Vocal control of acoustic information for sonar discriminations by the echolocating bat, Eptesicus fuscus

This study aimed to determine whether bats using frequency modulated (FM) echolocation signals adapt the features of their vocalizations to the perceptual demands of a particular sonar task. Quantitative measures were obtained from the vocal signals produced by echolocating bats (Eptesicus fuscus) that were trained to perform in two distinct perceptual tasks, echo delay and Doppler-shift discriminations. In both perceptual tasks, the bats learned to discriminate electronically manipulated playback signals of their own echolocation sounds, which simulated echoes from sonar targets. Both tasks utilized a single-channel electronic target simulator and tested the bat's in a two-alternative forced choice procedure. The results of this study demonstrate changes in the features of the FM bats' sonar sounds with echolocation task demands, lending support to the notion that this animal actively controls the echo information that guides its behavior.     

Stabilization of perceived echo amplitudes in echolocating bats. II. The acoustic behavior of the big brown bat, Eptesicus fuscus, when tracking moving prey.

Big brown bats, Eptesicus fuscus, can be trained to use echolocation to track a small microphone with a food reward attached when it is moved rapidly toward them. This situation mimics prey interception in the wild while allowing very precise recording of the sonar pulses emitted during tracking behavior. The results show that E. fuscus intensity compensates, reducing emitted intensity by 6 dB per halving of target range so that the intensity incident upon the target is constant and echo intensity increases by 6 dB per halving of range. This increase in echo intensity is effectively canceled by the reduction in auditory sensitivity due to automatic gain control (AGC) of 6 to 7 dB per halving of range. Intensity compensation behavior and AGC therefore form a dual-component, symmetrical system that stabilizes perceived echo amplitudes during target approach. The same system is present in the fishing bat, Noctilio leporinus, suggesting that it may be widespread in echolocating bats. Correlation analysis shows that, despite large changes in the duration of the pulses emitted by E. fuscus during an approach, the pulse frequency structure is such that the spatial image of the target perceived along the range axis is highly stable. Pulse duration is not reduced in the manner theoretically necessary to eliminate potential echo distortion effects due to AGC, but is reduced in such a way that this distortion is insignificant. During the terminal buzz, a high degree of temporal overlap (relative to pulse duration) occurs between emitted pulse and returning echo.     

Range resolution and the possible use of spectral information in the echolocating bat, Eptesicus fuscus

Individuals of the echolocating bat Eptesicus fuscus were trained to discriminate simulated two-wave-front targets with internal time delays of 0 to 100 microns between the wave fronts from a one-wave-front target. The ability of bats to discriminate between such targets can be referred to as range resolution. In Eptesicus fuscus, this ability is limited to distinct internal time delays (12, 32-40, and 52-100 microns) between the two wave fronts of a double-wave-front target. Analysis of the simulated two-wave-front echoes reveals periodic frequency minima in the spectrum. Position and separation of these spectral minima depend on the time delay between the two wave fronts. The occurrence of spectral minima within the frequency range of the first harmonic in the echo of the bats' echolocation call correlates to the bats' ability to discriminate a one-wave-front echo from two-wave-front echoes, suggesting that Eptesicus fuscus uses spectral differences within the first harmonic in echoes for range resolution.     

Spatial perception and adaptive sonar behavior

Bat echolocation is a dynamic behavior that allows for real-time adaptations in the timing and spectro-temporal design of sonar signals in response to a particular task and environment. To enable detailed, quantitative analyses of adaptive sonar behavior, echolocation call design was investigated in big brown bats, trained to rest on a stationary platform and track a tethered mealworm that approached from a starting distance of about 170 cm in the presence of a stationary sonar distracter. The distracter was presented at different angular offsets and distances from the bat. The results of this study show that the distance and the angular offset of the distracter influence sonar vocalization parameters of the big brown bat, Eptesicus fuscus. Specifically, the bat adjusted its call duration to the closer of two objects, distracter or insect target, and the magnitude of the adjustment depended on the angular offset of the distracter. In contrast, the bat consistently adjusted its call rate to the distance of the insect, even when this target was positioned behind the distracter. The results hold implications for understanding spatial information processing and perception by echolocation.     

Flying big brown bats emit a beam with two lobes in the vertical plane

The sonar beam of an echolocating bat forms a spatial window restricting the echo information returned from the environment. Investigating the shape and orientation of the sonar beam produced by a bat as it flies and performs various behavioral tasks may yield insight into the operation of its sonar system. This paper presents recordings of vertical and horizontal cross sections of the sonar beam produced by Eptesicus fuscus (big brown bats) as they fly and pursue prey in a laboratory flight room. In the horizontal plane the sonar beam consists of one large lobe and in the vertical plane the beam consists of two lobes of comparable size oriented frontally and ventrally. In level flight, the bat directs its beam such that the ventral lobe is pointed forward and down toward the ground ahead of its flight path. The bat may utilize the downward directed lobe to measure altitude without the need for vertical head movements.     

Range discrimination by big brown bats (Eptesicus fuscus) using altered model echoes: implications for signal processing

The sonar emissions of two big brown bats (Eptesicus fuscus) were modeled to create a "normal" echolocation signal for each bat which was then used as an artificial echo to synthesize a phantom target. The bat's task was to indicate which of two phantom targets (presented singly) was the "near" target and which the "far" target. Threshold range discrimination at a nominal target distance of 80 cm was about 0.6 cm for both bats. The normal signal was then modified to change the relative energy in each harmonic, the signal duration, the curvature of the frequency sweep, the absolute frequency, the phase of the second and third harmonics relative to the first, or the Doppler shift of the signal. To determine which modifications affected ranging performance, the altered models were used in tests of range discrimination that were interleaved on a day-to-day basis with tests using the normal model. Of the 12 modifications tested, only those changing the curvature of the frequency sweep affected performance. This result appears not to be predicted by current models of echo processing in FM bats. Eptesicus may be able to compensate for certain types of distortions of a returning echo, an ability possibly related to Doppler tolerance or to the characteristics of the natural variation in a bat's emissions.     

Echolocation call intensity and directionality in flying short-tailed fruit bats, Carollia perspicillata (Phyllostomidae)

The directionality of bat echolocation calls defines the width of bats' sonar "view," while call intensity directly influences detection range since adequate sound energy must impinge upon objects to return audible echoes. Both are thus crucial parameters for understanding biosonar signal design. Phyllostomid bats have been classified as low intensity or "whispering bats," but recent data indicate that this designation may be inaccurate. Echolocation beam directionality in phyllostomids has only been measured through electrode brain-stimulation of restrained bats, presumably excluding active beam control via the noseleaf. Here, a 12-microphone array was used to measure echolocation call intensity and beam directionality in the frugivorous phyllostomid, Carollia perspicillata, echolocating in flight. The results showed a considerably narrower beam shape (half-amplitude beam angles of approximately 16° horizontally and 14° vertically) and louder echolocation calls [source levels averaging 99 dB sound pressure level (SPL) root mean square] for C. perspicillata than was found for this species when stationary. This suggests that naturally behaving phyllostomids shape their sound beam to achieve a longer and narrower sonar range than previously thought. C. perspicillata orient and forage in the forest interior and the narrow beam might be adaptive in clutter, by reducing the number and intensity of off-axis echoes.     

Evaluation of the echolocation model for range estimation of multiple closely spaced objects

Experimental evidence indicates that bats can use frequency-modulated echolocation to identify objects with an accuracy of less than 1 μs. However, when modeling this process, it is difficult to estimate the delay times of multiple closely spaced objects by analyzing the echo spectrum, because the sequence of delay separations cannot be determined without information on the temporal changes in the interference patterns of the echoes. To extract the temporal changes, Gaussian chirplets with a carrier frequency compatible with bat emission sweep rates are introduced. The delay time for object 1 (T(1)) is estimated from the echo spectrum around the onset time. The T(2) is obtained by adding the T(1) to the delay separation between objects 1 and 2. Further objects are located in sequence by this procedure. Here echoes were measured from single and multiple objects at a low signal-to-noise ratio. It was confirmed that the delay time for a single object could be estimated with an accuracy of about 1.3 μs. The range accuracy was less than 6 μs when the frequency bandwidth was less than 10 kHz. The delay time for multiple closely spaced objects could be estimated with a high range resolution by extracting the interference pattern.     

An echolocation model for range discrimination of multiple closely spaced objects: transformation of spectrogram into the reflected intensity distribution

Using frequency-modulated echolocation, bats can discriminate the range of objects with an accuracy of less than a millimeter. However, bats' echolocation mechanism is not well understood. The delay separation of three or more closely spaced objects can be determined through analysis of the echo spectrum. However, delay times cannot be properly correlated with objects using only the echo spectrum because the sequence of delay separations cannot be determined without information on temporal changes in the interference pattern of the echoes. To illustrate this, Gaussian chirplets with a carrier frequency compatible with bat emission sweep rates were used. The delay time for object 1, T1, can be estimated from the echo spectrum around the onset time. The delay time for object 2 is obtained by adding T1 to the delay separation between objects 1 and 2 (extracted from the first appearance of interference effects). Further objects can be located in sequence by this same procedure. This model can determine delay times for three or more closely spaced objects with an accuracy of about 1 micros, when all the objects are located within 30 micros of delay separation. This model is applicable for the range discrimination of objects having different reflected intensities and in a noisy environment (0-dB signal-to-noise ratio) while the cross-correlation method is hard to apply to these problems.     

Transforming echoes into pseudo-action potentials for classifying plants.

Animals perceive their environment by converting sensory stimuli into action potentials, or temporal point processes, that are interpreted by the brain. This paper investigates the information content of point processes extracted from echoes from in situ plants in an effort to understand how bats recognize landmarks in the field. A mobile sonar converts echoes into biologically similar temporal point processes. termed pseudo-action potentials (PAPs), whose inter-PAP interval relates to echo amplitude. The sonar forms a sector scan of an object to produce a spatial-temporal PAP field. Classifier neurons apply delays and coincidence detection to the PAP field to identify three distinct echo types, glints, blobs, and fuzz, which characterize plant features. Glints are large amplitude echoes exhibiting coherence over successive echoes in the sector scan, typically produced by favorably oriented isolated specular reflectors. Blobs are large echoes lacking coherence, typically bordering glints or formed by collections of interfering reflectors. Fuzz represents weak echoes, typically produced by collection of weak scatterers or by reflectors on the beam periphery. A small mirror reflector models a flat leaf surface and motivates the glint criteria. Classifiers are applied to experimental data from two types of tree trunks, a glint-producing sycamore (Platanus occidenatalis) and a glint-absent Norway maple (Acer platanoides) and two plants, a glint-producing rhododendron (Rhododendron maximus) and a glint-absent yew (Taxus media). We speculate that our narrow-band sonar models the activity of a single frequency bin in the frequency-modulated (FM) sweep emitted by bats, and that one function of the frequency bins in the FM sweep is to form a sector scan of the environment.     

Classification of communication signals of the little brown bat

Little brown bats, Myotis lucifugus, are known for their ability to echolocate and utilize their echolocation system to navigate, and locate and identify prey. Their echolocation signals have been characterized in detail but their communication signals are less well understood despite their widespread use during social interactions. The goal of this study was to develop an automatic classification algorithm for characterizing the communication signals of little brown bats. Sound recordings were made overnight on five individual male bats (housed separately from a large group of captive bats) for 7 nights, using a bat detector and a digital recorder. The spectral and temporal characteristics of recorded sounds were first analyzed and classified by visual observation of a call's temporal pattern and spectral composition. Sounds were later classified using an automatic classification scheme based on multivariate statistical parameters in MATLAB. Human- and machine-based analysis revealed five discrete classes of bat's communication signals: downward frequency-modulated calls, steep frequency-modulated calls, constant frequency calls, broadband noise bursts, and broadband click trains.     

Clutter interference and the integration time of echoes in the echolocating bat, Eptesicus fuscus

The ability of the echolocating bat, Eptesicus fuscus, to detect a sonar target is affected by the presence of other targets along the same axis at slightly different ranges. If echoes from one target arrive at about the same delay as echoes from another target, clutter interference occurs and one set of echoes masks the other. Although the bat's sonar emissions and the echoes themselves are 2 to 5 ms long, echoes (of approximately equal sensation levels--around 15 dB SL) only interfere with each other if they arrive within 200 to 400 microseconds of the same arrival time. This figure is an estimate of the integration time of the bat's sonar receiver for echoes. The fine structure of the clutter-interference data reflects the reinforcement and cancellation of echoes according to their time separation. When clutter interference first occurs, the waveforms of test and cluttering echoes already overlap for much of their duration. The masking effect underlying clutter interference appears specifically due to overlap, not between raw echo waveforms, but between the patterns of mechanical excitation created when echoes pass through bandpass filters equivalent to auditory-nerve tuning curves. While the time scale of clutter interference is substantially shorter than the duration of echo waveforms, it still is much longer than the eventual width of a target's range-axis image expressed in terms of echo delay.     

Doppler-shift compensation in the Taiwanese leaf-nosed bat (Hipposideros terasensis) recorded with a telemetry microphone system during flight

Biosonar behavior was examined in Taiwanese leaf-nosed bats (Hipposideros terasensis; CF-FM bats) during flight. Echolocation sounds were recorded using a telemetry microphone mounted on the bat's head. Flight speed and three-dimensional trajectory of the bat were reconstructed from images taken with a dual high-speed video camera system. Bats were observed to change the intensity and emission rate of pulses depending on the distance from the landing site. Frequencies of the dominant second harmonic constant frequency component (CF2) of calls estimated from the bats' flight speed agreed strongly with observed values. Taiwanese leaf-nosed bats changed CF2 frequencies depending on flight speed, which caused the CF2 frequencies of the Doppler-shifted echoes to remain constant. Pulse frequencies were also estimated using echoes returning directly ahead of the bat and from its sides for two different flight conditions: landing and U-turn. Bats in flight may periodically alter their attended angles from the front to the side when emitting echolocation pulses.     

Echo-intensity compensation in echolocating bats (Pipistrellus abramus) during flight measured by a telemetry microphone

An onboard microphone (Telemike) was developed to examine changes in the basic characteristics of echolocation sounds of small frequency-modulated echolocating bats, Pipistrellus abramus. Using a dual high-speed video camera system, spatiotemporal observations of echolocation characteristics were conducted on bats during a landing flight task in the laboratory. The Telemike allowed us to observe emitted pulses and returning echoes to which the flying bats listened during flight, and the acoustic parameters could be precisely measured without traditional problems such as the directional properties of the recording microphone and the emitted pulse, or traveling loss of the sound in the air. Pulse intensity in bats intending to land exhibited a marked decrease by 30 dB within 2 m of the target wall, and the reduction rate was approximately 6.5 dB per halving of distance. The intensity of echoes returning from the target wall indicated a nearly constant intensity (-42.6 +/- 5.5 dB weaker than the pulse emitted in search phase) within a target distance of 2 m. These findings provide direct evidence that bats adjust pulse intensity to compensate for changes in echo intensity to maintain a constant intensity of the echo returned from the approaching target at an optimal range.     

The role of the external ear in vertical sound localization in the free flying bat, Eptesicus fuscus

The role of the external ear in sonar target localization for prey capture was studied by deflecting the tragus of six big brown bats, Eptesicus fuscus. The prey capture performance of the bat dropped significantly in the tragus-deflection condition, compared with baseline, control, and recovery conditions. Target localization error occurred in the tragus-deflected bat, and mainly in elevation. The deflection of the tragus did not abolish the prey capture ability of the bat, which suggests that other cues are available used for prey localization. Adaptive vocal and motor behaviors were also investigated in this study. The bat did not show significant changes in vocal behaviors but modified its flight trajectories in response to the tragus manipulation. The tragus-deflected bat tended to attack the prey item from above and had lower tangential velocity and larger bearing from the side, compared with baseline and recovery conditions. These findings highlight the contribution of the tragus to vertical sound localization in the free-flying big brown bat and demonstrate flight adaptations the bat makes to compensate altered acoustic cues.     

Transformation of external-ear spectral cues into perceived delays by the big brown bat,Eptesicus fuscus

The external-ear transfer function for big brown bats (Eptesicus fuscus) contains two prominent notches that vary from 30 to 55 kHz and from 70 to 100 kHz, respectively, as sound-source elevation moves from -40 to +10 degrees. These notches resemble a higher-frequency version of external-ear cues for vertical localization in humans and other mammals. However, they also resemble interference notches created in echoes when reflected sounds overlap at short time separations of 30-50 micros. Psychophysical experiments have shown that bats actually perceive small time separations from interference notches, and here we used the same technique to test whether external-ear notches are recognized as a corresponding time separation, too. The bats' performance reveals the elevation dependence of a time-separation estimate at 25-45 micros in perceived delay. Convergence of target-shape and external-ear cues onto echo spectra creates ambiguity about whether a particular notch relates to the object or to its location, which the bat could resolve by ignoring the presence of notches at external-ear frequencies. Instead, the bat registers the frequencies of notches caused by the external ear along with notches caused by the target's structure and employs spectrogram correlation and transformation (SCAT) to convert them all into a family of delay estimates that includes elevation.     

Accuracy of distance measurement in the bat Eptesicus fuscus: theoretical aspects and computer simulations

Behavioral experiments of Simmons [J. Acoust. Soc. Am. 54, 157-173 (1973) and Science 204, 1336-1338 (1979)] on the ranging accuracy in the bat Eptesicus fuscus have led to far-reaching postulates on the existence of optimal and phase-conserving processing mechanisms in the bat. In this paper, the results of computer simulations of these experiments are presented. Two receiver types are investigated: the fully coherent cross-correlation receiver and the cross-correlation receiver with envelope processing (semicoherent). It is shown that Simmons' experiments cannot be treated as a simple estimation of distance, but require at least two (range difference experiment; see Simmons, 1973) or four (range jitter experiment; see Simmons, 1979) echolocation sounds for one decision. The performance of the bat in both experiments is much worse than predicted for a coherent and a semicoherent receiver type. The bat's accuracy in Simmons' range difference experiment is at least 18 dB worse than predicted for an optimal receiver. The results of the jitter experiment cannot be interpreted in a simple way as proof that bats are able to evaluate phase information as in a fully coherent cross-correlation receiver.     

The acoustic basis for target discrimination by FM echolocating bats

Past experiments show that echolocating bats of the species Myotis lucifugus and Eptesicus fuscus can discriminate among airborne sonar targets presented in the context of pursuit maneuvers for the interception of prey. These bats distinguish between edible mealworms and inedible spheres of various sizes. Myotis can distinguish between disks and mealworms similar enough in size that the bat's performance requires the ability to perceive the acoustic equivalent of target shape. Previously observed small differences in the spectrum of echoes from mealworms and disks appear insufficient to distinguish these targets at the performance levels achieved by bats. We measured the acoustic properties of the targets by broadcasting ultrasonic impulses at mealworms, spheres, and disks and recording their echoes, displaying the results in terms of impulse echo waveforms and the frequency response of targets derived from the target transfer function. The echoes from disks and mealworms at various orientations convey the range-axis profile of the target (number and spacing of reflecting points or glints distributed at different ranges) in terms of the impulse structure of their waveforms and in terms of the locations and spacing of notches or nulls in their spectra. For targets that bats can discriminate and that reflect echoes which do not clearly differ in overall amplitude, the targets appear distinguishable from the acoustic representation of their range profile, which is a feature of targets that bats can perceive with great acuity.     

Target representation of naturalistic echolocation sequences in single unit responses from the inferior colliculus of big brown bats

Echolocating big brown bats (Eptesicus fuscus) emit trains of frequency-modulated (FM) biosonar signals whose duration, repetition rate, and sweep structure change systematically during interception of prey. When stimulated with a 2.5-s sequence of 54 FM pulse-echo pairs that mimic sounds received during search, approach, and terminal stages of pursuit, single neurons (N = 116) in the bat's inferior colliculus (IC) register the occurrence of a pulse or echo with an average of < 1 spike/sound. Individual IC neurons typically respond to only a segment of the search or approach stage of pursuit, with fewer neurons persisting to respond in the terminal stage. Composite peristimulus-time-histogram plots of responses assembled across the whole recorded population of IC neurons depict the delay of echoes and, hence, the existence and distance of the simulated biosonar target, entirely as on-response latencies distributed across time. Correlated changes in pulse duration, repetition rate, and pulse or echo amplitude do modulate the strength of responses (probability of the single spike actually occurring for each sound), but registration of the target itself remains confined exclusively to the latencies of single spikes across cells. Modeling of echo processing in FM biosonar should emphasize spike-time algorithms to explain the content of biosonar images.     

Cortical representation of spatiotemporal pattern of firing evoked by echolocation signals: population encoding of target features in real time.

Target perception in echolocating bats entails the generation of an acoustic image of the target in the auditory cortex. By integrating information conveyed in the sequence of acoustic echoes, the population of cortical neurons in hypothesized to encode different target features based on its spatiotemporal pattern of neural-spike firing during the course of echolocation. A biologically plausible approach to the cortical representation of target features is employed by using electrophysiological data recorded from the auditory cortex of the FM bat, Myotis lucifugus. A single-neuron model of delay-sensitive neurons is first approximated by the formulation of a Gaussian function with different variables to represent the delay-tuning properties of individual cortical neurons. A cortical region consisting of delay-sensitive neurons organized topographically according to best frequency (i.e., tontopically organized) is then modeled with multiple layers of the single-neuron model. A mechanism is developed to represent and encode the responses of these neurons based on time-dependent, incoming echo signals. The time-varying responses of the population of neurons are mapped spatially on the auditory-cortical surface as a cortical response map (CORMAP). The model is tested using phantom targets with single and multiple glints. These simulation results provide further validation of the current auditory framework as a biomimetic mechanism for capturing time-varying, acoustic stimuli impinging in the bat's ears, and the neural representation of acoustic stimulus features by saptiotemporal-firing patterns in the cortical population.