Role of auditory feedback for vocal production learning in the Egyptian fruit-bat.

Some species have evolved the ability to use the sense of hearing to modify existing vocalizations, or even create new ones. This ability corresponds to various forms of vocal production learning that are all possessed by humans, and independently displayed by distantly related vertebrates. Among mammals, a few species, including the Egyptian fruit-bat, would possess such vocal production learning abilities. Yet the necessity of an intact auditory system for the development of the Egyptian fruit-bat typical vocal repertoire has not been tested. Furthermore, a systematic causal examination of learned and innate aspects of the entire repertoire has never been performed in any vocal learner. Here we addressed these gaps by eliminating pups' sense of hearing at birth and assessing its effects on vocal production in adulthood. The deafening treatment enabled us to both causally test these bats vocal learning ability and discern learned from innate aspects of their vocalizations. Leveraging wireless individual audio recordings from freely interacting adults, we show that a subset of the Egyptian fruit-bat vocal repertoire necessitates auditory feedback. Intriguingly, these affected vocalizations belong to different acoustic groups in the vocal repertoire of males and females. These findings open the possibilities for targeted studies of the mammalian neural circuits that enable sexually dimorphic forms of vocal learning.

The fully automated bat (FAB) flight room: A human-free environment for studying navigation in flying bats and its initial application to the retrosplenial cortex.

BACKGROUND: Bats can offer important insight into the neural computations underlying complex forms of navigation. Up to now, this had been done with the confound of the human experimenter being present in the same environment the bat was navigating in. NEW METHOD: We, therefore, developed a novel behavioral setup, the fully automated bat (FAB) flight room, to obtain a detailed and quantitative understanding of bat navigation flight behavior while studying its relevant neural circuits, but importantly without human intervention. As a demonstration of the FAB flight room utility we trained bats on a four-target, visually-guided, foraging task and recorded neural activity from the retrosplenial cortex (RSC). RESULTS: We find that bats can be efficiently trained and engaged in complex, multi-target, visuospatial behavior in the FAB flight room. Wireless neural recordings from the bat RSC during the task confirm the multiplexed characteristics of single RSC neurons encoding spatial positional information, target selection, reward obtainment and the intensity of visual cues used to guide navigation. COMPARISON WITH EXISTING METHODS: In contrast to the methods introduced in previous studies, we now can investigate spatial navigation in bats without potential experimental biases that can be easily introduced by active physical involvement and presence of experimenters in the room. CONCLUSIONS: Combined, we describe a novel experimental approach for studying spatial navigation in freely flying bats and provide support for the involvement of bat RSC in aerial visuospatial foraging behavior.

Long-term and persistent vocal plasticity in adult bats.

Bats exhibit a diverse and complex vocabulary of social communication calls some of which are believed to be learned during development. This ability to produce learned, species-specific vocalizations - a rare trait in the animal kingdom - requires a high-degree of vocal plasticity. Bats live extremely long lives in highly complex and dynamic social environments, which suggests that they might also retain a high degree of vocal plasticity in adulthood, much as humans do. Here, we report persistent vocal plasticity in adult bats (Rousettus aegyptiacus) following exposure to broad-band, acoustic perturbation. Our results show that adult bats can not only modify distinct parameters of their vocalizations, but that these changes persist even after noise cessation - in some cases lasting several weeks or months. Combined, these findings underscore the potential importance of bats as a model organism for studies of vocal plasticity, including in adulthood.

Neuroethology of bat navigation.

Once a year about 15 million Mexican free-tailed bats (Tadarida brasiliensis) migrate up to 1,500 kilometers from wintering grounds, seamlessly flying over the Mexican border to enter the United States. Their destination is the Bracken Cave in southern Texas, which will be their summer home between the months of March through October. While residing there, these bats emerge every night at dusk from the narrow 100-foot-wide opening of this enormous cave and begin their nightly commute to foraging grounds located up to 50 kilometers away. Upon arrival, they will spend the night hunting for insects in mid-air while providing a valuable service to local farmers by keeping crop pests in check. Close to the break of dawn, as the night of hunting comes to an end, these bats will begin making their trip back to the roost.

Psychophysical evidence for auditory motion parallax.

Distance is important: From an ecological perspective, knowledge about the distance to either prey or predator is vital. However, the distance of an unknown sound source is particularly difficult to assess, especially in anechoic environments. In vision, changes in perspective resulting from observer motion produce a reliable, consistent, and unambiguous impression of depth known as motion parallax. Here we demonstrate with formal psychophysics that humans can exploit auditory motion parallax, i.e., the change in the dynamic binaural cues elicited by self-motion, to assess the relative depths of two sound sources. Our data show that sensitivity to relative depth is best when subjects move actively; performance deteriorates when subjects are moved by a motion platform or when the sound sources themselves move. This is true even though the dynamic binaural cues elicited by these three types of motion are identical. Our data demonstrate a perceptual strategy to segregate intermittent sound sources in depth and highlight the tight interaction between self-motion and binaural processing that allows assessment of the spatial layout of complex acoustic scenes.

Dependence of auditory spatial updating on vestibular, proprioceptive, and efference copy signals.

Humans localize sounds by comparing inputs across the two ears, resulting in a head-centered representation of sound-source position. When the head moves, information about head movement must be combined with the head-centered estimate to correctly update the world-centered sound-source position. Spatial updating has been extensively studied in the visual system, but less is known about how head movement signals interact with binaural information during auditory spatial updating. In the current experiments, listeners compared the world-centered azimuthal position of two sound sources presented before and after a head rotation that depended on condition. In the active condition, subjects rotated their head by ∼35° to the left or right, following a pretrained trajectory. In the passive condition, subjects were rotated along the same trajectory in a rotating chair. In the cancellation condition, subjects rotated their head as in the active condition, but the chair was counter-rotated on the basis of head-tracking data such that the head effectively remained fixed in space while the body rotated beneath it. Subjects updated most accurately in the passive condition but erred in the active and cancellation conditions. Performance is interpreted as reflecting the accuracy of perceived head rotation across conditions, which is modeled as a linear combination of proprioceptive/efference copy signals and vestibular signals. Resulting weights suggest that auditory updating is dominated by vestibular signals but with significant contributions from proprioception/efference copy. Overall, results shed light on the interplay of sensory and motor signals that determine the accuracy of auditory spatial updating.

Biosonar navigation above water I: estimating flight height.

Locomotion and foraging on the wing require precise navigation in more than just the horizontal plane. Navigation in three dimensions and, specifically, precise adjustment of flight height are essential for flying animals. Echolocating bats drink from water surfaces in flight, which requires an exceptionally precise vertical navigation. Here, we exploit this behavior in the bat, Phyllostomus discolor, to understand the biophysical and neural mechanisms that allow for sonar-guided navigation in the vertical plane. In a set of behavioral experiments, we show that for echolocating bats, adjustment of flight height depends on the tragus in their outer ears. Specifically, the tragus imposes elevation-specific spectral interference patterns on the echoes of the bats' sonar emissions. Head-related transfer functions of our bats show that these interference patterns are most conspicuous in the frequency range ∼55 kHz. This conspicuousness is faithfully preserved in the frequency tuning and spatial receptive fields of cortical single and multiunits recorded from anesthetized animals. In addition, we recorded vertical spatiotemporal response maps that describe neural tuning in elevation over time. One class of units that were very sharply tuned to frequencies ∼55 kHz showed unusual spatiotemporal response characteristics with a preference for paired echoes where especially the first echo originates from very low elevations. These behavioral and neural data provide the first insight into biosonar-based processing and perception of acoustic elevation cues that are essential for bats to navigate in three-dimensional space.

Biosonar navigation above water II: exploiting mirror images.

As in vision, acoustic signals can be reflected by a smooth surface creating an acoustic mirror image. Water bodies represent the only naturally occurring horizontal and acoustically smooth surfaces. Echolocating bats flying over smooth water bodies encounter echo-acoustic mirror images of objects above the surface. Here, we combined an electrophysiological approach with a behavioral experimental paradigm to investigate whether bats can exploit echo-acoustic mirror images for navigation and how these mirrorlike echo-acoustic cues are encoded in their auditory cortex. In an obstacle-avoidance task where the obstacles could only be detected via their echo-acoustic mirror images, most bats spontaneously exploited these cues for navigation. Sonar ensonifications along the bats' flight path revealed conspicuous changes of the reflection patterns with slightly increased target strengths at relatively long echo delays corresponding to the longer acoustic paths from the mirrored obstacles. Recordings of cortical spatiotemporal response maps (STRMs) describe the tuning of a unit across the dimensions of elevation and time. The majority of cortical single and multiunits showed a special spatiotemporal pattern of excitatory areas in their STRM indicating a preference for echoes with (relative to the setup dimensions) long delays and, interestingly, from low elevations. This neural preference could effectively encode a reflection pattern as it would be perceived by an echolocating bat detecting an object mirrored from below. The current study provides both behavioral and neurophysiological evidence that echo-acoustic mirror images can be exploited by bats for obstacle avoidance. This capability effectively supports echo-acoustic navigation in highly cluttered natural habitats.

Trawling bats exploit an echo-acoustic ground effect.

A water surface acts not only as an optic mirror but also as an acoustic mirror. Echolocation calls emitted by bats at low heights above water are reflected away from the bat, and hence the background clutter is reduced. Moreover, targets on the surface create an enhanced echo. Here, we formally quantified the effect of the surface and target height on both target detection and -discrimination in a combined laboratory and field approach with Myotis daubentonii. In a two-alternative, forced-choice paradigm, the bats had to detect a mealworm and discriminate it from an inedible dummy (20 mm PVC disc). Psychophysical performance was measured as a function of height above either smooth surfaces (water or PVC) or above a clutter surface (artificial grass). At low heights above the clutter surface (10, 20, or 35 cm), the bats' detection performance was worse than above a smooth surface. At a height of 50 cm, the surface structure had no influence on target detection. Above the clutter surface, also target discrimination was significantly impaired with decreasing target height. A detailed analysis of the bats' echolocation calls during target approach shows that above the clutter surface, the bats produce calls with significantly higher peak frequency. Flight-path reconstruction revealed that the bats attacked an target from below over water but from above over a clutter surface. These results are consistent with the hypothesis that trawling bats exploit an echo-acoustic ground effect, in terms of a spatio-temporal integration of direct reflections with indirect reflections from the water surface, to optimize prey detection and -discrimination not only for prey on the water but also for some range above.

Size does not matter: size-invariant echo-acoustic object classification.

Echolocating bats can not only extract spatial information from the auditory analysis of their ultrasonic emissions, they can also discriminate, classify and identify the three-dimensional shape of objects reflecting their emissions. Effective object recognition requires the segregation of size and shape information. Previous studies have shown that, like in visual object recognition, bats can transfer an echo-acoustic object discrimination task to objects of different size and that they spontaneously classify scaled versions of virtual echo-acoustic objects according to trained virtual-object standards. The current study aims to bridge the gap between these previous findings using a different class of real objects and a classification-instead of a discrimination paradigm. Echolocating bats (Phyllostomus discolor) were trained to classify an object as either a sphere or an hour-glass shaped object. The bats spontaneously generalised this classification to objects of the same shape. The generalisation cannot be explained based on similarities of the power spectra or temporal structures of the echo-acoustic object images and thus require dedicated neural mechanisms dealing with size-invariant echo-acoustic object analysis. Control experiments with human listeners classifying the echo-acoustic images of the objects confirm the universal validity of auditory size invariance. The current data thus corroborate and extend previous psychophysical evidence for sonar auditory-object normalisation and suggest that the underlying auditory mechanisms following the initial neural extraction of the echo-acoustic images in echolocating bats may be very similar in bats and humans.

Coordination of bat sonar activity and flight for the exploration of three-dimensional objects.

The unique combination of flight and echolocation has opened the nocturnal air space as a rich ecological niche for bats. By analysing echoes of their sonar emissions, bats discriminate and recognize three-dimensional (3-D) objects. However, in contrast to vision, the 3-D information that can be gained by ensonifying an object from only one observation angle is sparse. To date, it is unclear how bats synchronize echolocation and flight activity to explore the 3-D shape of ensonified objects. We have devised an experimental design that allows creating 3-D virtual echo-acoustic objects by generating in real-time echoes from the bat's emissions that depend on the bat's position relative to the virtual object. Bats were trained to evaluate these 3-D virtual objects differing in their azimuthal variation of either echo amplitude or spectral composition. The data show that through a very effective coordination of sonar and flight activity, bats analyse an azimuthal variation of echo amplitude with a resolution of approximately 16 dB and a variation of echo centre frequency of approximately 19%. Control experiments show that the bats can detect not only these variations but also perturbations in the spatial arrangement of these variations. The current experimental paradigm shows that echolocating bats assemble echo-acoustic object information - acquired sequentially in flight - to reconstruct the 3-D shape of the ensonified object. Unlike previous approaches, the recruitment of virtual objects allows for a direct quantification of this reconstruction success in a highly controlled experimental approach.

Bats' avoidance of real and virtual objects: implications for the sonar coding of object size.

Fast movement in complex environments requires the controlled evasion of obstacles. Sonar-based obstacle evasion involves analysing the acoustic features of object-echoes (e.g., echo amplitude) that correlate with this object's physical features (e.g., object size). Here, we investigated sonar-based obstacle evasion in bats emerging in groups from their day roost. Using video-recordings, we first show that the bats evaded a small real object (ultrasonic loudspeaker) despite the familiar flight situation. Secondly, we studied the sonar coding of object size by adding a larger virtual object. The virtual object echo was generated by real-time convolution of the bats' calls with the acoustic impulse response of a large spherical disc and played from the loudspeaker. Contrary to the real object, the virtual object did not elicit evasive flight, despite the spectro-temporal similarity of real and virtual object echoes. Yet, their spatial echo features differ: virtual object echoes lack the spread of angles of incidence from which the echoes of large objects arrive at a bat's ears (sonar aperture). We hypothesise that this mismatch of spectro-temporal and spatial echo features caused the lack of virtual object evasion and suggest that the sonar aperture of object echoscapes contributes to the sonar coding of object size.

Time-variant spectral peak and notch detection in echolocation-call sequences in bats.

Bats are able to recognize and discriminate three-dimensional objects in complete darkness by analyzing the echoes of their ultrasonic emissions. Bats typically ensonify objects from different aspects to gain an internal representation of the three-dimensional object shape. Previous work suggests that, as a result, bats rely on the echo-acoustic analysis of spectral peaks and notches. Dependent on the aspect of ensonification, this spectral interference pattern changes over time in an object-specific manner. The speed with which the bats' auditory system can follow time-variant spectral interference patterns is unknown. Here, we measured the detection thresholds for temporal variations in the spectral content of synthesized echolocation calls in the echolocating bat, Megaderma lyra. In a two-alternative, forced-choice procedure, bats were trained to discriminate synthesized echolocation-call sequences with time-variant spectral peaks or notches from echolocation-call sequences with invariant peaks or notches. Detection thresholds of the spectral modulations were measured by varying the modulation depth of the time-variant echolocation-call sequences for modulation rates ranging from 2 to 16 Hz. Both for spectral peaks and notches, modulation-detection thresholds were at a modulation depth of approximately 11% of the centre frequency. Interestingly, thresholds were relatively independent of modulation rate. Acknowledging reservations about direct comparisons of active-acoustic and passive-acoustic auditory processing, the effectual sensitivity and modulation-rate independency of the obtained results indicate that the bats are well capable of tracking changes in the spectral composition of echoes reflected by complex objects from different angles.

The number of functional olfactory receptor genes and the relative size of olfactory brain structures are poor predictors of olfactory discrimination performance with enantiomers.

The ability of four squirrel monkeys and three pigtail macaques to distinguish between nine enantiomeric odor pairs sharing an isopropenyl group at the chiral center was investigated in terms of a conditioning paradigm. All animals from both species were able to discriminate between the optical isomers of limonene, carvone, dihydrocarvone, dihydrocarveole and dihydrocarvyl acetate, whereas they failed to distinguish between the (+)- and (-)-forms of perillaaldehyde and limonene oxide. The pigtail macaques, but not the squirrel monkeys, also discriminated between the antipodes of perillaalcohol and isopulegol. A comparison of the across-task patterns of discrimination performance shows a high degree of similarity among the two primate species and also between these nonhuman primates and human subjects tested in an earlier study on the same tasks. These findings suggest that between-species comparisons of the relative size of olfactory brain structures or of the number of functional olfactory receptor genes are poor predictors of olfactory discrimination performance with enantiomers.