff, Polarized Light (Harvard University Press, Cambridge, Massachusetts, 1962).
  20. T. D. Lamb, P. A. McNaughton, and K.-W. Yau, “Spatial spread of activation and background desensitization in toad rod outer segments,” J. Physiol.319, 463–496 (1981).
    [PubMed]
  21. A. Dhatak and K. Thyagarajan, Introduction to Fiber Optics (Cambridge University Press, Cambridge, UK, 1998).

2009 (1)

V. I. Govardovskii, D. A. Korenyak, S. A. Shukolyukov, and L. V. Zueva, “Lateral diffusion of rhodopsin in photoreceptor membrane: a reappraisal,” Mol. Vis.15, 1717–1729 (2009).
[PubMed]

2007 (1)

N. W. Roberts and M. G. Needham, “A mechanism of polarized light sensitivity in cone photoreceptors of the goldfish Carassius auratus,” Biophys. J.93(9), 3241–3248 (2007).
[CrossRef] [PubMed]

2002 (1)

W. H. Xiong and K.-W. Yau, “Rod sensitivity during Xenopus development,” J. Gen. Physiol.120(6), 817–827 (2002).
[CrossRef] [PubMed]

1998 (1)

F. Rieke and D. A. Baylor, “Single-photon detection by rod cells of the retina,” Rev. Mod. Phys.70(3), 1027–1036 (1998).
[CrossRef]

1994 (1)

A. Koskelainen, K. Donner, G. Kalamkarov, and S. Hemilä, “Changes in the light-sensitive current of salamander rods upon manipulation of putative pH-regulating mechanisms in the inner and outer segment,” Vision Res.34(8), 983–994 (1994).
[CrossRef] [PubMed]

1984 (2)

D. A. Baylor, B. J. Nunn, and J. L. Schnapf, “The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis,” J. Physiol.357, 575–607 (1984).
[PubMed]

A. L. Hodgkin, P. A. McNaughton, B. J. Nunn, and K. W. Yau, “Effect of ions on retinal rods from Bufo marinus,” J. Physiol.350, 649–680 (1984).
[PubMed]

1983 (1)

J. L. Schnapf, “Dependence of the single photon response on longitudinal position of absorption in toad rod outer segments,” J. Physiol.343, 147–159 (1983).
[PubMed]

1982 (1)

P. B. Detwiler, J. D. Conner, and R. D. Bodoia, “Gigaseal patch clamp recordings from outer segments of intact retinal rods,” Nature300(5887), 59–61 (1982).
[CrossRef] [PubMed]

1981 (1)

T. D. Lamb, P. A. McNaughton, and K.-W. Yau, “Spatial spread of activation and background desensitization in toad rod outer segments,” J. Physiol.319, 463–496 (1981).
[PubMed]

1979 (2)

D. A. Baylor, T. D. Lamb, and K.-W. Yau, “The membrane current of single rod outer segments,” J. Physiol.288, 589–611 (1979).
[PubMed]

D. A. Baylor, T. D. Lamb, and K.-W. Yau, “Responses of retinal rods to single photons,” J. Physiol.288, 613–634 (1979).
[PubMed]

1975 (2)

D. A. Baylor and R. Fettiplace, “Light path and photon capture in turtle photoreceptors,” J. Physiol.248(2), 433–464 (1975).
[PubMed]

F. I. Hárosi, “Absorption spectra and linear dichroism of some amphibian photoreceptors,” J. Gen. Physiol.66(3), 357–382 (1975).
[CrossRef] [PubMed]

1973 (1)

F. L. Tobey and J. M. Enoch, “Directionality and waveguide properties of optically isolated rat rods,” Invest. Ophthalmol.12(12), 873–880 (1973).
[PubMed]

1942 (1)

S. Hecht, S. Shlaer, and M. H. Pirenne, “Energy, quanta and vision,” J. Gen. Physiol.25(6), 819–840 (1942).
[CrossRef] [PubMed]

Baylor, D. A.

F. Rieke and D. A. Baylor, “Single-photon detection by rod cells of the retina,” Rev. Mod. Phys.70(3), 1027–1036 (1998).
[CrossRef]

D. A. Baylor, B. J. Nunn, and J. L. Schnapf, “The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis,” J. Physiol.357, 575–607 (1984).
[PubMed]

D. A. Baylor, T. D. Lamb, and K.-W. Yau, “The membrane current of single rod outer segments,” J. Physiol.288, 589–611 (1979).
[PubMed]

D. A. Baylor, T. D. Lamb, and K.-W. Yau, “Responses of retinal rods to single photons,” J. Physiol.288, 613–634 (1979).
[PubMed]

D. A. Baylor and R. Fettiplace, “Light path and photon capture in turtle photoreceptors,” J. Physiol.248(2), 433–464 (1975).
[PubMed]

Bodoia, R. D.

P. B. Detwiler, J. D. Conner, and R. D. Bodoia, “Gigaseal patch clamp recordings from outer segments of intact retinal rods,” Nature300(5887), 59–61 (1982).
[CrossRef] [PubMed]

Conner, J. D.

P. B. Detwiler, J. D. Conner, and R. D. Bodoia, “Gigaseal patch clamp recordings from outer segments of intact retinal rods,” Nature300(5887), 59–61 (1982).
[CrossRef] [PubMed]

Detwiler, P. B.

P. B. Detwiler, J. D. Conner, and R. D. Bodoia, “Gigaseal patch clamp recordings from outer segments of intact retinal rods,” Nature300(5887), 59–61 (1982).
[CrossRef] [PubMed]

Donner, K.

A. Koskelainen, K. Donner, G. Kalamkarov, and S. Hemilä, “Changes in the light-sensitive current of salamander rods upon manipulation of putative pH-regulating mechanisms in the inner and outer segment,” Vision Res.34(8), 983–994 (1994).
[CrossRef] [PubMed]

Enoch, J. M.

F. L. Tobey and J. M. Enoch, “Directionality and waveguide properties of optically isolated rat rods,” Invest. Ophthalmol.12(12), 873–880 (1973).
[PubMed]

Fettiplace, R.

D. A. Baylor and R. Fettiplace, “Light path and photon capture in turtle photoreceptors,” J. Physiol.248(2), 433–464 (1975).
[PubMed]

Govardovskii, V. I.

V. I. Govardovskii, D. A. Korenyak, S. A. Shukolyukov, and L. V. Zueva, “Lateral diffusion of rhodopsin in photoreceptor membrane: a reappraisal,” Mol. Vis.15, 1717–1729 (2009).
[PubMed]

Hárosi, F. I.

F. I. Hárosi, “Absorption spectra and linear dichroism of some amphibian photoreceptors,” J. Gen. Physiol.66(3), 357–382 (1975).
[CrossRef] [PubMed]

Hecht, S.

S. Hecht, S. Shlaer, and M. H. Pirenne, “Energy, quanta and vision,” J. Gen. Physiol.25(6), 819–840 (1942).
[CrossRef] [PubMed]

Hemilä, S.

A. Koskelainen, K. Donner, G. Kalamkarov, and S. Hemilä, “Changes in the light-sensitive current of salamander rods upon manipulation of putative pH-regulating mechanisms in the inner and outer segment,” Vision Res.34(8), 983–994 (1994).
[CrossRef] [PubMed]

Hodgkin, A. L.

A. L. Hodgkin, P. A. McNaughton, B. J. Nunn, and K. W. Yau, “Effect of ions on retinal rods from Bufo marinus,” J. Physiol.350, 649–680 (1984).
[PubMed]

Kalamkarov, G.

A. Koskelainen, K. Donner, G. Kalamkarov, and S. Hemilä, “Changes in the light-sensitive current of salamander rods upon manipulation of putative pH-regulating mechanisms in the inner and outer segment,” Vision Res.34(8), 983–994 (1994).
[CrossRef] [PubMed]

Korenyak, D. A.

V. I. Govardovskii, D. A. Korenyak, S. A. Shukolyukov, and L. V. Zueva, “Lateral diffusion of rhodopsin in photoreceptor membrane: a reappraisal,” Mol. Vis.15, 1717–1729 (2009).
[PubMed]

Koskelainen, A.

A. Koskelainen, K. Donner, G. Kalamkarov, and S. Hemilä, “Changes in the light-sensitive current of salamander rods upon manipulation of putative pH-regulating mechanisms in the inner and outer segment,” Vision Res.34(8), 983–994 (1994).
[CrossRef] [PubMed]

Lamb, T. D.

T. D. Lamb, P. A. McNaughton, and K.-W. Yau, “Spatial spread of activation and background desensitization in toad rod outer segments,” J. Physiol.319, 463–496 (1981).
[PubMed]

D. A. Baylor, T. D. Lamb, and K.-W. Yau, “Responses of retinal rods to single photons,” J. Physiol.288, 613–634 (1979).
[PubMed]

D. A. Baylor, T. D. Lamb, and K.-W. Yau, “The membrane current of single rod outer segments,” J. Physiol.288, 589–611 (1979).
[PubMed]

McNaughton, P. A.

A. L. Hodgkin, P. A. McNaughton, B. J. Nunn, and K. W. Yau, “Effect of ions on retinal rods from Bufo marinus,” J. Physiol.350, 649–680 (1984).
[PubMed]

T. D. Lamb, P. A. McNaughton, and K.-W. Yau, “Spatial spread of activation and background desensitization in toad rod outer segments,” J. Physiol.319, 463–496 (1981).
[PubMed]

Needham, M. G.

N. W. Roberts and M. G. Needham, “A mechanism of polarized light sensitivity in cone photoreceptors of the goldfish Carassius auratus,” Biophys. J.93(9), 3241–3248 (2007).
[CrossRef] [PubMed]

Nunn, B. J.

D. A. Baylor, B. J. Nunn, and J. L. Schnapf, “The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis,” J. Physiol.357, 575–607 (1984).
[PubMed]

A. L. Hodgkin, P. A. McNaughton, B. J. Nunn, and K. W. Yau, “Effect of ions on retinal rods from Bufo marinus,” J. Physiol.350, 649–680 (1984).
[PubMed]

Pirenne, M. H.

S. Hecht, S. Shlaer, and M. H. Pirenne, “Energy, quanta and vision,” J. Gen. Physiol.25(6), 819–840 (1942).
[CrossRef] [PubMed]

Rieke, F.

F. Rieke and D. A. Baylor, “Single-photon detection by rod cells of the retina,” Rev. Mod. Phys.70(3), 1027–1036 (1998).
[CrossRef]

Roberts, N. W.

N. W. Roberts and M. G. Needham, “A mechanism of polarized light sensitivity in cone photoreceptors of the goldfish Carassius auratus,” Biophys. J.93(9), 3241–3248 (2007).
[CrossRef] [PubMed]

Schnapf, J. L.

D. A. Baylor, B. J. Nunn, and J. L. Schnapf, “The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis,” J. Physiol.357, 575–607 (1984).
[PubMed]

J. L. Schnapf, “Dependence of the single photon response on longitudinal position of absorption in toad rod outer segments,” J. Physiol.343, 147–159 (1983).
[PubMed]

Shlaer, S.

S. Hecht, S. Shlaer, and M. H. Pirenne, “Energy, quanta and vision,” J. Gen. Physiol.25(6), 819–840 (1942).
[CrossRef] [PubMed]

Shukolyukov, S. A.

V. I. Govardovskii, D. A. Korenyak, S. A. Shukolyukov, and L. V. Zueva, “Lateral diffusion of rhodopsin in photoreceptor membrane: a reappraisal,” Mol. Vis.15, 1717–1729 (2009).
[PubMed]

Tobey, F. L.

F. L. Tobey and J. M. Enoch, “Directionality and waveguide properties of optically isolated rat rods,” Invest. Ophthalmol.12(12), 873–880 (1973).
[PubMed]

Xiong, W. H.

W. H. Xiong and K.-W. Yau, “Rod sensitivity during Xenopus development,” J. Gen. Physiol.120(6), 817–827 (2002).
[CrossRef] [PubMed]

Yau, K. W.

A. L. Hodgkin, P. A. McNaughton, B. J. Nunn, and K. W. Yau, “Effect of ions on retinal rods from Bufo marinus,” J. Physiol.350, 649–680 (1984).
[PubMed]

Yau, K.-W.

W. H. Xiong and K.-W. Yau, “Rod sensitivity during Xenopus development,” J. Gen. Physiol.120(6), 817–827 (2002).
[CrossRef] [PubMed]

T. D. Lamb, P. A. McNaughton, and K.-W. Yau, “Spatial spread of activation and background desensitization in toad rod outer segments,” J. Physiol.319, 463–496 (1981).
[PubMed]

D. A. Baylor, T. D. Lamb, and K.-W. Yau, “The membrane current of single rod outer segments,” J. Physiol.288, 589–611 (1979).
[PubMed]

D. A. Baylor, T. D. Lamb, and K.-W. Yau, “Responses of retinal rods to single photons,” J. Physiol.288, 613–634 (1979).
[PubMed]

Zueva, L. V.

V. I. Govardovskii, D. A. Korenyak, S. A. Shukolyukov, and L. V. Zueva, “Lateral diffusion of rhodopsin in photoreceptor membrane: a reappraisal,” Mol. Vis.15, 1717–1729 (2009).
[PubMed]

Biophys. J. (1)

N. W. Roberts and M. G. Needham, “A mechanism of polarized light sensitivity in cone photoreceptors of the goldfish Carassius auratus,” Biophys. J.93(9), 3241–3248 (2007).
[CrossRef] [PubMed]

Invest. Ophthalmol. (1)

F. L. Tobey and J. M. Enoch, “Directionality and waveguide properties of optically isolated rat rods,” Invest. Ophthalmol.12(12), 873–880 (1973).
[PubMed]

J. Gen. Physiol. (3)

W. H. Xiong and K.-W. Yau, “Rod sensitivity during Xenopus development,” J. Gen. Physiol.120(6), 817–827 (2002).
[CrossRef] [PubMed]

F. I. Hárosi, “Absorption spectra and linear dichroism of some amphibian photoreceptors,” J. Gen. Physiol.66(3), 357–382 (1975).
[CrossRef] [PubMed]

S. Hecht, S. Shlaer, and M. H. Pirenne, “Energy, quanta and vision,” J. Gen. Physiol.25(6), 819–840 (1942).
[CrossRef] [PubMed]

J. Physiol. (7)

D. A. Baylor, T. D. Lamb, and K.-W. Yau, “The membrane current of single rod outer segments,” J. Physiol.288, 589–611 (1979).
[PubMed]

D. A. Baylor, T. D. Lamb, and K.-W. Yau, “Responses of retinal rods to single photons,” J. Physiol.288, 613–634 (1979).
[PubMed]

A. L. Hodgkin, P. A. McNaughton, B. J. Nunn, and K. W. Yau, “Effect of ions on retinal rods from Bufo marinus,” J. Physiol.350, 649–680 (1984).
[PubMed]

D. A. Baylor, B. J. Nunn, and J. L. Schnapf, “The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis,” J. Physiol.357, 575–607 (1984).
[PubMed]

J. L. Schnapf, “Dependence of the single photon response on longitudinal position of absorption in toad rod outer segments,” J. Physiol.343, 147–159 (1983).
[PubMed]

T. D. Lamb, P. A. McNaughton, and K.-W. Yau, “Spatial spread of activation and background desensitization in toad rod outer segments,” J. Physiol.319, 463–496 (1981).
[PubMed]

D. A. Baylor and R. Fettiplace, “Light path and photon capture in turtle photoreceptors,” J. Physiol.248(2), 433–464 (1975).
[PubMed]

Mol. Vis. (1)

V. I. Govardovskii, D. A. Korenyak, S. A. Shukolyukov, and L. V. Zueva, “Lateral diffusion of rhodopsin in photoreceptor membrane: a reappraisal,” Mol. Vis.15, 1717–1729 (2009).
[PubMed]

Nature (1)

P. B. Detwiler, J. D. Conner, and R. D. Bodoia, “Gigaseal patch clamp recordings from outer segments of intact retinal rods,” Nature300(5887), 59–61 (1982).
[CrossRef] [PubMed]

Rev. Mod. Phys. (1)

F. Rieke and D. A. Baylor, “Single-photon detection by rod cells of the retina,” Rev. Mod. Phys.70(3), 1027–1036 (1998).
[CrossRef]

Vision Res. (1)

A. Koskelainen, K. Donner, G. Kalamkarov, and S. Hemilä, “Changes in the light-sensitive current of salamander rods upon manipulation of putative pH-regulating mechanisms in the inner and outer segment,” Vision Res.34(8), 983–994 (1994).
[CrossRef] [PubMed]

Other (5)

W. A. Shurkliff, Polarized Light (Harvard University Press, Cambridge, Massachusetts, 1962).

G. Horvath and D. Varju, Polarized Light in Animal Vision (Springer-Verlag, Berlin, 2004).

J. E. Dowling, The Retina (Harvard University Press, Cambridge, Massachusetts, 1987).

E. N. Pugh, Jr. and T. D. Lamb, “Phototransduction in vertebrate rods and cones: molecular mechanisms of amplification, recovery and light adaptation,” in Molecular Mechanisms of Visual Transduction, Vol. 3. of Handbook of Biological Physics, D. G. Stavenga, W. J. de Grip, and E. N. Pugh, Jr., eds. (Elsevier science, 2000), Chap. 5, pp. 183–255.

A. Dhatak and K. Thyagarajan, Introduction to Fiber Optics (Cambridge University Press, Cambridge, UK, 1998).

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Figures (5)

Fig. 1
Fig. 1

Transverse (a) and axial (b) configurations for rod illumination. ROS and RIS, stand for outer and inner segment of the rod, respectively. The green stripe at the ROS shows a light absorption region. The insets show two orientations of light polarizations (red arrows) with respect to the membrane discs of the ROS, and the green arrow is a wave vector of light. The black arrows are orientations of dipole moments of rhodopsin molecules within the membrane discs [15].

Fig. 2
Fig. 2

(a) Optical layout. A cw 532nm Nd:YAG laser is chopped by a shutter and attenuated by a variable neutral density filter (NDF). Half-, quarter- and another half-wave plate (HWP1, QWP, HWP2) are used to control the polarization. A 50/50 non-polarizing beam-splitter (BS) splits the beam into two beams, and lenses (L) focus them into two single mode (SM) fibers. The intensity of the stimulus is measured with a single photon avalanche photodiode (APD). (b) Arrangement of the bent suction pipette and the bent tip of the optical fiber at the microscope chamber in the axial configuration (side view). Dashed arrow shows the tilt direction of the suction pipette from the initial position with the tip pointing downwards to the axial configuration. (c) Side-view of the 532 nm laser beam profile collimated by the rounded fiber tip (fiber lens) in a Ringer solution (top view). (d) Microscope image of the tapered fiber tip and the suction pipette with a constrained retinal rod (top view). The fiber tip is scanned in XYZ-directions, shown by red arrows. The horizontal arrow between two vertical dashed lines shows the distance between the fiber tip and the pipette.

Fig. 3
Fig. 3

(a) Waveforms of the cell response at different number of impinging photons in the axial configuration. The distance between the fiber tip and suction pipette is 40 μm. The color legend indicates the corresponding number of impinging photons. (b) Dependence of the normalized amplitude of the cell response in (a) on the number of impinging photons, measured by the APD. The amplitude is normalized by A0 = 21 pA, and the number of photons is normalized by n0 = 2500 photons/pulse which corresponds to a half saturating amplitude of 10.5 pA. The solid line is a fit by Michaelis function. Each waveform and plotted point in (a,b) is an average of 20 responses.

Fig. 4
Fig. 4

Results of a transverse scan of light intensity in Y-direction at different distances between the pipette and the fiber tip, represented by Z-direction in Fig. 2d. Zero displacement corresponds to the axial alignment of the cell and the fiber tip. Plotted points are amplitudes of the cell response normalized by the maximum achievable value (average of 15 responses with 3 different cells) and red solid lines are experimental fits with Gaussian curves. Insets show transversal beam profiles measured by the CCD at the corresponding distances from the fiber tip.

Fig. 5
Fig. 5

Polarization dependence of the normalized cell response in transverse (a) and axial (b) configurations to linear polarized light. Solid line in (a) is the fit of the experimental data with COD = 0.98. Each experiment was repeated for 5 different cells. At each given orientation of the HWP1 the response was averaged over 20 light pulses. Average amplitude of the cell response along with its standard deviation was normalized by the maximum response amplitude achievable for a given dependence.

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