Action Enhances Acoustic Cues for 3-D Target Localization by Echolocating Bats

Abstract

Under natural conditions, animals encounter a barrage of sensory information from which they must select and interpret biologically relevant signals. Active sensing can facilitate this process by engaging motor systems in the sampling of sensory information. The echolocating bat serves as an excellent model to investigate the coupling between action and sensing because it adaptively controls both the acoustic signals used to probe the environment and movements to receive echoes at the auditory periphery. We report here that the echolocating bat controls the features of its sonar vocalizations in tandem with the positioning of the outer ears to maximize acoustic cues for target detection and localization. The bat’s adaptive control of sonar vocalizations and ear positioning occurs on a millisecond timescale to capture spatial information from arriving echoes, as well as on a longer timescale to track target movement. Our results demonstrate that purposeful control over sonar sound production and reception can serve to improve acoustic cues for localization tasks. This finding also highlights the general importance of movement to sensory processing across animal species. Finally, our discoveries point to important parallels between spatial perception by echolocation and vision.

Abstract

As an echolocating bat tracks a moving target, it produces head waggles and adjusts the separation of the tips of its ears to enhance cues for target detection and localization. These findings suggest parallels in active sensing between echolocation and vision.

Author Summary

As animals operate in the natural environment, they must detect and process relevant sensory information embedded in complex and noisy signals. One strategy to overcome this challenge is to use active sensing or behavioral adjustments to extract sensory information from a selected region of the environment. We studied one of nature’s champions in auditory active sensing—the echolocating bat—to understand how this animal extracts task-relevant acoustic cues to detect and track a moving target. The bat produces high-frequency vocalizations and processes information carried by returning echoes to navigate and catch prey. This animal serves as an excellent model of active sensing because both sonar signal transmission and echo reception are under the animal’s active control. We used high-speed stereo video images of the bat’s head and ear movements, along with synchronized audio recordings, to study how the bat coordinates adaptive motor behaviors when detecting and tracking moving prey. We found that the bat synchronizes changes in sonar vocal production with changes in the movements of the head and ears to enhance acoustic cues for target detection and localization.