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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. 

A central aim of neuroethological research is to discover the mechanisms of natural behaviors in controlled laboratory studies. This goal, however, comes with challenges, namely the selection of experimental paradigms that allow full expression of natural behaviors. Here, we explore this problem in echolocating bats that evolved Doppler shift compensation (DSC) of sonar vocalizations to yield close matching between echo frequency and hearing sensitivity. We ask if behavioral tasks influence the precision of DSC in Pratt’s roundleaf bat, Hipposideros pratti , in three classic laboratory paradigms evoking audio-vocal adjustments: Stationary bats listening to echo playbacks, bats transported on a moving pendulum, and bats flying freely. We found that experimental conditions had a strong influence on the expression of the audiovocal frequency adjustments in bats. H. pratti exhibited robust DSC in both free-flying and moving-pendulum experiments but did not exhibit consistent audiovocal adjustments in echo playback experiments. H. pratti featured a maximum compensation magnitude of 87% and a compensation precision of 0.27% in the free flight experiment. Interestingly, in the moving pendulum experiment H. pratti displayed surprisingly high-precision DSC, with an 84% maximum compensation magnitude and a 0.27% compensation precision. Such DSC performance places H. pratti among the bat species exhibiting the most precise audio-vocal control of echo frequency. These data support the emerging view that Hipposiderid bats have a high-precision DSC system and highlight the importance of selecting experimental paradigms that yield the expression of robust natural behaviors. 

Fine audiovocal control is a hallmark of human speech production and depends on precisely coordinated muscle activity guided by sensory feedback. Little is known about shared audiovocal mechanisms between humans and other mammals. We hypothesized that real-time audiovocal control in bat echolocation uses the same computational principles as human speech. To test the prediction of this hypothesis, we applied state feedback control (SFC) theory to the analysis of call frequency adjustments in the echolocating bat, Hipposideros armiger. This model organism exhibits well-developed audiovocal control to sense its surroundings via echolocation. Our experimental paradigm was analogous to one implemented in human subjects. We measured the bats’ vocal responses to spectrally altered echolocation calls. Individual bats exhibited highly distinct patterns of vocal compensation to these altered calls. Our findings mirror typical observations of speech control in humans listening to spectrally altered speech. Using mathematical modeling, we determined that the same computational principles of SFC apply to bat echolocation and human speech, confirming the prediction of our hypothesis. 

Little is known about fine scale neural dynamics that accompany rapid shifts in spatial attention in freely behaving animals, primarily because reliable indicators of attention are lacking in standard model organisms engaged in natural tasks.  The echolocating bat can serve to bridge this gap, as it exhibits robust dynamic behavioral indicators of overt spatial attention as it explores its environment.  In particular, the bat actively shifts the aim of its sonar beam to inspect objects in different directions, akin to eye movements and foveation in humans and other visually dominant animals. Further, the bat adjusts the temporal features of sonar calls to attend to objects at different distances, yielding a metric of acoustic gaze along the range axis. Thus, an echolocating bat’s call features not only convey the information it uses to probe its surroundings, but also provide fine scale metrics of auditory spatial attention in 3D natural tasks. These explicit metrics of overt spatial attention can be leveraged to uncover general principles of neural coding in the mammalian brain. 

Most bat species have highly developed audio-vocal systems, which allow them to adjust the features of echolocation calls that are optimized for different sonar tasks, such as detecting, localizing, discriminating and tracking targets. Furthermore, bats can also produce a wide array of social calls to communicate with conspecifics. The acoustic properties of some social calls differ only subtly from echolocation calls, yet bats have the ability to distinguish them and reliably produce appropriate behavioral responses. Little is known about the underlying neural processes that enable the correct classification of bat social communication sounds. One approach to this question is to identify the brain regions that are involved in the processing of sounds that carry behavioral relevance. Here, we present preliminary data on neuronal activation, as measured by c-fos expression, in big brown bats (Eptesicus fuscus) exposed to either social calls, echolocation calls or kept in silence. We focused our investigation on five relevant brain areas; three within the canonical auditory pathway (auditory cortex, inferior colliculus and medial geniculate body) and two that are involved in the processing of emotive stimulus content (amygdala and nucleus accumbens). In this manuscript we report c-fos staining of the areas of interest after exposure to conspecific calls. We discuss future work designed to overcome experimental limitations and explore whether c-fos staining reveals anatomical segregation of neurons activated by echolocation and social call call categories. 

The mammalian superior colliculus (SC) and its non-mammalian homolog, the optic tectum are implicated in sensorimotor transformations. Historically, emphasis on visuomotor functions of the SC has led to a popular view that it operates as an oculomotor structure rather than a more general orienting structure. In this review, we consider comparative work on the SC/optic tectum, with a particular focus on non-visual sensing and orienting, which reveals a broader perspective on SC functions and their role in species-specific behaviors. We highlight several recent studies that consider ethological context and natural behaviors to advance knowledge of the SC as a site of multi-sensory integration and motor initiation in diverse species.