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Topographic representation of vocal frequency demonstrated by microstimulation of anterior cingulate cortex in the echolocating bat, Pteronotus parnelli parnelli.

1. A midline region of brain dorsal and anterior to the corpus callosum, presumably anterior cingulate cortex, has been explored for its role in the production of vocalization in the mustached bat, Pteronotus p. parnelli. 2. Vocalizations elicited by microstimulation were virtually indistinguishable from natural biosonar sounds. The spectral content, relative intensity of harmonic components, and durations of emitted pulses are comparable to spontaneous emissions. 3. The frequencies of elicited vocalizations were within the range typically used by the mustached bat during Doppler-shift compensation. The frequency of the second-harmonic constant-frequency component (CF2) covered the range from 57-62 kHz, but was most commonly emitted at frequencies of 59-61 kHz. 4. An increase in the frequency of vocalizations over a number of consecutive pulses towards a steady-state plateau is evident in both spontaneous vocalizations and emissions elicited by microstimulation just above threshold. Increasing the stimulus intensity caused the frequency of emissions to approach the steady state more rapidly. 5. The anterior cingulate cortex appears to be organized topographically for increasing frequency of elicited biosonar sounds along a rostrocaudal axis. The area from which biosonar emissions were elicited was overrepresented for a 2 kHz band of frequencies just below the bats' CF2 resting frequency. Audible vocalizations with a complex spectrum resembling social cries can also be elicited by microstimulation, but only in an area that is adjacent and posterior to the biosonar region. 6. Some examples of both elicited and spontaneous vocalizations contained a relative intensity pattern of the harmonic components which deviated from the typical pattern. This suggests that mustached bats are capable of actively altering the spectrum of their pulses to subserve different tasks in echolocation.

Animals↗

Frequency modulation patterns in the echolocation signals of two vespertilionid bats.

In this study we measure and classify frequency modulation patterns in echolocation signals of two species of bats. By using the derivative of an exponential model fitted to pulses emitted by Pipistrellus pipistrellus and Myotis myotis, we show that the modulation functions differ fundamentally between the two species and also vary within each species. This variation makes it unlikely that pulse design and the concomitant modulation pattern can be explained by a single common principle as previously suggested.

Animals↗

Mechanical adaptations for echolocation in the cochlea of the bat Hipposideros lankadiva.

The cochlear mechanics of bats with long constant-frequency components in their echolocation calls are sharply tuned to the dominant second harmonic constant frequency. Hipposiderid bats employ a shorter constant-frequency call component whose frequency is less stable than in long-constant-frequency bats. To investigate to what degree cochlear mechanics in hipposiderid bats are already specialized for the processing of constant frequencies, we recorded distortion-product otoacoustic emissions in Hipposideros lankadiva. Iso-distortion threshold curves for the 2f1-f2 distortion-product otoacoustic emission reveal a threshold maximum close to the second harmonic constant frequency, between 65.0 and 70.0 kHz, and a second insensitivity close to the first harmonic constant frequency. The group delay of the 2f1-f2 distortion is prolonged for both frequency ranges, indicating that a specialized cochlear resonance may act to absorb the constant-frequency call components. Compared to long-constant-frequency bats, the threshold maximum at the second harmonic constant frequency is less pronounced and the optimum cochlear frequency separation is larger. Distortion-product otoacoustic emission suppression tuning curves and neuronal tuning curves recorded from neurons in the cochlear nucleus display an increase of tuning sharpness close to the second harmonic constant-frequency range which is smaller than that reported for long-constant-frequency bats. Our data suggest that the cochlea of hipposiderid bats represents an intermediate state between that of non-specialized bats and long-constant-frequency bats.

Adaptation, Physiological↗

Arctiid moths and bat echolocation: broad-band clicks interfere with neural responses to auditory stimuli in the nuclei of the lateral lemniscus of the big brown bat.

Clicks emitted by arctiid moths interfere with the ranging ability of echolocating bats. To identify possible neural correlates of this interference, we recorded responses of single units in the nuclei of the lateral lemniscus to combinations of a broad-band click and a test signal (pure tones or frequency-modulated sweeps). In 77% of 87 units tested, clicks interfered with neural responses to the test stimuli. The interference fell into two categories: latency ambiguity and suppression. Units showing latency ambiguity responded to both the click and the test signal. However, when the click occurred within a window of approximately 3 ms before the onset of the test signal, the latency of the response to the test signal was affected. Units that were suppressed did not respond to clicks. Nevertheless, when a click was presented immediately before or simultaneously with a test signal, the response to the test signal was eliminated. Both types of units were found throughout the lateral lemniscus except for the columnar division of the ventral nucleus, where all units tested exhibited latency ambiguity. There is a close match between the single unit data and previous studies of range difference discrimination in the presence of clicks.

Acoustic Stimulation↗

Neural ensemble coding of target identity in echolocating bats.

Most insectivorous bats use echolocation to determine the identity of flying insects. Among the many target features that are so extracted, the insect's wingbeat pattern and frequency appear to serve as useful cues for identification. Biosonar pulses impinging on the fluttering wings of an insect are returned as echoes whose amplitudes vary with time, thus providing a characteristic signature of the insect. It has been shown previously that neurons in the inferior colliculus, a midbrain auditory nucleus, of the little brown bat respond to sound stimuli that mimic echoes from fluttering targets. To examine the manner in which target identity is represented in the inferior colliculus, an ensemble coding analysis using a filter-based approach was undertaken. The analysis indicates that a discrete subset of neurons in the inferior colliculus, the onset units, are strongly tuned to wingbeat frequencies of targets that the bat hunts, and that ensemble response reaches a maximum at a distinct phase of the prey capture maneuver: the late approach stage. On the basis of the analysis it is hypothesized that inferior colliculus neurons may play an important role in target detection-identification processing. Although ensemble coding of temporally sequenced information has not been analyzed in the auditory system so far, this study indicates that this method of coding may provide the information necessary to detect and identify targets during prey capture.

Acoustic Stimulation↗

Auditory spatial sensitivity of inferior collicular neurons of echolocating bats.

The sensitivity of 94 inferior collicular (IC) neurons of Eptesicus fuscus and Myotis lucifugus to spatial location of the acoustic stimulus were studied under free-field stimulus conditions. The best frequency (BF) and minimum threshold (MT) of each neuron were determined with sound delivered in front of the bat. Then the variation in discharge rate of the neuron was measured with a BF sound broadcast from a moving loudspeaker at different angular positions along the horizontal, vertical or diagonal plane of the frontal auditory space. A wide range of stimulus intensities above the MT of the neuron was used. Neurons were classified into 3 classes on the basis of their spatial sensitivity: (1) omnisensitive neurons (15%) were broadly tuned to sound delivered in the frontal auditory space and their responses did not show any correlation with sound location; (2) stimulus intensity-dependent neurons (28%) varied their discharge rates with sound location and intensity so that the peak of their spatial response profiles also varied with stimulus intensity; and (3) stimulus intensity-independent neurons (57%) varied their discharge rates only with sound location over a wide range of stimulus intensities so that their peak discharge always appeared at the same or a small range of angle. In most cases, the medial limbs of the spatial sensitivity curve for these neurons were extremely sharp and congruent. By moving the loudspeaker along the horizontal, vertical and diagonal planes, it was possible to approximate the boundary of the spatial response area of a neuron. Most IC neurons responded to sound delivered within 20 degrees ipsilateral, 60 degrees contralateral, 45 degrees up and 40 degrees down of the frontal auditory space, confirming previous similar studies. In general, an increasing stimulus repetition rate appeared to sharpen the spatial sensitivity curve of a neuron. Conversely, an increasing moving velocity of the stimulus decreased its response. The possible role of these 3 classes of neurons in echolocation and neural mechanisms underlying the spatial sensitivity of these neurons is discussed.

Acoustic Stimulation↗

A view of the world through the bat's ear: the formation of acoustic images in echolocation.

Echolocating bats perceive objects as acoustic images derived from echoes of the ultrasonic sounds they emit. They can detect, track, identify, and intercept flying insects using sonar. Many species, such as the big brown bat, Eptesicus fuscus, emit frequency-modulated sonar sounds and perceive the distance to targets, or target range, from the delay of echoes. For Eptesicus, a point-target's image has a sharpness along the range axis that is determined by the acuity of echo-delay perception, which is about 10 ns under favorable conditions. The image as a whole has a fine range structure that corresponds to the cross-correlation function between emissions and echoes. A complex target- which has reflecting points, called "glints", located at slightly different distances and reflects echoes containing overlapping components with slightly different delays--is perceived in terms of its range profile. The separation of the glints along the range dimension is encoded by the shape of the echo spectrum created by interference between overlapping echo components. However, Eptesicus transforms the echo spectrum back into an estimate of the original delay separation of echo components. The bat thus converts spectral cues into elements of an image expressed in terms of range. The absolute range of the nearest glint is encoded by the arrival time of the earliest echo component, and the spectrally encoded range separation of additional glints is referred to this time-encoded reference range for the image as a whole. Each individual glint is represented by a cross-correlation function for its own echo component, the nearest of which is computed directly from arrival-time measurements while further ones are computed by transformation of the echo spectrum. The bat then sums the cross-correlation functions for multiple glints to form the entire image of the complex target. Range and shape are two distinct features of targets that are separately encoded by the bat's auditory system, but the bat perceives unitary images that require fusion of these features to create a synthetic psychological dimension of range. The bat's use of cross-correlation-like images reveals neural computations that achieve fusion of stimulus features and offers an example of high-level operations involved in the formation of perceptual "wholes".

Animals↗

Directionality of sound pressure transformation at the pinna of echolocating bats.

The directionality of sound pressure transformation at the pinna of three species of bats was studied by measuring the sound pressure level of a tone (25 45 65 and 85 kHz) at the tympanic membrane as a function of azimuth and elevation of the sound source under free-field conditions. The tympanic sound pressure level varied with location of the sound source. The directionality of sound pressure transformation pattern of the pinna of each bat was studied by plotting isopressure contours. The area within each isopressure contour decreased with increasing tonal frequency. For each tonal frequency, the point of maximal sound pressure was always located in the frontal ipsilateral sound field. This point shifted medially with increasing tonal frequency along the horizontal plane in all species tested, but it shifted in a species-specific manner along the vertical plane. Removal or distortion of the pinna and tragus resulted in either uncircumscribed or irregular isopressure contours for all tonal frequencies tested. Acoustic pressure gain of the external ear reached 16-23 dB for frequencies at 15-18 kHz. The importance of the external ear to the directionality of the bat's echolocation system is discussed.

Acoustics↗

Echolocation, vocal learning, auditory localization and the relative size of the avian auditory midbrain nucleus (MLd).

The avian nucleus mesencephalicus lateralis, pars dorsalis (MLd) is an auditory midbrain nucleus that plays a significant role in a variety of acoustically mediated behaviours. We tested whether MLd is hypertrophied in species with auditory specializations: owls, the vocal learners and echolocaters. Using both conventional and phylogenetically corrected statistics, we find that the echolocating species have a marginally enlarged MLd, but it does not differ significantly from auditory generalists, such as pigeons, raptors and chickens. Similarly, all of the vocal learners tend to have relatively small MLds. Finally, MLd is significantly larger in owls compared to all other birds regardless of how the size of MLd is scaled. This enlargement is far more marked in asymmetrically eared owls than symmetrically eared owls. Variation in MLd size therefore appears to be correlated with some auditory specializations, but not others. Whether an auditory specialist possesses a hypertrophied MLd appears to be depend upon their hearing range and sensitivity as well as the ability to resolve small azimuthal and elevational angles when determining the location of a sound. As a result, the only group to possess a significantly large MLd consistently across our analyses is the owls. Unlike other birds surveyed, owls have a battery of peripheral and other central auditory system specializations that correlate well with their hearing abilities. The lack of differences among the generalists, vocal learners and echolocaters therefore reflects an overall similarity in hearing abilities, despite the specific life history requirements of each specialization and species. This correlation between the size of a neural structure and the sensitivity of a perceptual domain parallels a similar pattern in mammals.

Analysis of Variance↗

Spike-based VLSI modeling of the ILD system in the echolocating bat.

The azimuthal localization of objects by echolocating bats is based on the difference of echo intensity received at the two ears, known as the interaural level difference (ILD). Mimicking the neural circuitry in the bat associated with the computation of ILD, we have constructed a spike-based VLSI model that can produce responses similar to those seen in the lateral superior olive (LSO) and some parts of the inferior colliculus (IC). We further explore some of the interesting computational consequences of the dynamics of both synapses and cellular mechanisms.

Action Potentials↗

Use of an ultrasonic echolocation prosthesis by early visually deprived cats.

The aim of this study was to design an animal model of sensory substitution in the case of blindness. Six kittens were binocularly enucleated; as adults, they were fitted with an ultrasonic echolocation prosthesis. This device provided the animals with auditory signals that coded distance and direction of obstacles. Animals were trained by operant conditioning to use the prosthesis in various behavioral situation. The results showed that visually deprived animals tried to solve the task using natural information and that they only used artificial information provided by the prosthesis when they were unable to succeed with natural cues. Under these conditions, it was asserted that in a jumping test these animals evaluated depth by means of the prosthesis; in a locomotion task in a maze, it was also demonstrated that they could use the prosthesis for avoiding obstacles.

Animals↗

Seeing through sound: dolphins (Tursiops truncatus) perceive the spatial structure of objects through echolocation.

Experiment 1 tested a dolphin (Tursiops truncatus) for cross-modal recognition of 25 unique pairings of 8 familiar, complexly shaped objects, using the senses of echolocation and vision. Cross-modal recognition was errorless or nearly so for 24 of the 25 pairings under both visual to echoic matching (V-E) and echoic to visual matching (E-V). First-trial recognition occurred for 20 pairings under V-E and for 24 under E-V. Echoic decision time under V-E averaged only 1.88 s. Experiment 2 tested 4 new pairs of objects for 24 trials of V-E and 24 trials of E-V without any prior exposure of these objects. Two pairs yielded performance significantly above chance in both V-E and E-V. Also, the dolphin matched correctly on 7 of 8 1st trials with these pairs. The results support a capacity for direct echoic perception of object shape by this species and demonstrate that prior object exposure is not required for spontaneous cross-modal recognition.

Animals↗

Classification of virtual objects in the echolocating bat, Megaderma lyra.

Using echolocation, bats can not only locate objects in space but also discriminate objects of different shape. The acoustic image of an object is its impulse response (IR). The current experiments investigate whether bats just perceive changes in echo composition or whether bats perceive the IR itself through a detailed comparison of the emitted sound with the echo. The bat Megaderma lyra was trained to classify unknown virtual objects according to learned reference objects of different temporal and spectral composition. The bats' spontaneous classification was compared to predictions based on variousphysical and simulated peripheral auditory representations of the objects. The results show that the bats developed an accurate internal representation of the objects' IRs. In the auditory periphery, the IRs of small objects (< 4-6 cm) are coded along the tonotopic frequency axis.

Acoustics↗

Bottlenose dolphins perceive object features through echolocation.

How organisms (including people) recognize distant objects is a fundamental question. The correspondence between object characteristics (distal stimuli), like visual shape, and sensory characteristics (proximal stimuli), like retinal projection, is ambiguous. The view that sensory systems are 'designed' to 'pick up' ecologically useful information is vague about how such mechanisms might work. In echolocating dolphins, which are studied as models for object recognition sonar systems, the correspondence between echo characteristics and object characteristics is less clear. Many cognitive scientists assume that object characteristics are extracted from proximal stimuli, but evidence for this remains ambiguous. For example, a dolphin may store 'sound templates' in its brain and identify whole objects by listening for a particular sound. Alternatively, a dolphin's brain may contain algorithms, derived through natural endowments or experience or both, which allow it to identify object characteristics based on sounds. The standard method used to address this question in many species is indirect and has led to equivocal results with dolphins. Here we outline an appropriate method and test it to show that dolphins extract object characteristics directly from echoes.

Animals↗

Classification of natural textures in echolocation.

Through echolocation, a bat can perceive not only the position of an object in the dark; it can also recognize its 3D structure. A tree, however, is a very complex object; it has thousands of reflective surfaces that result in a chaotic acoustic image of the tree. Technically, the acoustic image of an object is its impulse response (IR), i.e., the sum of the reflections recorded when the object is ensonified with an acoustic impulse. The extraction of the acoustic IR from the ultrasonic echo and the detailed IR analysis underlies the bats' extraordinary object-recognition capabilities. Here, a phantom-object playback experiment is developed to demonstrate that the bat Phyllostomus discolor can evaluate a statistical property of chaotic IRs, the IR roughness. The IRs of the phantom objects consisted of up to 4,000 stochastically distributed reflections. It is shown that P. discolor spontaneously classifies echoes generated with these IRs according to IR roughness. This capability enables the bats to evaluate complex natural textures, such as foliage types, in a meaningful manner. The present behavioral results and their simulations in a computer model of the bats' ascending auditory system indicate the involvement of modulation-sensitive neurons in echo analysis.

Acoustics↗

Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory.

Echolocation signals were recorded from big brown bats, Eptesicus fuscus, flying in the field and the laboratory. In open field areas the interpulse intervals (IPI) of search signals were either around 134 ms or twice that value, 270 ms. At long IPI's the signals were of long duration (14 to 18-20 ms), narrow bandwidth, and low frequency, sweeping down to a minimum frequency (Fmin) of 22-25 kHz. At short IPI's the signals were shorter (6-13 ms), of higher frequency, and broader bandwidth. In wooded areas only short (6-11 ms) relatively broadband search signals were emitted at a higher rate (avg. IPI= 122 ms) with higher Fmin (27-30 kHz). In the laboratory the IPI was even shorter (88 ms), the duration was 3-5 ms, and the Fmin 30- 35 kHz, resembling approach phase signals of field recordings. Excluding terminal phase signals, all signals from all areas showed a negative correlation between signal duration and Fmin, i.e., the shorter the signal, the higher was Fmin. This correlation was reversed in the terminal phase of insect capture sequences, where Fmin decreased with decreasing signal duration. Overall, the signals recorded in the field were longer, with longer IPI's and greater variability in bandwidth than signals recorded in the laboratory.

Animals↗

Multiecho processing by an echolocating dolphin.

Bottlenose dolphins (Tursiops truncatus) use short, wideband pulses for echolocation. Individual waveforms have high-range resolution capability but are relatively insensitive to range rate. Signal-to-noise ratio (SNR) is not greatly improved by pulse compression because each waveform has small time-bandwidth product. The dolphin, however, often uses many pulses to interrogate a target, and could use multipulse processing to combine the resulting echoes. Multipulse processing could mitigate the small SNR improvement from pulse compression, and could greatly improve range-rate estimation, moving target indication, range tracking, and acoustic imaging. All these hypothetical capabilities depend upon the animal's ability to combine multiple echoes for detection and/or estimation. An experiment to test multiecho processing in a dolphin measured detection of a stationary target when the number N of available target echoes was increased, using synthetic echoes. The SNR required for detection decreased as the number of available echoes increased, as expected for multiecho processing. A receiver that sums binary-quantized data samples from multiple echoes closely models the N dependence of the SNR required by the dolphin. Such a receiver has distribution-tolerant (nonparametric) properties that make it robust in environments with nonstationary and/or non-Gaussian noise, such as the pulses created by snapping shrimp.

Acoustics↗

An echolocation model for the restoration of an acoustic image from a single-emission echo.

Bats can form a fine acoustic image of an object using frequency-modulated echolocation sound. The acoustic image is an impulse response, known as a reflected-intensity distribution, which is composed of amplitude and phase spectra over a range of frequencies. However, bats detect only the amplitude spectrum due to the low-time resolution of their peripheral auditory system, and the frequency range of emission is restricted. It is therefore necessary to restore the acoustic image from limited information. The amplitude spectrum varies with the changes in the configuration of the reflected-intensity distribution, while the phase spectrum varies with the changes in its configuration and location. Here, by introducing some reasonable constraints, a method is proposed for restoring an acoustic image from the echo. The configuration is extrapolated from the amplitude spectrum of the restricted frequency range by using the continuity condition of the amplitude spectrum at the minimum frequency of the emission and the minimum phase condition. The determination of the location requires extracting the amplitude spectra, which vary with its location. For this purpose, the Gaussian chirplets with a carrier frequency compatible with bat emission sweep rates were used. The location is estimated from the temporal changes of the amplitude spectra.

Animals↗