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Funding: The research was funded by the Human Frontiers Science Program (grant no. RGP0058/2016), awarded to L.W. and S.C.V. S.C.V. was supported by a Max Planck Research Group (MPRG) and a UKRI Future Leaders Fellowship (MR/T021985/1). M.S. was funded by a grant from Deutsche Forschungsgemeinschaft (no. wi1518/17). Human vocal development and speech learning require acoustic feedback, and humans who are born deaf do not acquire a normal adult speech capacity. Most other mammals display a largely innate vocal repertoire. Like humans, bats are thought to be one of the few taxa capable of vocal learning as they can acquire new vocalizations by modifying vocalizations according to auditory experiences. We investigated the effect of acoustic deafening on the vocal development of the pale spear-nosed bat. Three juvenile pale spear-nosed bats were deafened, and their vocal development was studied in comparison with an age-matched, hearing control group. The results show that during development the deafened bats increased their vocal activity, and their vocalizations were substantially altered, being much shorter, higher in pitch, and more aperiodic than the vocalizations of the control animals. The pale spear-nosed bat relies on auditory feedback for vocal development and, in the absence of auditory input, species-atypical vocalizations are acquired. This work serves as a basis for further research using the pale spear-nosed bat as a mammalian model for vocal learning, and contributes to comparative studies on hearing impairment across species. Publisher PDF

Tropical ecosystems are known for high species diversity. Adaptations permitting niche differentiation enable species to coexist. Historically, research focused primarily on morphological and behavioral adaptations for foraging, roosting, and other basic ecological factors. Another important factor, however, is differences in sensory capabilities. So far, studies mainly have focused on the output of behavioral strategies of predators and their prey preference. Understanding the coexistence of different foraging strategies, however, requires understanding underlying cognitive and neural mechanisms. In this study, we investigate hearing in bats and how it shapes bat species coexistence. We present the hearing thresholds and echolocation calls of 12 different gleaning bats from the ecologically diverse Phyllostomid family. We measured their auditory brainstem responses to assess their hearing sensitivity. The audiograms of these species had similar overall shapes but differed substantially for frequencies below 9 kHz and in the frequency range of their echolocation calls. Our results suggest that differences among bats in hearing abilities contribute to the diversity in foraging strategies of gleaning bats. We argue that differences in auditory sensitivity could be important mechanisms shaping diversity in sensory niches and coexistence of species.

Summary Echo-imaging evolved as the main remote sense under lightless conditions. It is most precise in the third dimension (depth) rather than in the visually dominating dimensions of azimuth and elevation. We asked how the auditory system accesses spatial information in the dimensions of azimuth and elevation with a sensory apparatus that is fundamentally different from vision. We quantified echo-acoustic parameters of surface-wave patterns with impulse-response recordings and quantified bats' perceptual sensitivity to such patterns with formal psychophysics. We demonstrate that the spectro-temporal auditory representation of a wave pattern implicitly encodes its spatial frequency. We further show that bats are much more sensitive to wave patterns of high spatial frequencies than of low spatial frequencies. We conclude that echo-imaging accesses spatial information by exploiting an inherent environmental high-pass filter for spatial frequency. The functional similarities yet mechanistic differences between visual and auditory system signify convergent evolution of spatial-information processing., Graphical Abstract, Highlights • Echo-imaging displays the depth dimension, but elevation or azimuth must be computed • Yet, the auditory representation of a surface pattern encodes its spatial frequency • Echolocating bats spot high spatial frequencies much better than low ones • Vision and hearing share functional similarities yet show mechanistic differences, Acoustics; Bioacoustics; Biological Sciences; Zoology

Humans possess mechanisms to suppress distracting early sound reflections, summarized as the precedence effect. Recent work shows that precedence is affected by visual stimulation. This paper investigates possible effects of visual stimulation on the perception of later reflections, i.e., reverberation. In a highly immersive audio-visual virtual reality environment, subjects were asked to quantify reverberation in conditions where simultaneously presented auditory and visual stimuli either match in room identity, sound source azimuth, and sound source distance, or diverge in one of these aspects. While subjects reliably judged reverberation across acoustic environments, the visual room impression did not affect reverberation estimates.

This study was financed by a Heisenberg Fellowship (DFG KN935 5-1) awarded to M.K. and a Human Frontier Science Program Research grant no. (RGP0058/2016) awarded to L.W. and S.C.V. S.C.V. was also funded by the Max Planck Society. M.D. received funding from a grant of the German Ministry of Education and Research (BMBF) to the German Centre for Vertigo and Balance Disorders (01EO1401). E.Z.L. was funded by a short-term stipend of the German Academic Exchange Program (DAAD) (no. 57438025) and a travelling fellowship of the Company of Biologists (JEBTF18113). Moreover, the research leading to these results has received funding from the European Research Council under the European Union's Horizon 2020 Programme (2014–2020)/ERC GA 804352. Differences in auditory perception between species are influenced by phylogenetic origin and the perceptual challenges imposed by the natural environment, such as detecting prey- or predator-generated sounds and communication signals. Bats are well suited for comparative studies on auditory perception since they predominantly rely on echolocation to perceive the world, while their social calls and most environmental sounds have low frequencies. We tested if hearing sensitivity and stimulus level coding in bats differ between high and low-frequency ranges by measuring auditory brainstem responses (ABRs) of 86 bats belonging to 11 species. In most species, auditory sensitivity was equally good at both high- and low-frequency ranges, while amplitude was more finely coded for higher frequency ranges. Additionally, we conducted a phylogenetic comparative analysis by combining our ABR data with published data on 27 species. Species-specific peaks in hearing sensitivity correlated with peak frequencies of echolocation calls and pup isolation calls, suggesting that changes in hearing sensitivity evolved in response to frequency changes of echolocation and social calls. Overall, our study provides the most comprehensive comparative assessment of bat hearing capacities to date and highlights the evolutionary pressures acting on their sensory perception. Publisher PDF

Funding: The research was funded by Human Frontiers Science Program Research Grant RGP0058/2016, awarded to L.W. and S.C.V.S.C.V is funded by a Max Planck Research Group Award from the Max Planck Gesellschaft. Vocal production learning (VPL), or the ability to modify vocalizations through the imitation of sounds, is a rare trait in the animal kingdom. While humans are exceptional vocal learners, few other mammalian species share this trait. Owing to their singular ecology and lifestyle, bats are highly specialized for the precise emission and reception of acoustic signals. This specialization makes them ideal candidates for the study of vocal learning, and several bat species have previously shown evidence supportive of vocal learning. Here we use a sophisticated automated set-up and a contingency training paradigm to explore the vocal learning capacity of pale spear-nosed bats. We show that these bats are capable of directional change of the fundamental frequency of their calls according to an auditory target. With this study, we further highlight the importance of bats for the study of vocal learning and provide evidence for the VPL capacity of the pale spear-nosed bat. Publisher PDF

Many echolocating bats forage close to vegetation - a chaotic arrangement of prey and foliage where multiple targets are positioned behind one another. Bats excel at determining distance: they measure the delay between outgoing call and returning echo. In their auditory cortex, delay-sensitive neurons form a topographic map, suggesting that bats can resolve echoes of multiple targets along the distance axis - a skill crucial for the forage-amongst-foliage scenario. We tested this hypothesis combining an auditory virtual reality with formal psychophysics: We simulated a prey item embedded in two foliage elements, one in front of and one behind the prey. The simulated spacing between “prey” (target) and “foliage” (maskers) was defined by the inter-masker delay (IMD). We trained Phyllostomus discolor bats to detect the target in the presence of the maskers, systematically varying both loudness and spacing of the maskers. We show that target detection is impaired when maskers are closely spaced (IMD

Echolocating bats measure target distance by the time delay between call and echo. Target movement such as the flutter of insect wings induces delay modulations. Perception of delay modulations has been studied extensively in bats, but only concerning how well bats discriminate flutter frequencies, never with regard to flutter magnitude. We used an auditory virtual reality approach to generate changes in echo delay that were independent of call repetition rate, mimicking fluttering insect wings. We show that in the frequency-modulating (FM) bat Phyllostomus discolor, the sensitivity for modulations in echo delay depends on the rate of the modulation, with bats being most sensitive at modulation rates below 20 Hz and above 50 Hz. The very short duration of their calls compels FM bats to evaluate slow modulations (

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

Summary The estimation of one’s distance to a potential threat is essential for any animal’s survival. Rattlesnakes inform about their presence by generating acoustic broadband rattling sounds. 1 Rattlesnakes generate their acoustic signals by clashing a series of keratinous segments onto each other, which are located at the tip of their tails. 1 , 2 , 3 Each tail shake results in a broadband sound pulse that merges into a continuous acoustic signal with fast-repeating tail shakes. This acoustic display is readily recognized by other animals 4 , 5 and serves as an aposematic threat and warning display, likely to avoid being preyed upon. 1 , 6 The spectral properties of the rattling sound 1 , 3 and its dependence on the morphology and size of the rattle have been investigated for decades 7 , 8 , 9 and carry relevant information for different receivers, including ground squirrels that encounter rattlesnakes regularly. 10 , 11 Combining visual looming stimuli with acoustic measurements, we show that rattlesnakes increase their rattling rate (up to about 40 Hz) with decreasing distance of a potential threat, reminiscent of the acoustic signals of sensors while parking a car. Rattlesnakes then abruptly switch to a higher and less variable rate of 60–100 Hz. In a virtual reality experiment, we show that this behavior systematically affects distance judgments by humans: the abrupt switch in rattling rate generates a sudden, strong percept of decreased distance which, together with the low-frequency rattling, acts as a remarkable interspecies communication signal. Video abstract Download : Download video (68MB)

The mammalian visual system is highly directional and mammals typically employ rapid eye movements to scan their environment. Both sound emission and hearing in echolocating bats are directional but not much is known about how bats use ear movements and possibly movements of the sound-emitting structures to scan space. Here, we investigated in a tightly controlled behavioural experiment how Phyllostomus discolor bats employ their echolocation system while being moved through differently structured environments: we monitored and reconstructed both a close-up of the facial structures in 3D, including the motile noseleaf and outer ears, and the sonar-beam of the bat while it was moved along reflectors. Despite the simple linear movement of the bats in the setup, the bats pointed their beam quite variably in azimuth with a standard deviation of about ±20 deg. This variation arises from yaw-type head rotations. Video analyses show that the bat's noseleaf twitches with every echolocation call. Second, we show that the bat's ears are raised to a rather stereotypical head-centred position with every echolocation call. Surprisingly, P. discolor can adjust the timing and the magnitude of these ear movements to the distance of the reflectors with millisecond precision. Our findings reveal echolocation-specific specialisations as well as general principles of scanning and stabilisation of a directional remote sense. The call-correlated movements of the facial structures may lead to a higher directionality of the echolocation system and may enable the bats to adjust their echo-acoustic gaze to dynamic environments.

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

Humans often have to focus on a single target sound while ignoring competing maskers in everyday situations. In such conditions, speech intelligibility (SI) is improved when a target speaker is spatially separated from a masker (spatial release from making, SRM) compared to situations where both are co-located. Such asymmetric spatial configurations lead to a ‘better-ear effect’ with improved signal-to-noise ratio (SNR) at one ear. However, maskers often surround the listener leading to more symmetric configurations where better-ear effects are absent in a long-term, wideband sense. Nevertheless, better-ear glimpses distributed across time and frequency persist and were suggested to account for SRM (Brungart and Iyer 2012). Here, speech reception was assessed using symmetric masker configurations while varying the spatio-temporal distribution of potential better-ear glimpses. Listeners were presented with a frontal target and eight single-talker maskers in four different symmetrical spatial configurations. Compared to the reference condition with co-located target and maskers, an SRM of up to 6 dB was observed. The SRM persisted when the frequency range of the maskers above or below 1500 Hz was replaced with stationary speech-shaped noise. Comparison to a recent short-time binaural SI model showed that better-ear glimpses can account for half the observed SRM, while binaural interaction utilizing phase differences is required to explain the other half.

Intense, low-frequency sound presented to the mammalian cochlea induces temporary changes of cochlear sensitivity, for which the term ‘Bounce’ phenomenon has been coined. Typical manifestations are slow oscillations of hearing thresholds or the level of otoacoustic emissions. It has been suggested that these alterations are caused by changes of the mechano-electrical transducer transfer function of outer hair cells (OHCs). Shape estimates of this transfer function can be derived from low-frequency-biased distortion product otoacoustic emissions (DPOAE). Here, we tracked the transfer function estimates before and after triggering a cochlear Bounce. Specifically, cubic DPOAEs, modulated by a low-frequency biasing tone, were followed over time before and after induction of the cochlear Bounce. Most subjects showed slow, biphasic changes of the transfer function estimates after low-frequency sound exposure relative to the preceding control period. Our data show that the operating point changes biphasically on the transfer function with an initial shift away from the inflection point followed by a shift towards the inflection point before returning to baseline values. Changes in transfer function and operating point lasted for about 180 s. Our results are consistent with the hypothesis that intense, low-frequency sound disturbs regulatory mechanisms in OHCs. The homeostatic readjustment of these mechanisms after low-frequency offset is reflected in slow oscillations of the estimated transfer functions.

Echolocating bats are known to fly and forage in complete darkness using the echoes of their actively emitted calls to navigate and to detect prey. However, under dim light conditions many bats can also rely on vision. Many flying animals have been shown to navigate by optic flow information, and recently, bats were shown to exploit echo-acoustic flow to navigate through dark habitats. Here we show for the bat Phyllostomus discolor that in lighted habitats where self-motion induced optic flow is strong, optic and echo-acoustic flow interact in their efficiency to guide navigation. Echo-acoustic flow showed a surprisingly strong effect compared to optic flow. We thus demonstrate multimodal interaction between two far-ranging spatial senses, vision and echolocation, available in this combination almost exclusively for bats and toothed whales. Our results highlight the importance of merging information from different sensory systems in a sensory-specialist animal to successfully navigate and hunt under difficult conditions.

Bats are navigation super-performers, flying at high speed through nocturnal forests. Numerous field observations and formal experiments have impressively shown how well bats tackle navigation in 3D with biosonar, i.e., the auditory analysis of self-generated ultrasonic emissions [1-7]. However, unlike in the visual system, where space is explicitly coded at very high resolution in the retinal fovea, the inner ear encodes frequency and time, not space. Spatial attributes of echoes are represented in the space-dependent filtering of the bats' pinnae [8, 9] and binaural computations, like interaural time and level differences [10, 11], as first proposed by Lord Rayleigh [12]. Remarkably, Rayleigh also provided a clear definition of spatial resolution: based on the shape of optical diffraction patterns arising from two closely spaced light sources, Rayleigh defined resolution as the capability to detect a trough in their joint light diffraction patterns [13, 14]. Here, we recruit Rayleigh's classical resolution paradigm to quantify how well bats can resolve multiple simultaneously presented reflectors in space. We show that biosonar spatial resolution in azimuth is no better than about 80° compared to a human visual resolution down to 0.02° [14]. We suggest that bats compensate this effective lack of spatial resolution by sequentially probing their environment in flight. Our data show that low-resolution environment perception is a viable alternative to high-resolution vision to support intelligent behavior in complex environments.

Echolocating bats are known to fly and forage in complete darkness, using the echoes of their actively emitted calls to navigate and to detect prey. However, under dim light conditions many bats can also rely on vision. Many flying animals have been shown to navigate by optic flow information and, recently, bats were shown to exploit echo-acoustic flow to navigate through dark habitats. Here, we show for the bat

Hearing is the primary sensory modality in bats, but its development is poorly studied. For newborns, hearing appears essential in maintaining contact with their mothers and to develop echolocation abilities. Here we measured auditory brainstem responses (ABRs) to clicks and narrowband tone pips covering a large frequency range (5-90 kHz) in juveniles (p7 to p200) and adults of the bat, Phyllostomus discolor. Tone-pip audiograms show that juveniles at p7 are already quite responsive, not only below 20 kHz but up to 90 kHz. Hearing sensitivity increases further until about p14 and is then refined, possibly correlated with growth and differentiation of the animals' outer ears. ABR amplitudes decrease within the first 3-4 months, inversely correlated with the bat weight and forearm length. ABR Wave I latency decreases with increasing stimulation level. ABR duration (measured between Waves I and V) is longer in juveniles and shortens with age which may reflect temporal refinement of auditory brainstem neurons to accommodate the exceptional temporal precision required for effective echolocation. Overall our data show that P. discolor bats have good hearing very early in life. The current method represents a fast and minimally invasive way of characterizing basic hearing in bats. (C) 2018 Published by Elsevier B.V.

>Human hearing is rather insensitive for very low frequencies (i.e. below 100 Hz). Despite this insensitivity, low-frequency sound can cause oscillating changes of cochlear gain in inner ear regions processing even much higher frequencies. These alterations outlast the duration of the low-frequency stimulation by several minutes, for which the term 'bounce phenomenon' has been coined. Previously, we have shown that the bounce can be traced by monitoring frequency and level changes of spontaneous otoacoustic emissions (SOAEs) over time. It has been suggested elsewhere that large receptor potentials elicited by low-frequency stimulation produce a net Ca(2+) influx and associated gain decrease in outer hair cells. The bounce presumably reflects an underdamped, homeostatic readjustment of increased Ca(2+) concentrations and related gain changes after low-frequency sound offset. Here, we test this hypothesis by activating the medial olivocochlear efferent system during presentation of the bounce-evoking low-frequency (LF) sound. The efferent system is known to modulate outer hair cell Ca(2+) concentrations and receptor potentials, and therefore, it should modulate the characteristics of the bounce phenomenon. We show that simultaneous presentation of contralateral broadband noise (100 Hz-8 kHz, 65 and 70 dB SPL, 90 s, activating the efferent system) and ipsilateral low-frequency sound (30 Hz, 120 dB SPL, 90 s, inducing the bounce) affects the characteristics of bouncing SOAEs recorded after low-frequency sound offset. Specifically, the decay time constant of the SOAE level changes is shorter, and the transient SOAE suppression is less pronounced. Moreover, the number of new, transient SOAEs as they are seen during the bounce, are reduced. Taken together, activation of the medial olivocochlear system during induction of the bounce phenomenon with low-frequency sound results in changed characteristics of the bounce phenomenon. Thus, our data provide experimental support for the hypothesis that outer hair cell calcium homeostasis is the source of the bounce phenomenon.

Some blind humans have developed the remarkable ability to detect and localize objects through the auditory analysis of self-generated tongue clicks. These echolocation experts show a corresponding increase in 'visual' cortex activity when listening to echo-acoustic sounds. Echolocation in real-life settings involves multiple reflections as well as active sound production, neither of which has been systematically addressed. We developed a virtualization technique that allows participants to actively perform such biosonar tasks in virtual echo-acoustic space during magnetic resonance imaging (MRI). Tongue clicks, emitted in the MRI scanner, are picked up by a microphone, convolved in real time with the binaural impulse responses of a virtual space, and presented via headphones as virtual echoes. In this manner, we investigated the brain activity during active echo-acoustic localization tasks. Our data show that, in blind echolocation experts, activations in the calcarine cortex are dramatically enhanced when a single reflector is introduced into otherwise anechoic virtual space. A pattern-classification analysis revealed that, in the blind, calcarine cortex activation patterns could discriminate left-side from right-side reflectors. This was found in both blind experts, but the effect was significant for only one of them. In sighted controls, 'visual' cortex activations were insignificant, but activation patterns in the planum temporale were sufficient to discriminate left-side from right-side reflectors. Our data suggest that blind and echolocation-trained, sighted subjects may recruit different neural substrates for the same active-echolocation task.

Bats are gregarious, highly vocal animals that possess a broad repertoire of social vocalisations. For in-depth studies of their vocal behaviours, including vocal flexibility and vocal learning, it is necessary to gather repeatable evidence from controlled laboratory experiments on isolated individuals. However, such studies are rare for one simple reason: eliciting social calls in isolation and under operant control is challenging and has rarely been achieved. To overcome this limitation, we designed an automated setup that allows conditioning of social vocalisations in a new context, and tracks spectro-temporal changes in the recorded calls over time. Using this setup, we were able to reliably evoke social calls from temporarily isolated lesser spear-nosed bats (Phyllostomus discolor). When we adjusted the call criteria that could result in food reward, bats responded by adjusting temporal and spectral call parameters. This was achieved without the help of an auditory template or social context to direct the bats. Our results demonstrate vocal flexibility and vocal usage learning in bats. Our setup provides a new paradigm that allows the controlled study of the production and learning of social vocalisations in isolated bats, overcoming limitations that have, until now, prevented in-depth studies of these behaviours.

Loud low-frequency sounds can induce temporary oscillatory changes in cochlear sensitivity, which have been termed the 'bounce' phenomenon. The origin of these sensitivity changes has been attributed to slow fluctuations in cochlear homeostasis, causing changes in the operating points of the outer hair cell mechano-electrical and electro-mechanical transducers. Here, we acquired three objective and subjective measures resulting in a comprehensive dataset of the bounce phenomenon in each of 22 normal-hearing human subjects. We analysed the level and phase of cubic and quadratic distortion product otoacoustic emissions and the auditory thresholds before and after presentation of a low-frequency stimulus (30 Hz sine wave, 120 dB SPL, 90 s) as a function of time. In addition, the perceived loudness of temporary, tinnitus-like sensations occurring in all subjects after cessation of the low-frequency stimulus was tracked over time. The majority of the subjects (70 %) showed a significant, biphasic change of quadratic, but not cubic, distortion product otoacoustic emissions of about 3-4 dB. Eighty-six percent of the tested subjects showed significant alterations of hearing thresholds after low-frequency stimulation. Four different types of threshold changes were observed, namely monophasic desensitisations (the majority of cases), monophasic sensitisations, biphasic alterations with initial sensitisation and biphasic alterations with initial desensitisation. The similar duration of the three bounce phenomenon measures indicates a common origin. The current findings are consistent with the hypothesis that slow oscillations of homeostatic control mechanisms and associated operating point shifts within the cochlea are the source of the bounce phenomenon.

Transcutaneous, electrical stimulation with electrodes placed on the mastoid processes represents a specific way to elicit vestibular reflexes in humans without active or passive subject movements, for which the term galvanic vestibular stimulation was coined. It has been suggested that galvanic vestibular stimulation mainly affects the vestibular periphery, but whether vestibular hair cells, vestibular afferents, or a combination of both are excited, is still a matter of debate. Galvanic vestibular stimulation has been in use since the late 18th century, but despite the long-known and well-documented effects on the vestibular system, reports of the effect of electrical stimulation on the adjacent cochlea or the ascending auditory pathway are surprisingly sparse. The present study examines the effect of transcutaneous, electrical stimulation of the human auditory periphery employing evoked and spontaneous otoacoustic emissions and several psychoacoustic measures. In particular, level growth functions of distortion product otoacoustic emissions were recorded during electrical stimulation with alternating currents (2 Hz, 1–4 mA in 1 mA-steps). In addition, the level and frequency of spontaneous otoacoustic emissions were followed before, during, and after electrical stimulation (2 Hz, 1–4 mA). To explore the effect of electrical stimulation on the retrocochlear level (i.e. on the ascending auditory pathway beyond the cochlea), psychoacoustic experiments were carried out. Specifically, participants indicated whether electrical stimulation (4 Hz, 2 and 3 mA) induced amplitude modulations of the perception of a pure tone, and of auditory illusions after presentation of either an intense, low-frequency sound (Bounce tinnitus) or a faint band-stop noise (Zwicker tone). These three psychoacoustic measures revealed significant perceived amplitude modulations during electrical stimulation in the majority of participants. However, no significant changes of evoked and spontaneous otoacoustic emissions could be detected during electrical stimulation relative to recordings without electrical stimulation. The present findings show that cochlear function, as assessed with spontaneous and evoked otoacoustic emissions, is not affected by transcutaneous electrical stimulation, at the currents used in this study. Psychoacoustic measures like pure tone perception, but also auditory illusions, are affected by electrical stimulation. This indicates that activity of the retrocochlear ascending auditory pathway is modulated during transcutaneous electrical stimulation.

Tinnitus is one of the three classical symptoms of Meniere's Disease (MD), an inner ear disease which is often accompanied by endolymphatic hydrops. Previous studies indicate that tinnitus in MD patients is dominated by low frequencies, whereas tinnitus in non-hydropic pathologies is typically higher in frequency. Tinnitus of rather low-frequency quality was also reported to occur for about 90 s in normal-hearing participants after presentation of intense, low-frequency (LF) sound (120 dB SPL, 30 Hz, 90 s). LF sound has been demonstrated to also cause temporary endolymphatic hydrops in animal models. Here, we quantify tinnitus in two study groups with chronic (MD patients) and presumably transient endolymphatic hydrops (normal-hearing participants after LF-exposure) with a psychophysical procedure. Participants matched their tinnitus either with a pure tone of adjustable frequency and level or with a noise of adjustable spectral shape and level. Sensation levels of matching stimuli were lower for MD patients (mean: 8 dB SL) than for normal-hearing participants (mean: 15 dB SL).Transient tinnitus after LF-exposure occurred in all normal-hearing participants (N=28). About half of the normal-hearing participants matched noise to their tinnitus, the other half a pure tone with frequencies below 2 kHz. MD patients matched their tinnitus with either high-frequency pure tones, mainly above 3 kHz, or with a noise. Despite a significant proportion of MD patients matching low-pass (roaring) noises to their tinnitus, the range of matched stimuli was more heterogeneous than previous data suggested. We propose that in those participants with noise-like tinnitus, the percept is probably generated by increased spontaneous activity of auditory nerve fibers with a broad range of characteristic frequencies, due to an impaired ion balance in the cochlea. For tonal tinnitus additional mechanisms are conceivable: Focal hair cell loss can result in decreased auditory nerve firing and a central auditory overcompensation. Also, normal-hearing participants after LF-exposure experience alterations in spontaneous otoacoustic emissions, which may contribute to a transient tonal tinnitus.

Some blind humans have developed echolocation, as a method of navigation in space. Echolocation is a truly active sense because subjects analyze echoes of dedicated, self-generated sounds to assess space around them. Using a special virtual space technique, we assess how humans perceive enclosed spaces through echolocation, thereby revealing the interplay between sensory and vocal-motor neural activity while humans perform this task. Sighted subjects were trained to detect small changes in virtual-room size analyzing real-time generated echoes of their vocalizations. Individual differences in performance were related to the type and number of vocalizations produced. We then asked subjects to estimate virtual-room size with either active or passive sounds while measuring their brain activity with fMRI. Subjects were better at estimating room size when actively vocalizing. This was reflected in the hemodynamic activity of vocal-motor cortices, even after individual motor and sensory components were removed. Activity in these areas also varied with perceived room size, although the vocal-motor output was unchanged. In addition, thalamic and auditory-midbrain activity was correlated with perceived room size; a likely result of top-down auditory pathways for human echolocation, comparable with those described in echolocating bats. Our data provide evidence that human echolocation is supported by active sensing, both behaviorally and in terms of brain activity. The neural sensory-motor coupling complements the fundamental acoustic motor-sensory coupling via the environment in echolocation.SIGNIFICANCE STATEMENTPassive listening is the predominant method for examining brain activity during echolocation, the auditory analysis of self-generated sounds. We show that sighted humans perform better when they actively vocalize than during passive listening. Correspondingly, vocal motor and cerebellar activity is greater during active echolocation than vocalization alone. Motor and subcortical auditory brain activity covaries with the auditory percept, although motor output is unchanged. Our results reveal behaviorally relevant neural sensory-motor coupling during echolocation.

The presentation of intense, low-frequency (LF) sound to the human ear can cause very slow, sinusoidal oscillations of cochlear sensitivity after LF sound offset, coined the "Bounce" phenomenon. Changes in level and frequency of spontaneous otoacoustic emissions (SOAEs) are a sensitive measure of the Bounce. Here, we investigated the effect of LF sound level and frequency on the Bounce. Specifically, the level of SOAEs was tracked for minutes before and after a 90-s LF sound exposure. Trials were carried out with several LF sound levels (93 to 108 dB SPL corresponding to 47 to 75 phons at a fixed frequency of 30 Hz) and different LF sound frequencies (30, 60, 120, 240 and 480 Hz at a fixed loudness level of 80 phons). At an LF sound frequency of 30 Hz, a minimal sound level of 102 dB SPL (64 phons) was sufficient to elicit a significant Bounce. In some subjects, however, 93 dB SPL (47 phons), the lowest level used, was sufficient to elicit the Bounce phenomenon and actual thresholds could have been even lower. Measurements with different LF sound frequencies showed a mild reduction of the Bounce phenomenon with increasing LF sound frequency. This indicates that the strength of the Bounce not only is a simple function of the spectral separation between SOAE and LF sound frequency but also depends on absolute LF sound frequency, possibly related to the magnitude of the AC component of the outer hair cell receptor potential.

The perceptual insensitivity to low frequency (LF) sound in humans has led to an underestimation of the physiological impact of LF exposure on the inner ear. It is known, however, that intense, LF sound causes cyclic changes of indicators of inner ear function after LF stimulus offset, for which the term "Bounce" phenomenon has been coined.Here, we show that the mechanical amplification of hair cells (OHCs) is significantly affected after the presentation of LF sound. First, we show the Bounce phenomenon in slow level changes of quadratic, but not cubic, distortion product otoacoustic emissions (DPOAEs). Second, Bouncing in response to LF sound is seen in slow, oscillating frequency and correlated level changes of spontaneous otoacoustic emissions (SOAEs). Surprisingly, LF sound can induce new SOAEs which can persist for tens of seconds. Further, we show that the Bounce persists under free-field conditions, i.e. without an in-ear probe occluding the auditory meatus. Finally, we show that the Bounce is affected by contralateral acoustic stimulation synchronised to the ipsilateral LF sound. These findings clearly demonstrate that the origin of the Bounce lies in the modulation of cochlear amplifier gain. We conclude that activity changes of OHCs are the source of the Bounce, most likely caused by a temporary disturbance of OHC calcium homeostasis. In the light of these findings, the effects of long-duration, anthropogenic LF sound on the human inner ear require further research.

Ultrasonic emissions of bats are directional and delimit the echo-acoustic space. Directionality is quantified by the aperture of the sonar beam. Recent work has shown that bats often widen their sonar beam when approaching movable prey or sharpen their sonar beam when navigating through cluttered habitats. Here we report how nose-emitting bats, Phyllostomus discolor, adjust their sonar beam to object distance. First, we show that the height and width of the bats sonar beam, as imprinted on a parabolic 45 channel microphone array, varies even within each animal and this variation is unrelated to changes in call level or spectral content. Second, we show that these animals are able to systematically decrease height and width of their sonar beam while focusing on the approaching object. Thus it appears that sonar beam sharpening is a further, facultative means of reducing search volume, likely to be employed by stationary animals when the object position is close and unambiguous. As only half of our individuals sharpened their beam onto the approaching object we suggest that this strategy is facultative, under voluntary control and that beam formation is likely mediated by muscular control of the acoustic aperture of the bats’ nose leaf.

Echolocation is typically associated with bats and toothed whales. To date, only few studies have investigated echolocation in humans. Moreover, these experiments were conducted with real objects in real rooms; a configuration in which features of both vocal emissions and perceptual cues are difficult to analyse and control. We investigated human sonar target-ranging in virtual echo-acoustic space, using a short-latency, real-time convolution engine. Subjects produced tongue clicks, which were picked up by a headset microphone, digitally delayed, convolved with individual head-related transfer functions and played back through earphones, thus simulating a reflecting surface at a specific range in front of the subject. In an adaptive 2-AFC paradigm, we measured the perceptual sensitivity to changes of the range for reference ranges of 1.7, 3.4 or 6.8 m. In a follow-up experiment, a second simulated surface at a lateral position and a fixed range was added, expected to act either as an interfering masker or a useful reference. The psychophysical data show that the subjects were well capable to discriminate differences in the range of a frontal reflector. The range–discrimination thresholds were typically below 1 m and, for a reference range of 1.7 m, they were typically below 0.5 m. Performance improved when a second reflector was introduced at a lateral angle of 45°. A detailed analysis of the tongue clicks showed that the subjects typically produced short, broadband palatal clicks with durations between 3 and 15 ms, and sound levels between 60 and 108 dB. Typically, the tongue clicks had relatively high peak frequencies around 6 to 8 kHz. Through the combination of highly controlled psychophysical experiments in virtual space and a detailed analysis of both the subjects’ performance and their emitted tongue clicks, the current experiments provide insights into both vocal motor and sensory processes recruited by humans that aim to explore their environment by echolocation.

Detection and localization of a target sound in the presence of concurrent, spatially distributed masking sounds is one of the most challenging tasks for the mammalian auditory system. Previous studies demonstrated that the ability to localize signals is decreased by interfering noise. In order to directly compare the behavioral performance in a signal processing task in noise between gerbils and humans in the free sound field, we quantified their localization ability for a low-frequency signal in the presence of six masking noise sources surrounding the subject. Thresholds were measured both for masking noises that were correlated or uncorrelated across the masking sources. Overall, the gerbils required a higher signal/noise ratio to detect the low-frequency signal than the humans; that is, the behavioral performance of the gerbils was considerably worse than that of the humans. Moreover, switching from maskers that were uncorrelated across the masking sources to correlated maskers resulted in more masking in gerbils but in a release from masking in humans. These results would suggest that the gerbil may not be a good animal model for binaural processing. However, simulations of the localization thresholds in a numerical model of binaural processing in gerbils and humans reveal that both the inferior overall performance in gerbils and the opposite effect of masker correlation on the detection thresholds can be attributed to the smaller head size and the wider peripheral auditory filters in gerbils. Thus, the current data indicate that the binaural processor itself (i.e., the evaluation of signals coming from the two ears) is equally sensitive in gerbils and humans. However, the physical limitations imposed by the small head prevent the gerbil from performing equally well in the current paradigm.

The effective use of echolocation requires not only measuring the delay between the emitted call and returning echo to estimate the distance of an ensonified object. To locate an object in azimuth and elevation, the bat's auditory system must analyze the returning echoes in terms of their binaural properties, i.e., the echoes' interaural intensity and time differences (IIDs and ITDs). The effectiveness of IIDs for echolocation is undisputed, but when bats ensonify complex objects, the temporal structure of echoes may facilitate the analysis of the echo envelope in terms of envelope ITDs. Using extracellular recordings from the auditory midbrain of the bat, Phyllostomus discolor, we found a population of neurons that are sensitive to envelope ITDs of echoes of their sonar calls. Moreover, the envelope-ITD sensitivity improved with increasing temporal fluctuations in the echo envelopes, a sonar parameter related to the spatial statistics of complex natural reflectors like vegetation. The data show that in bats envelope ITDs may be used not only to locate external, prey-generated rustling sounds but also in the context of echolocation. Specifically, the temporal fluctuations in the echo envelope, which are created when the sonar emission is reflected from a complex natural target, support ITD-mediated echolocation.

Due to its good low-frequency hearing, the Mongolian Gerbil (Meriones unguiculatus) has become a well-established animal model for human hearing. In humans, sound localization in reverberant environments is facilitated by the precedence effect, i.e., the perceptual suppression of spatial information carried by echoes. The current study addresses the question whether gerbils are a valid animal model for such complex spatial processing. Specifically, we quantify localization dominance, i.e., the fact that in the context of precedence, only the directional information of the sound which reaches the ear first dominates the perceived position of a sound source whereas directional information of the delayed echoes is suppressed. As localization dominance is known to be stimulus-dependent, we quantified the extent to which the spectral content of transient sounds affects localization dominance in the gerbil. The results reveal that gerbils show stable localization dominance across echo delays, well comparable to humans. Moreover, localization dominance systematically decreased with increasing center frequency, which has not been demonstrated in an animal before. These findings are consistent with an important contribution of peripheral-auditory processing to perceptual localization dominance. The data show that the gerbil is an excellent model to study the neural basis of complex spatial-auditory processing.

In everyday environments, sound reflections from walls and other objects arrive at the listener’s ear in addition to the direct sound radiated from a source. Humans have evolved mechanisms to perceptually suppress distracting early reflections, summarized as the precedence effect. Visual information of the surroundings influences the effectiveness of this mechanism. It has also been shown that similar compensation effects can occur for later reflections and reverberation, and that humans can estimate acoustic properties of a room from the visual impression. Taking these findings together, we hypothesize that the visual impression of a room affects the perception of its reverberation. The hypothesis was tested in a highly immersive audio-visual virtual reality environment consisting of a horizontal loudspeaker array in an acoustically treated chamber and a head-mounted display. In a magnitude estimation paradigm, subjects judged the perceived degree of reverberation in conditions where the simultaneously presented acoustic and visual stimuli were either matched regarding the room, sound source azimuth, and sound source distance, or diverged in one of those aspects. Audio-only control conditions served as a baseline. Preliminary results from six subjects suggest a predominant reliance on auditory input when quantifying perceived reverberation even in audio-visually conflicting conditions.

Flying animals need to react fast to rapid changes in their environment. Visually guided animals use optic flow, generated by their movement through structured environments. Nocturnal bats cannot make use of optic flow, but rely mostly on echolocation. Here we show that bats exploit echo-acoustic flow to negotiate flight through narrow passages. Specifically, bats' flight between lateral structures is significantly affected by the echo-acoustic salience of those structures, independent of their physical distance. This is true although echolocation, unlike vision, provides explicit distance cues. Moreover, the bats reduced the echolocation sound levels in stronger flow, likely to compensate for the increased summary target strength of the lateral reflectors. However, bats did not reduce flight velocity under stronger echo-acoustic flow. Our results demonstrate that sensory flow is a ubiquitous principle for flight guidance, independent of the fundamentally different peripheral representation of flow across the senses of vision and echolocation.

Auditory feedback plays an important role in vocal learning and, more generally, in fine-tuning the acoustic features of communication signals. So far, only a few studies have assessed the developmental onset of auditory feedback. The Lombard effect, a well-studied audio-vocal phenomenon, refers to an increase in vocal loudness of a subject in response to an increase in background noise. Here, we studied the time course of the Lombard effect in developing bats, Phyllostomus discolor. We show that infant bats produced louder vocalizations in noise than in silence at an age of only two weeks. In contrast, the infant bats' morphology and vocalizations changed gradually until two months of age. Furthermore, we found that the Lombard magnitude, i.e. how much the bats increased their vocal loudness in noise relative to silence, correlated positively with the age of the infant bats. We conclude that the Lombard effect features an early developmental origin, indicating a fast maturation of the underlying neural circuits for audio-vocal feedback.

The perceptual insensitivity to low frequency (LF) sound in humans has led to an underestimation of the physiological impact of LF exposure on the inner ear. It is known, however, that intense, LF sound causes cyclic changes of indicators of inner ear function after LF stimulus offset, for which the term “Bounce” phenomenon has been coined.

Many animal species adjust the spectral composition of their acoustic signals to variable environments. However, the physiological foundation of such spectral plasticity is often unclear. The source-filter theory of sound production, initially established for human speech, applies to vocalizations in birds and mammals. According to this theory, adjusting the spectral structure of vocalizations could be achieved by modifying either the laryngeal/syringeal source signal or the vocal tract which filters the source signal. Here we show that in Pale spear-nosed bats, spectral plasticity induced by moderate level background noise is dominated by the vocal tract rather than the laryngeal source signal. Specifically, we found that with increasing background noise levels, bats consistently decreased the spectral centroid of their echolocation calls up to 3.2 kHz, together with other spectral parameters. In contrast, noise-induced changes in fundamental frequency were small (maximally 0.1 kHz) and were inconsistent across individuals. Changes in spectral centroid did not correlate with changes in fundamental frequency, whereas correlated negatively with changes in call amplitude. Furthermore, while the bats consistently increased the call amplitude with increasing noise levels (the Lombard effect), increases in call amplitude typically did not lead to increases in fundamental frequency. In summary, our results suggest that at least to a certain degree echolocating bats are capable of adjusting call amplitude, fundament frequency, and spectral parameters independently.

This chapter is intended to identify some of the major challenges that only now emerge as technically feasible when studying hearing in bats. These technical advances include all aspects of biological research, from novel genetic tools to novel recording techniques of ultrasonic audio, high-speed video, and global positioning data. Most recently, on-board and telemetric recording techniques for both ultrasound and electrode signals allow for unprecedented insight into the neuroethology of bat hearing and echolocation from awake and behaving animals engaged in a clearly defined perceptual task. Only with these new techniques will we be able to address specializations in the bat vocalization and auditory systems, from its genetic foundations to its behavioral dynamics. We hope that the current chapter is received as an ‘appetizer’ for young biologists across disciplines to focus their scientific efforts onto the fascinating topic of how it is to be a bat that has made the nocturnal air space its home.

An echolocating bat produces echoes consisting of the convolution of echolocation call and the impulse response (IR) of the ensonified object. A crucial question in animal sonar is whether bats are able to extract this IR from the echo. The bat inner ear generates a frequency representation of call and echo and IR extraction in the frequency domain requires accurate analysis of both magnitude and phase information. Previous studies investigating the phase sensitivity of bats using a jitter paradigm reported a temporal acuity down to 10 ns, suggesting perfect sonar phase representation. In a phantom-target playback experiment, we investigate the perceptual phase sensitivity of the bat Phyllostomus discolor using a novel approach: instead of manipulating IR phase by changing IR delay (jitter paradigm), we randomized IR phase and thus lengthened the IR over time, leaving the magnitude spectrum unchanged. Our results show that phase sensitivity, as reflected in the analysis of signal duration, appears to be much lower than phase sensitivity, as reflected in the analysis of signal onset. The current data indicate that different temporal aspects of sonar processing are encoded with very different temporal resolution and thus an overall claim of "phase sensitivity" as such cannot be maintained.