Speed, spatial, and temporal tuning of rod and cone vision in mouse - PubMed (original) (raw)

Speed, spatial, and temporal tuning of rod and cone vision in mouse

Yumiko Umino et al. J Neurosci. 2008.

Abstract

Rods and cones subserve mouse vision over a 100 million-fold range of light intensity (-6 to 2 log cd m(-2)). Rod pathways tune vision to the temporal frequency of stimuli (peak, 0.75 Hz) and cone pathways to their speed (peak, approximately 12 degrees/s). Both pathways tune vision to the spatial components of stimuli (0.064-0.128 cycles/degree). The specific photoreceptor contributions were determined by two-alternative, forced-choice measures of contrast thresholds for optomotor responses of C57BL/6J mice with normal vision, Gnat2(cpfl3) mice without functional cones, and Gnat1-/- mice without functional rods. Gnat2(cpfl3) mice (threshold, -6.0 log cd m(-2)) cannot see rotating gratings above -2.0 log cd m(-2) (photopic vision), and Gnat1-/- mice (threshold, -4.0 log cd m(-2)) are blind below -4.0 log cd m(-2) (scotopic vision). Both genotypes can see in the transitional mesopic range (-4.0 to -2.0 log cd m(-2)). Mouse rod and cone sensitivities are similar to those of human. This parametric study characterizes the functional properties of the mouse visual system, revealing the rod and cone contributions to contrast sensitivity and to the temporal processing of visual stimuli.

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Figures

Figure 1.

Figure 1.

CSFs of C57BL/6J mice for rotating sine-wave gratings measured over a wide range of background light intensities. A, Spatial CSFs measured at a fixed temporal frequency of 1.5 Hz for which the mice are maximally sensitive (peak in B). The 1.5 Hz frequency was maintained by adjusting the speed of the rotating grating according to the relationship ft = sp fs. Equation 2 calculated the curves for background intensities 1.8 and −6.5 log cd m−2 using the parameters in Table 1. The curves for −2.7 and −5.4 log cd m−2 were calculated with Equation 2 using parameters adjusted for best fit (_R_2 > 0.8). B, Temporal CSFs measured at a fixed spatial frequency of 0.128 cycles/° for which the mice are maximally sensitive (peak in A). Experimental limitations precluded measurements of responses to frequencies >6 Hz. C, Spatial contrast sensitivity as a function of background illumination for the sine-wave grating parameters (arrows; fs = 0.128 cycles/°; ft = 1.5 Hz) that yielded maximal sensitivity at the highest intensity tested (1.8 log cd m−2). A background intensity of −6.0 log cd m−2 is equivalent to 0.001 photoisomerizations rod−1 s−1. NR, No optomotor response.

Figure 2.

Figure 2.

Photopic contrast sensitivity of C57BL/6J mice (light intensity, 1.8 log cd m−2). A, Family of spatial CSF measured at seven temporal frequencies (legend). B, Family of temporal CSF measured at seven spatial frequencies (legend). C, Family of spatial CSF measured at five speeds of rotation. D, Family of speed CSF measured at the same spatial frequencies as in B. Note that sensitivity is tuned to the speed of 15°/s. Continuous lines are calculated with Equation 2 and parameter values listed in Table 1; _R_2 > 0.86 in all plots (n = 4 mice). NR, No optomotor response.

Figure 3.

Figure 3.

Scotopic CSFs for C57BL/6J mice (light intensity, −4.5 log cd m−2). A, Family of spatial CSFs measured at six temporal frequencies (legend). B, Family of temporal CSFs measured at five spatial frequencies (legend) shows that sensitivity is tuned to temporal frequency of 0.75 Hz. C, Family of spatial CSFs measured at five speeds of rotation. D, Family of speed CSFs measured at the same spatial frequencies as in B. Continuous lines are sensitivity functions calculated with Equation 2 and parameter values listed in Table 1; _R_2 > 0.9 (n = 8 mice). NR, No optomotor response.

Figure 4.

Figure 4.

Normalized CSFs for photopic (A, B) and scotopic (C, D) illumination conditions. The fitted continuous curves are used to estimate the parameters in Table 1 (see Appendix). A, Spatial CSF at the same rotation speeds as in Figure 2_C_ and fitted with Equation A8; R_2 = 0.91 (n = 4). B, Speed CSF for the fixed spatial frequencies in Figure 2_D and fitted with Equation A9; R_2 = 0.9 (n = 4). C, Spatial CSF at the temporal frequencies in Figure 3_A and fitted with Equation A2; _R_2 = 0.85 (n = 8). D, Temporal CSF at four spatial frequencies and fitted with Equation A3; _R_2 = 0.98 (n = 8).

Figure 5.

Figure 5.

Speeds eliciting maximal contrast sensitivity plotted as a function of spatial frequency of the rotating sine-wave pattern under photopic (1.8 log cd m−2) and scotopic (−4.5 log cd m−2) illumination conditions. Equation 2 calculated the continuous and broken lines using the parameters in Table 1. The speed eliciting the maximal sensitivity was determined by fitting the (normalized) speed CSFs with the product of Equations A9 and A10 after substituting ft = sp fs for each mouse under photopic conditions. Likewise, for scotopic conditions, we determined the speed for maximum sensitivity by fitting the (normalized) speed CSFs with the product of Equations A3 and A4.

Figure 6.

Figure 6.

Comparison of CSFs for knock-out and control mice under photopic and scotopic conditions. A, Spatial CSFs for C57BL/6J mice (filled symbols and continuous curves) and for _Gnat1_−/− mice (unfilled symbols) measured for three temporal frequencies under bright photopic conditions of 1.8 log cd m−2. B, Temporal CSFs for C57BL/6J and _Gnat1_−/− mice for three spatial frequencies. Gnat2cpfl-3 mice did not respond under the photopic conditions (NR, red triangles). C, Temporal CSFs for Gnat2cpfl-3 (red triangles) and their control ALR/LtJ albino mice (gray circles) measured under scotopic conditions (−4.5 log cd m-2). _Gnat1_−/− mice did not respond (NR, white circles). Spatial frequency is 0.031 cycles/°. Red curve through the red triangles is calculated with Equation 2 using the following parameters: fto = 0.4 Hz, fso = 0.03 cycles/°, fsp = 80°/s, and k = 23 Hz−1. The black curve in C and all curves in A and B were calculated with the parameters in Table 1.

Figure 7.

Figure 7.

Spatial contrast sensitivity of rod (Gnat2cpfl-3), cone (_Gnat1_−/−) and rod–cone (C57BL/6J) vision mice plotted as a function of background intensity. A, Comparison of the sensitivities of three genotypes for a grating visible under both scoptopic and photopic conditions (fs = 0.031 cycles/°; ft = 0.4 Hz). B, Comparison of contrast sensitivities for a grating under photopic conditions (fs = 0.383 cycles/°; ft = 3 Hz). NR, No optomotor response. Top abscissa indicates the photoisomerizations rod−1 s−1, accounting for pupil contraction (Pennesi et al., 1998).

Figure 8.

Figure 8.

Schematic diagram of the linear model indicating the shift in tuning preference under photopic (A) and scotopic (B) conditions. Contour plots of the contrast sensitivities of wild-type C57BL/6J mice computed with Equation 2 for rotating gratings of different spatial and temporal frequencies under photopic (C, E) and scotopic (D, F) conditions (Table 1 parameters). Color scale from blue to orange encodes contrast sensitivity from low to high. White lines plot maximal sensitivities at constant temporal (dashed) and spatial (continuous) frequencies in C and D and maximal sensitivities at constant speed (dashed) and spatial frequency (continuous) in E and F.

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