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.

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.

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.

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.

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.

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.

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.

USVSEG: A robust method for segmentation of ultrasonic vocalizations in rodents.

Rodents' ultrasonic vocalizations (USVs) provide useful information for assessing their social behaviors. Despite previous efforts in classifying subcategories of time-frequency patterns of USV syllables to study their functional relevance, methods for detecting vocal elements from continuously recorded data have remained sub-optimal. Here, we propose a novel procedure for detecting USV segments in continuous sound data containing background noise recorded during the observation of social behavior. The proposed procedure utilizes a stable version of the sound spectrogram and additional signal processing for better separation of vocal signals by reducing the variation of the background noise. Our procedure also provides precise time tracking of spectral peaks within each syllable. We demonstrated that this procedure can be applied to a variety of USVs obtained from several rodent species. Performance tests showed this method had greater accuracy in detecting USV syllables than conventional detection methods.

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.

Brain Activity Related to Sound Symbolism: Cross-modal Effect of an Aurally Presented Phoneme on Judgment of Size.

Sound symbolism is the idea that a sound makes a certain impression (e.g., phoneme "p" is associated with an impression of smallness) and could be the psychological basis of the word-meaning association. In this study, we investigated the neural basis of sound symbolism. Subjects were required to compare the visual sizes of standard and target stimuli while listening to syllables assumed to create either a larger or smaller impression. Stimulus-response congruence is defined as the agreement between the target size and the syllable's impression. Behavioral data showed that the subjects displayed a longer reaction time under the incongruent condition than under the congruent condition, indicating that they tended to associate the object size with certain syllables. We used functional magnetic resonance imaging to evaluate the cerebral activity during the task, and found that both semantic- and phonetic-process-related areas of the brain (left middle temporal gyrus and right superior temporal gyrus, respectively) were activated under the incongruent condition. These results suggest that these regions are associated with the incongruence of sound symbolism.

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.

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.

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.

Bats enhance their call identities to solve the cocktail party problem.

Echolocating bats need to solve the problem of signal jamming by conspecifics when they are in a group. However, while several mechanisms have been suggested, it remains unclear how bats avoid confusion between their own echoes and interfering sounds in a complex acoustic environment. Here, we fixed on-board microphones onto individual frequency-modulating bats flying in groups. We found that group members broaden the inter-individual differences in the terminal frequencies of pulses, thereby decreasing the similarity of pulses among individuals. To understand what features most affect similarity between pulses, we calculated the similarity of signals mimicking pulses. We found that the similarity between those artificial signals was decreased most by manipulation of terminal frequency. These results demonstrate that the signal jamming problem is solved by this simple strategy, which may be universally used by animals that use active sensing, such as echolocating bats and electric fish, thereby transcending species and sensory modalities.

Organization of subcortical auditory nuclei of Japanese house bat (Pipistrellus abramus) identified with cytoarchitecture and molecular expression.

The auditory system of echolocating bats shows remarkable specialization likely related to analyzing echoes of sonar pulses. However, significant interspecies differences have been observed in the organization of auditory pathways among echolocating bats, and the homology of auditory nuclei with those of non-echolocating species has not been established. Here, in order to establish the homology and specialization of auditory pathways in echolocating bats, the expression of markers for glutamatergic, GABAergic, and glycinergic phenotypes in the subcortical auditory nuclei of Japanese house bat (Pipistrellus abramus) was evaluated. In the superior olivary complex, we identified the medial superior olive and superior paraolivary nuclei as expressing glutamatergic and GABAergic phenotypes, respectively, suggesting these nuclei are homologous with those of rodents. In the nuclei of the lateral lemniscus (NLL), the dorsal nucleus was found to be purely GABAergic, the intermediate nucleus was a mixture of glutamatergic and inhibitory neurons, the compact part of the ventral nucleus was purely glycinergic, and the multipolar part of the ventral nucleus expressed both GABA and glycine. In the inferior colliculus (IC), the central nucleus was found to be further subdivided into dorsal and ventral parts according to differences in the density of terminals and the morphology of large GABAergic neurons, suggesting specialization to sonar pulse structure. Medial geniculate virtually lacked GABAergic neurons, suggesting that the organization of the tectothalamic pathway is similar with that of rodents. Taken together, our findings revealed that specialization primarily occurs with regard to nuclei size and organization of the NLL and IC.