ABSTRACT Journal of Experimental Biology has a long history of reporting research discoveries on animal echolocation, the subject of this Centenary Review. Echolocating animals emit intense sound pulses and process echoes to localize objects in dynamic soundscapes. More than 1100 species of bats and 70 species of toothed whales rely on echolocation to operate in aerial and aquatic environments, respectively. The need to mitigate acoustic clutter and ambient noise is common to both aerial and aquatic echolocating animals, resulting in convergence of many echolocation features, such as directional sound emission and hearing, and decreased pulse intervals and sound intensity during target approach. The physics of sound transmission in air and underwater constrains the production, detection and localization of sonar signals, resulting in differences in response times to initiate prey interception by aerial and aquatic echolocating animals. Anti-predator behavioral responses of prey pursued by echolocating animals affect behavioral foraging strategies in air and underwater. For example, many insect prey can detect and react to bat echolocation sounds, whereas most fish and squid are unresponsive to toothed whale signals, but can instead sense water movements generated by an approaching predator. These differences have implications for how bats and toothed whales hunt using echolocation. Here, we consider the behaviors used by echolocating mammals to (1) track and intercept moving prey equipped with predator detectors, (2) interrogate dynamic sonar scenes and (3) exploit visual and passive acoustic stimuli. Similarities and differences in animal sonar behaviors underwater and in air point to open research questions that are ripe for exploration.
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Active head rolls enhance sonar-based auditory localization performance
Animals utilize a variety of active sensing mechanisms to perceive the world around them. Echolocating bats are an excellent model for the study of active auditory localization. The big brown bat ( Eptesicus fuscus ), for instance, employs active head roll movements during sonar prey tracking. The function of head rolls in sound source localization is not well understood. Here, we propose an echolocation model with multi-axis head rotation to investigate the effect of active head roll movements on sound localization performance. The model autonomously learns to align the bat’s head direction towards the target. We show that a model with active head roll movements better localizes targets than a model without head rolls. Furthermore, we demonstrate that active head rolls also reduce the time required for localization in elevation. Finally, our model offers key insights to sound localization cues used by echolocating bats employing active head movements during echolocation.
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- Award ID(s):
- 1734744
- NSF-PAR ID:
- 10280824
- Editor(s):
- Thaler, Lore
- Date Published:
- Journal Name:
- PLOS Computational Biology
- Volume:
- 17
- Issue:
- 5
- ISSN:
- 1553-7358
- Page Range / eLocation ID:
- e1008973
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Synopsis The hyoid apparatus in laryngeally echolocating bats is unique as it forms a mechanical connection between the larynx and auditory bullae, which has been hypothesized to transfer the outgoing echolocation call to the middle ear during call emission. Previous finite element modeling (FEM) found that hyoid-borne sound can reach the bulla at an amplitude likely heard by echolocating bats; however, that study did not model how or if the signal could reach the inner ear (or cochlea). One route that sound could take is via stimulation of the eardrum—similarly to that of air-conducted sound. We used micro computed tomography (μCT) data to build models of the hyoid apparatus and middle ear from six species of bats with variable morphology. Using FEM, we ran harmonic response analyses to measure the vibroacoustic response of the tympanic membrane due to hyoid-borne sound generated during echolocation and found that hyoid-borne sound in all six species stimulated the eardrum within a range likely heard by bats. Although there was variation in the efficiency between models, there are no obvious morphological patterns to account for it. This suggests that hyoid morphology in laryngeal echolocators is likely driven by other associated functions.
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Target tracking and interception in a dynamic world proves to be a fundamental challenge faced by both animals and artificial systems. To track moving objects under natural conditions, agents must employ strategies to mitigate interference and conditions of uncertainty. Animal studies of prey tracking and capture reveal biological solutions, which can inspire new technologies, particularly for operations in complex and noisy environments. By reviewing research on target tracking and interception by echolocating bats, we aim to highlight biological solutions that could inform new approaches to artificial sonar tracking and navigation systems. Most bat species use wideband echolocation signals to navigate dense forests and hunt for evasive insects in the dark. Importantly, bats exhibit rapid adaptations in flight trajectory, sonar beam aim, and echolocation signal design, which appear to be key to the success of these animals in a variety of tasks. The rich suite of adaptive behaviors of echolocating bats could be leveraged in new sonar tracking technologies by implementing dynamic sensorimotor feedback control of wideband sonar signal design, head, and ear movements.more » « less
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Temporal analysis of sound is fundamental to auditory processing throughout the animal kingdom. Echolocating bats are powerful models for investigating the underlying mechanisms of auditory temporal processing, as they show microsecond precision in discriminating the timing of acoustic events. However, the neural basis for microsecond auditory discrimination in bats has eluded researchers for decades. Combining extracellular recordings in the midbrain inferior colliculus (IC) and mathematical modeling, we show that microsecond precision in registering stimulus events emerges from synchronous neural firing, revealed through low-latency variability of stimulus-evoked extracellular field potentials (EFPs, 200–600 Hz). The temporal precision of the EFP increases with the number of neurons firing in synchrony. Moreover, there is a functional relationship between the temporal precision of the EFP and the spectrotemporal features of the echolocation calls. In addition, EFP can measure the time difference of simulated echolocation call–echo pairs with microsecond precision. We propose that synchronous firing of populations of neurons operates in diverse species to support temporal analysis for auditory localization and complex sound processing.more » « less
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Abstract Acute auditory processing in bats is typically associated with echolocation. A subset of bats, called gleaners, listens to prey-generated noise to hunt surface-dwelling prey. Gleaners depend less on echolocation to hunt and, therefore, accurate localization of prey-generated noise is necessary for foraging success. Here we studied azimuth sound localization behavior in the pallid bat, a gleaning bat in which spatial encoding has been studied extensively. We tested pallid bats on a relatively difficult open loop task (single sound, duration ≤ 200 ms). The bats were trained to face the midline when stimulus was presented, and this was confirmed with video analysis. Bats localized broadband noise (5–30 kHz) from 1 out of 11 speakers spaced evenly across the horizontal plane of the frontal sound field. Approach to the correct speaker was rewarded. Pallid bats show accurate localization near the midline with mean errors between 3–6°. Remarkably, the accuracy does not decline significantly at peripheral locations with bats averaging <~7° error upto 72° off midline. Manipulation of stimulus bandwidth shows that higher frequencies (20–30 kHz) are necessary for accurate localization. Comparative studies of gleaning bats will reveal convergent adaptations across auditory systems for non-echolocation-based behaviors in bats.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pcbi.1008973
