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Echo delay versus spectral cues for temporal hyperacuity in the big brown bat, Eptesicus fuscus.

Big brown bats can discriminate between echoes that alternate in delay (jitter) by as little as 10-15 ns and echoes that are stationary in delay. This delay hyperacuity seems so extreme that it has been rejected in favor of an explanation in terms of artifacts in echoes, most likely spectral in nature, that presumably are correlated with delay. Using different combinations of digital, analog, and cable delays, we dissociated the overall delay of jittering echoes from the size of the analog component of delay, which alone is presumed to determine the strength of the apparatus artifact. The bats' performance remains invariant with respect to the overall delay of the jittering echoes, not with respect to the amount of analog delay. This result is not consistent with the possible use of delay-related artifacts produced by the analog delay devices. Moreover, both electronic and acoustic measurements disclose no spectral cues or impedance-mismatch reflections in delayed signals, just time-delays. The absence of artifacts from the apparatus and the failure of overlap and interference from reverberation to account for the 10-ns result means that closing the gap between the level of temporal accuracy plausibly explained from physiology and the level observed in behavior may require a better understanding of the physiology.

Acoustic Stimulation↗

FM signals produce robust paradoxical latency shifts in the bat's inferior colliculus.

Previous studies in echolocating bats, Myotis lucifugus, showed that paradoxical latency shift (PLS) is essential for neural computation of target range and that a number of neurons in the inferior colliculus (IC) exhibit unit-specific PLS (characterized by longer first-spike latency at higher sound levels) in response to tone pulses at the unit's best frequency. The present study investigated whether or not frequency-modulated (FM) pulses that mimic the bat's echolocation sonar signals were equally effective in eliciting PLS. For two-thirds of PLS neurons in the IC, both FM and tone pulses could elicit PLS, but only FM pulses consistently produced unit-specific PLS. For the remainder of PLS neurons, only FM pulses effectively elicited PLS; these cells showed either no PLS or no response, to tone pulses. PLS neurons generally showed more pronounced PLS in response to narrow-band FM (each sweeping 20 kHz in 2 ms) pulse that contained the unit's best frequency. In addition, almost all PLS neurons showed duration-independent PLS to FM pulses, but the same units exhibited duration-dependent PLS to tone pulses. Taken together, when compared to tone pulses, FM stimuli can provide more reliable estimates of target range.

Acoustic Stimulation↗

The effect of sound intensity on duration-tuning characteristics of bat inferior collicular neurons.

Previous studies have shown that inferior collicular neurons of the big brown bat, Eptesicus fuscus, serve as short-, band-, long- and all-pass filters for sound durations. Neurons with band-, short- and long-pass filtering characteristics discharged maximally to a specific sound duration or a range of sound durations. In contrast, neurons with all-pass filtering characteristics do not have duration selectivity. To determine if duration-tuning characteristics of collicular neurons were tolerant to changes in sound intensity, we examined the duration-tuning characteristics of collicular neurons using a wide range of sound intensities. Duration-tuning characteristics examined included the type, bandwidth and slope of duration-tuning curves. Sound intensity delivered within 20 dB of minimum threshold did not affect duration-tuning characteristics of all collicular neurons studied. Sound intensities at still higher levels did not affect the tuning characteristics of two-thirds of collicular neurons but decreased the duration selectivity and changed the duration-tuning curves of the remaining one-third of neurons from one type to another. However, these two groups of duration-tuning collicular neurons were not separately organized inside the inferior colliculus. The biological relevance of these findings to bat echolocation is discussed.

Acoustic Stimulation↗

The inferior colliculus of the mustached bat has the frequency-vs-latency coordinates.

In the mustached bat, the central auditory system contains FM-FM (delay-tuned) neurons which are specialized for processing target-distance information carried by echo delays. Mechanisms for creating the FM-FM neurons involve delay lines, coincidence detection and amplification. A neural basis for delay lines can be a map representing response latencies. The aim of the present study is to explore whether the central nucleus of the inferior colliculus has a latency axis incorporated into iso-best frequency slabs. Responses of single or multiple neurons were recorded from the inferior colliculus of unanesthetized mustached bats with tungsten-wire electrodes, and their response latencies were measured with tone bursts at their best frequencies and best amplitudes or 65 dB SPL. In the dorsoventral electrode penetrations across the inferior colliculus, response latency systematically shortens from approximately 12 to approximately 4 ms. Tonotopic representation in the inferior colliculus is somewhat complex. Iso-best frequency slabs are tilted and/or curved, but they orient more or less ventrodorsally. Nevertheless, the latency axis is evident in each iso-best frequency slab, regardless of best frequency. The inferior colliculus has the frequency-vs-latency coordinates.

Acoustic Stimulation↗

Bat sonar: an alternative interpretation of the 10-ns jitter result.

In 1990 Simmons et al. reported evidence of a time resolution hitherto unknown in any animal, namely a 10-ns jitter detection threshold in echolocating bats. This result is discussed. The calibration data from the original papers are examined. Observations indicating other cues than delay being presented to the bats are given. We offer an alternative explanation for the psychometric jitter function, based on the assumption of a subtle distortion due to impedance mismatch in the delay-producing apparatus. We also report that effects of impedance mismatch are detectable by a human subject in a model experiment.

Acoustic Stimulation↗

Bicuculline application affects discharge pattern and pulse-duration tuning characteristics of bat inferior collicular neurons.

This study examines the contribution of GABAergic inhibition to the discharge pattern and pulse duration tuning characteristics of 101 bat inferior collicular neurons by means of bicuculline application to their recording sites. When stimulated with single pulses 56 (55%) neurons discharged 1 or 2 impulses (phasic responders), 42 (42%) discharged 3-10 impulses (phasic bursters) and 3 (3%) discharged impulses throughout the stimulus duration (tonic responders). Bicuculline application increased the number of impulses and changed the discharge patterns of 66 neurons. Using 50% difference between maximal and minimal responses as a criterion, the duration tuning characteristics of these neurons can be described as band-pass (20, 20%), long-pass (17, 17%), short-pass (33, 32%), and all-pass (31, 31%). Each band-pass neuron discharged maximally to a specific duration (the best duration) which was at least 50% larger than the neuron's responses to a long-duration pulse and a short-duration pulse. In contrast, each long- or short-pass neuron discharged maximally to a range of long or short duration pulses. Bicuculline application changed the duration tuning characteristics of 65 neurons. Possible mechanisms underlying duration tuning characteristics and the behavioral relevance to bat echolocation are discussed.

Acoustic Stimulation↗

Evolutionary adaptations of cochlear function in Jamaican mormoopid bats.

Mormoopid bat species have their echolocation system adapted to different hunting strategies. To study the corresponding mechanical properties of their inner ear, we measured distortion-product otoacoustic emissions to assess cochlear sensitivity and tuning. Mormoops blainvillii, Pteronotus macleayii and P. quadridens use frequency-modulated echolocation signals, sometimes preceded by a short narrowband signal component. Their distortion-product otoacoustic emission-threshold curves are most sensitive between 30 and 50 kHz and show no adaptation to the narrowband echolocation components. In contrast, the constant-frequency bat P. parnellii always uses long constant-frequency call components. Its inner ear is maximally sensitive at 62 kHz, the echo-frequency of the dominant constant-frequency component, and pronounced insensitivities at 61 and 93 kHz (CF2 and CF3 call frequency) are the major evolutionary change in comparison to its relatives. Furthermore, in P. parnellii, the optimum cochlear frequency separation is minimal at 62 and 93 kHz, associated with enhanced cochlear tuning, while for the other mormoopids there is no indication of enhanced tuning. The phylogeny of mormoopids, assessed by mitochondrial DNA analysis, shows a close relationship between the Pteronotus species. This suggests that major cochlear redesign, associated with the acquisition of echolocation-call specific cochlear processing in P. parnellii, has occurred within a relatively short evolutionary time scale.

Acoustic Stimulation↗

Frequency discrimination of brief tonal steps as a function of frequency in the lesser bulldog bat.

In a two-alternative, forced-choice task lesser bulldog bats were trained to distinguish between a pure tone pulse and a pulse composed of a series of brief tonal steps oscillating between two different frequencies. The tone-step pulse gradually approximates the pure tone pulse as the frequency difference between the steps becomes progressively smaller. Frequency difference limens for the brief tonal frequency steps were determined for a broad range of ultrasonic frequencies. The variation in tone-step difference limens with frequency appears to be correlated to the frequency structure of the bat's short-constant-frequency/frequency-modulated echolocation sound. There was a marked decline in the value of the relative frequency difference limens (Weber ratio) over a fairly narrow range of frequencies above the constant frequency and a sharp increase in threshold above this range. The relative thresholds for frequency discrimination were small and uniform over the frequency range of the frequency-modulated sweep and increased for frequencies below the frequency-modulated sweep. Thus, the most accurate frequency-discrimination abilities occur over a narrow frequency range around the frequency of the constant-frequency component of returning echoes. Frequency discrimination over the range of frequencies of the frequency-modulated component is relatively good.

Acoustic Stimulation↗

Neural inhibition sharpens auditory spatial selectivity of bat inferior collicular neurons.

This study examines the role of neural inhibition in auditory spatial selectivity of inferior collicular neurons of the big brown bat, Eptesicus fuscus, using a two-tone inhibition paradigm. Two-tone inhibition decreases auditory spatial response areas but increases the slopes of directional sensitivity curves of inferior collicular neurons. Inferior collicular neurons have either directionally-selective or hemifield directional sensitivity curves. A directionally-selective curve always has a peak which is at least 50% larger than the minimum. A hemifield directional sensitivity curve rises from an ipsilateral angle by more than 50% and either reaches a plateau or declines by less than 50% over a range of contralateral angles. Two-tone inhibition does not change directionally-selective curves but changes most hemifield directional sensitivity curves into directionally-selective curves. Auditory spatial selectivity determined both with and without two-tone inhibition increases with increasing best-excitatory frequency. Sharpening of auditory spatial selectivity by two-tone inhibition is larger for neurons with smaller differences between excitatory and inhibitory best frequencies. The effect of two-tone inhibition on auditory spatial selectivity increases with increasing inhibitory tone intensity but decreases with increasing intertone interval. The implications of these findings in bat echolocation are discussed.

Animals↗

Temporally patterned sound pulse trains affect intensity and frequency sensitivity of inferior collicular neurons of the big brown bat, Eptesicus fuscus.

This study examined the effect of temporally patterned pulse trains on intensity and frequency sensitivity of inferior collicular neurons of the big brown bat, Eptesicus fuscus. Intensity sensitivity of inferior collicular neurons was expressed by the dynamic range and slope of rate-intensity functions. Inferior collicular neurons with non-monotonic rate-intensity functions have smaller dynamic ranges and larger slopes than neurons with monotonic or saturated rate-intensity functions. Intensity sensitivity of all inferior collicular neurons improved by increasing the number of non-monotonic rate-intensity functions when the pulse repetition rate of pulse trains increased from 10 to 30 pulses per second. Intensity sensitivity of 43% inferior collicular neurons further improved when the pulse repetition rate of pulse trains increased still from 30 to 90 pulses per second. Frequency sensitivity of inferior collicular neurons was expressed by the Q10, Q20, and Q30 values of threshold frequency tuning curves and bandwidths of isointensity frequency tuning curves. Threshold frequency tuning curves of all inferior collicular neurons were V-shape and mirror-images of their counterpart isointensity frequency tuning curves. The Q10, Q20, and Q30 values of threshold frequency tuning curves of all inferior collicular neurons progressively increased and bandwidths of isointensity frequency tuning curves decreased with increasing pulse repetition rate in temporally patterned pulse trains. Biological relevance of these findings to bat echolocation is discussed.

Animals↗

Facultative hypothermia as a thermoregulatory strategy in the phyllostomid bats, Carollia perspicillata and Sturnira lilium.

The present study questions whether hypothermia is an artifact due to captivity-induced stress or a thermoregulatory strategy for bats of the neotropical family Phyllostomidae. In Guanacaste, Costa Rica, Carollia perspicillata and Sturnira lilium exhibited a bimodal distribution of body temperatures when submitted to an ambient temperature of 21 degrees C. Body temperature was highly correlated with body mass in both species. C. perspicillata of mass > or = 20 g and S. lilium of mass > or = 17 g remained normothermic (body temperature > 37 degrees C), whereas at masses below 18 g and 13 g, respectively, > 80% of individuals were hypothermic (body temperature < or 32 degrees C). In two treatment groups for each species, we restricted food intake to ca. 20% of body mass on either night 1 or night 4 following capture. Hypothermia was significantly related to food-restriction, but not time in captivity. Metabolic rate (ml O2. g-1 h-1) at ambient temperature = 21 degrees C was MR = e(-2.11 + 0.101 Tb) (r2 = 0.7, P < 0.001) for C. perspicillata and MR = e(-2.62 + 0.115 Tb) (r2 = 0.89) for S. lilium. Free-ranging, radio tagged C. perspicillata exhibited daily depression of body temperature to 33-34 degrees C. We conclude that hypothermia is an thermoregulatory strategy that allows phyllostomid bats to adjust metabolic rate to feeding success and the level of fat stores.

Adaptation, Physiological↗

Functional organization of the dorsal cochlear nucleus of the horseshoe bat (Rhinolophus rouxi) studied by GABA and glycine immunocytochemistry and electron microscopy.

Unique among mammals, the dorsal cochlear nucleus (DCN) of horseshoe bats consists of two functionally and anatomically distinct subdivisions: a laminated ventral portion that processes the frequency range below the constant frequency (CF) component of the echolocation signal and a nonlaminated dorsal portion that is specialized for processing the CF-signal range (76 kHz and higher). Using conventional transmission electron microscopy and postembedding immunocytochemistry for the inhibitory neurotransmitters GABA and glycine on semithin-alternating sections, we present further evidence that the ventral laminated subdivision of DCN conserves the main elements of microcircuitry and GABA/glycine labeling patterns typical for the mammalian DCN: (i) the main cell types and synaptic inventory of the granule cell/cartwheel cell system of the superficial layers are present as well as (ii) the tuberculoventral cell system of the deep layers. The nonlaminated dorsal subdivision lacks the granule cell/cartwheel cell system and is composed of a mixture of fusiform projection neurons with tuberculoventral cell analogues. Thus the inhibitory tuberculoventral system known to play an important role in temporal and spectral processing in VCN is conserved throughout the DCN of horseshoe bats, whereas functional components of cerebellar-like circuits are reduced in a specialized region that processes the dominant biosonar component.

Animals↗

Neuroarchitecture of the auditory cortex in the rufous horseshoe bat (Rhinolophus rouxi).

This study describes the location and anatomical subdivisions of the auditory cortex of the horseshoe bat, Rhinolophus rouxi. The basic cyto- and myeloarchitectural features and cytochrome oxidase reactivity patterns are evaluated in brains where auditory fields have been previously established neurophysiologically (Radtke-Schuller and Schuller 1995). Thus, the neuroanatomical findings from these brains and additional analyzed material are related to neurophysiological characteristics. The neocortex of Rhinolophus shows a typical mammalian six-layered organization. It is poorly laminated, has a low density of granular elements, a wide layer I, and a phylogenetically old pyramidal cell type in a sharply accentuated layer II. These features are generally considered 'primitive' or conservative. Frontal, parietal, temporal and occipital regions can be distinguished. In the temporal cortex, layers III and IV are found to be markedly thicker than layer V, in contrast to the parietal region, where a prominent layer V, containing a high concentration of large pyramidal cells is the most outstanding feature. The entire temporal region, most of the parietal and parts of the occipital region are responsive to auditory stimuli. The primary auditory field corresponds to most of the temporal region. The fields of the parietal region almost completely coincide with the dorsal fields of the auditory cortex. Border zones between the temporal, parietal, and occipital regions correspond to the posterior auditory field. The non-primary fields of the auditory cortex occupy a larger area of the bat's neocortex than the primary field. The accentuated neuroarchitectural features, like cortical thickness and staining intensity, are shown to coincide with the physiological representation of biologically significant parameters.

Animals↗

Seed dispersal by wind, birds, and bats between Philippine montane rainforest and successional vegetation.

In the moist Neotropics, vertebrate frugivores have a much greater role in the dispersal of forest and successional woody plants than wind, and bats rather than birds play the dominant role in dispersing early successional species. I investigated whether these patterns also occurred in a Philippine montane rainforest and adjacent successional vegetation. I also asked whether seed mass was related to probability of dispersal between habitats. A greater number of woody species and stems in the forest produced vertebrate-dispersed seeds than wind-dispersed seeds. Although input of forest seeds into the successional area was dominated by vertebrate-dispersed seeds in terms of species richness, wind-dispersed seeds landed in densities 15 times higher. Frugivorous birds dispersed more forest seeds and species into the successional area than bats, and more successional seeds and species into the forest. As expected, seed input declined with distance from source habitat. Low input of forest seeds into the successional area at the farthest distance sampled, 40 m from forest edge, particularly for vertebrate-dispersed seeds, suggests very limited dispersal out of forest even into a habitat in which woody successional vegetation provides perches and fruit resources. For species of vertebrate-dispersed successional seeds, probability of dispersal into forest declined significantly with seed mass.

Altitude↗

Pulau virus; a new member of the Nelson Bay orthoreovirus species isolated from fruit bats in Malaysia.

After the outbreak of Nipah virus (NiV) in 1998-99, which resulted in 105 human deaths and the culling of more than one million pigs, a search was initiated for the natural host reservoir of NiV on Tioman Island off the east coast of Malaysia. Three different syncytia-forming viruses were isolated from fruit bats on the island. They were Nipah virus, Tioman virus (a novel paramyxovirus related to Menangle virus), and a reovirus, named Pulau virus (PuV), which is the subject of this study. PuV displayed the typical ultra structural morphology of a reovirus and was neutralised by serum against Nelson Bay reovirus (NBV), a reovirus isolated from a fruit bat (Pteropus poliocephalus) in Australia over 30 years ago. PuV was fusogenic and formed large syncytia in Vero cells. Comparison of dsRNA segments between PuV and NBV showed distinct mobility differences for the S1 and S2 segments. Complete sequence analysis of all four S segments revealed a close relationship between PuV and NBV, with nucleotide sequence identity varying from 88% for S3 segment to 56% for the S1 segment. Similarly phylogenetic analysis of deduced protein sequences confirmed that PuV is closely related to NBV. In this paper we discuss the similarities and differences between PuV and NBV which support the classification of PuV as a novel mammalian, fusogenic reovirus within the Nelson Bay orthoreovirus species, in the genus Orthoreovirus, family Reoviridae.

Animals↗

Genetic divergence and phylogeography in the genus Nyctalus (Mammalia, Chiroptera): implications for population history of the insular bat Nyctalus azoreum.

We used three mitochondrial DNA fragments with different substitution rates (ND1, Cyt b and the CR) to infer phylogenetic relationships among six species of the genus Nyctalus, and compare levels of genetic divergence between the insular, vulnerable Nyctalus azoreum and its continental counterpart to assess the origins of the Azorean bat. The larger species found throughout the Palaearctic region (N. lasiopterus, N. aviator and N. noctula) share a unique chromosome formula (2n=42) and form a monophyletic clade in our reconstructions. Nyctalus plancyi (=velutinus), a Chinese taxon with 2n=36 chromosomes, is sometimes included in N. noctula, but is genetically very divergent from the latter and deserves full species status. All Cyt b and CR haplotypes of N. azoreum are closely related and only found in the Azores archipelago, but when compared to continental sequences of N. leisleri, levels of mtDNA divergence are unusually low for mammalian species. This contrasts with the high level of differentiation that N. azoreum has attained in its morphology, ecology, and echolocation calls, suggesting a recent split followed by fast evolutionary change. The molecular data suggest that N. azoreum originated from a European population of N. leisleri, and that the colonisation of the Azores occurred at the end of the Pleistocene. The Madeiran populations of N. leisleri also appear to have a European origin, whereas those of the Canary Islands probably came from North Africa. In spite of its recent origin and low genetic divergence, the Azorean bat is well differentiated and consequently represents a unique evolutionary unit with great conservation value.

Animals↗

The myoglobin of the fruit-bat (Rousettus aegyptiacus).

The myoglobin of the fruit-bat (Rousettus aegyptiacus) has been investigated. It has 153 amino acid residues. When the possible therian ancestral myoglobin is taken into consideration, the myoglobin of the fruit-bat resembles most closely that of the hedgehog.

Amino Acid Sequence↗

Neurons in the cerebellum of echolocating bats respond to acoustic signals.

Single neurons responding to auditory stimuli (40 msec duration, 0.5 msec rise-decay time) could be isolated from rather large areas of the cerebellar vermis and hemispheres of an echolocating bat, Eptesicus fuscus. These neurons had latencies between 4 and 13 msec and best frequencies between 22 and 77 kHz. The Q10-dB values of their tuning curves were between 1.4 and 16.6. When acoustic stimuli were delivered though the earphones, tuning curves measured from each ear alone were nearly identical in shape and best frequency. The minimum thresholds of these neurons were between 12 and 65 dB SPL. Apparently, these are suitable for reception of the bat's echolocating signals.

Acoustic Stimulation↗