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PubMed1999

Facilitatory and inhibitory frequency tuning of combination-sensitive neurons in the primary auditory cortex of mustached bats.

Mustached bats, Pteronotus parnellii parnellii, emit echolocation pulses that consist of four harmonics with a fundamental consisting of a constant frequency (CF(1-4)) component followed by a short, frequency-modulated (FM(1-4)) component. During flight, the pulse fundamental frequency is systematically lowered by an amount proportional to the velocity of the bat relative to the background so that the Doppler-shifted echo CF(2) is maintained within a narrowband centered at approximately 61 kHz. In the primary auditory cortex, there is an expanded representation of 60.6- to 63. 0-kHz frequencies in the "Doppler-shifted CF processing" (DSCF) area where neurons show sharp, level-tolerant frequency tuning. More than 80% of DSCF neurons are facilitated by specific frequency combinations of approximately 25 kHz (BF(low)) and approximately 61 kHz (BF(high)). To examine the role of these neurons for fine frequency discrimination during echolocation, we measured the basic response parameters for facilitation to synthesized echolocation signals varied in frequency, intensity, and in their temporal structure. Excitatory response areas were determined by presenting single CF tones, facilitative curves were obtained by presenting paired CF tones. All neurons showing facilitation exhibit at least two facilitative response areas, one of broad spectral tuning to frequencies centered at BF(low) corresponding to a frequency in the lower half of the echolocation pulse FM(1) sweep and another of sharp tuning to frequencies centered at BF(high) corresponding to the CF(2) in the echo. Facilitative response areas for BF(high) are broadened by approximately 0.38 kHz at both the best amplitude and 50 dB above threshold response and show lower thresholds compared with the single-tone excitatory BF(high) response areas. An increase in the sensitivity of DSCF neurons would lead to target detection from farther away and/or for smaller targets than previously estimated on the basis of single-tone responses to BF(high). About 15% of DSCF neurons show oblique excitatory and facilitatory response areas at BF(high) so that the center frequency of the frequency-response function at any amplitude decreases with increasing stimulus amplitudes. DSCF neurons also have inhibitory response areas that either skirt or overlap both the excitatory and facilitatory response areas for BF(high) and sometimes for BF(low). Inhibition by a broad range of frequencies contributes to the observed sharpness of frequency tuning in these neurons. Recordings from orthogonal penetrations show that the best frequencies for facilitation as well as excitation do not change within a cortical column. There does not appear to be any systematic representation of facilitation ratios across the cortical surface of the DSCF area.

Animals↗
PubMed2001

Medial superior olive of the big brown bat: neuronal responses to pure tones, amplitude modulations, and pulse trains.

The structure and function of the medial superior olive (MSO) is highly variable among mammals. In species with large heads and low-frequency hearing, MSO is adapted for processing interaural time differences. In some species with small heads and high-frequency hearing, the MSO is greatly reduced in size; in others, including those echolocating bats that have been examined, the MSO is large. Moreover, the MSO of bats appears to have undergone different functional specializations depending on the type of echolocation call used. The echolocation call of the mustached bat contains a prominent CF component, and its MSO is predominantly monaural; the free-tailed bat uses pure frequency-modulated calls, and its MSO is predominantly binaural. To further explore the relation of call structure to MSO properties, we recorded extracellularly from 97 single neurons in the MSO of the big brown bat, Eptesicus fuscus, a species whose echolocation call is intermediate between that of the mustached bat and the free-tailed bat. The best frequencies of MSO neurons in the big brown bat ranged from 11 to 79 kHz, spanning most of the audible range. Half of the neurons were monaural, excited by sound at the contralateral ear, while the other half showed evidence of binaural interactions, supporting the idea that the binaural characteristics of MSO neurons in the big brown bat are midway between those of the mustached bat and the free-tailed bat. Within the population of binaural neurons, the majority were excited by sound at the contralateral ear and inhibited by sound at the ipsilateral ear; only 21% were excited by sound at either ear. Discharge patterns were characterized as transient ON (37%), primary-like (33%), or transient OFF (23%). When presented with sinusoidally amplitude modulated tones, most neurons had low-pass filter characteristics with cutoffs between 100 and 300 Hz modulation frequency. For comparison with the sinusoidally modulated sounds, we presented trains of tone pips in which the pulse duration and interstimulus interval were varied. The results of these experiments indicated that it is not the modulation frequency but rather the interstimulus interval that determines the low-pass filter characteristics of MSO neurons.

Acoustic Stimulation↗
PubMed2006

Tiger moth responses to a simulated bat attack: timing and duty cycle.

Many night-flying insects perform complex, aerobatic escape maneuvers when echolocating bats initiate attack. Tiger moths couple this kinematic defense with an acoustic reply to a bat's biosonar-guided assault. The jamming hypothesis for the function of these moth sounds assumes that tiger moth clicks presented at high densities, temporally locked to the terminal phase of the bat attack will produce the greatest jamming efficacy. Concomitantly, this hypothesis argues that moths warning bats of bad tasting chemicals sequestered in their tissues should call early to give the bat time to process the meaning of the warning signal and that moths calling at low duty cycles are more likely to employ such an aposematic strategy. We report here the first investigation of a tiger moth assemblage's response to playback of a bat echolocation attack sequence. This assemblage of arctiid moths first answered the echolocation attack sequence 960+/-547 ms (mean +/- s.d.) from the end of the bat attack. The assemblage reached a half-maximum response shortly after the first response, at 763+/-479 ms from the end of the terminal buzz. Tiger moth response reached a maximum at 475+/-344 ms from the end of the sequence; during the approach phase, well before the onset of the terminal buzz. In short, much of tiger moth response to bat attack occurs outside of the jamming hypotheses' predictions. Furthermore, no relationship exists between the duty cycle of a tiger moth's call (and thus the call's probability of jamming the bat) and its temporal response to bat attack. These data call into doubt the assumptions behind the jamming hypothesis as currently stated but do not directly test the functionality of arctiid sounds in disrupting echolocation in bat-moth aerial battles.

Animals↗
PubMed1993

The gleaning attacks of the northern long-eared bat, Myotis septentrionalis, are relatively inaudible to moths.

This study empirically tests the prediction that the echolocation calls of gleaning insectivorous bats (short duration, high frequency, low intensity) are acoustically mismatched to the ears of noctuid moths and are less detectable than those of aerially hawking bats. We recorded auditory receptor cell action potentials elicited in underwing moths (Catocala spp.) by echolocation calls emitted during gleaning attacks by Myotis septentrionalis (the northern long-eared bat) and during flights by the aerial hawker Myotis lucifugus (the little brown bat). The moth ear responds inconsistently and with fewer action potentials to the echolocation calls emitted by the gleaner, a situation that worsened when the moth's ear was covered by its wing (mimicking a moth resting on a surface). Calls emitted by the aerial-hawking bat elicited a significantly stronger spiking response from the moth ear. Moths with their ears covered by their wings maintained their relative hearing sensitivity at their best frequency range, the range used by most aerial insectivorous bats, but showed a pronounced deafness in the frequency range typically employed by gleaning bats. Our results (1) support the prediction that the echolocation calls of gleaners are acoustically inconspicuous to the ears of moths (and presumably other nocturnal tympanate insects), leaving the moths particularly vulnerable to predation, and (2) suggest that gleaners gain a foraging advantage against eared prey.

Acoustics↗
PubMed2002

Doppler-shift compensation behavior in horseshoe bats revisited: auditory feedback controls both a decrease and an increase in call frequency.

Among mammals, echolocation in bats illustrates the vital role of proper audio-vocal feedback control particularly well. Bats adjust the temporal, spectral and intensity parameters of their echolocation calls depending on the characteristics of the returning echo signal. The mechanism of audio-vocal integration in both mammals and birds is, however, still largely unknown. Here, we present behavioral evidence suggesting a novel audio-vocal control mechanism in echolocating horseshoe bats (Rhinolophus ferrumequinum). These bats compensate for even subtle frequency shifts in the echo caused by flight-induced Doppler effects by adjusting the frequency of their echolocation calls. Under natural conditions, when approaching background targets, the bats usually encounter only positive Doppler shifts. Hence, we commonly believed that, during this Doppler-shift compensation behavior, horseshoe bats use auditory feedback to compensate only for these increases in echo frequency (=positive shifts) by actively lowering their call frequency below the resting frequency (the call frequency emitted when not flying and not experiencing Doppler shifts). Re-investigation of the Doppler-shift compensation behavior, however, shows that decreasing echo frequencies (=negative shifts) are involved as well: auditory feedback from frequencies below the resting frequency, when presented at similar suprathreshold intensity levels as higher echo frequencies, cause the bat's call frequency to increase above the resting frequency. However, compensation for negative shifts is less complete than for positive shifts (22% versus 95%), probably because of biomechanical restrictions in the larynx of bats. Therefore, Doppler-shift compensation behavior involves a quite different neural substrate and audio-vocal control mechanism from those previously assumed. The behavioral results are no longer consistent with solely inhibitory feedback originating from frequencies above the resting frequency. Instead, we propose that auditory feedback follows an antagonistic push/pull principle, with inhibitory feedback lowering and excitatory feedback increasing call frequencies. While the behavioral significance of an active compensation for echo frequencies below RF remains unclear, these behavioral results are crucial for determining the neural implementation of audio-vocal feedback control in horseshoe bats and possibly in mammals in general.

Animals↗
PubMed2004

Acoustic identification of eight species of bat (mammalia: chiroptera) inhabiting forests of southern hokkaido, Japan: potential for conservation monitoring.

Assessing the impact of forest management on bat communities requires a reliable method for measuring patterns of habitat use by individual species. A measure of activity can be obtained by monitoring echolocation calls, but identification of species is not always straightforward. We assess the feasibility of using analysis of time-expanded echolocation calls to identify free-flying bats in the Tomakomai Experimental Forest of Hokkaido University, Hokkaido, northern Japan. Echolocation calls of eight bat species were recorded in one or more of three conditions: from hand-released individuals, from bats flying in a confined space and from bats emerging from their roost. Sonograms of 171 calls from 8 bat species were analyzed. These calls could be categorized into 3 types according to their structure: FM/CF/FM type (Rhinolophus ferrumequinum), FM types (Murina leucogaster, Murina ussuriensis, Myotis macrodactylus and Myotis ikonnikovi) and FM/QCF types (Eptesicus nilssonii, Vespertilio superans and Nyctalus aviator). Sonograms of the calls of R. ferrumequinum could easily be distinguished from those of all other species by eye. For the remaining calls, seven parameters (measures of frequency, duration and inter-call interval) were examined using discriminant function analysis, and 92% of calls were correctly classified to species. For each species, at least 80% of calls were correctly classified. We conclude that analysis of echolocation calls is a viable method for distinguishing between species of bats in the Tomakomai Experimental Forest, and that this approach could be applied to examine species differences in patterns of habitat-use within the forest.

Acoustics↗
PubMed1992

Frequency tuning properties of neurons in the inferior colliculus of an FM bat.

We examined frequency tuning characteristics of single neurons in the inferior colliculus of the echolocating bat, Eptesicus fuscus, in order to determine whether there are different classes of spectral selectivity at this level and to relate frequency tuning properties to the design of the echolocation signal. In unanesthetized but tranquilized animals, we recorded responses from 363 single units to pure tones, frequency-modulated (FM) sweeps, or broad-band noise. Most units were selective for stimulus type; 50% responded only to pure tones, 14% responded only to FM sweeps, and 5% responded only to noise. The remainder responded to two or more types of stimuli. Tuning curves could be classified as follows: 1) V-shaped tuning curves (57%) were the most common type; 2) closed tuning curves (20%) had thresholds at both low and high sound levels; 3) narrow filters (14%) had Q values above 20 at 10 dB and 30 dB above threshold or 10 dB and 40 dB above threshold; 4) frequency-opponent tuning (6%) was found in units with high spontaneous activity; within a center range of frequencies, firing rate increased above spontaneous level, but at higher or lower frequencies, firing rate decreased below spontaneous level; 5) double-tuned units (3%) had two best frequencies (BF). The most clear evidence of topographic distribution was seen for filter units, which were only found in the dorsal part of the 20-30 kHz isofrequency contour. Filter units were also the most clearly related to the echolocation signal of the bat. Their BFs were all within the range of the dominant frequency (approximately 20-30 kHz) that Eptesicus uses during the searching phase of echolocation.

Acoustic Stimulation↗
PubMed2000

Structure and function of the bat superior olivary complex.

The superior olivary complex (SOC) is a mammalian auditory brainstem structure that contains several nuclei. Some of them are part of the ascending system projecting to higher auditory centers, others belong to the descending system projecting to the cochlear nuclei or the cochlea itself. The main nuclei of the ascending system, the lateral and medial superior olive (LSO, MSO), as well as the lateral and medial nuclei of the trapezoid body (LNTB, MNTB), have been traditionally associated with sound localization. Here we review the results of recent studies on the main SOC nuclei in echolocating bats. These studies suggest that some SOC structures and functions are highly conserved across mammals (e.g., the LSO, which is associated with interaural intensity difference processing), while others are phylogenetically highly variable in both form and function (e.g., the MSO, traditionally associated with interaural time difference processing). For the MSO, these variations indicate that we should broaden our view regarding what functions the MSO might participate in, since its function in echolocation seems to lie in the context of pattern recognition rather than sound localization. Furthermore, across bat species, variations in the form and physiology of the MSO can be linked to specific behavioral adaptations associated with different echolocation strategies. Finally, the comparative approach, including auditory specialists such as bats, helps us to reach a more comprehensive view of the functional anatomy of auditory structures that are still poorly understood, like the nucleus of the central acoustic tract (NCAT).

Animals↗
PubMed1982

Cytoarchitecture of auditory system in lower brainstem of the mustache bat, Pteronotus parnellii.

To begin an investigation of the auditory pathways in the brainstem of the mustache bat, we examined the cytoarchitecture of the cochlear nuclei, superior olivary complex, nuclei of the lateral lemniscus, and inferior colliculus. Although all of these auditory centers are hypertrophied in this echolocating bat, only some areas have unusual cytoarchitectural features: 1) In the anterior part of the anteroventral cochlear nucleus we do not find the large spherical cells seen in other mammals; instead, very small spherical cells are found in this area. 2) In the posterior part of the anteroventral cochlear nucleus there is a region containing a homogeneous population of very large multipolar cells. 3) The medial superior olive is unusually large for an animal with a small head. 4) The most striking observations are seen in the lateral lemniscus. The ventral nucleus of the lateral lemniscus has a distinct columnar organization. The intermediate area of the lateral lemniscus contains a large and very distinct nucleus. Each of these cytoarchitectural features distinguishes the auditory system of this bat from that of other mammals. The results raise questions about whether or not there are unique subdivisions in the auditory pathways of echolocating bats. The results also identify these unusual nuclei as candidates to play a role in the special auditory functions related to echolocation.

Animals↗
PubMed1991

Auditory properties of the superior colliculus in the horseshoe bat, Rhinolophus rouxi.

Auditory response properties were studied in the superior colliculus (SC) of the echolocating horseshoe bat Rhinolophus rouxi, a long CF-FM bat, by the use of stationary, dichotic stimuli. The most striking finding in the horseshoe bat was an enormous overrepresentation of neurons with best frequencies in the range of the constant frequency component of the species specific echolocation call (72% of the auditory neurons). These neurons had response thresholds as low as 0 dB SPL and were narrowly tuned with Q10dB--values up to 400, just as in the nuclei of the primary auditory pathway in this species. This overrepresentation may suggest the importance of the superior colliculus in the context of echolocation behavior. While noise stimuli were not particularly effective, other auditory response properties were similar to those described in other mammals. 65% of the SC neurons in the horseshoe bat responded only to monaural stimulation of one ear, primarily the contralateral one. 32% of the neurons received monaural input from both ears. The proportion of neurons responsive to ipsilateral stimulation (41%) was rather high. Mean response latency was 8.9 ms for contralateral stimulation. A tonotopic organization is lacking, but high-frequency neurons are less frequent in rostral SC.

Acoustic Stimulation↗
PubMed2006

Vocal communication in adult greater horseshoe bats, Rhinolophus ferrumequinum.

Whereas echolocation in horseshoe bats is well studied, virtually nothing is known about characteristics and function of their communication calls. Therefore, the communication calls produced by a group of captive adult greater horseshoe bats were recorded during various social interactions in a free-flight facility. Analysis revealed that this species exhibited an amazingly rich repertoire of vocalizations varying in numerous spectro-temporal aspects. Calls were classified into 17 syllable types (ten simple syllables and seven composites). Syllables were combined into six types of simple phrases and four combination phrases. The majority of syllables had durations of more than 100 ms with multiple harmonics and fundamental frequencies usually above 20 kHz, although some of them were also audible to humans. Preliminary behavioral observations indicated that many calls were emitted during direct interaction with and in response to social calls from conspecifics without requiring physical contact. Some echolocation-like vocalizations also appeared to clearly serve a communication role. These results not only shed light upon a so far widely neglected aspect of horseshoe bat vocalizations, but also provide the basis for future studies on the neural control of the production of communicative vocalizations in contrast to the production of echolocation pulse sequences.

Age Factors↗
PubMed2006

Is duration tuning a transient process in the inferior colliculus of guinea pigs?

Duration selectivity appears to be a fundamental neural encoding mechanism found throughout the animal kingdom. Previous studies reported that band-pass duration-tuned neurons typically show offset responses and occupy a small portion of auditory neurons in non-echolocation mammals relative to echolocation bats. Therefore, duration tuning is generally weaker in non-echolocation mammals. In the present study, duration tuning was analyzed for 207 neurons recorded in the inferior colliculus (IC) of guinea pigs. Duration tuning was found to be stronger in the onset component of the responses from sustained, on-off and pause neurons than had been reported previously, when a short analysis window was applied. The need for an appropriate time window for duration tuning analysis was also supported by the fact that the on and off responses from an on-off neuron may show different duration tuning features. Therefore, duration tuning appears to be a transient neural coding process in the IC of guinea pigs. Duration tuning for these types of neurons may have been blurred by the use of a relatively unselective, long window.

Acoustic Stimulation↗
PubMed2004

Directionality of hearing in two CF/FM bats, Pteronotus parnellii and Rhinolophus rouxi.

The head-related transfer function (HRTF) has been measured in two CF/FM bats, Pteronotus parnellii and Rhinolophus rouxi from 575 positions in the frontal hemisphere. P. parnellii showed an increase of the elevation angle of the axis of highest pinna gain with increasing frequency followed by a specific decrease at 75 kHz. Such a drop of elevation angle of the acoustic axis was not seen in R. rouxi. The HRTF further showed a spectral notch dependent on elevation and frequency in P. parnellii, but not in R. rouxi. The functional implications of this difference between both bat species are discussed. Frequencies at maximum pinna gain values did not clearly match the frequencies of the harmonics of the echolocation calls whereas spatial resolution of interaural intensity differences was best in a frequency range that included the higher harmonics of the echolocation calls in both bat species. However, specializations of HRTF patterns matching the exact frequencies of the harmonics of the echolocation calls could not be observed in both bat species.

Acoustic Stimulation↗
PubMed2005

Acoustical dead zones and the spatial aggregation of whale strandings.

Cetacean strandings display a marked geographical clustering. We propose a simple, two-dimensional ray-dynamics model of cetacean echolocation to examine the role played by coastline topography in influencing the location and clustering of stranding sites. We find that a number of coastlines known to attract cetacean strandings produce acoustical "Dead Zones" where echolocation signals are severely distorted by purely geometric effects. Using available cetacean stranding data bases from four disparate areas, we show that the geographical clusters in the observations correlate strongly with the regions of distorted echolocation signals as predicted by the model.

Acoustics↗
PubMed2003

Hearing in American leaf-nosed bats. III: Artibeus jamaicensis.

We determined the audiogram of the Jamaican fruit-eating bat (Phyllostomidae: Artibeus jamaicensis), a relatively large (40-50 g) species that, like other phyllostomids, uses low-intensity echolocation calls. A conditioned suppression/avoidance procedure with a fruit juice reward was used for testing. At 60 dB SPL the hearing range of A. jamaicensis extends from 2.8 to 131 kHz, with an average best sensitivity of 8.5 dB SPL at 16 kHz. Although their echolocation calls are low-intensity, the absolute sensitivity of A. jamaicensis and other 'whispering' bats does not differ from that of other mammals, including other bats. The high-frequency hearing of A. jamaicensis and other Microchiroptera is slightly higher than expected on the basis of selective pressure for passive sound localization. Analysis suggests that the evolution of echolocation may have been accompanied by the extension of their high-frequency hearing by an average of one-half octave. With respect to low-frequency hearing, all bats tested so far belong to the group of mammals with poor low-frequency hearing, i.e., those unable to hear below 500 Hz.

Animals↗
PubMed2003

Sound-evoked efferent effects on cochlear mechanics of the mustached bat.

The influence of the crossed medial efferent system on cochlear mechanics of the mustached bat was tested by measuring delayed evoked otoacoustic emissions (DEOAEs), cochlear microphonics, distortion product otoacoustic emissions (DPOAEs) and stimulus frequency otoacoustic emissions. Contralaterally delivered sinusoids, broadband noise and bat echolocation calls were used for acoustic stimulation of the efferent system. With all four measures we found a level-dependent suppression under stimulation with both broadband noise and echolocation calls. In addition, the sharply tuned cochlear resonance of the mustached bat which is involved in processing echolocation signals at 61 kHz shifted upward in frequency by several 100 Hz. Presentation of sinusoids did not have any significant effect. DEOAEs and DPOAEs were in some cases enhanced during contralateral presentation of the bat calls at moderate intensities. The most important function of the efferent system in the mustached bat might be the control of the extraordinarily fine-tuned resonator of this species, which is close to instability as evident from the very pronounced evoked otoacoustic emissions which sometimes convert into spontaneous otoacoustic emissions of high level.

Acoustic Stimulation↗
PubMed1999

Sound duration selectivity in the pallid bat inferior colliculus.

Neurons selective for sound duration have been reported in the auditory midbrain and cortex of several specialized vertebrate species that process behaviorally relevant signals of stereotypic duration. This study examines duration selectivity in the inferior colliculus (IC) of the pallid bat to determine if this selectivity is limited to regions that serve echolocation, or if it extends to low-frequency regions that serve passive listening. It also focuses on the temporal response properties of duration-selective neurons to elucidate mechanisms that may underlie the creation of this selectivity. Of 140 neurons tested, 36% were selective for short durations of </=7 ms, and acted as short-pass or bandpass duration filters. Sixteen percent, termed long duration neurons, differed in that they required minimum sound durations of 5-50 ms before responding, and all acted as long-pass duration filters. Short duration neurons were equally common in the high-frequency region serving echolocation and the lateral low-frequency region that serves passive listening, indicating that selectivity for short duration sounds was not associated only with the specialized function of echolocation. Long duration neurons were most common in the medial low-frequency region IC. Selectivity for short and long duration sounds was therefore not uniformly distributed across the IC. Analyses of the temporal response properties of short duration neurons, and the application of bicuculline to block gamma-aminobutyric acid-A receptors, were used to infer the synaptic interactions that underlie the creation of duration selectivity, the role of inhibition in its creation, and whether a coincidence mechanism proposed by Casseday et al. (Science 264 (1994) 847-850) is consistent with the behavior of the duration-selective neurons recorded in the pallid bat IC. Present results suggest that while some neurons do behave in a manner that is consistent with the coincidence mechanism, the behaviors of others suggest that more than one mechanism may create a selectivity for short duration sounds.

Animals↗
PubMed1996

Object representation in the bottlenose dolphin (Tursiops truncatus): integration of visual and echoic information.

A dolphin performed a 3-alternative matching-to-sample task in different modality conditions (visual/echoic, both vision and echolocation: visual, vision only; echoic, echolocation only). In Experiment 1, training occurred in the dual-modality (visual/echoic) condition. Choice accuracy in tests of all conditions was above chance without further training. In Experiment 2, unfamiliar objects with complementary similarity relations in vision and echolocation were presented in single-modality conditions until accuracy was about 70%. When tested in the visual/echoic condition, accuracy immediately rose (95%), suggesting integration across modalities. In Experiment 3, conditions varied between presentation of sample and alternatives. The dolphin successfully matched familiar objects in the cross-modal conditions. These data suggest that the dolphin has an object-based representational system.

Animals↗