Doppler detection triggers instantaneous escape behavior in scanning bats.

Animals must instantaneously escape from predators for survival, which requires quick detection of approaching threats. Although the neural mechanisms underlying the perception of looming objects have been extensively studied in the visual system, little is known about their auditory counterparts. Echolocating bats use their auditory senses to perceive not only the soundscape, but also the physical environment through active sensing. Although object movement induces both echo delay changes and Doppler shifts, the actual information required to perceive movement has been unclear. Herein, we addressed this question by playing back phantom echoes mimicking an approaching target to horseshoe bats and found that they relied only on Doppler shifts. This suggests that the bats do not perceive object motion in the spatiotemporal dimension (i.e., positional variation), as in vision, but rather take advantage of acoustic sensing by directly detecting velocity, thereby enabling them to respond instantaneously to approaching threats.

Discrimination of object information by bat echolocation deciphered from acoustic simulations.

High-precision visual sensing has been achieved by combining cameras with deep learning. However, an unresolved challenge involves identifying information that remains elusive for optical sensors, such as occlusion spots hidden behind objects. Compared to light, sound waves have longer wavelengths and can, therefore, collect information on occlusion spots. In this study, we investigated whether bats could perform advanced sound sensing using echolocation to acquire a target's occlusion information. We conducted a two-alternative forced choice test on Pipistrellus abramus with five different targets, including targets with high visual similarity from the front, but different backend geometries, i.e. occlusion spots or textures. Subsequently, the echo impulse responses produced by these targets, which were difficult to obtain with real measurements, were computed using three-dimensional acoustic simulations to provide a detailed analysis consisting of the acoustic cues that the bats obtained through echolocation. Our findings demonstrated that bats could effectively discern differences in target occlusion spot structure and texture through echolocation. Furthermore, the discrimination performance was related to the differences in the logarithmic spectral distortion of the occlusion-related components in the simulated echo impulse responses. This suggested that the bats obtained occlusion information through echolocation, highlighting the advantages of utilizing broadband ultrasound for sensing.

The distress context of social calls evokes a fear response in the bat Pipistrellus abramus.

Bats primarily use sound information, including echolocation, for social communication. Bats under stressful conditions, for example when confronted by a predator, will emit aggressive social calls. The presentation of aggressive social calls, including distress calls (DCs), is known to increase heart rate (fH), but how this change in fH is related to the bat's sound perception and how this evokes behaviors such as the fear response is unknown. Herein, we show that the perception of a distress context induces freezing behavior as a fear response in bats. We found that bats responded by freezing and displayed increased fH when they were presented with a conspecific donor bat in a distress situation evoked by gentle poking with a cotton swab. In addition, when we presented two types of auditory oddball paradigms with different probabilities of DCs and echolocation calls (ECs), the bats' fH increased when DCs were presented as deviant or control stimuli within standard ECs but did not increase when DCs were presented as standard stimuli. These results suggest that the situational context created by the frequency of sound presentation, rather than simply a single sound feature, induces fH increases and freezing as fear responses in bats.

A glimpse into the foraging and movement behaviour of Nyctalus aviator; a complementary study by acoustic recording and GPS tracking.

Species of open-space bats that are relatively large, such as bats from the genus Nyctalus, are considered as high-risk species for collisions with wind turbines (WTs). However, important information on their behaviour and movement ecology, such as the locations and altitudes at which they forage, is still fragmentary, while crucial for their conservation in light of the increasing threat posed by progressing WT construction. We adopted two different methods of microphone array recordings and GPS-tracking capturing data from different spatio-temporal scales in order to gain a complementary understanding of the echolocation and movement ecology of Nyctalus aviator, the largest open-space bat in Japan. Based on microphone array recordings, we found that echolocation calls during natural foraging are adapted for fast flight in open-space optimal for aerial-hawking. In addition, we attached a GPS tag that can simultaneously monitor feeding buzz occurrence, and confirmed that foraging occurred at 300 m altitude and that the flight altitude in mountainous areas is consistent with the turbine conflict zone, suggesting that the birdlike noctule is a high-risk species in Japan. Further investigations on this species could provide valuable insights into their foraging and movement ecology, facilitating the development of a risk assessment regarding WTs.

Feasibility evaluation of transtympanic laser stimulation of the cochlea from the outer ear.

Infrared laser stimulation has been studied as an alternative approach to auditory prostheses. This study evaluated the feasibility of infrared laser stimulation of the cochlea from the outer ear, bypassing the middle ear function. An optic fiber was inserted into the ear canal, and a laser was used to irradiate the cochlea through the tympanic membrane in Mongolian gerbils. A pulsed infrared laser (6.9 mJ/cm2) and clicking sound (70 peak-to-peak equivalent sound pressure level) were presented to the animals. The amplitude of the laser-evoked cochlear response was systematically decreased following insertion of a filter between the tympanic membrane and cochlea; however, the auditory-evoked cochlear response did not decrease. The filter was removed, and the laser-evoked response returned to around the original level. The amplitude ratio and the relative change in response amplitude before and during filter insertion significantly decreased as the absorbance of the infrared filter increased. These results indicate that laser irradiation could bypass the function of the middle ear and directly activate the cochlea. Therefore, laser irradiation from the outer ear is a possible alternative for stimulating the cochlea, circumventing the middle ear.

Effect of bat pinna on sensing using acoustic finite difference time domain simulation.

The practicality of the finite-difference time-domain (FDTD) method was confirmed by comparing head-related transfer functions obtained from a three-dimensional (3D) digital model of a bat (Rhinolophus ferrumequinum nippon) head with acoustic experiments using a 3D printed physical model. Furthermore, we simulated the auditory directionality using a 3D digital model that was modified based on the pinna movement of a bat during echolocation and found that the alternating movements of the left and right pinna result in a binaural sound pressure difference for vertical sources. Using the FDTD method, suitable for simulating acoustics in large spaces, we could analyze in detail the binaural echoes that bats receive and the acoustic cues they use for echolocation.

Reconstruction of echoes reaching bats in flight from arbitrary targets by acoustic simulation.

Echolocating bats perceive their environment by emitting ultrasonic pulses and listening to echoes that are reflected back from their surroundings. Behavioral decisions of bats are mainly dependent on echo information, and acoustical analysis of echoes is useful for understanding their behavioral decisions. To date, echoes have been measured using a telemetry microphone mounted on the bat's head; however, due to technical difficulties, it was not enough to measure all the echoes reaching the bats in flight. In this paper, we propose an approach to reconstruct the echoes of bats in flight using finite-difference time-domain (FDTD) method simulations based on the measured flight path, speed, and sound information from behavioral experiments. As a result, echoes from any target in flight can be correctly reconstructed, including the Doppler effect. We also analyzed the spatiotemporal transition among attended walls for Doppler shift compensation (DSC) during circling flight in the context of DSC behavior and found that the bats switch their attention to different walls and focus on the wall ahead of them in the direction of flight.

Analysis of echolocation behavior of bats in "echo space" using acoustic simulation.

BACKGROUND: Echolocating bats use echo information to perceive space, control their behavior, and adjust flight navigation strategies in various environments. However, the echolocation behavior of bats, including echo information, has not been thoroughly investigated as it is technically difficult to measure all the echoes that reach the bats during flight, even with the conventional telemetry microphones currently in use. Therefore, we attempted to reproduce the echoes received at the location of bats during flight by combining acoustic simulation and behavioral experiments with acoustic measurements. By using acoustic simulation, echoes can be reproduced as temporal waveforms (including diffracted waves and multiple reflections), and detailed echo analysis is possible even in complex obstacle environments. RESULTS: We visualized the spatiotemporal changes in the echo incidence points detected by bats during flight, which enabled us to investigate the "echo space" revealed through echolocation for the first time. We then hypothesized that by observing the differences in the "echo space" before and after spatial learning, the bats' attentional position would change. To test this hypothesis, we examined how the distribution of visualized echoes concentrated at the obstacle edges after the bats became more familiar with their environment. The echo incidence points appeared near the edge even when the pulse direction was not toward the edge. Furthermore, it was found that the echo direction correlated with the turn rate of the bat's flight path, revealing for the first time the relationship between the echo direction and the bat's flight path. CONCLUSIONS: We were able to clarify for the first time how echoes space affects echolocation behavior in bats by combining acoustic simulations and behavioral experiments.

Discriminating predation attempt outcomes during natural foraging using the post-buzz pause in the Japanese large-footed bat, Myotis macrodactylus.

Bats emit a series of echolocation calls with an increasing repetition rate (the terminal buzz) when attempting to capture prey. This is often used as an acoustic indicator of prey-capture attempts. However, because it is directly linked to foraging efficiency, predation success is a more useful measure than predation attempts in ecological research. The characteristics of echolocation calls that consistently signify predation success across different situations have not been identified. Owing to additional influencing factors, identification of these characteristics is particularly challenging for wild bats foraging in their natural environment compared with those in flight chambers. This study documented the natural foraging behavior of wild Japanese large-footed bats (Myotis macrodactylus) using synchronized acoustic and video recordings. From the video recordings, we could assign 137 attacks to three outcome categories: prey captured (51.8%), prey dropped (29.2%) and failed attempt (19%). Based on previous indications from laboratory studies that the length of the silent interval following the terminal buzz (post-buzz pause) might reflect the prey-capture outcome, we compared post-buzz pause durations among categories of attack outcomes. The post-buzz pause was longest in the case of successful capture, suggesting that the length of the post-buzz pause is a useful acoustic indicator of predation success during natural foraging in M. macrodactylus. Our finding will advance the study of bat foraging behavior using acoustic data, including estimations of foraging efficiency and analyses of feeding habitat quality.

Echo reception in group flight by Japanese horseshoe bats, Rhinolophus ferrumequinum nippon.

The ability to detect behaviourally relevant sensory information is crucial for survival. Especially when active-sensing animals behave in proximity, mutual interferences may occur. The aim of this study was to examine how active-sensing animals deal with mutual interferences. Echolocation pulses and returning echoes were compared in spaces of various sizes (wide and narrow) in Rhinolophus ferrumequinum nippon flying alone or in a group of three bats. We found that in the narrow space, the group-flying bats increased the duration and bandwidth of the terminal frequency-modulated component of their vocalizations. By contrast, the frequency of the returning echoes did not differ in the presence of conspecifics. We found that their own echo frequencies were compensated within the narrow frequency ranges by Doppler shift compensation. By contrast, the estimated frequencies of the received pulses emitted by the other bats were much more broadly distributed than their echoes. Our results suggest that the bat auditory systems are sharply tuned to a narrow frequency to filter spectral interference from other bats.

Music in Noise: Neural Correlates Underlying Noise Tolerance in Music-Induced Emotion.

Music can be experienced in various acoustic qualities. In this study, we investigated how the acoustic quality of the music can influence strong emotional experiences, such as musical chills, and the neural activity. The music's acoustic quality was controlled by adding noise to musical pieces. Participants listened to clear and noisy musical pieces and pressed a button when they experienced chills. We estimated neural activity in response to chills under both clear and noisy conditions using functional magnetic resonance imaging (fMRI). The behavioral data revealed that compared with the clear condition, the noisy condition dramatically decreased the number of chills and duration of chills. The fMRI results showed that under both noisy and clear conditions the supplementary motor area, insula, and superior temporal gyrus were similarly activated when participants experienced chills. The involvement of these brain regions may be crucial for music-induced emotional processes under the noisy as well as the clear condition. In addition, we found a decrease in the activation of the right superior temporal sulcus when experiencing chills under the noisy condition, which suggests that music-induced emotional processing is sensitive to acoustic quality.

Effectiveness of time-varying echo information for target geometry identification in bat-inspired human echolocation.

Bats use echolocation through flexible active sensing via ultrasounds to identify environments suitable for their habitat and foraging. Mimicking the sensing strategies of bats for echolocation, this study examined how humans acquire new acoustic-sensing abilities, and proposes effective strategies for humans. A target geometry identification experiment-involving 15 sighted people without experience of echolocation-was conducted using two targets with different geometries, based on a new sensing system. Broadband frequency-modulated pulses with short inter-pulse intervals (16 ms) were used as a synthetic echolocation signal. Such pulses mimic buzz signals emitted by bats for echolocation prior to capturing their prey. The study participants emitted the signal from a loudspeaker by tapping on Android devices. Because the signal included high-frequency signals up to 41 kHz, the emitted signal and echoes from a stationary or rotating target were recorded using a 1/7-scaled miniature dummy head. Binaural sounds, whose pitch was down-converted, were presented through headphones. This way, time-varying echo information was made available as an acoustic cue for target geometry identification under a rotating condition, as opposed to a stationary one. In both trials, with (i.e., training trials) and without (i.e., test trials) answer feedback immediately after the participants answered, the participants identified the geometries under the rotating condition. Majority of the participants reported using time-varying patterns in terms of echo intensity, timbre, and/or pitch under the rotating condition. The results suggest that using time-varying patterns in echo intensity, timbre, and/or pitch enables humans to identify target geometries. However, performance significantly differed by condition (i.e., stationary vs. rotating) only in the test trials. This difference suggests that time-varying echo information is effective for identifying target geometry through human echolocation especially when echolocators are unable to obtain answer feedback during sensing.

Two-dimensional shape discrimination by sighted people using simulated virtual echoes.

In this study, a new research method using psychoacoustic experiments and acoustic simulations is proposed for human echolocation research. A shape discrimination experiment was conducted for sighted people using pitch-converted virtual echoes from targets of dissimilar two-dimensional (2D) shapes. These echoes were simulated using a three-dimensional acoustic simulation based on a finite-difference time-domain method from Bossy, Talmat, and Laugier [(2004). J. Acoust. Soc. Am. 115, 2314-2324]. The experimental and simulation results suggest that the echo timbre and pitch determined based on the sound interference may be effective acoustic cues for 2D shape discrimination. The newly developed research method may lead to more efficient future studies of human echolocation.

Auditory cortical activity elicited by infrared laser irradiation from the outer ear in Mongolian gerbils.

Infrared neural stimulation has been studied for its potential to replace an electrical stimulation of a cochlear implant. No studies, however, revealed how the technic reliably evoke auditory cortical activities. This research investigated the effects of cochlear laser stimulation from the outer ear on auditory cortex using brain imaging of activity-dependent changes in mitochondrial flavoprotein fluorescence signal. An optic fiber was inserted into the gerbil's ear canal to stimulate the lateral side of the cochlea with an infrared laser. Laser stimulation was found to activate the identified primary auditory cortex. In addition, the temporal profile of the laser-evoked responses was comparable to that of the auditory responses. Our results indicate that infrared laser irradiation from the outer ear has the capacity to evoke, and possibly manipulate, the neural activities of the auditory cortex and may substitute for the present cochlear implants in future.

Modulation of acoustic navigation behaviour by spatial learning in the echolocating bat Rhinolophus ferrumequinum nippon.

Using echolocation, bats receive acoustic information on their surroundings, which is assumed to help them sophisticatedly navigate complex environments. In this study, to understand spatial learning and acoustic sensing in bats, we investigated how flight and echolocation control changed in Rhinolophus ferrumequinum nippon as they learnt about their surroundings in an obstacle course that they flew through repeatedly. In these experiments, two testing environments (acoustically permeable and acoustically reflective) were prepared using chains and acrylic boards as obstacles to evaluate the interactive effects of spatial learning and flight environments. We found that bats reduced the meandering width of their flights and pulse emissions, and also seemed to reduce their shifts in pulse direction as they learnt more about their environments in both conditions. Throughout all our experiments, the bats with slower flight speeds tended to emit more pulses, which suggests that the number of pulse emissions reflects the echolocation tactics of each bat. The maximum flight speed was especially increased in the acoustically permeable condition, with frequent emissions of multiple pulses (≧triplets) in the early stages of flight, suggesting that bats adjust their flight plan based on how much of their surroundings they are able to sense in advance.

Auditory-induced visual illusions in rodents measured by spontaneous behavioural response.

When two brief sounds are presented with a short flash of light, we often perceive that the flash blinks twice. This phenomenon, called the "sound-induced flash illusion", has been investigated as an example of how humans finely integrate multisensory information, more specifically, the temporal content of perception. However, it is unclear whether nonhuman animals experience the illusion. Therefore, we investigated whether the Mongolian gerbil, a rodent with relatively good eyesight, experiences this illusion. The novel object recognition (NOR) paradigm was used to evaluate the gerbil's natural (i.e., untrained) capacity for multimodal integration. A light-emitting diode embedded within an object presented time-varying visual stimuli (different flashing patterns). The animals were first familiarised with repetitive single flashes. Then, various sound stimuli were introduced during test trials. An increase in exploration suggested that the animals perceived a flashing pattern differently only when the contradicting sound (double beeps) was presented simultaneously with a single flash. This result shows that the gerbil may experience the sound-induced flash illusion and indicates for the first time that rodents may have the capacity to integrate temporal content of perception in a sophisticated manner as do humans.

Three forebrain structures directly inform the auditory midbrain of echolocating bats.

Echolocating bats emit various types of vocalizations for navigation and communication, and need to pay attention to vocal sounds. Projections from forebrain centers to auditory centers are involved in the attention to vocalizations, with the inferior colliculus (IC) being the main target of the projections. Here, using a retrograde tracer, we demonstrate that three forebrain structures, namely, the medial prefrontal cortex (mPFC), amygdala, and auditory cortex (AC), send direct descending projections to the central nucleus of IC. We found that all three structures projected to the bilateral IC. A comparison of the patterns of retrogradely labeled cells across animals suggests that the ipsilateral AC-IC projection is topographically organized, whereas mPFC-IC or amygdala-IC projections did not show clear topographic organization. Together with evidence from previous studies, these results suggest that three descending projections to the IC form loops between the forebrain and IC to make attention to various vocal sounds.

STEFTR: A Hybrid Versatile Method for State Estimation and Feature Extraction From the Trajectory of Animal Behavior.

Animal behavior is the final and integrated output of brain activity. Thus, recording and analyzing behavior is critical to understand the underlying brain function. While recording animal behavior has become easier than ever with the development of compact and inexpensive devices, detailed behavioral data analysis requires sufficient prior knowledge and/or high content data such as video images of animal postures, which makes it difficult for most of the animal behavioral data to be efficiently analyzed. Here, we report a versatile method using a hybrid supervised/unsupervised machine learning approach for behavioral state estimation and feature extraction (STEFTR) only from low-content animal trajectory data. To demonstrate the effectiveness of the proposed method, we analyzed trajectory data of worms, fruit flies, rats, and bats in the laboratories, and penguins and flying seabirds in the wild, which were recorded with various methods and span a wide range of spatiotemporal scales-from mm to 1,000 km in space and from sub-seconds to days in time. We successfully estimated several states during behavior and comprehensively extracted characteristic features from a behavioral state and/or a specific experimental condition. Physiological and genetic experiments in worms revealed that the extracted behavioral features reflected specific neural or gene activities. Thus, our method provides a versatile and unbiased way to extract behavioral features from simple trajectory data to understand brain function.

Bat-inspired signal design for target discrimination in human echolocation.

Echolocating bats exhibit sophisticated sonar behaviors using ultrasounds with actively adjusted acoustic characteristics (e.g., frequency and time-frequency structure) depending on the situation. In this study, the utility of ultrasound in human echolocation was examined. By listening to ultrasonic echoes with a shifted pitch to be audible, the participants (i.e., sighted echolocation novices) could discriminate the three-dimensional (3D) roundness of edge contours. This finding suggests that sounds with suitable wavelengths (i.e., ultrasounds) can provide useful information about 3D shapes. In addition, the shape, texture, and material discrimination experiments were conducted using ultrasonic echoes binaurally measured with a 1/7 scaled miniature dummy head. The acoustic and statistical analyses showed that intensity and timbre cues were useful for shape and texture discriminations, respectively. Furthermore, in the discrimination of objects with various features (e.g., acrylic board and artificial grass), the perceptual distances between objects were more dispersed when frequency-modulated sweep signals were used than when a constant-frequency signal was used. These suggest that suitable signal design, i.e., echolocation sounds employed by bats, allowed echolocation novices to discriminate the 3D shape and texture. This top-down approach using human subjects may be able to efficiently help interpret the sensory perception, "seeing by sound," in bat biosonar.

Biosonar interpulse intervals and pulse-echo ambiguity in four species of echolocating bats.

In complex biosonar scenes, the delay of echoes represents the spatial distribution of objects in depth. To avoid overlap of echo streams from successive broadcasts, individual echolocation sounds should only be emitted after all echoes of previous sounds have returned. However, close proximity of obstacles demands rapid pulse updates for steering to avoid collisions, which often means emitting a new sound before all of the previous echoes have returned. When two echo streams overlap, there is ambiguity about assigning echoes to the corresponding broadcasts. In laboratory tests of flight in dense, cluttered scenes, four species of echolocating bats exhibited different patterns of pulse emissions to accommodate potential pulse-echo ambiguity. Miniopterus fuliginosus emitted individual FM pulses only after all echoes of previous pulses had returned, with no alternating between long and short intervals. Pipistrellus abramus and Eptesicus fuscus alternated between emitting long FM pulse intervals to receive all echoes before the next pulse, and short intervals to update the rapidly changing scene while accepting partial overlap of successive echo streams. Rhinolophus ferrumequinum nippon transmitted CF/FM pulses in alternating short and long intervals, usually two to four closely spaced sounds that produced overlapping echo streams, followed by a longer interval that separated echo streams. Rhinolophus f. nippon is a statistical outlier from the three FM species, which are more similar to each other. The repeated overlap of CF/FM echo streams suggests that CF components have a distinct role in rejection of clutter and mitigation of ambiguity.