Representation of frequency-modulated sweeps in the cochlear nucleus of the big brown bat.

The cochlear nucleus (CN) receives ipsilateral input from the auditory nerve and projects to other auditory brainstem nuclei. Little is known about CN processing of signals used for echolocation. This study recorded multiple unit activity in the CN of anesthetized big brown bats (Eptesicus fuscus) to ultrasonic frequency-modulated (FM) sweeps differing in sweep direction. FM up-sweeps evoke larger peak amplitudes at shorter onset latencies and with smaller amplitude-latency trading ratios than FM down-sweeps. Variability of onset latencies is in the tens of microsecond ranges, indicating sharp temporal precision in the CN for coding of FM signals.

Population registration of echo flow in the big brown bat's auditory midbrain.

Echolocating big brown bats (Eptesicus fuscus) perceive their surroundings by broadcasting frequency-modulated (FM) ultrasonic pulses and processing returning echoes. Bats echolocate in acoustically cluttered environments containing multiple objects, where each broadcast is followed by multiple echoes at varying time delays. The bat must decipher this complex echo cascade to form a coherent picture of the entire acoustic scene. Neurons in the bat's inferior colliculus (IC) are selective for specific acoustic features of echoes and time delays between broadcasts and echoes. Because of this selectivity, different subpopulations of neurons are activated as the bat flies through its environment, while the physical scene itself remains unchanging. We asked how a neural representation based on variable single-neuron responses could underlie a cohesive perceptual representation of a complex scene. We recorded local field potentials from the IC of big brown bats to examine population coding of echo cascades similar to what the bat might encounter when flying alongside vegetation. We found that the temporal patterning of a simulated broadcast followed by an echo cascade is faithfully reproduced in the population response at multiple stimulus amplitudes and echo delays. Local field potentials to broadcasts and echo cascades undergo amplitude-latency trading consistent with single-neuron data but rarely show paradoxical latency shifts. Population responses to the entire echo cascade move as a unit coherently in time as broadcast-echo cascade delay changes, suggesting that these responses serve as an index for the formation of a cohesive perceptual representation of an acoustic scene.NEW & NOTEWORTHY Echolocating bats navigate through cluttered environments that return cascades of echoes in response to the bat's broadcasts. We show that local field potentials from the big brown bat's auditory midbrain have consistent responses to a simulated echo cascade varying across echo delays and stimulus amplitudes, despite different underlying individual neuronal selectivities. These results suggest that population activity in the midbrain can build a cohesive percept of an auditory scene by aggregating activity over neuronal subpopulations.

Signal envelope and speech intelligibility differentially impact auditory motion perception.

Our acoustic environment contains a plethora of complex sounds that are often in motion. To gauge approaching danger and communicate effectively, listeners need to localize and identify sounds, which includes determining sound motion. This study addresses which acoustic cues impact listeners' ability to determine sound motion. Signal envelope (ENV) cues are implicated in both sound motion tracking and stimulus intelligibility, suggesting that these processes could be competing for sound processing resources. We created auditory chimaera from speech and noise stimuli and varied the number of frequency bands, effectively manipulating speech intelligibility. Normal-hearing adults were presented with stationary or moving chimaeras and reported perceived sound motion and content. Results show that sensitivity to sound motion is not affected by speech intelligibility, but shows a clear difference for original noise and speech stimuli. Further, acoustic chimaera with speech-like ENVs which had intelligible content induced a strong bias in listeners to report sounds as stationary. Increasing stimulus intelligibility systematically increased that bias and removing intelligible content reduced it, suggesting that sound content may be prioritized over sound motion. These findings suggest that sound motion processing in the auditory system can be biased by acoustic parameters related to speech intelligibility.

The impact of temporal fine structure and signal envelope on auditory motion perception.

The majority of psychoacoustic research investigating sound localization has utilized stationary sources, yet most naturally occurring sounds are in motion, either because the sound source itself moves, or the listener does. In normal hearing (NH) listeners, previous research showed the extent to which sound duration and velocity impact the ability of listeners to detect sound movement. By contrast, little is known about how listeners with hearing impairments perceive moving sounds; the only study to date comparing the performance of NH and bilateral cochlear implant (BiCI) listeners has demonstrated significantly poorer performance on motion detection tasks in BiCI listeners. Cochlear implants, auditory protheses offered to profoundly deaf individuals for access to spoken language, retain the signal envelope (ENV), while discarding temporal fine structure (TFS) of the original acoustic input. As a result, BiCI users do not have access to low-frequency TFS cues, which have previously been shown to be crucial for sound localization in NH listeners. Instead, BiCI listeners seem to rely on ENV cues for sound localization, especially level cues. Given that NH and BiCI listeners differentially utilize ENV and TFS information, the present study aimed to investigate the usefulness of these cues for auditory motion perception. We created acoustic chimaera stimuli, which allowed us to test the relative contributions of ENV and TFS to auditory motion perception. Stimuli were either moving or stationary, presented to NH listeners in free field. The task was to track the perceived sound location. We found that removing low-frequency TFS reduces sensitivity to sound motion, and fluctuating speech envelopes strongly biased the judgment of sounds to be stationary. Our findings yield a possible explanation as to why BiCI users struggle to identify sound motion, and provide a first account of cues important to the functional aspect of auditory motion perception.

Echo interval and not echo intensity drives bat flight behavior in structured corridors.

To navigate in the natural environment, animals must adapt their locomotion in response to environmental stimuli. The echolocating bat relies on auditory processing of echo returns to represent its surroundings. Recent studies have shown that echo flow patterns influence bat navigation, but the acoustic basis for flight path selection remains unknown. To investigate this problem, we released bats in a flight corridor with walls constructed of adjacent individual wooden poles, which returned cascades of echoes to the flying bat. We manipulated the spacing and echo strength of the poles comprising each corridor side, and predicted that bats would adapt their flight paths to deviate toward the corridor side returning weaker echo cascades. Our results show that the bat's trajectory through the corridor was not affected by the intensity of echo cascades. Instead, bats deviated toward the corridor wall with more sparsely spaced, highly reflective poles, suggesting that pole spacing, rather than echo intensity, influenced bat flight path selection. This result motivated investigation of the neural processing of echo cascades. We measured local evoked auditory responses in the bat inferior colliculus to echo playback recordings from corridor walls constructed of sparsely and densely spaced poles. We predicted that evoked neural responses would be discretely modulated by temporally distinct echoes recorded from the sparsely spaced pole corridor wall, but not by echoes from the more densely spaced corridor wall. The data confirm this prediction and suggest that the bat's temporal resolution of echo cascades may drive its flight behavior in the corridor.

Echolocation and flight behavior of the bat Hipposideros armiger terasensis in a structured corridor.

In this study, the echolocation and flight behaviors of the Taiwanese leaf-nosed bat (Hipposideros armiger terasensis), which uses constant-frequency (CF) biosonar signals combined with a frequency-modulated (FM) sweep, are compared with those of the big brown bat (Eptesicus fuscus), which uses FM signals alone. The CF-FM bat flew through a corridor bounded by vertical poles on either side, and the inter-pole spacing of the walls was manipulated to create different echo flow conditions. The bat's flight trajectories and echolocation behaviors across corridor conditions were analyzed. Like the big brown bat, the Taiwanese leaf-nosed bat centered its flight trajectory within the corridor when the pole spacing was the same on the two walls. However, the two species showed different flight behaviors when the pole spacing differed on the two walls. While the big brown bat deviated from the corridor center towards the wall with sparse pole spacing, the Taiwanese leaf-nosed bat did not. Further, in comparison to E. fuscus, H. a. terasensis utilized different echolocation patterns showing a prevalence of grouping sounds into clusters of three. These findings indicate that the two species' distinct sonar signal designs contribute to their differences in flight trajectories in a structured corridor.

Dynamic Echo Information Guides Flight in the Big Brown Bat.

Animals rely on sensory feedback from their environment to guide locomotion. For instance, visually guided animals use patterns of optic flow to control their velocity and to estimate their distance to objects (e.g., Srinivasan et al., 1991, 1996). In this study, we investigated how acoustic information guides locomotion of animals that use hearing as a primary sensory modality to orient and navigate in the dark, where visual information is unavailable. We studied flight and echolocation behaviors of big brown bats as they flew under infrared illumination through a corridor with walls constructed from a series of individual vertical wooden poles. The spacing between poles on opposite walls of the corridor was experimentally manipulated to create dense/sparse and balanced/imbalanced spatial structure. The bats' flight trajectories and echolocation signals were recorded with high-speed infrared motion-capture cameras and ultrasound microphones, respectively. As bats flew through the corridor, successive biosonar emissions returned cascades of echoes from the walls of the corridor. The bats flew through the center of the corridor when the pole spacing on opposite walls was balanced and closer to the side with wider pole spacing when opposite walls had an imbalanced density. Moreover, bats produced shorter duration echolocation calls when they flew through corridors with smaller spacing between poles, suggesting that clutter density influences features of the bat's sonar signals. Flight speed and echolocation call rate did not, however, vary with dense and sparse spacing between the poles forming the corridor walls. Overall, these data demonstrate that bats adapt their flight and echolocation behavior dynamically when flying through acoustically complex environments.

Broadband noise exposure does not affect hearing sensitivity in big brown bats (Eptesicus fuscus).

In many vertebrates, exposure to intense sounds under certain stimulus conditions can induce temporary threshold shifts that reduce hearing sensitivity. Susceptibility to these hearing losses may reflect the relatively quiet environments in which most of these species have evolved. Echolocating big brown bats (Eptesicus fuscus) live in extremely intense acoustic environments in which they navigate and forage successfully, both alone and in company with other bats. We hypothesized that bats may have evolved a mechanism to minimize noise-induced hearing losses that otherwise could impair natural echolocation behaviors. The hearing sensitivity of seven big brown bats was measured in active echolocation and passive hearing tasks, before and after exposure to broadband noise spanning their audiometric range (10-100 kHz, 116 dB SPL re. 20 µPa rms, 1 h duration; sound exposure level 152 dB). Detection thresholds measured 20 min, 2 h or 24 h after exposure did not vary significantly from pre-exposure thresholds or from thresholds in control (sham exposure) conditions. These results suggest that big brown bats may be less susceptible to temporary threshold shifts than are other terrestrial mammals after exposure to similarly intense broadband sounds. These experiments provide fertile ground for future research on possible mechanisms employed by echolocating bats to minimize hearing losses while orienting effectively in noisy biological soundscapes.

Target shape perception and clutter rejection use the same mechanism in bat sonar.

Big brown bats (Eptesicus fuscus) emit frequency-modulated (FM) biosonar sounds containing two or more harmonic sweeps. Echoes from frontally located targets arrive with first and second harmonics intact, leading to focused delay images. Echoes from offside or distant objects arrive with the second harmonic relatively weaker (lowpass-filtered), leading to defocused images, which prevents their clutter interference effects (Bates et al. J Exp Biol 214:394-401, 2011). Realistic targets contain several glints at slightly different distances and reflect several echoes at correspondingly different delays. The bat registers the delay of the nearest glint's echoes in the time domain. The delays of echoes from the farther glints are registered in the frequency domain, from interference nulls in the spectrum. Lowpass-filtering of echoes directly affects the image of the nearest glint by defocusing the delay image. However, lowpass-filtering also is superimposed on the interference spectrum used to register the farther glints, which distorts the pattern of interference nulls, defocusing the farther glints inversely, in the spectral domain, before they are perceived as delays. Differences in blurring between time-domain and frequency-domain parts of images identifies separate computational paths to perceptually reconstruct objects and prevent interference from off-side or distant clutter.

Active Listening in a Bat Cocktail Party: Adaptive Echolocation and Flight Behaviors of Big Brown Bats, Eptesicus fuscus, Foraging in a Cluttered Acoustic Environment.

In their natural environment, big brown bats forage for small insects in open spaces, as well as in vegetation and in the presence of acoustic clutter. While searching and hunting for prey, bats experience sonar interference, not only from densely cluttered environments, but also from calls of conspecifics foraging in close proximity. Previous work has shown that when two bats compete for a single prey item in a relatively open environment, one of the bats may go silent for extended periods of time, which can serve to minimize sonar interference between conspecifics. Additionally, pairs of big brown bats have been shown to adjust frequency characteristics of their vocalizations to avoid acoustic interference in echo processing. In this study, we extended previous work by examining how the presence of conspecifics and environmental clutter influence the bat's echolocation behavior. By recording multichannel audio and video data of bats engaged in insect capture in open and cluttered spaces, we quantified the bats' vocal and flight behaviors. Big brown bats flew individually and in pairs in an open and cluttered room, and the results of this study shed light on the different strategies that this species employs to negotiate a complex and dynamic environment.

Flow sensing in developing Xenopus laevis is disrupted by visual cues and ototoxin exposure.

We explored how lateral line cues interact with visual cues to mediate flow sensing behaviors in the nocturnal developing frog, Xenopus laevis, by exposing animals to current flows under different lighting conditions and after exposure to the ototoxin gentamicin. Under dark conditions, Xenopus tadpoles move downstream at the onset of current flow, then turn, and orient toward the direction of the flow with high accuracy. Postmetamorphic froglets also exhibit positive rheotaxis but with less accuracy and longer latency. The addition of discrete light cues to an otherwise dark environment disrupts rheotaxis and positioning. Orientation is less accurate, latency to orient is longer, and animals do not move as far downstream in the presence of light. Compared with untreated tadpoles tested in the dark, tadpoles exposed to gentamicin show less accurate rheotaxis with longer latency and do not move as far downstream in response to flow. These effects are compounded by the presence of light cues. The disruptive effects of light on flow sensing in Xenopus emphasize the disturbances to natural behaviors that may be produced by anthropogenic illumination in nocturnal habitats.

Spatial release from simultaneous echo masking in bat sonar.

Big brown bats (Eptesicus fuscus) use biosonar to navigate and locate objects in their surroundings. During natural foraging, they often encounter echoes returned by a target of interest located to the front while other, often stronger, clutter echoes are returned from objects, such as vegetation, located to the sides or above. Nevertheless, bats behave as if they do not suffer interference from this clutter. Using a two-choice delay discrimination procedure, bats were tested for the masking effectiveness of clutter echoes on target echoes when the target echoes were delivered from the bat's front while clutter echoes were delivered from 90° overhead, a direction of lowpass filtering by the external ears. When clutter echoes are presented from the front at the same delay as target echoes, detection performance declines and clutter masking occurs. When the clutter echoes are presented at the same delay but from overhead, discrimination performance is unaffected and no masking occurs. Thus there is masking release for simultaneous off-axis lowpass clutter compared to masking by simultaneous clutter from the front. The bat's performance for simultaneous target and clutter echoes indicates a new role for the mechanism that separates overlapping echoes by decomposing the bat's auditory time-frequency representation.

High resolution acoustic measurement system and beam pattern reconstruction method for bat echolocation emissions.

Measurements of the transmit beam patterns emitted by echolocating bats have previously been limited to cross-sectional planes or averaged over multiple signals using sparse microphone arrays. To date, no high-resolution measurements of individual bat transmit beams have been reported in the literature. Recent studies indicate that bats may change the time-frequency structure of their calls depending on the task, and suggest that their beam patterns are more dynamic than previously thought. To investigate beam pattern dynamics in a variety of bat species, a high-density reconfigurable microphone array was designed and constructed using low-cost ultrasonic microphones and custom electronic circuitry. The planar array is 1.83 m wide by 1.42 m tall with microphones positioned on a 2.54 cm square grid. The system can capture up to 228 channels simultaneously at a 500 kHz sampling rate. Beam patterns are reconstructed in azimuth, elevation, and frequency for visualization and further analysis. Validation of the array measurement system and post-processing functions is shown by reconstructing the beam pattern of a transducer with a fixed circular aperture and comparing the result with a theoretical model. To demonstrate the system in use, transmit beam patterns of the big brown bat, Eptesicus fuscus, are shown.