Spatial acuity and prey detection in weakly electric fish

Abstract

It is well-known that weakly electric fish can exhibit extreme temporal acuity at the behavioral level, discriminating time intervals in the submicrosecond range. However, relatively little is known about the spatial acuity of the electrosense. Here we use a recently developed model of the electric field generated by Apteronotus leptorhynchus to study spatial acuity and small signal extraction. We show that the quality of sensory information available on the lateral body surface is highest for objects close to the fish's midbody, suggesting that spatial acuity should be highest at this location. Overall, however, this information is relatively blurry and the electrosense exhibits relatively poor acuity. Despite this apparent limitation, weakly electric fish are able to extract the minute signals generated by small prey, even in the presence of large background signals. In fact, we show that the fish's poor spatial acuity may actually enhance prey detection under some conditions. This occurs because the electric image produced by a spatially dense background is relatively "blurred" or spatially uniform. Hence, the small spatially localized prey signal "pops out" when fish motion is simulated. This shows explicitly how the back-and-forth swimming, characteristic of these fish, can be used to generate motion cues that, as in other animals, assist in the extraction of sensory information when signal-to-noise ratios are low. Our study also reveals the importance of the structure of complex electrosensory backgrounds. Whereas large-object spacing is favorable for discriminating the individual elements of a scene, small spacing can increase the fish's ability to resolve a single target object against this background.

Figure 1. Electric Images Produced by Two Prey-Like Objects and Determination of S_min

The head is at position 0 m along the rostro–caudal axis. The midbody is at 0.11 m, and the tail is at 0.21 m. All interobject distances are center-to-center, and object-to-fish lateral distances (i.e., perpendicular to fish midline) are from object center to skin surface. (A) Electric field potential in the presence of two identical prey-like objects (modeled as 0.3-cm diameter discs with a conductivity of 0.0303 S/m; water conductivity: 0.023 S/m). Objects do not affect the field much due to their small size and conductivity similar to the water. The S_min (14 mm) is also shown for a specific prey position (left prey located 0.11 m caudally from the tip of the head and 0.012 m laterally to the skin). The potential at different points is measured with respect to a reference electrode placed laterally to the fish in the far field, near the zero potential line [9]. (B) Overlays of electric images for three different object locations illustrating the increase in image amplitude in the caudal direction (x) and the decrease in amplitude for increasing lateral distances (y). (x,y) = (0.05, 0.03), (0.05, 0.015), (0.1, 0.015) m. As described in Materials and Methods, these images are computed as the difference between the transdermal potentials measured with and without the object present. (C) Overlays of electric images for three distinct interprey distances (see inset). Blue trace shows S_min, when the two peaks in the electric image are just noticeable. Computation of the images is as in (B). Location of more-rostral prey as in (A).

Figure 2. Effect of Object Location and Conductivity on Spatial Electroacuity

In all panels, see fish insets for approximate lateral and rostro–caudal locations where S_min was calculated. Error bars represent the sampling that was used to calculate the S_min (either 0.5 or 1 mm). Lateral distance is measured as object center to fish skin (as in Figure 1). (A) Effect of lateral distance on S_min for three distinct object diameters (rostro–caudal location, x = 0.11 m). Red, 0.3 cm (prey size); green, 1 cm; blue, 2 cm. Object conductivity fixed at 0.0303 S/m (prey conductivity). (B) Effect of rostro–caudal position on S_min for same object sizes and conductivity as (A), with a lateral distance of 0.012 m. (C) Effect of lateral distance on S_min for three distinct object conductivities (rostro–caudal location, x = 0.11m). Red, 0.0005 S/m (plant conductivity); green, 0.0303 S/m (prey conductivity); blue, 0.5 S/m. Object diameters fixed at 0.3 cm (prey size). (D) Effect of rostro–caudal position on S_min for same object diameter and conductivities as in (C), with a lateral distance of 0.012 m.

Figure 3. Electric Image of a Plant-Like Background

All images in both panels are computed as the difference in transdermal potentials, with and without objects (as described in Materials and Methods). (A) Electric images produced by six distinct background widths, which differ in number of objects (see inset). Red, 1; orange, 3; yellow, 5; green, 7, blue, 9; purple, 11. The 2 cm–diameter discs have a conductivity of 0.0005 S/m to mimic the plant Hygrophilia. Discs are located 0.05 m away laterally from the fish's midline and are separated, one from another, by 0.03 m. All series of objects are centered near the fish's midpoint (red object in inset) and color in inset denotes external objects of a given series. (B) Electric images due to backgrounds with three different interobject spacings: blue, 0.03 m (same as panel A); green, 0.06 m; red, 0.09 m. Otherwise, objects are identical to those in panel (A).

Figure 4. Electric Image of a Plant-Like Background in the Presence and Absence of a Prey Object

All images in both panels are computed as the difference in transdermal potentials, with and without objects (as described in Materials and Methods). (A) Six fish positions (see inset, top) for which the electric images (bottom) produced by a 15-disc Hygrophilia plant-like background (0.05 m lateral to fish, as in Figure 3) were calculated. Electric images are barely distinguishable from one another. Fish positions differ from one another by 0.02 m, 0.02 m, 0.03 m, 0.005 m, and 0.015 m (see inset). (B) Same as in panel (A) except a Daphnia-like prey object (0.3-cm diameter as in Figure 1) was added at a lateral distance of 0.008 m from the skin.

Figure 5. Transdermal Potential at Two Distinct Points on the Fish's Body During Simulated Motion

To calculate each image, 21 different fish positions were used. In all cases, images are the raw transdermal potential with the mean removed to more easily compare the different curves. Black arrow shows direction of the simulated scanning motion used to generate the time series shown, with a scanning speed of 0.1 m/s. The legend in (A) applies to all panels. (A) Transdermal potential at a skin location 0.11 m caudal from the tip of the fish's head (point A in inset) for three different conditions: background alone (green), the background and prey (blue), and prey alone (red). Background objects are as in Figures 3 and 4. The spacing between the individual objects in the background is 0.03 m; the lateral distance of the background is 0.05 m from the midline. The lateral distance of the prey object (as in Figure 4) is 0.008 m. (B) Same as in panel (A) except for a larger interobject spacing (0.06 m) in the background. (C) Same as in panel (A) except that the background objects are randomly spaced, as shown by the inset, with same mean spacing as (B). (D–F) Same as the upper panels (A–C, respectively) except that the transdermal potential is shown for a skin position 0.085 m caudal from the tip of the fish's head (point B in inset).

Figure 6. Prey Detectibility and Background Sparseness

(Left axis, blue trace) SNR ratio between the prey and background transdermal potential time series and the background-only time series (i.e., between blue and green traces in Figure 5A; see Materials and Methods for more details). Each point represents the mean SNR of ten locations (over an ~0.01 m–wide patch of skin) centered 0.05 m caudal from the tip of the fish's head. SNR is shown as a function of interobject spacing of the background. (Right axis, green trace) Theoretical discriminability (see Materials and Methods) between two background-type objects as a function of their spacing, using the same object size (2-cm diameter) and lateral distance (0.05 m) as in Figure 5.