The archerfish uses motor adaptation in shooting to correct for changing physical conditions

Abstract

The archerfish is unique in its ability to hunt by shooting a jet of water from its mouth that hits insects situated above the water's surface. To aim accurately, the fish needs to overcome physical factors including changes in light refraction at the air-water interface. Nevertheless, archerfish can still hit the target with a high success rate under changing conditions. One possible explanation for this extraordinary ability is that it is learned by trial and error through a motor adaptation process. We tested this possibility by characterizing the ability of the archerfish to adapt to perturbations in the environment to make appropriate adjustments to its shots. We introduced a perturbing airflow above the water tank of the archerfish trained to shoot at a target. For each trial shot, we measured the error, i.e., the distance between the center of the target and the center of the water jet produced by the fish. Immediately after the airflow perturbation, there was an increase in shot error. Then, over the course of several trials, the error was reduced and eventually plateaued. After the removal of the perturbation, there was an aftereffect, where the error was in the opposite direction but washed out after several trials. These results indicate that archerfish can adapt to the airflow perturbation. Testing the fish with two opposite airflow directions indicated that adaptation took place within an egocentric frame of reference. These results thus suggest that the archerfish is capable of motor adaptation, as indicated by data showing that the fish produced motor commands that anticipated the perturbation.

Keywords: Snell's law; adaptation; archerfish; neuroscience; toxotes.

Figure 1.. The archerfish needs to correct for physical factors in shooting.

The viewing angle of a target above the water level is shifted toward the zenith due to Snell’s law. The fish needs to correct for this shift to hit the target in its actual position. The jet itself is affected by gravity and it does not proceed straight from the fish’s mouth to the target. In addition, wind can affect the trajectory of the shot.

Figure 2.. Schematic view of the experimental setup.

(A) Water tank with a cover and a target above it. Airflow applied horizontally to the water’s surface deflects the fish’s shot. (B) An example from a video capturing the experiment. The airflow was oriented from right to left. The water jet is visible just before the impact at the target. (C) Experimental timeline of the first experiment: 5–10 shots before the introduction of the airflow, 10–15 shots with the airflow, 5–10 shots after the removal of the airflow. (D) Experimental timeline of the second experiment: 5–10 shots before the introduction of the airflow, 8–12 shots with the airflow in one direction, 15–20 shots with the airflow in the opposite direction, 5–10 shots after the removal of the airflow.

Figure 3.. Examples of fish responses to the perturbation.

(A) Experiment 1 setup: airflow in direction 1 – with the fish shot. (B) Experiment 1 setup: airflow in direction 2 – against the fish shot. (C) Example sessions for three fish that had to adapt to the perturbation in direction 1. Error was around zero during the baseline condition, increased with the introduction of the perturbation, and diminished with time. After the removal of the perturbation, the error was in the opposite direction. (D) Example sessions for the fish that had to adapt to the perturbation in direction 2. (E) All sessions for one example fish with the perturbation in direction 1. (F) All sessions of one example fish with the perturbation in direction 2.

Figure 4.. The archerfish can correct for perturbation using motor adaptation.

(A) Response of three fish to the perturbation. Direction of the airflow is with the fish shots. Black dots are the error values across the sessions, the black line is the mean error value, and the SE is highlighted in green. (B) Response of three fish to the perturbation. Direction of the airflow is against the fish shots. (C) For three fish that shoot in direction 1: Mean value of the error and 95% highest density interval (HDI) for epoch 1 – the baseline, epoch 2 – first two trials after the introduction of the airflow, epoch 4 – last two trials before the termination of the perturbation, epoch 5 – first two trials after the termination of the perturbation. (D) For the four fish that shot in direction 2: Mean value of the error and 95% HDI.

Figure 5.. Adaptation in two directions sequentially reveals that motor adaptation is performed in the fish’s egocentric reference frame.

(A) Experimental setup: Airflow applied horizontally to the water’s surface deflects the fish’s shot. The fish first adapted to the perturbation in one direction and then enforced the switch direction of the shoot. (B) For the fish that changed direction from shooting in the direction with the perturbation to against the perturbation: mean error value and SE for the baseline trials, trials at the beginning and at the end of the adaptation period, trials at the beginning and the end of the adaptation period in the opposite direction and the beginning and the end of the washout period. (C–D) For the fish that changed direction from shooting in the direction against the perturbation to shooting with the perturbation: mean error value and SE for the baseline trials, trials at the beginning and the end of the adaptation period, trials at the beginning and the end of the adaptation period with reversed direction and at the beginning and the end of the washout period. (E) Mean value of the error and 95% highest density interval (HDI) for epoch 1 – the baseline, epoch 2 – first two trials after the introduction of the airflow, epoch 4 – last two trials before the change in the direction, epoch 5 – first two trials after the direction change, epoch 7 – last two trials before the termination of the perturbation, epoch 8 – first two trials after the termination of the perturbation.