Knorr AG et al. (2021), Image motion with color contrast suffices to el...

XB-ART-58021

Sci Rep 2021 Apr 19;111:8445. doi: 10.1038/s41598-021-87835-2.

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Image motion with color contrast suffices to elicit an optokinetic reflex in Xenopus laevis tadpoles.

Knorr AG , Gravot CM , Glasauer S , Straka H .

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The optokinetic reflex is a closed-loop gaze-stabilizing ocular motor reaction that minimizes residual retinal image slip during vestibulo-ocular reflexes. In experimental isolation, the reflex is usually activated by motion of an achromatic large-field visual background with strong influence of radiance contrast on visual motion estimation and behavioral performance. The presence of color in natural environments, however, suggests that chromatic cues of visual scenes provide additional parameters for image motion detection. Here, we employed Xenopus laevis tadpoles to study the influence of color cues on the performance of the optokinetic reflex and multi-unit optic nerve discharge during motion of a large-field visual scene. Even though the amplitude of the optokinetic reflex decreases with smaller radiance contrast, considerable residual eye movements persist at the 'point of equiluminance' of the colored stimuli. Given the color motion preferences of individual optic nerve fibers, the underlying computation potentially originates in retinal circuits. Differential retinal ganglion cell projections and associated ocular motor signal transformation might further reinforce the color dependency in conceptual correspondence with head/body optomotor signaling. Optokinetic reflex performance under natural light conditions is accordingly influenced by radiance contrast as well as by the color composition of the moving visual scene.

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Species referenced: Xenopus laevis
Genes referenced: plin1

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	Figure 1. Color patterns and wavelength spectrum of large-field visual motion stimuli. (A) Schematics of color motion stimuli with black–white (A1), black–blue (A2), black–red (A3) and red–blue (A4) vertical stripes that were projected onto a cylindrical screen around the centered semi-intact preparation of a Xenopus tadpole. (B) Spectra of white, black, blue and red light emitted by the projectors at maximal intensity. (C) Graph depicting the method to identify the point of equiluminance; note that the intensity of the blue stripes was held constant, whereas the intensity of the red stripes was gradually altered. Figure assembled with Affinity Designer (version 1.8.3).
	Figure 2. Color information contributes to large-field visual motion-induced eye movements of semi-intact preparations of Xenopus tadpoles. (A) Representative movements of the left (le) and right (ri) eye (position, black traces) evoked by alternating motion of a red-blue vertical striped pattern at constant velocity (± 10°/s; red trace). (B) Typical examples of eye movements in a given preparation (position, black traces) evoked by alternating motion of a black–white, black–blue, black–red and red–blue vertical striped pattern (see color-code) at constant velocity (± 10°/s; red traces). (C) Individual (grey traces) and averaged (black trace; n = 34) normalized OKR amplitudes evoked by a red-blue vertical striped motion pattern as function of the radiance of the red stripes; the inset illustrates a typical example of residual eye movements at the POE. (D) Bar plot depicting the response amplitude evoked by chromatic stimuli (CR) at the POE, determined individually for each animal, and control baseline amplitude (Grey). **, p < 0.01 (paired t-test). Figure assembled with Affinity Designer (version 1.8.3).
	Figure 3. Color-dependent differential OKR performance of semi-intact preparations of Xenopus tadpoles. (A) Bar plot depicting the relative OKR amplitude for large-field visual motion stimuli with different color combinations; note the larger responses when black stripes were paired with blue or red compared to black–white stripes; ***, p < 0.0001 (n = 34; Mann–Whitney U-test). (B) Scatter plot depicting relative chromatic response (OKR amplitude at POE; see “Methods”) magnitudes (n = 34 animals) as function of the difference in amplitude between the conditions: red–black and white–black (B1) and blue–black and white–black (B3); (B2) illustrates the difference in response magnitudes between blue–black and white–black (x-axis) and red–black and white–black (y-axis); despite the mathematical coupling, there is a significant correlation between blue/white and red/white response magnitudes (expected correlation due to coupling: ρ = 0.48). Figure assembled with Affinity Designer (version 1.8.3).
	Figure 4. Retinal ganglion cell spike discharge during visual image motion stimulation with different color combinations in isolated optic nerves—eyes of Xenopus tadpoles. (A) Representative multi-unit spike discharge of the optic nerve in response to large-field visual motion stimulation with a black–white striped vertical pattern (red trace); the trace on the right is a magnified view of a single motion cycle (grey area) of the trace on the left; note the bidirectional velocity sensitivity (red arrow heads). (B) Raster plot of spike trains of four isolated individual units with different radiance or color preferences; units respond preferentially to high radiance contrast (unit 1), to blue or red versus black (unit 2) or to red or blue stimulus combinations (units 3 and 4). (C) Bar plot depicting relative spike counts of all isolated units (n = 25) during visual motion stimulation with different color combinations (icons on top). (D) Histogram of color preferences of n = 25 individual retinal ganglion cell units (RGC, blue). Negative color preference indicates preferential responses to achromatic stimuli, positive values indicate larger responses to single-colored visual motion. Red and yellow curves depict distributions from Gaussian mixture models with one (red, M1) or two (yellow, M2) components fitted to the data. (E) Peri-stimulus time histogram of the average spike discharge (200 ms bin width) over a single image motion cycle at 0.125 Hz (8 s) of two single units (E1,E2) at the POE; note the residual directional response of the unit in (E1); red sinusoids represent stimulus cycles. Figure assembled with Affinity Designer (version 1.8.3).
	Figure 5. Peri-stimulus time histogram of retinal ganglion cell activity in isolated optic nerves—eyes of Xenopus tadpoles. (A–D) Peri-stimulus time histogram of the average spike discharge (200 ms bin width) over a single image motion cycle at 0.125 Hz (8 s) of the four units with different radiance or color preferences depicted in Fig. 4B as units 1–4; units respond preferentially to high radiance contrast (A), to blue or red versus black (B) or to red or blue stimulus combinations (C,D); black/white and color stripe combinations are indicated by the icons above the top row; red sinusoids represent stimulus cycles. Figure assembled with Affinity Designer (version 1.8.3).

References [+] :

Beck, Instrumentation for measuring oculomotor performance and plasticity in larval organisms. 2004, Pubmed, Xenbase