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Discrimination of jittered sonar echoes by the echolocating bat, Eptesicus fuscus: the shape of target images in echolocation.

1. Behavioral experiments with jittering echoes examined acoustic images of sonar targets in the echolocating bat, Eptesicus fuscus, along the echo delay or target range axis. Echo phase, amplitude, bandwidth, and signal-to-noise ratio were manipulated to assess the underlying auditory processes for image formation. 2. Fine delay acuity is about 10 ns. Calibration and control procedures indicate that this represents temporal acuity rather than spectral discrimination. Jitter discrimination curves change in phase when the phase of one jittering echo is shifted by 180 degrees relative to the other, showing that echo phase is involved in delay estimation. At an echo detectability index of about 36 dB, fine acuity is 40 ns, which is approximately as predicted for the delay accuracy of an ideal receiver. 3. Compound performance curves for 0 degrees and 180 degrees phase conditions match the crosscorrelation function of the echoes. The locations of both 0 degrees and 180 degrees phase peaks in the performance curves shift along the time axis by an amount that matches neural amplitude-latency trading in Eptesicus, confirming a temporal basis for jitter discrimination.

Acoustic Stimulation

Spatial processing within the mustache bat echolocation system: possible mechanisms for optimization.

1. The directionality of an echolocation system is determined by the acoustic properties of both the emitter and receiver, i.e., by the radiation pattern of the emitted pulse and the directionally of the external ears. We measured the directionality of the echolocation system of the greater mustache bat (Pteronotus parnellii) at the 30 kHz, 60 kHz and 90 kHz harmonics of its echolocation pulse by summing, at points throughout the frontal sound field, the echo attenuation due to the spread of pulse energy and the attenuation due to the spread of pulse energy and the attenuation due to the directionality of its external ears. The pulse radiation pattern at the 3 harmonics was measured by comparing the output of a microphone moved throughout the frontal sound field against a second reference microphone at the center of the field. External ear directionality at the 3. harmonics was measured by presenting free-field sounds throughout the frontal sound field, and recording the intensity thresholds of cochlear microphonic potentials, and the intensity thresholds of monaural neurons in the inferior colliculus tuned to one of the 3 harmonics. 2. When compared with ear directionality, the echolocation system was found to be more directional for the center of the sound field in several respects. At all harmonics, attenuation of sounds originating in the peripheral part of the field was increased by 10 to 13 dB. Areas of maximum sound intensity contracted toward the center of the field. Also, the isointensity contours of the echolocation system were more radially symmetrical about the center of the field. 3. At 60 kHz, sound intensity along the azimuth within the echolocation system was nearly constant 26 degrees to either side of the center of the field. This suggests that the radiation pattern of the echolocation pulse and the directionality of the external ears complement one another to produce an acoustic environment at the center of the sound field in which stimulus intensity is stabilized to allow more effective analysis of various aspects of the echolocation target. In particular, we suggest that this intensity stabilization may allow the bat to more effectively resolve the interaural intensity differences it uses to localize prey. 4. Predictions of the azimuthal spatial tuning of binaurally sensitive neurons in the inferior colliculus within the echolocation system were compared with their spatial tuning when only ear directionality is considered.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation

No cost of echolocation for bats in flight.

Echolocation has evolved in relatively few animal species. One constraint may be the high cost of producing pulses, the echoes of which can be detected over useful distances. The energy cost of echolocation in a small (6 g) insectivorous bat, when hanging at rest, was recently measured at 0.067 Joules per pulse, implying a mean cost for echolocation in flight of 9.5 x basal metabolic rate (range 7 to 12x). Because flight is very costly, whether the costs of echolocation and flying are additive is an important question. We measured the energy costs of flight in two species of small echolocating Microchiroptera using a novel combination of respirometry and doubly-labelled water. Flight energy expenditure (adjusted for body mass) was not significantly different between echolocating bats and non-echolocating bats and birds. The low cost of echolocation for flying vertebrates may have been a significant factor favouring its evolution in these groups.

Animals

Ontogenesis of the echolocation system in the rufous horseshoe bat, Rhinolophus rouxi (audition and vocalization in early postnatal development).

1. The development of vocalization and hearing was studied in Sri Lankan horseshoe bats (Rhinolophus rouxi) during the first postnatal month. The young bats were caught in a nursing colony of rhinolophids in which birth took place within a two week period. 2. The new-born bats emitted isolation calls through the mouth. At the beginning these calls consisted of pure tones with frequencies below 10 kHz (Fig. 1). During the first postnatal week the call frequency increased to about 15 kHz, and the fundamental was augmented by two to four harmonics. No evoked potentials to pure tone stimuli could be elicited in the inferior colliculus of this age group, i.e., auditory processing at the midbrain level was not demonstrable. 3. Evoked potentials were first recorded in the second week, broadly tuned to 15-45 kHz, with a maximum sensitivity between 15-25 kHz. In the course of the second week, however, higher frequencies up to 60 kHz became progressively incorporated into the audiogram (Fig. 3). The fundamental frequency of the multiharmonic isolation calls, emitted strictly through the mouth, increased to about 20 kHz. 4. In the bats' third postnatal week an increased hearing sensitivity (auditory filter) emerged, sharply tuned at frequencies between 57 and 60 kHz (Fig. 4e). The same individuals were also the first to emit long constant frequency echolocation calls through the nostrils (Fig. 4c). The energy of the calls was arranged in harmonic frequency bands with the second harmonic exactly tuned to the auditory filter. These young bats continued to emit isolation calls through the mouth, which were, however, not harmonically related to the echolocation calls (Fig. 4b, d). 5. During the fourth week, both the auditory filter and the matched echolocation pulses (the second harmonic) shifted towards higher frequencies (Fig. 5). During the fifth week the fundamental frequency of the calls was progressively attenuated, and both the second harmonic of the pulses and the auditory filter reached the frequency range typical for adult bats of 73-78 kHz (Fig. 6). 6. The development of audition and vocalization is discussed with regard to possible interactions of both subsystems, and their incorporation into the active orientation system of echolocation.

Aging

Functional laminar and columnar organization of the auditory centers in echolocating Japanese greater horseshoe bats.

During echolocation, bats coordinately employ the vocalization system to emit orientation sounds and the auditory system to hear returning echoes. The brain in these animals should be functionally organized to process such biologically significant sounds. Here we utilized the autoradiographic 2-deoxy-[14C]glucose (DG) method to visualize functional organization of the auditory centers of echolocating Japanese greater horseshoe bats, Rhinolophus ferrumequinum nippon. Autoradiographic color images made from the brains of echolocating bats revealed a functional laminar structure in the inferior colliculus. Furthermore, a functional columnar organization appeared in the auditory cortex during echolocation. These laminar and columnar organization were not observed in the brain of resting bats.

Acoustic Stimulation

Target detection, shape discrimination, and signal characteristics of an echolocating false killer whale (Pseudorca crassidens).

This study demonstrated the ability of a false killer whale (Pseudorca crassidens) to discriminate between two targets and investigated the parameters of the whale's emitted signals for changes related to test conditions. Target detection performance comparable to the bottlenose dolphin's (Tursiops truncatus) has previously been reported for echolocating false killer whales. No other echolocation capabilities have been reported. A false killer whale, naive to conditioned echolocation tasks, was initially trained to detect a cylinder in a "go/no-go" procedure over ranges of 3 to 8 m. The transition from a detection task to a discrimination task was readily achieved by introducing a spherical comparison target. Finally, the cylinder was successfully compared to spheres of two different sizes and target strengths. Multivariate analyses were used to evaluate the parameters of emitted signals. Duncan's multiple range tests showed significant decreases (df = 185, p less than 0.05) in both source level and bandwidth in the transition from detection to discrimination. Analysis of variance revealed a significant decrease in the number of clicks over test conditions [F(5.26) = 5.23, p less than 0.0001]. These data suggest that the whale relied on cues relevant to target shape as well as target strength, that changes in source level and bandwidth were task-related, that the decrease in clicks was associated with learning experience, and that Pseudorca's ability to discriminate shapes using echolocation may be comparable to that of Tursiops truncatus.

Animals

Discrimination of wingbeat motion by bats, correlated with echolocation sound pattern.

Bats of the species Rhinolophus rouxi, Hipposideros lankadiva and Eptesicus fuscus were trained to discriminate between two simultaneously presented artificial insect wingbeat targets moving at different wingbeat rates. During the discrimination trials, R. rouxi, H. lankadiva and E. fuscus emitted long-CF/FM, short-CF/FM and FM echolocation sounds respectively. R. rouxi, H. lankadiva and E. fuscus were able to discriminate a difference in wingbeat rate of 2.7 Hz, 9.2 Hz and 15.8 Hz, respectively, between two simultaneously presented targets at an absolute wingbeat rate of 60 Hz, using a criterion of 75% correct responses. The performance of the different bat species is correlated with the echolocation signal design used by each species, particularly with the presence and relative duration of a narrowband component preceding a broadband FM component. These results provide behavioral evidence supporting the hypothesis that bats that use CF/FM echolocation sounds have adaptations for the perception of insect wingbeat motion and that long-CF/FM species are more specialized for this task than short CF/FM species.

Animals

A comparison of signal detection between an echolocating dolphin and an optimal receiver.

An electronic simulated target apparatus was used in a two-experiment study to compare the target detection performance of an echolocating bottlenose dolphin with an optimal receiver. Random Gaussian noise with a relatively flat spectrum from 20 to 160 kHz was used as a masking source. Experiment I was conducted to establish a technique for estimating the echo energy-to-noise ratio, Ee/N, at the dolphin's threshold of detection. Dolphins typically vary the amplitude of their emitted signal over a large range making it difficult to estimate Ee/N. In the first part of experiment I, the simulated echo was a double click, the pulses separated by 200 microseconds, with each pulse being a replica of the dolphin's transmitted signal. A staircase psychophysical procedure was used to obtain the detection threshold, and the echo energy-to-noise ratio based on the highest amplitude click emitted per trial, (Ee/N)max, was determined at each reversal point. The second echo type consisted of one of the animal's echolocation clicks, previously measured, digitized and stored in an erasable programmable read-only memory (EPROM). The electronic target simulator was modified so that every time the dolphin emitted an echolocation signal, the EPROM was triggered to produce two pulses separated by 200 microseconds. On any trial, the EPROM signal was played back at a fixed amplitude, regardless of the amplitude of the dolphin's emitted signal. The Ee/N obtained with the EPROM signal at threshold was found to be 2.9 dB lower than (Ee/N)max obtained with the normal phantom target. Therefore an estimate of Ee/N can be obtained by subtracting 2.9 dB from (Ee/N)max.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals

Echolocation performance of the vampire bat (Desmodus rotundus).

The neotropical vampire bats (Desmodus rotundus) echolocate using ultrasonic pulses like those of the Latin American phyllostomatid bats. In this paper the orally produced echolocation sounds of Desmodus are analysed and the performance of the echolocation system is studied in two-choice training experiments on two vampire bats. Ability to detect objects is relatively limited; both animals were capable of discerning the presence of a 1 cm wide metal strip at a distance of 50 cm, but they failed with 0.5 cm wide strips. The ultrasonic pulses produced at a distance of 50 cm appear to sample an area with a diameter of 2.5 to 3.0 cm (i.e., the solid angle tested with each pulse is 3 degrees to 3 degrees 40' in extent).

Animals

[Correlation model of object recognition by echolocating animals].

The model proposed in an attempt to find out physical bases of object perception during echolocation. It is shown that echolocational perception can be provided with correlational treatment of corresponding signals. The character of objects is determined by the comparison by echo probing accepted in the given cycle with typical distortions remembered in the course of individual experience of the animal. The distortions take place during the reflection of the probing impulse from these or those objects. "Binding" of the objects according to distance may be carried out by using the choice of typical distortions for corresponding correction of the copy of probing impulse, serving as a bearing signal of distance correlometer. The response of correlometer to the echo from correctly perceived target increases. The block-scheme of such correlation perception during echolocation is given. Performance of some experiments allowing to check and refine the model considered.

Animals

Matching-to-sample by an echolocating dolphin (Tursiops truncatus).

An adult male dolphin was trained to perform a three-alternative delayed matching-to-sample task while wearing eyecups to occlude its vision. Sample and comparison stimuli consisted of a small and a large PVC plastic tube, a water-filled stainless steel sphere, and a solid aluminum cone. Stimuli were presented under water and the dolphin was allowed to identify the stimuli through echolocation. The echolocation clicks emitted by the dolphin to each sample and each comparison stimulus were recorded and analyzed. Over 48 sessions of testing, choice accuracy averaged 94.5% correct. This high level of accuracy was apparently achieved by varying the number of echolocation clicks emitted to various stimuli. Performance appeared to reflect a preexperimental stereotyped search pattern that dictated the order in which comparison items were examined and a complex sequential-sampling decision process. A model for the dolphin's decision-making processes is described.

Animals

[Calculation of potential accuracy in measuring the angular coordinates of targets by the echolocator of bats using the equal-signal zone method].

Potential accuracy in measuring the course to a target is calculated. This accuracy is physically achievable it the hypothesis that an accurate measurement of angular coordinates of the target of bat's echolocator is realized by the method similar to that of equally signaling zone in radiolocation is true. Possible application of such a method is based on the "pulsation" of direction diagram in the course of radiation of the probing impulse. In this case crossing of partial diagrams of radiation corresponding to high- and low-frequancy regions of the impulse form the equally signaling zine. If the target is in this direction the amplitudes of autocorrelation functions formed by corresponding regions of reflected and probing impulses will be equal. The minimal error of the method is limited by the optimum duration of each of the compared correlation functions, which forms the basis for derivation of the formula evaluating this error. Numerical calculation of the accuracy of measurements of the angle achievable for the echolocator of Myotis blythi is performed by this formula proceeding from average experimental values of the echolocator characteristics. The model under consideration is shown to agree with a number of experimental data.

Animals

Common principle of guidance by echolocation and vision.

1. Using echolocation, bats move as gracefully as birds through the cluttered environment, suggesting common principles of optic and acoustic guidance. We tested the idea by analysing braking control of bats (Macroderma gigas) flying through a narrow aperture with eyes covered and uncovered. 2. Though braking control would seem to require rapid detection of distance and velocity and computation of deceleration, simpler control is possible using the tau function of any sensory variable S that is a power function of distance to aperture. Tau function of S is tau (S) = S/S (the dot means time derivative). Controlled braking is achievable by keeping tau (S) constant. 3. Previous experiments indicated the tau (S) constant procedure is followed by humans and birds in visually controlling braking. Analysis of the bats' flight trajectories indicated they too followed the braking procedure using echolocation. 4. The tau function of echo-delay or of echo-intensity or of angle subtended by directions of echoes from two points on the approach surface could be used to control braking. Aperture size was modulated during flight on some trials in an attempt to test between these possibilities, but the results were inconclusive.

Animals

A blind mobility aid modeled after echolocation of bats.

A new model of a mobility aid for the blind was designed using microprocessor and ultrasonic devices. This mobility aid was evaluated based on psychophysical experiments. In this model, a downswept FM ultrasound signal is emitted from a transmitting array with broad directional characteristics in order to detect obstacles. The ultrasound reflections from the obstacles are picked up by a two-channel receiver. The frequency of the emitted ultrasound is swept from 70 to 40 kHz within 1 ms, so it has almost the same characteristics as the ultrasound a bat produces for echolocation. The frequency of the reflected ultrasound wave is down converted by about 50:1 by using a microcomputer with A/D and D/A converters. These audible waves are then presented binaurally through earphones. In this method obstacles may be perceived as localized sound images corresponding to the direction and the size of the obstacles. From the results of psychophysical experiments, it was found that downswept FM ultrasound was superior for the recognition of small obstacles compared to other ultrasonic schemes. With it a blind person can recognize a 1-mm-diameter wire. It was also proved that the blind could discriminate between several obstacles at the same time without any virtual images. This mobility aid, modeled after the bat's echolocation system, is very effective at detecting small obstacles placed in front of the head.

Animals

Detection of complex echoes in noise by an echolocating dolphin.

Dolphins echolocate with short broadband acoustic signals that have good time resolution properties. Received echoes are often complex, with many resolvable highlights or components caused by reflection of the incident signal from external and internal boundaries of a target and from different propagational modes within a target. A series of experiments was performed to investigate how dolphins perceive complex echoes. Echoes were produced by a microprocessor-controlled electronic target simulator that captured each emitted click and retransmitted the signal back to the animal after an appropriate time delay. The use of this "phantom" target allowed for precise control of the number of highlights, the time separation between highlights, and the relative amplitudes of highlights in the simulated echoes. An echolocating dolphin was trained to perform a target detection task in the presence of masking noise using these phantom echoes. The properties of simulated echoes were systematically varied, and corresponding shifts in the dolphin's detection threshold were observed, allowing for inferences of how the dolphin perceived echoes. The dolphin performed like an energy detector with an integration time of approximately 264 microseconds.

Acoustic Stimulation

Is the structure of bat echolocation calls an adaptation to the mammalian hearing system?

A common feature of most bat echolocation calls is their hyperbolalike frequency modulation. It is proposed that these calls evolved as an adaptation to the filters in the peripheral hearing system. From an analysis of 420 echolocation sounds of Eptesicus fuscus, the bandwidths of filters giving a minimal error of time-delay estimation are predicted; these could be compared to neurophysiological findings.

Adaptation, Physiological

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.

Animals