Color Discrimination with Broadband Photoreceptors

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Color Discrimination with Broadband Photoreceptors Christopher Schnaitmann, Christian Garbers, Thomas Wachtler, Hiromu Tanimoto  Current Biology  Volume 23, Issue 23, Pages 2375-2382 (December 2013) DOI: 10.1016/j.cub.2013.10.037 Copyright © 2013 Elsevier Ltd Terms and Conditions

Figure 1 Color Discrimination Learning in Drosophila (A) Composition of opsin types in pale and yellow ommatidia. Six outer photoreceptors (R1–R6; gray) express Rh1. R7 expresses Rh3 or Rh4, and R8 expresses Rh5 or Rh6, depending on the ommatidia class (pale or yellow). (B) Normalized spectral sensitivities of the different Rhodopsins in the Drosophila eye. Rh1 alone is maximally sensitive at 478 nm; an accessory pigment (UVAP) underlies the UV sensitivity of R1–R6 (gray). Data were adapted from [5]. (C) Emission spectra of LEDs used in behavioral experiments. (D–F) Visual discrimination learning of the fly. Conditioned stimuli, one of which is paired with a sugar reward, and test stimuli are depicted with three circles. (D) Wild-type flies show significant memory in the bright blue/bright green and in the intensity discrimination tasks (n = 9–18). (E) Flies choose the color cues despite 10-fold intensity mismatch between training and test (n = 16–20). (F) Flies show significant color learning despite the conflicting 10-fold intensity inversion between training and test (n = 15–16). Note that intensity learning would result in a negative learning index. Bars and error bars represent means and SEM, respectively. ∗∗p < 0.01; ∗∗∗p < 0.001; ns, no significance. See also Figure S1. Current Biology 2013 23, 2375-2382DOI: (10.1016/j.cub.2013.10.037) Copyright © 2013 Elsevier Ltd Terms and Conditions

Figure 2 Models of Color Opponent Processing Predict a Contribution of the Outer Photoreceptors to Color Discrimination Fits of models employing different combinations of color opponent signals (gray curves) to wavelength discrimination in Drosophila [20, 21]. Goodness of fit is measured by root-mean-square error corrected for the number of degrees of freedom (RMSE). (A) Standard model with opponent combinations of inner photoreceptor signals. (B) The model with the inner photoreceptors including “interommatidial” opponency (i.e., Rh3-Rh4 and Rh5-Rh6) fits slightly better than the standard model. (C) A model including outer receptor signals achieves a substantially better fit. Note that this model has the same number of parameters as the model in (B). Data points and error bars represent means and SEM, respectively. See also Figure S2. Current Biology 2013 23, 2375-2382DOI: (10.1016/j.cub.2013.10.037) Copyright © 2013 Elsevier Ltd Terms and Conditions

Figure 3 Targeted norpA Rescue Restores Photoreceptor Function (A) ERG traces to dark-blue stimulation of flies with targeted rescues of norpA using different rh-GAL4 drivers (n = 4–8 per genotype). For the rescue with rh3-GAL4 or without a driver, ERG traces in response to a UV LED (410 nm) or bright blue are plotted, respectively. (B) The norpA rescue in all photoreceptor types fully restores bright-blue/bright-green discrimination learning to the wild-type level, while norpA mutant flies containing the rescue construct without driver exhibit no significant discrimination (n = 9–17). (C) The choice of the rescue flies in all photoreceptors is based on color rather than intensity in the intensity inversion experiment (n = 12–20). Bars and error bars represent means and SEM, respectively. ∗∗p < 0.01; ∗∗∗p < 0.001; ns, no significance. See also Figure S3. Current Biology 2013 23, 2375-2382DOI: (10.1016/j.cub.2013.10.037) Copyright © 2013 Elsevier Ltd Terms and Conditions

Figure 4 Minimal Sets of Photoreceptors for Color Discrimination (A) norpA rescue flies with functional yellow, but not pale, ommatidia significantly discriminate bright blue and bright green (n = 10–17). (B) Bright-blue/bright-green discrimination of flies with pairwise norpA rescue in yellow ommatidia. Rescue flies with rh1-GAL4/rh4-GAL4 or rh4-GAL4/rh6-GAL4 show significant discrimination, while rescue flies with rh1-GAL4/rh6-GAL4 cannot discriminate the stimuli (n = 8–17). (C) norpA mutants with directed photoreceptor rescues in the intensity inversion task. Pairwise rescues with rh1-GAL4/rh4-GAL4 or rh4-GAL4/rh6-GAL4 show significant color preference rather than intensity preference as the wild-type or “yellow rescue” flies. Rescue flies with rh1-GAL4/rh6-GAL4 significantly choose the intensity cue (n = 12–30). For wild-type and norpA[7];UAS-norpA/+ in (A) and (C), the same data are plotted as in Figure 3. Bars and error bars represent means and SEM, respectively. ∗p < 0.05; ∗∗p < 0.01; ∗∗∗p < 0.001; ns, no significance. See also Figures S4 and S5. Current Biology 2013 23, 2375-2382DOI: (10.1016/j.cub.2013.10.037) Copyright © 2013 Elsevier Ltd Terms and Conditions

Figure 5 Lamina Monopolar Cells Are Required for Color Discrimination (A) L1, L2, and L3 receive direct input from the outer photoreceptors R1–R6 and convey their signals to different layers in the medulla. Outputs of inner and outer receptors can converge in the medulla as well as in the downstream lobula complex. Cells labeled by the GAL4 drivers used in the blocking experiments are colored with dark orange or light orange or red outline (Dm8, distal medulla cell type; Mt, medulla tangential cell type; Pm, proximal medulla cell type). (B) Blocking L1–L3 and Dm8 with Shits1 and ortC2-GAL4 specifically impaired bright-blue/bright-green discrimination (n = 13–18). (C) Intensity discrimination is not impaired with the same blockade (n = 15–16). (D) Blocking DM8 and a few L1 cells with splitGAL4 driver vglut∩ortC2-GAL4 does not significantly impair bright-blue/bright-green discrimination (n = 12–19). (E) Bright-blue/bright-green discrimination is significantly impaired by blocking L1, L2, and two other cell types with R48A08-GAL4 (n = 8–13). (F) Intensity discrimination is not impaired with the same blockade (n = 17–23). Bars and error bars represent means and SEM, respectively. ∗∗p < 0.01; ∗∗∗p < 0.001; ns, no significance. Current Biology 2013 23, 2375-2382DOI: (10.1016/j.cub.2013.10.037) Copyright © 2013 Elsevier Ltd Terms and Conditions