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.

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.

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.

Adaptive frequency shifts of echolocation sounds in Miniopterus fuliginosus according to the frequency-modulated pattern of jamming sounds.

When flying in a group, echolocating bats have to separate their own echoes from pulses and echoes belonging to other individuals to extract only the information necessary for their own navigation. Previous studies have demonstrated that frequency-modulated (FM) bats change the terminal frequencies (TFs) of downward FM pulses under acoustic interference. However, it is not yet clear which acoustic characteristics of the jamming signals induce the TF shift according to the degree of acoustic interference. In this study, we examined changes in the acoustic characteristics of pulses emitted by Miniopterus fuliginosus while presenting jamming stimuli with different FM patterns to the bat flying alone. Bats significantly altered their TFs when responding to downward (dExp) and upward (uExp) exponential FM sounds as well as to a constant-frequency (CF) stimulus, by approximately 1-2 kHz (dExp: 2.1±0.9 kHz; uExp: 1.7±0.3 kHz; CF: 1.3±0.4 kHz) but not for linear FM sounds. The feature common to the spectra of these three jamming stimuli is a spectrum peak near the TF frequency, demonstrating that the bats shift the TF to avoid masking of jamming sounds on the TF frequency range. These results suggest that direct frequency masking near the TF frequency range induces the TF shift, which simultaneously decreases the similarity between their own echolocation sounds and jamming signals.

Hearing sensitivity evaluated by the auditory brainstem response in Miniopterus fuliginosus.

This study evaluated the hearing sensitivity of Miniopterus fuliginosus, a frequency-modulating (FM) bat species, by measuring the auditory brainstem responses in the inferior colliculus. The average audiogram was U-shaped. The mean threshold decreased gradually as the frequency increased from 16 to 40 kHz and then decreased rapidly as the frequency reached 46 kHz, with the peak sensitivity occurring at the terminal portion of the echolocation pulse between frequencies of 44 and 56 kHz. The shape of audiogram of M. fuliginosus is consistent with other FM bats, and is compared with its vocalization behavior.

Acoustic characteristics used by Japanese macaques for individual discrimination.

The vocalizations of primates contain information about speaker individuality. Many primates, including humans, are able to distinguish conspecifics based solely on vocalizations. The purpose of this study was to investigate the acoustic characteristics used by Japanese macaques in individual vocal discrimination. Furthermore, we tested human subjects using monkey vocalizations to evaluate species specificity with respect to such discriminations. Two monkeys and five humans were trained to discriminate the coo calls of two unfamiliar monkeys. We created a stimulus continuum between the vocalizations of the two monkeys as a set of probe stimuli (whole morph). We also created two sets of continua in which only one acoustic parameter, fundamental frequency (f0) or vocal tract characteristic (VTC), was changed from the coo call of one monkey to that of another while the other acoustic feature remained the same (f0 morph and VTC morph, respectively). According to the results, the reaction times both of monkeys and humans were correlated with the morph proportion under the whole morph and f0 morph conditions. The reaction time to the VTC morph was correlated with the morph proportion in both monkeys, whereas the reaction time in humans, on average, was not correlated with morph proportion. Japanese monkeys relied more consistently on VTC than did humans for discriminating monkey vocalizations. Our results support the idea that the auditory system of primates is specialized for processing conspecific vocalizations and suggest that VTC is a significant acoustic feature used by Japanese macaques to discriminate conspecific vocalizations.

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.

Safety evaluations for transtympanic laser stimulation of the cochlea in Mongolian gerbils (Meriones unguiculatus).

Infrared laser stimulation of the cochlea has been proposed as a possible alternative to conventional auditory prostheses. Whereas previous studies have focused primarily on the short-term effects of laser stimulation, the practical application of this technics requires an investigation into whether prolonged laser exposure can induce neural responses and safely. This study assessed the effect of laser-induced damage to the cochlea on auditory perception using Mongolian gerbils (Meriones unguiculatus) trained with a classical conditioning task. The broadband noise was presented as a conditioned stimulus, and reward licking was recorded as a conditioned response. After training, the subject's cochlea was exposed to a continuous pulsed laser for 15 h. Broadband noise of various intensities was presented without pairing it with water before and after laser exposure to assess the decrease in auditory perception due to laser-induced injury. The licking rate did not change after laser exposure of 6.6 W/cm2 or weaker but drastically decreased after 26.4 W/cm2 or higher. These findings showed, for the first time, that the safety margin of long-term, at least several hours, cochlear laser stimulation exists and will contribute to the appropriate delimitation of the safe and effective laser stimulation parameters in future research.

Subjective Audibility Modulates the Susceptibility to Sound-Induced Flash Illusion: Effect of Loudness and Auditory Masking.

When a brief flash is presented along with two brief sounds, the single flash is often perceived as two flashes. This phenomenon is called a sound-induced flash illusion, in which the auditory sense, with its relatively higher reliability in providing temporal information, modifies the visual perception. Decline of audibility due to hearing impairment is known to make subjects less susceptible to the flash illusion. However, the effect of decline of audibility on susceptibility to the illusion has not been directly investigated in subjects with normal hearing. The present study investigates the relationship between audibility and susceptibility to the illusion by varying the sound pressure level of the stimulus. In the task for reporting the number of auditory stimuli, lowering the sound pressure level caused the rate of perceiving two sounds to decrease on account of forward masking. The occurrence of the illusory flash was reduced as the intensity of the second auditory stimulus decreased, and was significantly correlated with the rate of perceiving the two auditory stimuli. These results suggest that the susceptibility to sound-induced flash illusion depends on the subjective audibility of each sound.

Cortico-striatal activity associated with fidget spinner use: an fMRI study.

Fidget spinners are said to be a very successful toy, and it's said that it has a good impact on attention for children with ADHD and hand motor control. However, there is limited scientific evidence to support these claims, and there is a lack of data on neurobiological responses to rotating fidget spinners. To better understand the mechanism whereby fidget spinners affect motor behavior, we tried to identify the neural correlates of rotating fidget spinners using functional magnetic resonance imaging and non-magnetic fidget spinners with five types of ease of rotation. As a result, we confirmed that the pre/postcentral gyrus, middle temporal gyrus, supplementary motor area (SMA), cerebellum, and striatum are activated when rotating spinners. Furthermore, the SMA was activated more with easier-to-rotate spinners. Additionally, a psychophysiological interaction analysis revealed increased functional connectivity between the SMA and the caudate while rotating fidget spinners compared to just holding them. These results suggest that the fine motor control associate with spinning a fidget spinner is supported by the cortico-striatal circuits involved in planning and reward.

Convergence of reference frequencies by multiple CF-FM bats (Rhinolophus ferrumequinum nippon) during paired flights evaluated with onboard microphones.

The constant frequency component of the second harmonic (CF(2)) of echolocation sounds in Rhinolophus ferrumequinum nippon were measured using onboard telemetry microphones while the bats exhibited Doppler-shift compensation during flights with conspecifics. (1) The CF(2) frequency of pulses emitted by individual bats at rest (F (rest)) showed a long-term gradual decline by 0.22 kHz on average over a period of 3 months. The mean neighboring F (rest) (interindividual differences in F (rest) between neighboring bats when the bats were arranged in ascending order according to F (rest)) ranged from 0.08 to 0.11 kHz among 18 bats in a laboratory colony. (2) The standard deviation of observed echo CF(2) (reference frequency) for bats during paired flights ranged from 50 to 90 Hz, which was not significantly different from that during single flights. This finding suggests that during paired flights, bats exhibit Doppler-shift compensation with the same accuracy as when they fly alone. (3) In 60% (n = 29) of the cases, the difference in the reference frequency between two bats during paired flights significantly decreased compared to when the bats flew alone. However, only 15% of the cases (n = 7) showed a significant increase during paired flights. The difference in frequency between two bats did not increase even when the reference frequencies of the individuals were not statistically different during single flights.

Classification of vocalizations in the Mongolian gerbil, Meriones unguiculatus.

The Mongolian gerbil (Meriones unguiculatus) has been an important model system in auditory physiology, but its natural sounds are not well known. Vocalizations produced by colonies of adult gerbils were recorded during various social interactions in a standard laboratory animal-rearing facility. Sound recordings were made continuously for 24 h. This species exhibited a rich repertoire of vocalizations that varied in spectrotemporal structure. Calls were classified into 13 distinct syllable types. These syllables were further categorized into eight simple syllables and five composite syllables, which could be described by combinations of two to three simple syllables. The durations of individual syllables ranged from 30 to 330 ms with fundamental frequencies of 5 to 50 kHz. Those with lower fundamental frequencies typically contained more harmonic components (up to nine). Analysis of syllable sequences indicated that syllables may be combined into three types of simple phrases. These results provide a basis for future studies not only of the behavioral significance of vocalization, but also of the neural basis of vocal communication in the Mongolian gerbil.

Behavioral evidence for auditory induction in a species of rodent: Mongolian gerbil (Meriones unguiculatus).

When a segment of sound of interest is interrupted by a loud extraneous noise, humans perceive that the missing sound continues during the intrusive noise. This restoration of auditory information occurs in perceptions of both speech and non-speech sounds (e.g., tone bursts), a phenomenon referred to as auditory induction. In this study, Mongolian gerbils were trained with standard Go/No-Go operant conditioning to discriminate continuous tone bursts (the Go stimulus) from tone bursts with a silent gap in the middle (the No-Go stimulus). Noise was added to Go and No-Go stimuli to determine the condition under which induction would occur. The Mongolian gerbils engaged in Go responses to No-Go stimuli only when the noise spectrally surrounding the tone was of the same duration as the silent portion of the No-Go stimulus; these results match those previously reported in primates (humans and macaque monkeys). The result presents not only the evidence of the auditory induction in a rodent species but also suggests that similar mechanisms for restoring missing sounds are shared among mammals. Additionally, our findings demonstrated that the rodent can serve as a valuable animal model for future studies of perceptual restoration.

Vocalization of echolocation-like pulses for interindividual interaction in horseshoe bats (Rhinolophus ferrumequinum).

Although much is known about the echolocation of horseshoe bats (Rhinolophus spp.), little is known about the characteristics and function of their communication calls. This study focused on a stereotyped behavior of a bat approaching a companion animal in the colony, and examined their interaction and vocalization during this behavior. The bats emit echolocation-like vocalizations when approaching each other and these vocalizations contain a "buildup" pulse sequence, in which the frequency of the pulse increases gradually to normal echolocation pulse frequencies. The results suggest that the echolocation-like pulses serve an important role in communication within the colony.

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.

Vocalization during agonistic encounter in Mongolian gerbils: Impact of sexual experience.

Behaviors and vocalizations associated with aggression are essential for animals to survive, reproduce, and organize social hierarchy. Mongolian gerbils (Meriones unguiculatus) are highly aggressive and frequently emit calls. We took advantage of these features to study the relationship between vocalizations and aggressive behaviors in virgin and sexually experienced male and female Mongolian gerbils through the same-sex resident-intruder test. Both sexes of resident gerbils exhibited aggressive responses toward intruders. Multiparous females exhibited the most aggressive responses among the four groups. We also confirmed two groups of vocalizations during the encounters: high-frequency (>24.6 kHz) and low-frequency (<24.6 kHz). At the timing of high-frequency vocalizations observed during the tests, the vast majority (96.2%) of the behavioral interactions were non-agonistic. While, at the timing of low-frequency vocalizations observed during the tests, around half (45%) of the behavioral interactions were agonistic. Low-frequency vocalizations were observed mainly during encounters in which multiparous females were involved. These results suggest that high- and low-frequency vocalizations relate to non-agonistic and agonistic interactions, respectively. In addition to affecting aggressive behavior, sexual experience also affects vocalization during encounters. These findings provide new insights into the modulatory effects of sex and sexual experience on vocalizations during agonistic encounters.

Vocalization control in Mongolian gerbils (Meriones unguiculatus) during locomotion behavior.

The vocalization behavior of Mongolian gerbils, a model animal of auditory physiology, was examined. A pair of gerbils was placed in a chamber, and their species-specific vocalizations and locomotive behaviors were recorded and analyzed. Two types of calls were predominantly produced: high-frequency upward frequency-modulated (HU-FM) calls and low-frequency multi-harmonic frequency-modulated (LM-FM) calls. Emission rates of HU-FM calls significantly decreased as the distance between the two gerbils increased, and playback of simulated HU-FM calls increased the emission rates. Acoustic analysis of HU-FM calls showed that the calls exhibited a stereotypic spectro-temporal structure including a fixed inter-onset interval (100-175 ms) and that individual differences in the frequency could convey the body size of the callers. The timing of HU-FM calls was highly synchronized with jump movements when an animal vocalized while jumping, suggesting the existence of tight locomotor-vocal coupling. Conversely, LM-FM calls were observed only when the gerbils tactilely contacted with each other while fighting over a food. These results suggest that Mongolian gerbils change the rates of call emissions and call types (e.g., LM-FM or HU-FM calls) in response to changes in visual and possibly tactile and auditory information. The functions of both calls are discussed in terms of their acoustic structures.

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.

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.