Hunt JE et al. (2020), An Innate Color Preference Displayed by Xenopus...

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Front Behav Neurosci 2020 May 12;14:71. doi: 10.3389/fnbeh.2020.00071.

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An Innate Color Preference Displayed by Xenopus Tadpoles Is Persistent and Requires the Tegmentum.

Hunt JE , Bruno JR , Pratt KG .

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Many animals, especially those that develop externally, are equipped with innate color preferences that promote survival. For example, Xenopus tadpoles are known to phototax most robustly towards mid-spectrum ("green") wavelengths of light while avoiding shorter ("blue") wavelengths. The innate preference to phototax towards green likely promotes survival by guiding the tadpoles to green aquatic plants-their source of both food and safety. Here, we characterize the dynamics and circuitry that give rise to this intriguing hard-wired behavior. Using a novel open-field experimental paradigm we found that free-swimming tadpoles indeed spend most of their time in the green portion of the test dish, whether green is pitted against white (brighter than green) or black (darker than green). This preference was modest yet incredibly persistent over time, which, according to the shell game model of predator-prey interactions, minimizes being found by the predator. Furthermore, we found that this innate preference for the color green was experience-independent, and manifested mainly via profoundly slower swimming speeds while in the green region of the test dish. Ablation experiments showed that, at the circuit level, the color-guided swimming behavior requires the tegmentum, but not the optic tectum (OT). Lastly, we determined that exposing tadpoles to the selective serotonin reuptake inhibitor (SSRI) trazodone switched the tadpoles' preference from color-based to luminance-based, implicating two distinct visual circuits in the tadpole, one that is associated with color-driven behaviors, another associated with luminance-driven behaviors.

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Species referenced: Xenopus
Genes referenced: pigy slc12a3

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	Figure 1. Tadpoles spend significantly more time in the green region of test dish when green is pitted against either white (brighter than green) or black (darker than green). (A) Experimental design: 1/4th of the floor of the test dish, the region of interest (ROI), is colored either green (shown here), blue, or red. The colors are approximately equiluminant. Ten tadpoles are transferred into the dish and videotaped for either 1 h or 30 min as they swim freely around the dish, and videos are analyzed off-line. (B) Bar graph showing the average number of tadpoles residing for different colored ROIs, pitted against black or white (*p < 0.05). The dashed line represents the percentage of tadpoles expected to be in the ROI if no preference. (C) Normalized frequency (Y-axis) of observing a given number of tadpoles in a given ROI (X-axis). (D) Plot showing the average number of tadpoles (out of 10 total) in the green quadrant at each minute, across 60 min. Notice that the average strength of preference for the green quadrant is modest yet stable over time, and is established by minute 2 of the trial. The trace/function represents 18 trials. The dashed line represents the average number of tadpoles expected to be in the green quadrant, at any given point in time, if no preference.
	Figure 2. Tadpoles swim slower in the green region of the test dish. (A, far left) Schematic showing the arbitrary white quadrant used for quantifying swimming speeds in the white region; (right) dot plot of swimming speeds while in the white and green region of the test dish (***p < 0.001). Each dot represents the recorded speed of an individual tadpole. (B) Merged video frames showing (left and middle panels) single tadpoles slowing down upon entering the green region of the dish, and (right) a tadpole speeding upon swimming out of the green and into the white region. The faster the tadpole is swimming, the greater distance traveled between frames and visa versa. (C) Dot plot showing the number of times a given tadpole entered a designated white quadrant of the dish, and the number of times they entered the green quadrant (ns = not significant). The probability of freely-swimming tadpoles to enter the green quadrant of the dish is not statistically different from the probability of their moving into a designated white quadrant.
	Figure 3. Ablation studies indicate that the preference for the green region of the dish requires the tegmentum but not the OT. (A) Overhead view of stage 48 tadpole brain. OT (region inside black square) is a major component of the amphibian midbrain; the blue horizontal line indicates the approximate position along the rostrocaudal axis at which the OT is most extensive. The tegmentum resides directly ventral to this region of the OT, and so is not visible in this image. OB, olfactory bulb; OT, optic tectum; R, rostral; C, caudal. (B, schematic) Cross-section of this region. The dorsal optic tectum and ventral tegmentum are separated in space by the large MV. For optic tectum ablations, the pipette is advanced at an oblique angle to ablate specifically the OT; (B, micrograph) cross-section showing an ablated tectal lobe. D, Dorsal; MV, Middle Ventricle; TSC, torus semicircularis; Teg, Tegmentum. (C, schematic) Cross-section showing that for tegmentum ablations, the pipette is advanced at a steeper angle. (C, micrograph) Cross-section showing an ablated tegmentum. The dashed-line-enclosed regions are the regions that have been ablated. Here, only one hemisphere is ablated to readily compare â€œnormalâ€ and â€œablatedâ€ structures. For the experiments, both hemispheres are ablated. Red vertical lines on the schematics indicate the midline. Scale bar = 100 Î¼m for both images. (D) Bar graph summarizing the effects of dark-rearing, tectal ablation, and tegmental ablation (*p < 0.05). Only the tegmental-ablated show a significant loss in preference for green compared to controls. (E) Dot plots showing swimming speeds of tegmentum-ablated tadpoles while in the white and green region of the test dish, and speeds of control tadpoles in an all-white dish. Each dot represents an individual tadpoleâ€™s swimming speed. Notice that average swimming speeds for tegmental-ablated tadpoles are similar across the green and white test dish, and are also similar to swimming speeds of control tadpoles in an all-white dish.
	Figure 4. Exposing Xenopus tadpoles to the selective serotonin reuptake inhibitor (SSRI) trazodone switches the preference for the green region of the dish to the brightest region of the dish, regardless of color. (A) A schematic of the green vs. white test and corresponding dot plot showing the average percentage of tadpoles in the green region as a function of trazodone concentration (p < 0.01, p < 0.001). Each connected set of symbols represents the average values for a given clutch. The overall average (shown in black) represents the data obtained from seven different clutches of tadpoles. Acute exposure to trazodone (light green diamonds) and chronic exposure (gray-ish green circles) appeared to elicit the same effect. (B) Four of the seven clutches tested in the green vs. white test (shown in panel A) were also tested in the green vs. black test (p < 0.05). These data are also displayed as a dot plot showing the average percentage of tadpoles in the green region as a function of trazodone concentration.

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