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Research ArticleNew Research, Cognition and Behavior

Visual Temporal Contrast Sensitivity in the Behaving Mouse Shares Fundamental Properties with Human Psychophysics

Yumiko Umino, Rose Pasquale and Eduardo Solessio
eNeuro 30 July 2018, 5 (4) ENEURO.0181-18.2018; https://doi.org/10.1523/ENEURO.0181-18.2018
Yumiko Umino
Department of Ophthalmology, Center for Vision Research, SUNY Upstate Medical University, Syracuse, New York 13210
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Rose Pasquale
Department of Ophthalmology, Center for Vision Research, SUNY Upstate Medical University, Syracuse, New York 13210
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Eduardo Solessio
Department of Ophthalmology, Center for Vision Research, SUNY Upstate Medical University, Syracuse, New York 13210
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  • Figure 1.
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    Figure 1.

    An operant behavior assay to determine temporal contrast sensitivity in the mouse. A, Layout of the experimental chamber used to measure TCS in mice with an operant behavior assay. B, Testing paradigm (for details, see Materials and Method). C, Performance scoring table. D, E, Probability of Hit versus FA for two different mice (WT14 and WT15) measured over the course of 5 successive days in response to 50% (open symbols) and 90% (closed symbols) contrast flicker and mean background illumination producing ∼8200 ph/s/μm2 at the retina (Table 1, light calibration details). Each symbol represents the Hit vs FA pair for 100 trial blocks measured during a daily session. A total of four blocks was measured in each session. Error bars indicate representative 95% intervals (estimated as per Macmillan and Creelman, 2005). In gray are ROC curves for d´ = 0, 1, 2, and 3, respectively. In black are ROC curves for d´ = 0.45 and 1.68 in D and d´ = 0.75 and 1.94 in E fitting Hit vs FA pairs for 50% and 90% contrast, respectively.

  • Figure 2.
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    Figure 2.

    Values of d´ were stable during daily sessions. A, Hit vs FA pairs for four WT mice measured on different days clustered about the ROC curves implied by the pooled value of d´. Stimulus conditions (flicker frequency, contrast, illuminance at the cornea, and retinal illumination) for WT56, WT57, and WT59 were as follows: 12 Hz, 50%, 3000 ph/s/μm2; for WT69, 21 Hz, 40%, 8200 ph/s/μm2. The values of d´ for each mouse were: WT57, 0.65; WT59, 1.18; WT56, 1.32; and WT69, 1.63, respectively. For comparison, ROC curves for d´ = 0 (main diagonal), 1, 2, and 3 are also shown (gray ROC curves, rising in order away from the main diagonal). The negative diagonal (dashed line) indicates unbiased behavior. Open symbols, Hit vs FA pairs every 100 trials; closed symbols, daily totals (400 trials). B, Values of d´ for the corresponding 100 trial blocks (estimated with Eq. 1; Materials and Methods). C, Changes in response bias expressed in terms of criterion location (Eq. 2; Materials and Methods). Note that for clarity purposes some of the symbols have been displaced laterally.

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    Figure 3.

    No significant long-term trends in d´. A, d´ values varied from day to day about a steady mean. d´ values of two C57BL/6J mice (WT) and two mice GNAT2 cpfl3 (G2) over the course of 10–12 consecutive days. The daily experimental sessions consisted of 100 trials in response to sinusoidal flicker stimulation. Individual contrast levels were adjusted during a pretrial run to elicit a d´ = 2 and were kept constant thereafter. Continuous lines represent linear regression fits (see text). The histograms at the right of each plot show the distribution of average d´ values estimated by sampling with replacement (n = 400 bootstrap samples) of the data in the respective plots. Flicker parameters were 21 Hz presented on a background illuminance level producing an estimated retinal irradiance of 8200 ph/s/μm2. B, Corresponding values of CL. Continuous lines represent the zero (unbiased behavior) axis.

  • Figure 4.
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    Figure 4.

    d´ is a bias-free measure of temporal contrast sensitivity in mice. A, ROCs implied by d´ can predict empirical data. Empirical ROC curves of three mice (two WT mice and one GNAT2 cpfl3 mouse labeled WTY, WTR, and G2Y, respectively) determined by varying the reward schedules. Mice were first tested with 100%:100% reward schedules, and successively with 100%:70% and 100%:50% reward schedules, or alternatively, with 70%:100% and 50%:100% reward schedules. Open symbols indicate daily pHit and pFA pair values, closed symbols represent the average ± SEM, n = 5-6 trials. The data are well fit by the model: d´ = z(pHit) − z(pFA), where z(pHit) and z(pFA) are the z score values (in SD units) of pHits and pFA. Model predictions are illustrated by the continuous ROCs with maximum likelihood predicted d´ values of 1.66 (WTY), 2.49 (WTR), and 1.73 (G2Y; Table 2). For reference, ROCs for d´ = 0, 1, 2, and 3 are indicated in gray. B, Same as in A, but plotted on z-coordinates. Note that in these coordinates the ROCs have unitary slopes, which is consistent with the notion that d´ sensitivity estimates do not depend on the location of the decision criteria (Macmillan and Creelman, 2005). C, CL derived from the empirical ROC curves decreases linearly with the logarithm of the reward schedule ratio. Continuous black lines indicate regression fits (R 2 > 0.9) with Equation 5, and q values of 1.75 (WTY), 2.4 (WTR), and 1.4 (G2Y).

  • Figure 5.
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    Figure 5.

    Linear psychometric functions and determination of empirical thresholds. A, Top, Representative set of PFs for a WT mouse measured on different days. Flicker stimulus parameters were 18 Hz flicker and a mean irradiance level of 3000 ph/s/μm2. The contrast range sampled was 35–60% in 5% intervals. Linear regression parameters were cTH = 31%, slope = 0.068 d´/% contrast, R 2 = 0.58, p < 0.001. Bottom, Scatter plot of the residuals. Consistent with linearity. we did not observe any bends, thinning, or thickening in the scatter of the residuals. B, Linear fits of the PFs in A. The respective cTh values were determined at the point where the extrapolated lines intersect the line defined by d´ = 1. In this dataset, threshold values ranged from 20% to 35% contrast. C, Family of PFs measured from a WT mouse in response to flickering lights at the indicated frequencies. The mean retinal irradiance was 8200 ph/s/μm2. Each PF represents the cumulative average of two to three measurements. Linear regression (R 2 > 0.70) was applied to determine the slope and empirical threshold where each PF intersects the line defined by d´ = 1. D, Slopes of PFs do not change with flicker frequency. The plot shows slopes of PFs vs frequency for five different mice at mean background light levels delivering 8200 ph/s/μm2. The slope of the PFs remains constant and does not change with frequency (linear regression, p = 0.8). E, Slopes of PFs are constant over the mesopic range. The plot compares the mean values of the PF slopes measured at 8200 (black circles), 440 (red triangles), and 9.2 (green squares) ph/s/μm2. Note that mice do not respond to flicker frequencies >24 Hz when exposed to 440 ph/s/μm2, or >12 Hz when exposed to 9.4 ph/s/μm2. Pairwise comparisons at 3, 6, and 12 Hz reveal no significant differences in mean slope values (two-way RM ANOVA, Holm–Sidak method, α = 0.05). Symbols represent the average ± SEM (n = 5). Note that for clarity purposes some of the symbols have been displaced laterally. F, cTh_SEM values estimated from cumulative averages of two (circles) or three (triangles) PFs using bootstrapping techniques and plotted as a function of cumulative R 2. Box plot indicates distribution quartiles for cumulative R 2 > 0.70 (indicated with gray arrow in plot).

  • Figure 6.
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    Figure 6.

    Contrast thresholds decrease with mean irradiance. A–C, Empirical thresholds of WT mice measured as a function of flicker frequency determined at three different background illumination levels, dim (9.2 ph/s/μm2 at the retina; A), intermediate (440 ph/s/μm2; B), and bright (8200 ph/s/μm2; C). The contrast thresholds for each mouse were determined from families of psychometric functions, as defined in Figure 5C. Note that for clarity purposes some of the symbols have been displaced laterally. D–F, Corresponding TCSFs estimated from the contrast threshold functions in A–C.

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    Figure 7.

    Mouse TCSFs have classic properties of human TCSFs. A, CFF increases with irradiance. Statistical analysis: RM ANOVA, significant differences between groups, #p < 0.001, *p < 0.05, with Bonferroni method. Symbols represent the average ± SEM (n = 3–5; for values, see Fig. 7-1). Linear fit represents predictions according to the Ferry–Porter law (see text for details). B, Comparison of average mouse TCSFs in Figure 6D–F at indicated irradiance levels. Statistical analysis: two-way RM ANOVA, #p < 0.001; *p < 0.05, comparisons for factor irradiance at 8200 vs 9.2 and 8200 vs 440 ph/s/μm2 are indicated with black and red symbols, respectively, using the Holm–Sidak method (see text for details). Symbols represent the average ± SEM (n = 5; for values, see Fig. 7-1). C, Human temporal contrast sensitivity functions adapted from Kelly (1961) illustrate the classic properties of adaptation to increasing illuminance levels (see text). Retinal illuminance levels for each function are indicated in Trolands (Td) and can be converted to equivalent rates of photoisomerization by applying the conversion relation previously established for primates wherein 1 Td = 11 R*/rod/s (Hood et al., 1999).

Tables

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    Table 1.

    Corneal illumination, pupil size, and corresponding retinal irradiance

    Corneal irradianceat 500 nm (ph/s/μm2)Photopic corneal illumination (p lux)Scotopic corneal illumination (s lux)Pupil area (mm2)Retinal irradianceat 500 nm (ph/s/μm2)Rate of isomerizations per rod (R*/rod/s)
    WTG2WTG2WTG2
    460,00047.43090.330.4382001100072009600
    48,0004.932.21.121.643000440026003800
    50000.513.361.581.48440410380360
    540.00550.03633.093.859.21.1810
    DarkDarkDark3.723.83NANANANA
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    Table 2.

    Best fitting parameters for the estimated ROC curves of three different mice shown in Figure 4A–C

    ParameterWTYG2YWTR
    d´1.661.732.49
    d´ SE0.0660.070.08
    SD ratio1.030.791.02
    SD/SE ratio0.150.150.24
    Goodness-of-fit p value0.060.080.1
    Ratio SD different from 1 p value0.840.140.91
    Convergence ratio800/800800/800800/800
    • d´SE = SE of d´; ratio SD = ratio of signal (flicker) to noise (nonflicker) SDs; convergence ratio = number of simulations that converged to total number of simulations.

Movies

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  • Movie 1.

    Short clip showing the behavioral responses of a mouse during a typical test session. The flicker test consisted of a sinusoidally varying full-field illumination superimposed on the steady adapting light. Stimulus variables were mean illuminance of 309 s lux delivering an estimated 8200 ph/s/μm2 at the retina, temporal frequency of 18 Hz, and 70% contrast. Presentation of flicker vs nonflicker stimuli in a trial was chosen randomly and with equal probabilities of 0.5. The mouse was trained to visit the left nose-poke port (near the bottom of the image) when it detects flicker, and the right nose-poke port in response to nonflicker stimulus. Output variables were the number of Hits (correctly reporting presence of flicker), FAs (report flicker when nonflicker presented), Misses (report nonflicker when flicker presented), and CRs (correctly reporting presence of nonflicker), as indicated by score table on the top of the video. See main text for details. The mouse was rewarded after each correct response (Hits and CRs) with a small amount of Ensure pumped into the reward tray. The activation of the pump during delivery can be heard in the audio track. Download Table 2-1, PDF file.

Extended Data

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  • Figure 7-1

    Extended data legend. Download Figure 7-1, PDF file.

  • Table 1-1

    Temporal contrast sensitivity vs temporal frequency. Download Table 1-1, PDF file.

  • Table 2-1

    Critical flicker frequency vs retinal irradiance. Download Table 2-1, PDF file.

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eneuro: 5 (4)
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July/August 2018
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Visual Temporal Contrast Sensitivity in the Behaving Mouse Shares Fundamental Properties with Human Psychophysics
Yumiko Umino, Rose Pasquale, Eduardo Solessio
eNeuro 30 July 2018, 5 (4) ENEURO.0181-18.2018; DOI: 10.1523/ENEURO.0181-18.2018

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Visual Temporal Contrast Sensitivity in the Behaving Mouse Shares Fundamental Properties with Human Psychophysics
Yumiko Umino, Rose Pasquale, Eduardo Solessio
eNeuro 30 July 2018, 5 (4) ENEURO.0181-18.2018; DOI: 10.1523/ENEURO.0181-18.2018
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Keywords

  • forced-choice design
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  • operant behavior
  • temporal contrast sensitivity
  • theory of signal detection

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