Echolocating Bats Have Evolved Decreased Susceptibility to Noise-Induced Temporary Hearing Losses.

Glenis Long championed the application of quantitative psychophysical methods to understand comparative hearing abilities across species. She contributed the first psychophysical studies of absolute and masked hearing sensitivities in an auditory specialist, the echolocating horseshoe bat. Her data demonstrated that this bat has hyperacute frequency discrimination in the 83-kHz range of its echolocation broadcast. This specialization facilitates the bat's use of Doppler shift compensation to separate echoes of fluttering insects from concurrent echoes of non-moving objects. In this review, we discuss another specialization for hearing in a species of echolocating bat that contributes to perception of echoes within a complex auditory scene. Psychophysical and behavioral studies with big brown bats show that exposures to long duration, intense wideband or narrowband ultrasonic noise do not induce significant increases in their thresholds to echoes and do not impair their ability to orient through a naturalistic sonar scene containing multiple distracting echoes. Thresholds of auditory brainstem responses also remain low after intense noise exposures. These data indicate that big brown bats are not susceptible to temporary threshold shifts as measured in comparable paradigms used with other mammals, at least within the range of stimulus parameters that have been tested so far. We hypothesize that echolocating bats have evolved a decreased susceptibility to noise-induced hearing losses as a specialization for echolocation in noisy environments.

Echo detection thresholds in big brown bats (Eptesicus fuscus) vary with echo spectral content.

Echolocating big brown bats (Eptesicus fuscus) broadcast downward frequency-modulated sweeps covering the ultrasonic range from 100-23 kHz in two harmonics. They perceive target range from the time delay between each broadcast and its returning echo. Previous experiments indicated that the bat's discrimination acuity for broadcast-echo delay declines when the lowest frequencies (23-35 kHz) in the first harmonic of an echo are removed. This experiment examined whether echo detection is similarly impaired. Results show that detection thresholds for echoes missing these lowest frequencies are raised. Increased thresholds for echoes differing in spectra facilitates the bat's ability to discriminate against clutter.

Temporal coherence of harmonic frequencies affects echo detection in the big brown bat, Eptesicus fuscus.

Echolocating big brown bats (Eptesicus fuscus) broadcast frequency modulated (FM) ultrasonic pulses containing two prominent harmonic sweeps (FM1, FM2). Both harmonics typically return as echoes at the same absolute time delay following the broadcast, making them coherent. Electronically splitting FM1 and FM2 allows their time delays to be controlled separately, making them non-coherent. Earlier work shows that big brown bats discriminate coherent from split harmonic, non-coherent echoes and that disruptions of harmonic coherence produce blurry acoustic images. A psychophysical experiment on two trained big brown bats tested the hypothesis that detection thresholds for split harmonic, non-coherent echoes are higher than those for coherent echoes. Thresholds of the two bats for detecting 1-glint echoes with coherent harmonics were around 35 and 36 dB sound pressure level, respectively, while thresholds for split harmonic echoes were about 10 dB higher. When the delay of FM2 in split harmonic echoes is shortened by 75 µs to offset neural amplitude-latency trading and restore coherence in the auditory representation, thresholds decreased back down to those estimated for coherent echoes. These results show that echo detection is affected by loss of harmonic coherence, consistent with the proposed broader role of coherence across frequencies for auditory perception.

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

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

Connexin36 RNA Expression in the Cochlear Nucleus of the Echolocating Bat, Eptesicus fuscus.

PURPOSE: The echolocating bat is used as a model for studying the auditory nervous system because its specialized sensory capabilities arise from general mammalian auditory percepts such as pitch and sound source localization. These percepts are mediated by precise timing within neurons and networks of the lower auditory brainstem, where the gap junction protein Connexin36 (CX36) is expressed. Gap junctions and electrical synapses in the central nervous system are associated with fast transmission and synchronous patterns of firing within neuronal networks. The purpose of this study was to identify areas where CX36 was expressed in the bat cochlear nucleus to shed light on auditory brainstem networks in a hearing specialist animal model. METHODS: We investigated the distribution of CX36 RNA throughout the cochlear nucleus complex of the echolocating big brown bat, Eptesicus fuscus, using in situ hybridization. As a qualitative comparison, we visualized Gjd2 gene expression in the cochlear nucleus of transgenic CX36 reporter mice, species that hear ultrasound but do not echolocate. RESULTS: In both the bat and the mouse, CX36 is expressed in the anteroventral and in the dorsal cochlear nucleus, with more limited expression in the posteroventral cochlear nucleus. These results are generally consistent with previous work based on immunohistochemistry. CONCLUSION: Our data suggest that the anatomical substrate for CX36-mediated electrical neurotransmission is conserved in the mammalian CN across echolocating bats and non-echolocating mice.

Oscillatory discharges in the auditory midbrain of the big brown bat contribute to coding of echo delay.

Subsequent to his breakthrough discovery of delay-tuned neurons in the bat's auditory midbrain and cortex, Albert Feng proposed that neural computations for echo delay involve intrinsic oscillatory discharges generated in the inferior colliculus (IC). To explore further the presence of these neural oscillations, we recorded multiple unit activity with a novel annular low impedance electrode from the IC of anesthetized big brown bats and Seba's short-tailed fruit bats. In both species, responses to tones, noise bursts, and FM sweeps contain long latency components, extending up to 60 ms post-stimulus onset, organized in periodic, oscillatory-like patterns at frequencies of 360-740 Hz. Latencies of this oscillatory activity resemble the wide distributions of single neuron response latencies in the IC. In big brown bats, oscillations lasting up to 30 ms after pulse onset emerge in response to single FM pulse-echo pairs, at particular pulse-echo delays. Oscillatory responses to pulses and evoked responses to echoes overlap extensively at short echo delays (5-7 ms), creating interference-like patterns. At longer echo delays, responses are separately evident to both pulses and echoes, with less overlap. These results extend Feng's reports of IC oscillations, and point to different processing mechanisms underlying perception of short vs long echo delays.

Non-invasive auditory brainstem responses to FM sweeps in awake big brown bats.

We introduce two EEG techniques, one based on conventional monopolar electrodes and one based on a novel tripolar electrode, to record for the first time auditory brainstem responses (ABRs) from the scalp of unanesthetized, unrestrained big brown bats. Stimuli were frequency-modulated (FM) sweeps varying in sweep direction, sweep duration, and harmonic structure. As expected from previous invasive ABR recordings, upward-sweeping FM signals evoked larger amplitude responses (peak-to-trough amplitude in the latency range of 3-5 ms post-stimulus onset) than downward-sweeping FM signals. Scalp-recorded responses displayed amplitude-latency trading effects as expected from invasive recordings. These two findings validate the reliability of our noninvasive recording techniques. The feasibility of recording noninvasively in unanesthetized, unrestrained bats will energize future research uncovering electrophysiological signatures of perceptual and cognitive processing of biosonar signals in these animals, and allows for better comparison with ABR data from echolocating cetaceans, where invasive experiments are heavily restricted.

Amplitude discrimination is predictably affected by echo frequency filtering in wideband echolocating bats.

Big brown bats echolocate using wideband frequency-modulated (FM) ultrasonic pulses, perceiving target range from echo delay and target size from echo amplitude. Echolocation pulses contain two prominent down-sweeping harmonics (FM1, ∼55-22 kHz; FM2, ∼100-55 kHz), which are affected differently by propagation to the target and back to the bat. Previous work demonstrates that big brown bats utilize the low frequencies in FM1 for target ranging, while FM2 only contributes if FM1 is also present. The present experiments test the hypothesis that the bat's ability to discriminate echo amplitude is also affected by selectively attenuating FM1 or FM2 in target or nontarget echoes. Bats were trained to perform an amplitude discrimination task with virtual echo targets located 83 cm away. Echo delay was fixed and echo amplitude was varied, while either FM1 or FM2 was attenuated by highpass or lowpass filtering. Bats' performance decreased when lower frequencies were attenuated in target echoes and when higher frequencies were attenuated in nontarget echoes. Performance was reversed in the opposite filtering conditions. The bat's ability to distinguish between virtual targets varying in amplitude at the same simulated range indicates a high level of focused attention for perceptual isolation of target from non-target echoes.

In-vivo functional and structural retinal imaging using multiwavelength photoacoustic remote sensing microscopy.

Many important eye diseases as well as systemic disorders manifest themselves in the retina. Retinal imaging technologies are rapidly growing and can provide ever-increasing amounts of information about the structure, function, and molecular composition of retinal tissue in-vivo. Photoacoustic remote sensing (PARS) is a novel imaging modality based on all-optical detection of photoacoustic signals, which makes it suitable for a wide range of medical applications. In this study, PARS is applied for in-vivo imaging of the retina and estimating oxygen saturation in the retinal vasculature. To our knowledge, this is the first time that a non-contact photoacoustic imaging technique is applied for in-vivo imaging of the retina. Here, optical coherence tomography is also used as a well-established retinal imaging technique to navigate the PARS imaging beams and demonstrate the capabilities of the optical imaging setup. The system is applied for in-vivo imaging of both microanatomy and the microvasculature of the retina. The developed system has the potential to advance the understanding of the ocular environment and to help in monitoring of ophthalmic diseases.

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

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

Spatiotemporal patterning of acoustic gaze in echolocating bats navigating gaps in clutter.

We challenged four big brown bats to maneuver through abrupt turns in narrow corridors surrounded by dense acoustic clutter. We quantified bats' performance, sonar beam focus, and sensory acquisition rate. Performance was excellent in straight corridors, with sonar beam aim deviating less than 5° from the corridor midline. Bats anticipated an upcoming abrupt turn to the right or left by slowing flight speed and shifting beam aim to "look" proactively into one side of the corridor to identify the new flightpath. All bats mastered the right turn, but two bats consistently failed the left turn. Bats increased their sensory acquisition rate when confronting abrupt turns in both successful and failed flights. Limitations on biosonar performance reflected failures to switch beam aim and to modify a learned spatial map, rather than failures to update acquisition rate.

A comprehensive computational model of animal biosonar signal processing.

Computational models of animal biosonar seek to identify critical aspects of echo processing responsible for the superior, real-time performance of echolocating bats and dolphins in target tracking and clutter rejection. The Spectrogram Correlation and Transformation (SCAT) model replicates aspects of biosonar imaging in both species by processing wideband biosonar sounds and echoes with auditory mechanisms identified from experiments with bats. The model acquires broadband biosonar broadcasts and echoes, represents them as time-frequency spectrograms using parallel bandpass filters, translates the filtered signals into ten parallel amplitude threshold levels, and then operates on the resulting time-of-occurrence values at each frequency to estimate overall echo range delay. It uses the structure of the echo spectrum by depicting it as a series of local frequency nulls arranged regularly along the frequency axis of the spectrograms after dechirping them relative to the broadcast. Computations take place entirely on the timing of threshold-crossing events for each echo relative to threshold-events for the broadcast. Threshold-crossing times take into account amplitude-latency trading, a physiological feature absent from conventional digital signal processing. Amplitude-latency trading transposes the profile of amplitudes across frequencies into a profile of time-registrations across frequencies. Target shape is extracted from the spacing of the object's individual acoustic reflecting points, or glints, using the mutual interference pattern of peaks and nulls in the echo spectrum. These are merged with the overall range-delay estimate to produce a delay-based reconstruction of the object's distance as well as its glints. Clutter echoes indiscriminately activate multiple parts in the null-detecting system, which then produces the equivalent glint-delay spacings in images, thus blurring the overall echo-delay estimates by adding spurious glint delays to the image. Blurring acts as an anticorrelation process that rejects clutter intrusion into perceptions.

Bat biosonar signals.

The Reflections series takes a look back on historical articles from The Journal of the Acoustical Society of America that have had a significant impact on the science and practice of acoustics.

Label-free, non-contact, in vivo ophthalmic imaging using photoacoustic remote sensing microscopy.

We present, to the best of our knowledge, the first label-free, non-contact, in vivo imaging of the ocular vasculature using photoacoustic remote sensing (PARS) microscopy. Both anterior and posterior segments of a mouse eye were imaged. Vasculature of the iris, sclera, and retina tissues were clearly resolved. To the best of our knowledge, this is the first study showing non-contact photoacoustic imaging conducted on in vivo ocular tissue. We believe that PARS microscopy has the potential to advance the diagnosis and treatment of ocular diseases.

Long-latency optical responses from the dorsal inferior colliculus of Seba's fruit bat.

We used a novel microendoscope system to record simultaneously optical activity (fluorescence of a calcium indicator dye) and electrical activity (multi-unit activity and local field potentials) from the dorsal inferior colliculus of the echolocating bat, Carollia perspicillata. Optically recorded calcium responses to wide-band noise and to frequency-modulated bursts were recorded at probe depths down to 1300 µm, with the majority of active sites encountered at more shallow depths down to 800 µm. Calcium activity exhibited long latencies, within the time span of 50-100 ms after stimulus onset, significantly longer than onset latencies of either multi-unit activity or local field potentials. Latencies and amplitude/latency trading of these electrical responses were consistent with those seen in standard electrophysiological recordings, confirming that the microendoscope was able to record both neural and optical activity successfully. Optically recorded calcium responses rose and decayed slowly and were correlated in time with long-latency negative deflections in local field potentials. These data suggest that calcium-evoked responses may reflect known, sustained inhibitory interactions in the inferior colliculus.

How frequency hopping suppresses pulse-echo ambiguity in bat biosonar.

Big brown bats transmit wideband FM biosonar sounds that sweep from 55 to 25 kHz (first harmonic, FM1) and from 110 to 50 kHz (second harmonic, FM2). FM1 is required to perceive echo delay for target ranging; FM2 contributes only if corresponding FM1 frequencies are present. We show that echoes need only the lowest FM1 broadcast frequencies of 25 to 30 kHz for delay perception. If these frequencies are removed, no delay is perceived. Bats begin echo processing at the lowest frequencies and accumulate perceptual acuity over successively higher frequencies, but they cannot proceed without the low-frequency starting point in their broadcasts. This reveals a solution to pulse-echo ambiguity, a serious problem for radar or sonar. In dense, extended biosonar scenes, bats have to emit sounds rapidly to avoid collisions with near objects. But if a new broadcast is emitted when echoes of the previous broadcast still are arriving, echoes from both broadcasts intermingle, creating ambiguity about which echo corresponds to which broadcast. Frequency hopping by several kilohertz from one broadcast to the next can segregate overlapping narrowband echo streams, but wideband FM echoes ordinarily do not segregate because their spectra still overlap. By starting echo processing at the lowest frequencies in frequency-hopped broadcasts, echoes of the higher hopped broadcast are prevented from being accepted by lower hopped broadcasts, and ambiguity is avoided. The bat-inspired spectrogram correlation and transformation (SCAT) model also begins at the lowest frequencies; echoes that lack them are eliminated from processing of delay and no longer cause ambiguity.

Big brown bats are challenged by acoustically-guided flights through a circular tunnel of hoops.

Mines and caves provide essential roosting places for bats, but often they are obstructed to prevent entry by humans. To allow bats to access their roosts, metal corrugated culvert pipes are sometimes installed. Wildlife surveys indicate, however, that bats may abandon caves having corrugated culvert entrances. Culverts may be confusing to bats due to the complex patterns of echoes returned by the regular, ring-like corrugations. We tested the hypothesis that a circular tunnel composed of successive hoops is difficult for big brown bats (Eptesicus fuscus) to navigate. Experiments challenged bats with flights through a tunnel of round plastic hoops or a corridor flanked left and right by rows of plastic hanging chains. The bats swerved sideways and left the pathway on more flights in the hoop tunnel compared to only rarely in the chain corridor. Even during successful flights through the hoops, bats changed the temporal patterning of their echolocation pulses to compress them into more sonar sound groups. From prior research, this active reaction is an indicator of a perceptually more difficult task. To allow bats access to mines through culverts without affecting their echolocation behavior, smoothing or masking the regular corrugations inside with concrete may be effective.

Echolocation while drinking: Pulse-timing strategies by high- and low-frequency FM bats.

During nightly foraging activity, echolocating bats drink by flying low over the water surface and dipping the lower jaw while avoiding further bodily contact with the water. This task poses different sensorimotor challenges than flying in the open to forage for insects. Of interest is how bats adjust the timing of their echolocation pulses to accommodate the surrounding scene, from the progressively nearer water surface itself to objects at longer distances. Drinking behavior has been described in only a few of the roughly 1,000 echolocating bat species, and in none of the 110 species in the Indian subcontinent. Here, we describe how bats emitting frequency-modulated (FM) echolocation pulses behaved while drinking from a swimming pool in urban northeast India. At least two different bat species were present, using 1st-harmonic frequencies sweeping down to about 35 Hz ("low frequency") and down to about 50 kHz ("high frequency"), separable at a 40 kHz boundary. Over entire drinking maneuvers, intervals between broadcast pulses accommodate both the proximate task of registering the water surface while drinking and registering echoes from the farther reaches of the scene. During approach to the water, both low and high frequency bats emit longer, more stable interpulse intervals that matched the time interval covering echo arrival-times out to the frequency-dependent maximum operating range. High frequency bats use shorter interpulse intervals than low frequency bats, consistent with the shorter operating range at higher frequencies. Bats then accelerate their pulse rate to guide the dive down to drinking, with low frequency bats continuing to decrease pulse intervals and high frequency bats maintaining a more steady interval during the drinking buzz. The circumstance that both groups were engaged in the same task made this a natural experiment on the behavior during approach.