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Hearing in American leaf-nosed bats. II: Carollia perspicillata.

We determined the audiograms of two short-tailed fruit bats (Carollia perspicillata), 18-g phyllostomids from Central and South America. For testing, we used a conditioned suppression/avoidance procedure with a fruit juice reward. At an intensity of 60 dB SPL, the hearing of C. perspicillata extends from 5.2 to 150 kHz, showing a best sensitivity of 0 dB at 25 kHz and a secondary region of sensitivity at 71 kHz. Although C. perspicillata is frugivorous and therefore does not rely on sonar for detecting and pursuing insects, its audiogram is similar to that of insectivorous bats; similarly, there is no suggestion of unusual sensitivity associated with its low-intensity echolocation calls. The behavioral audiogram is compared to previously published physiological estimates of hearing.

Animals↗

Temporal integration in the echolocating bat, Megaderma lyra.

Temporal integration is a crucial feature of auditory temporal processing. We measured the psychophysical temporal integration of acoustic intensity in the echolocating bat Megaderma lyra using a two-alternative forced-choice procedure. A measuring paradigm was chosen in which the absolute threshold for pairs of short tone pips was determined as a function of the temporal separation between the pips. The time constants determined with this paradigm are a crucial characteristic of the sonar system of M. lyra, a species orientating in its environment by very short broadband sonar calls emitted at high rates. Two different carrier frequencies for the tone pips were used to obtain data from the lower and the higher half of the hearing area of M. lyra. Both in the lower and in the higher frequency range, M. lyra showed very short time constants of about 220 microseconds. Our results are comparable to data from the echolocating dolphin, Tursiops truncatus, showing click integration times of about 260 microseconds and to estimates of auditory temporal integration in the context of echo clutter interference in the big brown bat.

Acoustic Stimulation↗

Tonic efferent-induced cochlear damping in roosting and echolocating mustached bats.

The activity of the medial olivocochlear (MOC) efferent system in mustached bats, Pteronotus p. parnellii, was studied by monitoring changes in the mechanical properties of the cochlea. The changing properties were expressed by the decay time (DT) of cochlear microphonic potentials produced by transient-induced ringing (Henson et al., 1995). Tape-recorded roost noise (biosonar and communication sounds) produced sudden, marked decreases in DT when presented to the contralateral ear of animals adapted to the quiet. When the animals were first removed from their roosts the DT was relatively short (1.2-1.5 ms) but this gradually lengthened by about 0.5-1.0 ms as they rested in a quiet chamber. The time required to reach a stable, quiet-adapted state after noise exposure varied with SPL and exposure time; in many experiments recovery was in the range of 90-120 min. When quiet-adapted bats were isolated and allowed to fly and echolocate for 20 min, the DTs measured within a few minutes after the end of the flight were also short and only slowly returned to longer preflight values. The administration of a single dose of gentamicin, which blocks MOC effects, greatly reduced the amount of suppression (damping) observed after periods of noise and echolocation sound exposure. We conclude that tonic MOC activity is induced by the natural vocalizations and roost noise and this activity probably regulates and protects the highly resonant cochlear partition.

Adaptation, Physiological↗

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↗

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↗

Tonotopic representation and space map in the non-primary auditory cortex of the mustached bat.

As auditory system has no sensory epithelium into which auditory space are projected, we studied the physiological map of the auditory space in the non-primary auditory cortex of the mustached bat by using the echo of their orientation sound. Ten bats were used as experimental subjects. Tungsten wire electrodes were inserted obliquely in the dorsomedial (DM) and ventroposterior (VP) areas of the non-primary auditory cortex. When single neuron was isolated, best frequency (BF), best azymuth (BAZ) and best elevation (BEL) were measured and were plotted on a schematic figure. To mimic its biosonar, one loudspeaker, delivering synthesized orientation sounds, was placed in front of the animal, and another loudspeaker delivering synthesized echo was mounted on a movable hoop. Tonotopic representation was observed but complicated in both areas, and those areas could be divided into several subdivisions consisting of the neuron groups characterized by three frequency bands. The neurons were thought to be related to the processing of biosonar informations from the facts that their BFs agreed with the scope of the FM sweep of each echo harmonics. The magnitude of the response showed rapid increase at their BAZ or BEL, so that the neurons seemed to tune to a certain direction in the auditory space. Especially in the DM area, neurons assumed a systematic arrangement of their BAZs on the cerebral surface and showed some tendency of a systematic arrangement of their BELs. The DM area was thought to have a kind of neural map of the auditory space.

Acoustic Stimulation↗

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↗

Small and neutral Tc(v)O BAT, bisaminoethanethiol (N2S2) complexes for developing new brain imaging agents.

Bisaminoethanethiol (BAT) ligands with various gem-dimethyl and amide groups were prepared, and the corresponding neutral Tc-99m complexes were prepared and evaluated for their relative stabilities by ligand-exchange reactions. It was demonstrated that technetium complexes containing gem-dimethyl substituents have higher lipophilicities, whereas those with an amide group possess greater stability, which enhances ligand-exchange reaction. The most interesting observation was that the brain uptake in rats is not determined only by lipophilicity. Apparently, Tc-99m complexes with an amide functional group display lower brain uptakes in rats compared to those without an amide group. The brain uptake was strongly influenced by substituents on the BAT ligand. These factors are critically important and should be taken into consideration when designing Tc-99m-labeled agents for CNS receptor imaging.

Animals↗

Seasonal biochemical plasticity of a flight muscle in a bat, Murina leucogaster.

Cellular and biochemical responses of the pectoral muscle to variation in seasonal activity were studied in the bat, Murina leucogaster ognevi. We collected bats in mid-hibernation (February), end-hibernation (April), and mid-summer (August) to track major activity periods in their annual cycle. Our findings indicated that myofiber cross-sectional area decreased to 68% between mid- and end-hibernation, but returned to the winter level in mid-summer. Total soluble protein and total RNA concentrations were not altered over these sampling periods. Oxidative potential gauged by citrate synthase activity increased 1.47-fold from mid- to end-hibernation and then remained at the similar level in mid-summer. Glycolytic potential gauged by lactate dehydrogenase activity changed little between mid- and end-hibernation but increased 1.42-fold in summer, compared with the winter level. Thus, the myofibers underwent disuse atrophy during hibernation, while enzymatic catalytic function recovered towards the level of mid-summer.

Adenosine Triphosphatases↗

A novel approach for collecting samples from fruit bats for isolation of infectious agents.

During the outbreak of Nipah virus encephalitis involving pigs and humans in peninsular Malaysia in 1998/1999, a conventional approach was initially undertaken to collect specimens from fruit bats by mist-netting and shooting, as an integral part of wildlife surveillance of the natural reservoir host of Nipah virus. This study describes a novel method of collecting fruit bats' urine samples using plastic sheets for isolation of Nipah virus. This novel approach resulted in the isolation of several other known and unidentified infectious agents besides Nipah virus.

Animals↗

Discrimination between dog-related and vampire bat-related rabies viruses in Brazil by strain-specific reverse transcriptase-polymerase chain reaction and restriction fragment length polymorphism analysis.

BACKGROUND: There is a geographical overlap between the two main rabies epidemiological cycles maintained by dogs and vampire bats in Latin America. The geographical and temporal coincidence of rabies outbreaks of respective origins is not unusual in rural areas of Latin America. These circumstances make it difficult to discriminate the intraspecies and interspecies transmission pathways of rabies. OBJECTIVE: This study was conducted to develop techniques to discriminate dog-related and vampire bat-related rabies virus isolates (DRRV and VRRV, respectively) in Brazil. STUDY DESIGN: The 1396 nucleotides of the nucleoprotein gene of a total of 27 DRRV and VRRV were sequenced. Strain-specific (SS) primers were developed based on these sequences. Forty-nine rabies virus strains isolated from animals and humans in several parts of Brazil were examined by reverse transcriptase-polymerase chain reaction (RT-PCR) with SS primers. These rabies viruses were also amplified by RT-PCR with general rabies primers and the PCR products were cut by three restriction enzymes, Blp I, Bsu36 I and BspE I. RESULTS: All the DRRV and VRRV were distinguished by RT-PCR with SS primers. The PCR products obtained from DRRV were cut at one site by Blp I, but not by Bsu36 I. The PCR products obtained from VRRV were cut at one or two sites by Bsu36 I, but not by Blp I. Blp I and Bsu36 I clearly discriminated DRRV and VRRV in restriction fragment length polymorphysim (RFLP) assays. The results of SS RT-PCR and RFLP were consistent. CONCLUSION: SS RT-PCR and RFLP assays have been developed for determining the origins of rabies virus isolates in Brazil. These assays are simple and rapid, and will be useful for identifying the rabies virus reservoirs of field isolates in Brazil, especially when used together.

Amino Acid Sequence↗

Potential use of chemical cues for colony-mate recognition in the big brown bat, Eptesicus fuscus.

Bats should benefit from recognition of their roost-mates when colonies form stable social units that persist over time. We used Y-maze experiments and gas chromatography-olfactometry (GC-O) to evaluate whether female big brown bats Eptesicus fuscus (Chiroptera: Vespertilionidae) use chemical cues to distinguish among conspecifics. In dual-choice Y-maze experiments, females chose the scent of another female from their own roost over a conspecific female from a different roost in a majority of trials. Analysis of total body odors using GC-O suggests that individuals from a given colony may share a more common odor signature with roost-mates than with non-roost-mate conspecifics. Using four principle components derived from 15 odor variables, discriminant function analysis correctly assigned most individuals to the correct colony.

Animal Communication↗

A possible neuronal basis for representation of acoustic scenes in auditory cortex of the big brown bat.

Behavioural studies and field observations demonstrate that echolocating bats simultaneously perceive range, direction and shape of multiple objects in the environment as acoustic images derived from echoes. Cortical echo delay-tuned neurons contribute to the perception of object range, because focal inactivation of these neurons disrupts behavioural discrimination of range. We report here that response properties of delay-tuned neurons in the cortical tonotopic area of the bat, Eptesicus, transform the sequential arrival times of echoes with different delays into a concurrent, accumulating neural representation of multiple objects at different ranges. The sharpness of delay tuning systematically increases at each best delay in a subpopulation of these neurons while responses to echoes at different delays are accumulated. The resulting concurrent, multiresolution representation of echo delay corresponds to neural implementation of a common representation of images used in computational vision and may provide the basis for representing acoustic images of multiple objects as acoustic 'scenes'.

Acoustic Stimulation↗

Strong population substructure is correlated with morphology and ecology in a migratory bat.

Examining patterns of inter-population genetic diversity can provide valuable information about both historical and current evolutionary processes affecting a species. Population genetic studies of flying and migratory species such as bats and birds have traditionally shown minimal population substructure, characterized by high levels of gene flow between populations. In general, strongly substructured mammalian populations either are separated by non-traversable barriers or belong to terrestrial species with low dispersal abilities. Species with female philopatry (the tendency to remain in or consistently return to the natal territory) might show strong substructure when examined with maternally inherited mitochondrial DNA, but this substructure generally disappears when biparentally inherited markers are used, owing to male-mediated gene flow. Male-biased dispersal is considered typical for mammals, and philopatry in both sexes is rare. Here we show strong population substructure in a migratory bat species, and philopatry in both sexes, as indicated by concordance of nuclear and mtDNA findings. Furthermore, the genetic structure correlates with local biomes and differentiation in wing morphology. There is therefore a close correlation of genetic and morphological differentiation in sympatric subspecific populations of this mammalian species.

Animals↗

Ultraviolet vision in a bat.

Most mammals, with the exception of primates, have dichromatic vision and correspondingly limited colour perception. Ultraviolet vision was discovered in mammals only a decade ago, and in the few rodents and marsupials where it has been found, ultraviolet light is detected by an independent photoreceptor. Bats orient primarily by echolocation, but they also use vision. Here we show that a phyllostomid flower bat, Glossophaga soricina, is colour-blind but sensitive to ultraviolet light down to a wavelength of 310 nm. Behavioural experiments revealed a spectral-sensitivity function with maxima at 510 nm (green) and above 365 nm (ultraviolet). A test for colour vision was negative. Chromatic adaptation had the same threshold-elevating effects on ultraviolet and visible test lights, indicating that the same photoreceptor is responsible for both response peaks (ultraviolet and green). Thus, excitation of the beta-band of the visual pigment is the most likely cause of ultraviolet sensitivity. This is a mechanism for ultraviolet vision that has not previously been demonstrated in intact mammalian visual systems.

Adaptation, Physiological↗

Echolocation signals reflect niche differentiation in five sympatric congeneric bat species.

Echolocating bats can be divided into guilds according to their preferred habitat and foraging behaviour, which coincide with distinct adaptations in wing morphology and structure of echolocation signals. Although coarse structuring of niche space between different guilds is generally accepted, it is not clear how niches differ within guilds, or whether there is fine-grained niche differentiation reflected in echolocation signal structure. Using a standardized performance test, here we show clutter-dependent differences in prey-capture success for bats from five species of European Myotis. These species are morphologically similar, sympatric, and all belong to the guild labelled "edge space aerial/trawling foragers". We further demonstrate a strong correlation between the prey-detection ability of the species and the respective search-call bandwidth. Our findings indicate that differences in echolocation signals contribute to within-guild niche differentiation. This is the first study relating sensory abilities of a set of potentially competing animal species to a direct measure of their respective foraging performance, suggesting an important role of sensory ecology in the structuring of animal communities.

Acoustics↗

The role of swarming sites for maintaining gene flow in the brown long-eared bat (Plecotus auritus).

Bat-swarming sites where thousands of individuals meet in late summer were recently proposed as 'hot spots' for gene flow among populations. If, due to female philopatry, nursery colonies are genetically differentiated, and if males and females of different colonies meet at swarming sites, then we would expect lower differentiation of maternally inherited genetic markers among swarming sites and higher genetic diversity within. To test these predictions, we compared genetic variance from three swarming sites to 14 nursery colonies. We analysed biparentally (five nuclear and one sex-linked microsatellite loci) and maternally (mitochondrial D-loop, 550 bp) inherited molecular markers. Three mtDNA D-loop haplolineages that were strictly separated at nursery colonies were mixed at swarming sites. As predicted by the 'extra colony-mating hypothesis', genetic variance among swarming sites (V(ST)) for the D-loop drastically decreased compared to the nursery population genetic variance (V(PT)) (31 and 60%, respectively), and genetic diversity increased at swarming sites. Relatedness was significant at nursery colonies but not at swarming sites, and colony relatedness of juveniles to females was positive but not so to males. This suggests a breakdown of colony borders at swarming sites. Although there is behavioural and physiological evidence for sexual interaction at swarming sites, this does not explain why mating continues throughout the winter. We therefore propose that autumn roaming bats meet at swarming sites across colonies to start mating and, in addition, to renew information about suitable hibernacula.

Animals↗