Abstract

We studied the effect of rod–cone interactions on mesopic visual reaction time (RT). Rod and cone photoreceptor excitations were independently controlled using a four-primary photostimulator. It was observed that (1) lateral rod–cone interactions increase the cone-mediated RTs; (2) the rod–cone interactions are strongest when rod sensitivity is maximal in a dark surround, but weaker with increased rod activity in a light surround; and (3) the presence of a dark surround nonselectively increased the mean and variability of chromatic (+L-M, S-cone) and luminance (L+M+S) RTs independent of the level of rod activity. The results demonstrate that lateral rod–cone interactions must be considered when deriving mesopic luminous efficiency using RT.

© 2013 Optical Society of America

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    [CrossRef]

2013

A. J. Zele, M. L. Maynard, and B. Feigl, “Rod and cone pathway signaling and interaction under mesopic illumination,” J. Vis. 13(1):21, 1–19 (2013).
[CrossRef]

2012

2010

D. Cao and J. Pokorny, “Rod and cone contrast gains derived from reaction time distribution modeling,” J. Vis. 10(2):11, 1–15 (2010).
[CrossRef]

D. Cao, B. B. Lee, and H. Sun, “Combination of rod and cone inputs in parasol ganglion cells of the magnocellular pathway,” J. Vis. 10(2):11, 1–15 (2010).
[CrossRef]

B. M. O’Donell, J. F. Barraza, and E. M. Colombo, “The effect of chromatic and luminance information on reaction times,” Vis. Neurosci. 27, 119–129 (2010).
[CrossRef]

J. M. Medina and J. A. Diaz, “S-cone excitation ratios for reaction times to blue-yellow suprathreshold changes at isoluminance,” Ophthalmic Physiolog. Opt. 30, 511–517 (2010).
[CrossRef]

2009

J. D. Crook, C. M. Davenport, B. B. Peterson, O. S. Packer, P. B. Detwiler, and D. M. Dacey, “Parallel ON and OFF cone bipolar inputs establish spatially coextensive receptive field structure of blue-yellow ganglion cells in primate retina,” J. Neurosci. 29, 8372–8387 (2009).
[CrossRef]

G. D. Field, M. Greschner, J. L. Gauthier, C. Rangel, J. Shlens, A. Sher, D. W. Marshak, A. M. Litke, and E. J. Chichilnisky, “High-sensitivity rod photoreceptor input to the blue-yellow color opponent pathway in macaque retina,” Nat. Neurosci. 12, 1159–1164 (2009).
[CrossRef]

A. Vassilev, A. Murzac, M. B. Zlatkova, and R. S. Anderson, “On the search for an appropriate metric for reaction time to suprathreshold increments and decrements,” Vis. Res. 49, 524–529 (2009).
[CrossRef]

2008

A. J. Zele, D. Cao, and J. Pokorny, “Rod–cone interactions and the temporal impulse response of the cone pathway,” Vis. Res. 48, 2593–2598 (2008).
[CrossRef]

D. Cao, J. Pokorny, V. C. Smith, and A. J. Zele, “Rod contributions to color perception: linear with rod contrast,” Vis. Res. 48, 2586–2592 (2008).
[CrossRef]

D. Cao, A. J. Zele, and J. Pokorny, “Chromatic discrimination in the presence of incremental and decremental rod pedestals,” Vis. Neurosci. 25, 399–404 (2008).
[CrossRef]

2007

D. Cao, A. J. Zele, and J. Pokorny, “Linking impulse response functions to reaction time: rod and cone reaction time data and a computational model,” Vis. Res. 47, 1060–1074 (2007).
[CrossRef]

A. J. Zele, D. Cao, and J. Pokorny, “Threshold units: a correct metric for reaction time?” Vis. Res. 47, 608–611 (2007).
[CrossRef]

E. J. Wagenmakers and S. Brown, “On the linear relation between the mean and the standard deviation of a response time distribution,” Psychol. Rev. 114, 830–841 (2007).
[CrossRef]

Y. Akashi, M. S. Rea, and J. D. Bullough, “Driver decision making in response to peripheral moving targets under mesopic light levels,” Lighting Res. Technol. 39, 53–67 (2007).
[CrossRef]

2006

D. Cao, A. J. Zele, and J. Pokorny, “Dark-adapted rod suppression of cone flicker detection: evaluation of receptoral and postreceptoral interactions,” Vis. Neurosci. 23, 531–537 (2006).
[CrossRef]

J. M. Medina and J. A. Diaz, “Postreceptoral chromatic-adaptation mechanisms in the red-green and blue-yellow systems using simple reaction times,” J. Opt. Soc. Am. A 23, 993–1007 (2006).
[CrossRef]

H. C. Walkey, J. A. Harlow, and J. L. Barbur, “Characterising mesopic spectral sensitivity from reaction times,” Vis. Res. 46, 4232–4243 (2006).
[CrossRef]

H. C. Walkey, J. A. Harlow, and J. L. Barbur, “Changes in reaction time and search time with background luminance in the mesopic range,” Ophthalmic Physiolog. Opt. 26, 288–299 (2006).

2005

H. C. Walkey, J. L. Barbur, J. A. Harlow, A. Hurden, I. R. Moorhead, and J. A. Taylor, “Effective contrast of colored stimuli in the mesopic range: a metric for perceived contrast based on achromatic luminance contrast,” J. Opt. Soc. Am. A 22, 17–28 (2005).
[CrossRef]

D. Cao, J. Pokorny, and V. C. Smith, “Matching rod percepts with cone stimuli,” Vis. Res. 45, 2119–2128 (2005).
[CrossRef]

M. J. Puts, J. Pokorny, J. Quinlan, and L. Glennie, “Audiophile hardware in vision science; the soundcard as a digital to analog converter,” J. Neurosci. Methods 142, 77–81 (2005).
[CrossRef]

2004

J. Pokorny, H. Smithson, and J. Quinlan, “Photostimulator allowing independent control of rods and the three cone types,” Vis. Neurosci. 21, 263–267 (2004).
[CrossRef]

H. Sun, L. Ruttiger, and B. B. Lee, “The spatiotemporal precision of ganglion cell signals: a comparison of physiological and psychophysical performance with moving gratings,” Vis. Res. 44, 19–33 (2004).
[CrossRef]

V. J. Uzzell and E. J. Chichilnisky, “Precision of spike trains in primate retinal ganglion cells,” J. Neurophysiol. 92, 780–789 (2004).
[CrossRef]

H. E. Smithson and J. D. Mollon, “Is the S-opponent chromatic sub-system sluggish?” Vis. Res. 44, 2919–2929 (2004).
[CrossRef]

2003

D. J. McKeefry, N. R. Parry, and I. J. Murray, “Simple reaction times in color space: the influence of chromaticity, contrast, and cone opponency,” Investig. Ophthalmol. Vis. Sci. 44, 2267–2276 (2003).
[CrossRef]

2001

H. C. Walkey, J. L. Barbur, J. A. Harlow, and W. Makous, “Measurements of chromatic sensitivity in the mesopic range,” Color Res. Appl. 26, S36–S42 (2001).
[CrossRef]

A. J. Anderson and A. J. Vingrys, “Multiple processes mediate flicker sensitivity,” Vis. Res. 41, 2449–2455 (2001).
[CrossRef]

H. Sun, J. Pokorny, and V. C. Smith, “Brightness induction from rods,” J. Vis. 1(1):4, 32–41 (2001).
[CrossRef]

H. Sun, J. Pokorny, and V. C. Smith, “Rod–cone interaction assessed in inferred magnocellular and parvocellular postreceptoral pathways,” J. Vis. 1(1):5, 42–54 (2001).
[CrossRef]

2000

F. Rieke and D. A. Baylor, “Origin and functional impact of dark noise in retinal cones,” Neuron 26, 181–186 (2000).
[CrossRef]

1999

J. Kremers and S. Meierkord, “Rod–cone-interactions in deuteranopic observers: models and dynamics,” Vis. Res. 39, 3372–3385 (1999).
[CrossRef]

1998

Y. He, A. Bierman, and M. Rea, “A system of mesopic photometry,” Lighting Res. Technol. 30, 175–181 (1998).
[CrossRef]

S. Weiss, J. Kremers, and J. Maurer, “Interaction between rod and cone signals in responses of lateral geniculate neurons in dichromatic marmosets (Callithrix jacchus),” Vis. Neurosci. 15, 931–943 (1998).
[CrossRef]

1997

B. B. Lee, V. C. Smith, J. Pokorny, and J. Kremers, “Rod inputs to macaque ganglion cells,” Vis. Res. 37, 2813–2828 (1997).
[CrossRef]

Y. He, M. Rea, A. Bierman, and J. Bullough, “Evaluating light source efficacy under mesopic conditions using reaction times,” J. Illum. Eng. Soc. 26, 125–138 (1997).

M. Gur, A. Beylin, and D. M. Snodderly, “Response variability of neurons in primary visual cortex (V1) of alert monkeys,” J. Neurosci. 17, 2914–2920 (1997).

G. Lange, N. Denny, and T. E. Frumkes, “Suppressive rod–cone interactions: evidence for separate retinal (temporal) and extraretinal (spatial) mechanisms in achromatic vision,” J. Opt. Soc. Am. A 14, 2487–2498 (1997).
[CrossRef]

B. Spehar and Q. Zaidi, “Surround effects on the shape of the temporal contrast-sensitivity function,” J. Opt. Soc. Am. A 14, 2517–2525 (1997).
[CrossRef]

1996

1995

O. Ukkonen, J. Rovamo, and R. Nasanen, “Effect of location and orientation uncertainty on rms contrast sensitivity with and without spatial noise in peripheral and foveal vision,” Optom. Vis. Sci. 72, 387–395 (1995).
[CrossRef]

1993

L. J. Croner, K. Purpura, and E. Kaplan, “Response variability in retinal ganglion cells of primates,” Proc. Natl. Acad. Sci. USA 90, 8128–8130 (1993).
[CrossRef]

R. Ratliff, “Methods for dealing with reaction time outliers,” Psychol. Bull. 114, 510–532 (1993).
[CrossRef]

P. Lennie, J. Pokorny, and V. C. Smith, “Luminance,” J. Opt. Soc. Am. A 10, 1283–1293 (1993).
[CrossRef]

1990

B. B. Lee, J. Pokorny, V. C. Smith, P. R. Martin, and A. Valberg, “Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers,” J. Opt. Soc. Am. A 7, 2223–2236 (1990).
[CrossRef]

K. Purpura, D. Tranchina, E. Kaplan, and R. M. Shapley, “Light adaptation in the primate retina: analysis of changes in gain and dynamics of monkey retinal ganglion cells,” Vis. Neurosci. 4, 75–93 (1990).
[CrossRef]

1987

1983

V. Virsu and B. B. Lee, “Light adaptation in cells of macaque lateral geniculate nucleus and its relation to human light adaptation,” J. Neurophysiol. 50, 864–878 (1983).

1982

J. L. Barbur, “Reaction-time determination of the latency between visual signals generated by rods and cones,” Ophthalmic Physiolog. Opt. 2, 179–185 (1982).
[CrossRef]

1979

M. J. Nissen, J. Pokorny, and V. C. Smith, “Chromatic information processing,” J. Exp. Psychol. Hum. Learn. Mem. 5, 406–419 (1979).
[CrossRef]

1977

M. J. Nissen and J. Pokorny, “Wavelength effects on simple reaction time,” Percept. Psychophys. 22, 457–462 (1977).
[CrossRef]

1973

J. D. Mollon and J. Krauskopf, “Reaction time as a measure of the temporal response properties of individual colour mechanisms,” Vis. Res. 13, 27–40 (1973).
[CrossRef]

R. J. Mansfield, “Latency functions in human vision,” Vis. Res. 13, 2219–2234 (1973).
[CrossRef]

1972

W. A. Rushton and D. S. Powell, “The rhodopsin content and the visual threshold of human rods,” Vis. Res. 12, 1073–1081 (1972).
[CrossRef]

U. T. Keesey, “Flicker and pattern detection: a comparison of thresholds,” J. Opt. Soc. Am. 62, 446–448 (1972).
[CrossRef]

1970

1969

1966

T. Wiesel and D. H. Hubel, “Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey,” J. Neurophysiol. 29, 1115–1156 (1966).

1964

D. H. Kelly, “Sine waves and flicker fusion,” Doc. Ophthalmol. 18, 16–35 (1964).
[CrossRef]

1960

J. Levinson, “Fusion of complex flicker II,” Science 131, 1438–1440 (1960).
[CrossRef]

1915

H. Woodrow, “Reaction to the cessation of stimuli and their nervous mechanism,” Psychol. Rev. 22, 423–452 (1915).
[CrossRef]

1914

H. Piéron, “Recherches sur les lois de variation des temps de latence sensorielle en fonction des intensités excitatrices,” L’Année Psychologique. 20, 2–96 (1914).

1886

W. Abney and E. R. Festing, “Colour photometry,” Phil. Trans. R. Soc. London 177, 423–456 (1886).
[CrossRef]

Abney, W.

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Y. J. He, M. Rea, A. Bierman, and J. Bullough, “Evaluating light source efficacy under mesopic conditions using reaction times,” in Iesna Annual Conference Proceedings Technical Papers (1996), pp. 236–257.

Rea, M. S.

Y. Akashi, M. S. Rea, and J. D. Bullough, “Driver decision making in response to peripheral moving targets under mesopic light levels,” Lighting Res. Technol. 39, 53–67 (2007).
[CrossRef]

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F. Rieke and D. A. Baylor, “Origin and functional impact of dark noise in retinal cones,” Neuron 26, 181–186 (2000).
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O. Ukkonen, J. Rovamo, and R. Nasanen, “Effect of location and orientation uncertainty on rms contrast sensitivity with and without spatial noise in peripheral and foveal vision,” Optom. Vis. Sci. 72, 387–395 (1995).
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H. Sun, L. Ruttiger, and B. B. Lee, “The spatiotemporal precision of ganglion cell signals: a comparison of physiological and psychophysical performance with moving gratings,” Vis. Res. 44, 19–33 (2004).
[CrossRef]

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K. Purpura, D. Tranchina, E. Kaplan, and R. M. Shapley, “Light adaptation in the primate retina: analysis of changes in gain and dynamics of monkey retinal ganglion cells,” Vis. Neurosci. 4, 75–93 (1990).
[CrossRef]

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G. D. Field, M. Greschner, J. L. Gauthier, C. Rangel, J. Shlens, A. Sher, D. W. Marshak, A. M. Litke, and E. J. Chichilnisky, “High-sensitivity rod photoreceptor input to the blue-yellow color opponent pathway in macaque retina,” Nat. Neurosci. 12, 1159–1164 (2009).
[CrossRef]

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G. D. Field, M. Greschner, J. L. Gauthier, C. Rangel, J. Shlens, A. Sher, D. W. Marshak, A. M. Litke, and E. J. Chichilnisky, “High-sensitivity rod photoreceptor input to the blue-yellow color opponent pathway in macaque retina,” Nat. Neurosci. 12, 1159–1164 (2009).
[CrossRef]

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[CrossRef]

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[CrossRef]

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J. Pokorny, H. Smithson, and J. Quinlan, “Photostimulator allowing independent control of rods and the three cone types,” Vis. Neurosci. 21, 263–267 (2004).
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Spehar, B.

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D. Cao, B. B. Lee, and H. Sun, “Combination of rod and cone inputs in parasol ganglion cells of the magnocellular pathway,” J. Vis. 10(2):11, 1–15 (2010).
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Taylor, J. A.

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K. Purpura, D. Tranchina, E. Kaplan, and R. M. Shapley, “Light adaptation in the primate retina: analysis of changes in gain and dynamics of monkey retinal ganglion cells,” Vis. Neurosci. 4, 75–93 (1990).
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Ukkonen, O.

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S. Weiss, J. Kremers, and J. Maurer, “Interaction between rod and cone signals in responses of lateral geniculate neurons in dichromatic marmosets (Callithrix jacchus),” Vis. Neurosci. 15, 931–943 (1998).
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A. Vassilev, A. Murzac, M. B. Zlatkova, and R. S. Anderson, “On the search for an appropriate metric for reaction time to suprathreshold increments and decrements,” Vis. Res. 49, 524–529 (2009).
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H. Sun, J. Pokorny, and V. C. Smith, “Brightness induction from rods,” J. Vis. 1(1):4, 32–41 (2001).
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Neuron

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J. Pokorny, H. Smithson, and J. Quinlan, “Photostimulator allowing independent control of rods and the three cone types,” Vis. Neurosci. 21, 263–267 (2004).
[CrossRef]

D. Cao, A. J. Zele, and J. Pokorny, “Chromatic discrimination in the presence of incremental and decremental rod pedestals,” Vis. Neurosci. 25, 399–404 (2008).
[CrossRef]

K. Purpura, D. Tranchina, E. Kaplan, and R. M. Shapley, “Light adaptation in the primate retina: analysis of changes in gain and dynamics of monkey retinal ganglion cells,” Vis. Neurosci. 4, 75–93 (1990).
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Figures (3)

Fig. 1.
Fig. 1.

Schematic of the spatial configuration used in the four experimental conditions A through D. In all conditions, the 2° diameter test field (2 photopic Td) is positioned at 7.5° temporal eccentricity and set within a 13° diameter surround field. Condition A: rod and cone excitations are equal in the center and surround fields. This is the control equiluminant condition. There are three additional conditions with variable levels of rod activity (B, C, D). Condition B: cone excitations are equal in the center and surround fields, but the surround has higher rod excitation than the center (+L-M=20% rod contrast; L+M+S and S=40% rod contrast). The surround rod contrast effect is determined by comparison of conditions A and B. Condition C: the dark surround generates maximum rod sensitivity outside the stimulus area to promote lateral rod–cone interactions. Condition D: cone-isolated RTs measured after offset of a bleach light during the cone plateau of the dark-adaptation curve. The effect of rod contrast in the surround is determined by comparing condition B with the control condition A. The effect of lateral rod–cone interaction is determined by comparison of condition C with condition D. The effect of the dark surround is determined by comparison of condition A with conditions C and D.

Fig. 2.
Fig. 2.

RT data for mesopic rod and cone signaling mediated via the inferred MC, PC, and KC pathways. All data were measured in condition A shown in Fig. 1. The left and right columns show the mean RT data (±SEM) for two observers measured on the equiluminant center and surround fields that were metameric to an (EES (upper row), had higher L/(L+M) (middle row) or higher S-cone excitation (lower row). The symbols specify the six photoreceptor excitation conditions: circles (L+M+S: variable cone luminance with a constant rod excitation and cone chromaticity); squares (L+M+S+R: variable rod and cone-mediated luminance with in phase modulation of rod and cone excitations and a constant cone chromaticity); asterisks (L-cone: variable L-cone excitation, therefore both cone chromaticity and luminance were changing, constant M, S, rod excitation); upward triangles (+L-M: variable l=L/(L+M), constant S, rod excitation, and constant cone luminance); downward triangles (S-cone: variable S-cone excitation, constant L, M, rod excitation, and constant cone luminance); diamonds (rod: variable rod excitation, constant L, M, S excitation therefore constant cone chromaticity and cone luminance). The solid lines show the best-fitting Piéron functions.

Fig. 3.
Fig. 3.

Effect of rod–cone interactions on cone-mediated luminance and chromatic RT. The left and right columns show the mean RT data (+SEM) for the two observers at the maximum stimulus contrast measured for the L+M+S stimulus (upper row), the +L-M stimulus (middle row) and the S-cone stimulus (lower row). Data are for the EES adapting chromaticity. The labels and schematics A through D identify the four experimental conditions defined in Fig. 1.

Tables (1)

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Table 1. Coefficient of Variation of the Luminance (L+M+S) and Chromatic (+L-M, S) RTs Measured on Light and Dark Surrounds

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