Active control of acoustic field-of-view in a biosonar system

Abstract

Active-sensing systems abound in nature, but little is known about systematic strategies that are used by these systems to scan the environment. Here, we addressed this question by studying echolocating bats, animals that have the ability to point their biosonar beam to a confined region of space. We trained Egyptian fruit bats to land on a target, under conditions of varying levels of environmental complexity, and measured their echolocation and flight behavior. The bats modulated the intensity of their biosonar emissions, and the spatial region they sampled, in a task-dependant manner. We report here that Egyptian fruit bats selectively change the emission intensity and the angle between the beam axes of sequentially emitted clicks, according to the distance to the target, and depending on the level of environmental complexity. In so doing, they effectively adjusted the spatial sector sampled by a pair of clicks-the "field-of-view." We suggest that the exact point within the beam that is directed towards an object (e.g., the beam's peak, maximal slope, etc.) is influenced by three competing task demands: detection, localization, and angular scanning-where the third factor is modulated by field-of-view. Our results suggest that lingual echolocation (based on tongue clicks) is in fact much more sophisticated than previously believed. They also reveal a new parameter under active control in animal sonar-the angle between consecutive beams. Our findings suggest that acoustic scanning of space by mammals is highly flexible and modulated much more selectively than previously recognized.

Figure 1. The inter-click beam angle is increased at the moment of locking when the bat is approaching a single object.

(A) Schematic of single trial showing flight trajectory and direction of echolocation clicks in an Egyptian fruit bat (black lines). Dots at circumference, microphones; arrow, point of locking onto target. (B) Illustration of the inter-click angle. Black lines, direction of beam's peak; gray ellipse, polar representation of the sonar beam. (C) Examples of seven trials in which the inter-click angle abruptly increased around time 0 ( = the moment of locking). (D) Population average inter-click angle along the bats' approach to a single object. The angle was normalized separately for each bat to its average un-locked angle (see Materials and Methods). Error bars, mean ± s.e.m.; computed in 0.4-s bins.

Figure 2. The inter-click angle increases with the increase in environmental complexity.

(A) Top, schematic of the three experimental setups. Bottom, inter-click angle in the different experimental conditions. U, unlocked; L, locked; E-L, instances of early-locking prior to the final locking. Note increase in inter-click angle with environmental complexity. (B–C) Increase in inter-click angle along the approach, during multiple-object experiments. (B) In these experiments, the inter-click angle along the approach had a higher value (higher than in the one-object setup) and exhibited a gradual increase after the final locking onto the landing target. (C) When using the bat's entrance between the nets as an alternative locking criterion, it became evident that most of the increase in inter-click angle has occurred between 1 and 0.5 s before the bats entered in-between the nets. Note different x-axis in (B) and (C). Error bars, mean ± s.e.m.

Figure 3. Lingual echolocators modify the intensity of their emissions according to the environmental complexity and the stage of target approach.

(A) Examples of six trials, showing that emission intensity gradually decreases with time along the approach. Average is depicted by thick gray line. (B) Population average intensity plotted as function of time relative to locking, for the one-object and multiple-object setups. Error bars, mean ± s.e.m. The two curves were shifted by 30 ms relative to each other, for display purposes only. (C) Examples of the same six trials as in (A), with intensity plotted as function of distance to target. Average is depicted by thick gray line. Note decrease in intensity that began 80–100 cm before landing. (D) Click intensity increased with the environmental complexity. Intensity was not lower when the bats were locked on the target before the final locking (dark gray bar marked E-L).

Figure 4. Combined effect of the changes in click intensity and changes in inter-click angle, across the different experimental setups.

(A) Multiple-object experiment. (B) One-object experiment. (C) No-object experiment. Dashed gray lines depict the effective increase in field-of-view due to the combined increases in inter-click angle and click intensity; here we assumed a constant hearing threshold at normalized intensity of 1. Horizontal dashed lines, normalized intensity = 1; note that in all panels, this intensity was kept constant by the bats around their region of interest (see text). In all panels, “+” symbols depict the point of maximum-slope of the right beam (the locked beam when there are two): Note how the maximum slope changes position from being lateral (right) to the target in the multiple-object experiments, to pointing straight at the target in the one-object experiments, to being medial (left) to the target in the no-object experiments.