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Hearing in American leaf-nosed bats. I: Phyllostomus hastatus.

We determined the audiogram of Phyllostomus hastatus (the greater spear-nosed bat), a large, omnivorous American leaf-nosed bat native to Central and South America. A conditioned suppression/avoidance procedure with a fruit juice reward was used for testing. At an intensity of 60 dB sound pressure level (SPL re 20 microN/m(2)), the hearing range of P. hastatus extends from 1.8 to 105 kHz, with a best sensitivity of 1 dB SPL at 20 kHz. Both its high-frequency and low-frequency hearing are not unusual for a small mammal. Despite its use of low-intensity echolocation calls there was no evidence for unusual sensitivity to either the frequencies used for echolocation or to the main frequencies of its communication calls, suggesting no selective "tuning" of the audiogram. Its behavioral pure-tone thresholds are lower than the multi-unit thresholds in the inferior colliculus.

Acoustic Stimulation↗

Processing of sinusoidally amplitude modulated signals in the nuclei of the lateral lemniscus of the big brown bat, Eptesicus fuscus.

Changes in amplitude are a characteristic feature of most natural sounds, including the biosonar signals used by bats for echolocation. Previous evidence suggests that the nuclei of the lateral lemniscus play an important role in processing timing information that is essential for target range determination in echolocation. Neurons that respond to unmodulated tones with a sustained discharge are found in the dorsal nucleus (DNLL), intermediate nucleus (INLL) and multipolar cell division of the ventral nucleus (VNLLm). These neurons provide a graded response over a broad dynamic range of intensities, and would be expected to provide information about the amplitude envelope of a modulated signal. Neurons that respond only at the onset of a tone make up a small proportion of cells in DNLL, INLL and VNLLm, but are the only type found in the columnar division of the ventral nucleus (VNLLc). Onset neurons in VNLLc maintain a constant latency across a wide range of stimulus frequencies and intensities, thus providing a precise marker for when a sound begins. To determine how these different functional classes of cells respond to amplitude changes, we presented sinusoidally amplitude modulated (SAM) signals monaurally to awake, restrained bats and recorded the responses of single neurons extracellularly. There were clear differences in the ability of neurons in the different cell groups to respond to SAM. In the VNLLm, INLL and DNLL, 90% of neurons responded to SAM with a synchronous discharge. Neurons in the VNLLc responded poorly or not at all to SAM signals. This finding was unexpected given the precise onset responses of VNLLc neurons to unmodulated tones and their ability to respond synchronously to sinusoidally frequency modulated (SFM) signals. Among neurons that responded synchronously to SAM, synchronization as a function of modulation rate described either a bandpass or a lowpass function, with the majority of bandpass functions in neurons that responded to unmodulated tones with a sustained discharge. The maximal modulation rates that elicited synchronous responses were similar for the different cell groups, ranging from 320 Hz in VNLLm to 230 Hz in DNLL. The range of best modulation rates was greater for SAM than for SFM; this was also true of the range of maximal modulation rates at which synchronous discharge occurred. There was little correlation between a neuron's best modulation rate or maximal modulation rate for SAM signals and those for SFM signals, suggesting that responsiveness to amplitude and frequency modulations depends on different neural processing mechanisms.

Acoustic Stimulation↗

Evidence for a spectral basis of texture perception in bat sonar.

Bats obtain information about the structure of objects in the outside world from their echolocation signals, an extremely useful method when hunting non-flying prey in densely cluttered habitats, for example. Information about object structure is contained both in the time and in the spectral interference patterns of signals reflected from surfaces at different distances from the bat. I report here an experiment designed to test the extent to which bats use these two types of information. A 'phantom target' is generated by playing back to an echolocating bat signals that mimic the result of reflection from two planes set at different distances. The ability of the bat to discriminate between two such targets is investigated as a function of the separations of the planes. Several of the results do not fit the hypothesis that the bat simply uses time-delay information: the very small time difference that can be discriminated, the fall off in ability to discriminate planes at a particular separation and the symmetry of the discrimination ability measured in the frequency domain. The empirical data can best be fitted by a function based on spectral correlation.

Animals↗

Effect of acoustic clutter on prey detection by bats.

Bats that capture animal prey from substrates often emit characteristic echolocation calls that are short-duration, frequency-modulated (FM) and broadband. Such calls seem to be suited to locating prey in uncluttered habitats, including flying prey, but may be less effective for finding prey among cluttered backgrounds because echoes reflecting from the substrate mask the acoustic signature of prey. Perhaps these call designs serve primarily for spatial orientation. Furthermore, it has been unclear whether the acoustic image conveyed by FM echoes enables fine texture discrimination, or whether gleaning bats that forage in echo-cluttering environments must locate prey by using other cues, such as prey-generated sounds. Here we show that two species of insectivorous gleaning bats perform badly when compelled to detect silent and immobile prey in clutter, but are very efficient at capturing noisy prey items among highly cluttered backgrounds, and both dead or live prey in uncluttered habitats. These findings suggest that the short, broadband FM echolocation calls associated with gleaning bats are not adapted to detecting prey in clutter.

Acoustics↗

Harmonic-hopping in Wallacea's bats.

Evolutionary divergence between species is facilitated by ecological shifts, and divergence is particularly rapid when such shifts also promote assortative mating. Horseshoe bats are a diverse Old World family (Rhinolophidae) that have undergone a rapid radiation in the past 5 million years. These insectivorous bats use a predominantly pure-tone echolocation call matched to an auditory fovea (an over-representation of the pure-tone frequency in the cochlea and inferior colliculus) to detect the minute changes in echo amplitude and frequency generated when an insect flutters its wings. The emitted signal is the accentuated second harmonic of a series in which the fundamental and remaining harmonics are filtered out. Here we show that three distinct, sympatric size morphs of the large-eared horseshoe bat (Rhinolophus philippinensis) echolocate at different harmonics of the same fundamental frequency. These morphs have undergone recent genetic divergence, and this process has occurred in parallel more than once. We suggest that switching harmonics creates a discontinuity in the bats' perception of available prey that can initiate disruptive selection. Moreover, because call frequency in horseshoe bats has a dual function in resource acquisition and communication, ecological selection on frequency might lead to assortative mating and ultimately reproductive isolation and speciation, regardless of external barriers to gene flow.

Acoustics↗

The central acoustic tract and audio-vocal coupling in the horseshoe bat, Rhinolophus rouxi.

Doppler shift compensation (DSC) behaviour in horseshoe bats is a remarkable example of sensorimotor feedback that stabilizes the echo frequency at the bat's optimum hearing range regardless of motion-induced frequency shifts in the echoes. Searching for a related neural interface, the nucleus of the central acoustic tract (NCAT) was investigated in the echolocating horseshoe bat, Rhinolophus rouxi, using various neurophysiological and tracer methods. The NCAT receives bilateral auditory input from the cochlear nuclei and sends projections to regions outside the classical acoustic pathway like the pretectal area or the superior colliculus. The binaural input is excitatory from the contralateral and inhibitory from the ipsilateral ear to 53% of the units, and auditory responses were biased to frontal and contralateral directions. The best frequencies of NCAT neurons match a narrow range above the main frequency component of the bat's species-specific echolocation call (62% of the units), and the neurons exhibit extremely sharp tuning (Q10dB up to 632). DSC is degraded by unilateral electrical or pharmacological microstimulation of the NCAT, and heavily impaired by unilateral lesion of the region. Altogether, the efferents of the NCAT to prevocal areas, the tuning of its neurons to the DSC-relevant echo frequency range, and the possibility to affect DSC by manipulation of the NCAT, support the assumption that the nucleus plays an important role in audio-vocal control in the horseshoe bat.

Acoustic Stimulation↗

Tonotopic organization and parcellation of auditory cortex in the FM-bat Carollia perspicillata.

In the short-tailed fruit bat (Carollia perspicillata), the auditory cortex was localized autoradiographically and studied electrophysiologically in detail by using metal microelectrodes and 10-ms tone stimuli. Because, in the weakly-anaesthetized preparation, neuronal responses to pure-tones were even found throughout the non-primary auditory cortex, characteristic frequencies and minimum thresholds of neuron clusters (multiunits) could be mapped consistently and used to define auditory cortical fields conventionally (i.e. as in studies of auditory cortex of non-echolocating mammals). Thus, within the electrophysiologically demarcated auditory cortex, six auditory fields were defined by criteria, as for example a gradient of characteristic frequencies (primary auditory cortex, AI; anterior auditory field, AAF; secondary auditory cortex, AII), reversal of the gradient across the field border (AI, AAF), uniform representation of a restricted band of frequencies (i.e. > 60 kHz; high-frequency fields I and II, HFI and HFII), and transition from low to high minimum thresholds or vice versa [dorsoposterior field (DP), AII, HFI, HFII]. As supportive evidence for the distinction of these auditory cortical fields, differences in neuronal response properties were also used. In comparison with other mammals (e.g. cat and mouse), both the relative position of the auditory fields (mainly AI, AAF, DP and AII) and the representational principles for sound parameters within these forebrain areas seem to reflect a 'fundamental plan' (discussion below) of mammalian auditory cortical organization. Two coherent dorsally displaced high-frequency representations (HFI, HFII) covering approximately 40% of the total auditory cortical surface seem particularly suited for the processing of the dominant biosonar second and third harmonic of this species, and hence can be regarded as an adaptation for echolocation.

Acoustic Stimulation↗

Correlated evolution between hearing sensitivity and social calls in bats.

Echolocating bats are auditory specialists, with exquisite hearing that spans several octaves. In the ultrasonic range, bat audiograms typically show highest sensitivity in the spectral region of their species-specific echolocation calls. Well-developed hearing in the audible range has been commonly attributed to a need to detect sounds produced by prey. However, bat pups often emit isolation calls with low-frequency components that facilitate mother-young reunions. In this study, we examine whether low-frequency hearing in bats exhibits correlated evolution with (i) body size; (ii) high-frequency hearing sensitivity or (iii) pup isolation call frequency. Using published audiograms, we found that low-frequency hearing sensitivity is not dependent on body size but is related to high-frequency hearing. After controlling for high-frequency hearing, we found that low-frequency hearing exhibits correlated evolution with isolation call frequency. We infer that detection and discrimination of isolation calls have favoured enhanced low-frequency hearing because accurate parental investment is critical: bats have low reproductive rates, non-volant altricial young and must often identify their pups within large crèches.

Animals↗

Acoustic divergence in two cryptic Hipposideros species: a role for social selection?

We present evidence that a relatively widespread and common bat from South East Asia comprises two morphologically cryptic but acoustically divergent species. A population of the bicoloured leaf-nosed bat (Hipposideros bicolor) from Peninsular Malaysia exhibits a bimodal distribution of echolocation call frequencies, with peaks in the frequency of maximum energy at ca. 131 and 142 kHz. The two phonic types are genetically distinct, with a cytochrome b sequence divergence of just under 7%. We consider the mechanisms by which acoustic divergence in these species might arise. Differences in call frequency are not likely to effect resource partitioning by detectable prey size or functional range. However, ecological segregation may be achieved by differences in microhabitat use; the 131kHz H. bicolor is characterized by significantly longer forearms, lower wing loading, a lower aspect ratio and a more rounded wingtip, features that are associated with greater manoeuvrability in flight that may enable it to forage in more cluttered environments relative to the 142 kHz phonic type. We suggest that acoustic divergence in these species is a consequence of social selection for a clear communication channel, which is mediated by the close link between the acoustic signal and receptor systems imposed by the highly specialized nature of the hipposiderid and rhinolophid echolocation system.

Animals↗

Biosonar behaviour of free-ranging porpoises.

Detecting objects in their paths is a fundamental perceptional function of moving organisms. Potential risks and rewards, such as prey, predators, conspecifics or non-biological obstacles, must be detected so that an animal can modify its behaviour accordingly. However, to date few studies have considered how animals in the wild focus their attention. Dolphins and porpoises are known to actively use sonar or echolocation. A newly developed miniature data logger attached to a porpoise allows for individual recording of acoustical search efforts and inspection distance based on echolocation. In this study, we analysed the biosonar behaviour of eight free-ranging finless porpoises (Neophocaena phocaenoides) and demonstrated that these animals inspect the area ahead of them before swimming silently into it. The porpoises inspected distances up to 77 m, whereas their swimming distance without using sonar was less than 20 m. The inspection distance was long enough to ensure a wide safety margin before facing real risks or rewards. Once a potential prey item was detected, porpoises adjusted their inspection distance from the remote target throughout their approach.

Animals↗

Acoustic flow perception in cf-bats: extraction of parameters.

The narrow-band portions of the echolocation pulses seen in cf-bats are a hypothetical substrate for target localization. This localization could be based on estimates of echo envelope amplitude and carrier frequency together with their derivatives. Evaluation of these parameters is referred to as "acoustic flow" in loose analogy to optic flow. It is assessed whether the requirements for this task may be reconciled with known principles of auditory function. For the evaluation of a single echo, this seems to be the case: auditory filter shapes provide sufficient frequency resolution; at the same time envelopes are preserved well and some noise removal is achieved. Nevertheless, should bats not be endowed with additional capabilities for noise removal, analysis of acoustic flow would be limited to favorable signal-to-noise ratios. Multiple, temporally overlapping echoes are probable in any realistic echolocation scenario. In this case, additional auditory processing steps have to be postulated, which allow simultaneous estimation of multiple carrier frequencies and reduction of demodulation distortions.

Acoustics↗

Sound localization in a new-world frugivorous bat, Artibeus jamaicensis: acuity, use of binaural cues, and relationship to vision.

Passive sound-localization acuity and its relationship to vision were determined for the echolocating Jamaican fruit bat (Artibeus jamaicensis). A conditioned avoidance procedure was used in which the animals drank fruit juice from a spout in the presence of sounds from their right, but suppressed their behavior, breaking contact with the spout, whenever a sound came from their left, thereby avoiding a mild shock. The mean minimum audible angle for three bats for a 100-ms noise burst was 10 degrees-marginally superior to the 11.6 degrees threshold for Egyptian fruit bats and the 14 degrees threshold for big brown bats. Jamaican fruit bats were also able to localize both low- and high-frequency pure tones, indicating that they can use both binaural phase- and intensity-difference cues to locus. Indeed, their ability to use the binaural phase cue extends up to 6.3 kHz, the highest frequency so far for a mammal. The width of their field of best vision, defined anatomically as the width of the retinal area containing ganglion-cell densities at least 75% of maximum, is 34 degrees. This value is consistent with the previously established relationship between vision and hearing indicating that, even in echolocating bats, the primary function of passive sound localization is to direct the eyes to sound sources.

Animals↗

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.

Acoustics↗

Comparison of target detection capabilities of the beluga and bottlenose dolphin.

The echolocation detection capabilities of a beluga (Delphinapterus leucas) and an Atlantic bottlenose dolphin (Tursiops truncatus) were directly compared in a target detection experiment. Both animals were trained to detect targets in the presence of masking noise. Targets were stainless-steel, water-filled spheres 7.62 and 22.86 cm in diameter. Target ranges of 16.5 and 40 m were used with the 7.62-cm sphere and 80 m with the 22.86-cm sphere. Masking noise with a flat spectrum from 40-160 kHz was projected from a spherical transducer placed 4 or 5 m, depending on the target distance, from the animal hoop station in line with the target. Target detection performance was determined as a function of masking noise level at each target range. The echo-to-noise ratio (Ee/No)max for the beluga at the 75% correct response threshold was approximately 1.0 dB compared to about 10 dB for the dolphin. The differences of each animal's detection performance across the three ranges were consistent with target strength and transmission loss differences. It is speculated that the difference in performance between the two species may be due to differences in critical bandwidth, signal processing capability, or echolocation strategy.

Acoustic Stimulation↗

Ubiquity of hyperacuity.

A decision as to whether two line segments are colinear, as on a vernier scale (--/-- vs --/--), can be made with high sensitivity by the human visual system. Just-noticeable vernier displacement is much smaller than the separation required to resolve two parallel lines, i.e., to perceive them as two lines rather than one. Vernier acuity is thus also called "hyperacuity." Similar effects have been discovered in bat echolocation, for discrimination of a range-jittered point target from a nonjittered target, in the jamming avoidance response (JAR) of electric fish, and in differential pitch sensitivity experiments with human subjects. Are jitter sensitivity in echolocation, JAR in electroreception, differential pitch sensitivity in audition, and vernier acuity in vision based on the same general principle? The results in this article indicate that such phenomena are indeed similar from the viewpoint of detection theory, and that experimental performance can be used to behaviorally estimate auditory parameters such as bandwidth, beamwidth, and temporal resolution, as well as to test different signal processing models without resort to masking. Applications of the hyperacuity effect to radar, sonar, and medical ultrasound are suggested.

Animals↗

Acoustic image representation of a point target in the bat Eptesicus fuscus: evidence for sensitivity to echo phase in bat sonar.

Echolocating bats, Eptesicus fuscus, were trained in two distinct behavioral tasks to investigate the images they perceive of a sonar point target. In the first task, bats were trained in a two-alternative forced-choice procedure to detect electronically simulated target echoes at a range of approximately 57 cm. Half of the trials in the detection task contained echoes from a stationary target (simulated by a fixed echo delay) and half contained echoes from a jittering target (simulated by an echo delay alternating between two time values over successive sonar emissions). In the second task, bats were trained in a two-alternative forced-choice procedure to discriminate between electronically simulated stationary and jittering targets, centered about a range of 57 cm. Both target detection and target jitter discrimination performance were assessed as a function of jitter magnitude, with jitter values ranging from 0-60 microseconds (corresponding to a change in distance of 0 to 10.3 mm). In both detection and discrimination tasks, the bat's performance changed cyclically with the magnitude of echo jitter. Specifically, when the phase of the playback echoes was unchanged, performance levels were poorest at 0 and 30 microseconds, and when the phase of the echoes alternated by 180 deg from one to the next, performance levels were poorest at 15 and 40-50 microseconds. The results suggest that Eptesicus is sensitive to the phase reversal of echoes and thus have implications for assessing receiver models of echolocation.

Acoustic Stimulation↗

Analysis of acoustic elements and syntax in communication sounds emitted by mustached bats.

Mustached bats, Pteronotus parnellii parnellii spend most of their lives in the dark and use their auditory system for acoustic communication as well as echolocation. The sound spectrograms of their communication sounds or "calls" revealed that this species produces a rich variety of calls. These calls consist of one or more of the 33 different types of discrete sounds or "syllables" that are emitted singly and/or in combination. These syllables can be further classified as 19 simple syllables, 14 composites, and three subsyllables. Simple syllables consist of characteristic geometric patterns of CF (constant frequency), FM (frequency modulation), and NB (noise burst) sounds that are defined quantitatively using statistical criteria. Composites consist of simple syllables or subsyllables conjoined without any silent interval. Most syllable types exhibit a large intrinsic variation in their physical structure compared to the stereotypic echolocation pulses. Syllable domains are defined on the basis of multiple parameters, although these can be collapsed onto three dimensions that capture 99% of the measured variation among different types of syllables. Temporal analysis of multisyllabic constructs reveals several syntactical rules for syllable transitions.

Acoustics↗

Target range-sensitive neurons in the auditory cortex of the mustache bat.

Echolocating bats determine distance to targets by the time delay between their emitted biosonar pulses and the returning echoes. By varying the delay between synthetic pulses and echoes in stimulus pairs at various repetition rates and durations, neurons have been found in the auditory cortex of the mustache bat (Pteronotus parnellii rubiginosus) which are sensitive to target range during the search, approach, and terminal phases of prey capture or landing. Two classes of range-sensitive neurons were found: (i) tracking neurons, whose best delay for response to an echo following the emitted pulse becomes shorter and narrower as the bat closes in on the target, and (ii) range-tuned neurons, whose best delay is constant, and which respond to the target only when it is within a certain narrow fixed range. Range-tuned neurons are specialized for processing echoes only during a particular period of the search, approach, or terminal phases of echolocation, and they provide support for a theory of ranging in bats that incorporates groups of neurons with a spectrum of preferred echo delays to detect target distance.

Action Potentials↗