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PubMed2002

Microbat paraphyly and the convergent evolution of a key innovation in Old World rhinolophoid microbats.

Molecular phylogenies challenge the view that bats belong to the superordinal group Archonta, which also includes primates, tree shrews, and flying lemurs. Some molecular studies also challenge microbat monophyly and instead support an alliance between megabats and representative rhinolophoid microbats from the families Rhinolophidae (horseshoe bats, Old World leaf-nosed bats) and Megadermatidae (false vampire bats). Another molecular study ostensibly contradicts these results and supports traditional microbat monophyly, inclusive of representative rhinolophoids from the family Nycteridae (slit-faced bats). Resolution of the microbat paraphyly/monophyly issue is essential for reconstructing the temporal sequence and deployment of morphological character state changes associated with flight and echolocation in bats. If microbats are paraphyletic, then laryngeal echolocation either evolved more than once in different microbats or was lost in megabats after evolving in the ancestor of all living bats. To examine these issues, we used a 7.1-kb nuclear data set for nine outgroups and twenty bats, including representatives of all rhinolophoid families. Phylogenetic analyses and statistical tests rejected both Archonta and microbat monophyly. Instead, bats are in the superorder Laurasiatheria and microbats are paraphyletic. Further, the superfamily Rhinolophoidea is polyphyletic. The rhinolophoid families Rhinolophidae and Megadermatidae belong to the suborder Yinpterochiroptera along with rhinopomatids and megabats. The rhinolophoid family Nycteridae belongs to the suborder Yangochiroptera along with vespertilionoids, noctilionoids, and emballonuroids. These results resolve the apparent conflict between previous molecular studies that sampled different rhinolophoid families. An important implication of rhinolophoid polyphyly is independent evolution of key anatomical innovations associated with the nasal-emission of echolocation pulses.

Amino Acid Sequence↗
PubMed2006

Classification of communication signals of the little brown bat.

Little brown bats, Myotis lucifugus, are known for their ability to echolocate and utilize their echolocation system to navigate, and locate and identify prey. Their echolocation signals have been characterized in detail but their communication signals are less well understood despite their widespread use during social interactions. The goal of this study was to develop an automatic classification algorithm for characterizing the communication signals of little brown bats. Sound recordings were made overnight on five individual male bats (housed separately from a large group of captive bats) for 7 nights, using a bat detector and a digital recorder. The spectral and temporal characteristics of recorded sounds were first analyzed and classified by visual observation of a call's temporal pattern and spectral composition. Sounds were later classified using an automatic classification scheme based on multivariate statistical parameters in MATLAB. Human- and machine-based analysis revealed five discrete classes of bat's communication signals: downward frequency-modulated calls, steep frequency-modulated calls, constant frequency calls, broadband noise bursts, and broadband click trains.

Algorithms↗
PubMed2006

Neural mechanisms underlying selectivity for the rate and direction of frequency-modulated sweeps in the auditory cortex of the pallid bat.

Frequency-modulated (FM) sweeps are common in vocalizations, including human speech. Selectivity for FM sweep rate and direction is present in the auditory cortex of many species. The present study sought to determine the mechanisms underlying FM sweep selectivity in the auditory cortex of pallid bats. In the pallid bat inferior colliculus (IC), two mechanisms underlie selectivity for FM sweep rate. The first mechanism depends on duration tuning for tones that arises as a consequence of early inhibition generated by an excitatory tone. The second mechanism depends on a narrow band of delayed high-frequency inhibition. Direction selectivity depends on a broad band of early low-frequency inhibition. Here, the contributions of these mechanisms to cortical FM sweep selectivity were determined in pentobarbital-anesthetized pallid bats. We show that the majority of cortical neurons tuned to echolocation frequencies are selective for the downward direction and rate of FM sweeps. Unlike in IC neurons tuned in the echolocation range, duration tuning is rare in cortical neurons with similar tuning. As in the IC, consistent spectrotemporal differences exist between low- and high-frequency sidebands. A narrow band of delayed high-frequency inhibition is necessary for FM rate selectivity. Low-frequency inhibition has a broad bandwidth, early arrival time, and creates direction selectivity. Cortical neurons respond better to slower FM rates and exhibit broader rate tuning than IC neurons. Relative arrival time of high-frequency inhibition is slower in the cortex than in the IC. Thus whereas similar mechanisms shape direction selectivity of neurons tuned in the echolocation range in the IC and the cortex, only one of the two mechanisms underlying rate selectivity in the IC is present in the cortex.

Acoustic Stimulation↗
PubMed2002

A comparative analysis of brain size in relation to foraging ecology and phylogeny in the Chiroptera.

Variations in total brain mass and in the mass of three brain regions (main olfactory bulb, hippocampus, auditory nuclei) were examined using a data set for 63 species of bats (Chiroptera). Using both conventional and phylogenetically based analysis of covariance (log body mass as covariate), we tested several hypotheses that relate total brain mass or the size of the components to variation in foraging ecology, categorized as phytophagous, gleaner, and aerial insectivore. In some analyses, the category phytophagous was split into phytophagous pteropodid and phytophagous phyllostomid to examine differences between two distinct clades of bats. Because the Megachiroptera orient primarily by vision and olfaction, whereas all other bats rely on laryngeal echolocation to locate their prey, we hypothesized that the former would differ in size of the main olfactory bulb, as compared with all other bats. This hypothesis was supported by our analyses. Our more general prediction was that insectivorous bats, which rely heavily on echolocation for the pursuit and capture of their prey, would have larger auditory nuclei than do phytophagous species. This, too, was supported. We also compared phytophagous (fruit or nectar consuming) bats in two families, the Pteropodidae and the Phyllostomidae. We hypothesized that the phyllostomids, which use echolocation while foraging, would have larger auditory nuclei. Although statistical power is low in phylogenetically informed comparisons of the two clades, we did find weak evidence in support of this hypothesis. We conclude that bat brains show evidence of adaptation to foraging ecology.

Adaptation, Physiological↗
PubMed1996

The closed-loop nature of the tymbal response in the dogbane tiger moth, Cycnia tenera (Lepidoptera, Arctiidae).

The dogbane tiger moth, Cycnia tenera, emits ultrasonic sounds by rhythmically buckling a pair of tymbals when stimulated by pulsed sounds resembling bat echolocation. We monitored the central pattern generator governing this response by recording the motor output of the tymbal branch of the metathoracic leg nerve. The rhythm of the tymbal motor pattern can be altered midway (500 m/sec from its initiation) by changing the period and, to a lesser degree, the intensity of the stimulus. The tymbal response of C. tenera is therefore closed-looped to stimulus pulse period and intensity. Our results suggest that C. tenera relies less on the changes in an attacking bat's echolocation intensity when responding with this behaviour because this acoustic parameter may be a more unreliable indicator of the proximity of the bat than its echolocation call period.

Acoustic Stimulation↗
PubMed1992

The effect of pulse repetition rate on the delay sensitivity of neurons in the auditory cortex of the FM bat, Myotis lucifugus.

1. Echo delay is the primary cue used by echolocating bats to determine target range. During target-directed flight, the repetition rate of pulse emission increases systematically as range decreases. Thus, we examined the delay tuning of 120 neurons in the auditory cortex of the bat, Myotis lucifugus, as repetition rate was varied. 2. Delay sensitivity was exhibited in 77% of the neurons over different ranges of pulse repetition rates (PRRs). Delay tuning typically narrowed and eventually disappeared at higher PRRs. 3. Two major types of delay-sensitive neurons were found: i) delay-tuned neurons (59%) had a single fixed best delay, while ii) tracking neurons (22%) changed their best delay with PRR. 4. PRRs from 1-100/s were represented by the population of delay-sensitive neurons, with the majority of neurons delay-sensitive at PRRs of at least 10-20/s. Thus, delay-dependent neurons in Myotis are most active during the search phase of echolocation. 5. Delay-sensitive neurons that also responded to single sounds were common. At PRRs where delay sensitivity was found, the responses to single sounds were reduced and the responses to pulse-echo pairs at particular delays were greater than the single-sound responses. In facilitated neurons (53%), the maximal delay-dependent response was always larger than the best single-sound responses, whereas in enhanced neurons (47%), these responses were comparable. The presence of neurons that respond maximally to single sounds at one PRR and to pulse-echo pairs with particular echo delays at other PRRs suggests that these neurons perform echo-ranging in conjunction with other biosonar functions during target pursuit.

Acoustic Stimulation↗
PubMed1992

The influence of stimulus duration on the delay tuning of cortical neurons in the FM bat, Myotis lucifugus.

1. Echolocating bats use echo delay as the primary cue to determine target distance. During target-directed flight, the emitted pulses increase in repetition rate and shorten in duration as distance decreases. To determine how these parameters affect the delay tuning of neurons in the auditory cortex of the awake bat, Myotis lucifugus, we examined the responses of 104 delay-sensitive neurons as the pulse repetition rate (PRR) and duration were independently varied. Stimulus duration of 4, 2 and 1 ms and PRR of 5-100/s were used for both the pulse and echo to determine delay sensitivity. These parameter ranges span those used during the search, approach, and the initial terminal phases of echolocation. 2. As the stimulus duration was shortened, the range of PRRs for delay sensitivity was extended to higher rates in 41% of the neurons, narrowed or disappeared in 40%, and remained unchanged in 4%. The remaining 15% were not categorized since it was not possible to determine a trend in which the range of delay-sensitive PRRs changed with stimulus duration. 3. Three types of tracking neurons (i.e., neurons that change their best delay during target-directed flight) were found. For the first type, the best delay (BD) shortened with shorter stimulus duration, for the second type, BD shortened with both shorter stimulus durations and higher PRRs, and for the third type, BD shortened with higher PRRs. 4. These results suggest that the stimulus parameters of sonar emission influence delay tuning and hence processing by cortical neurons in FM bats.

Acoustic Stimulation↗
PubMed1993

Passive sound localization of prey by the pallid bat (Antrozous p. pallidus).

The pallid bat (Antrozous p. pallidus) uses passive sound localization to capture terrestrial prey. This study of captive pallid bats examined the roles of echolocation and passive sound localization in prey capture, and focused on their spectral requirements for accurate passive sound localization. Crickets were used as prey throughout these studies. All tests were conducted in dim, red light in an effort to preclude the use of vision. Hunting performance did not differ significantly in red light and total darkness, nor did it differ when visual contrast between the terrestrial prey and the substrate was varied, demonstrating that the bats did not use vision to locate prey. Our bats apparently used echolocation for general orientation, but not to locate prey. They did not increase their pulse emission rate prior to prey capture, suggesting that they were not actively scanning prey. Instead, they required prey-generated sounds for localization. The bats attended to the sound of walking crickets for localization, and also attacked small, inanimate objects dragged across the floor. Stationary and/or anesthetized crickets were ignored, as were crickets walking on substrates that greatly attenuated walking sounds. Cricket communication sounds were not used in prey localization; the bats never captured stationary, calling crickets. The accuracy of their passive sound localization was tested with an open-loop passive sound localization task that required them to land upon an anesthetized cricket tossed on the floor. The impact of a cricket produced a single 10-20 ms duration sound, yet with this information, the bats were able to land within 7.6 cm of the cricket from a maximum distance of 4.9 m. This performance suggests a sound localization accuracy of approximately +/- 1 degree in the horizontal and vertical dimensions of auditory space. The lower frequency limit for accurate sound localization was between 3-8 kHz. A physiological survey of frequency representation in the pallid bat inferior colliculus suggests that this lower frequency limit is around 5 kHz.

Animals↗
PubMed1996

The degradation of distance discrimination in big brown bats (Eptesicus fuscus) caused by different interference signals.

The ability of two big brown bats (Eptesicus fuscus) to discriminate the distance to an electronically synthesized "phantom" target by echolocation was tested in the presence of interfering signals presented slightly before the target echo. Interfering signals were chosen to have differing degrees of similarity to the typical echolocation emission used by the bat in this task (which was the signal used to create the phantom target), and we predicted that the degree of disruption of ranging would be proportional to the similarity of the interference to the target echo. This prediction was not confirmed; rather, all interference signals not identical to the target echo increased the threshold to about twice that found with no interference. When the interference was identical to the target echo, the threshold increased to about 4 times that with no interference. When each bat was presented with phantom target "echoes" appropriate for the other bat, its range discrimination threshold increased about ten fold, and in this case the degree of interference of different signals was related to their similarity to the target echo, not to their similarity to the bat's "normal" signal. We suggest that Eptesicus may suppress interference by a more sophisticated strategy than simple linear matched filtering.

Animals↗
PubMed1986

Response properties of FM-FM combination-sensitive neurons in the auditory cortex of the mustached bat.

For echolocation, the mustached bat, Pteronotus parnellii rubiginosus, emits orientation sounds (pulses) and listens to echoes. Each pulse is made up of 8 components, of which 4 are constant frequencies (Cf 1.4) and 4 are frequency-modulated (FM 1-4). Target-range information, conveyed by the time delay of the echo FM from the pulse FM, is processed in this species by specialized neurons in a part of the auditory cortex known as the FM-FM area. These cortical neurons are responsive to pulse-echo pairs at specific echo delays. The essential components in the sound pair include the pulse FM1 followed by an echo FMn (n = 2, 3 or 4). Downward sweeping FM1-FMn sounds that are similar to those the animal naturally hears during echolocation are the most effective in evoking facilitative responses. Most FM-FM neurons, however, still exhibit facilitative responses to stimulus pairs consisting of upward sweeping FM sounds and/or pure tones at frequencies found in FM sweeps. The magnitude of facilitation is altered by changes in echo rather than pulse amplitude. Neurons characterized by shorter best delays (or echoes from closer targets) do not require larger best echo amplitudes for facilitation.

Animals↗
PubMed2002

The effect of preceding sonar emission on temporal integration in the bat, Megaderma lyra.

The present study investigated whether and to which extent temporal integration in bats is influenced by echolocation behavior. One way to quantify temporal integration is to measure the detection threshold for a pair of short tone pips as a function of the temporal separation between the pips. To asses the effect of preceding sonar emission on temporal integration in the bat, Megaderma lyra, the detection thresholds of identical subjects were measured in a passive as well as in an active paradigm. In the passive paradigm, the presentation of the pip pairs was independent of the bats' sonar emissions; in the active paradigm, the presentation was triggered by the bats' sonar emissions. In both cases, the bats showed a very short integration time in the range of 100-200 micros. Moreover, the comparison of the active and passive results within each bat revealed no systematic differences in the two measuring paradigms. These results indicate that temporal integration is not influenced by echolocation. Simulations with a computer model of cochlear filtering based on measurements of M. lyra cochlear tuning suggest that the perceptual temporal integration is dominated by the integration of the cochlear filters.

Animals↗
PubMed2004

Auditory sensitivity and frequency selectivity in greater spear-nosed bats suggest specializations for acoustic communication.

We investigated the relationship between auditory sensitivity, frequency selectivity, and the vocal repertoire of greater spear-nosed bats ( Phyllostomus hastatus). P. hastatus commonly emit three types of vocalizations: group-specific foraging calls that range from 6 to 11 kHz, low amplitude echolocation calls that sweep from 80 to 40 kHz, and infant isolation calls from 15 to 100 kHz. To determine if hearing in P. hastatus is differentially sensitive or selective to frequencies in these calls, we determined absolute thresholds and masked thresholds using an operant conditioning procedure. Both absolute and masked thresholds were lowest at 15 kHz, which corresponds with the peak energy of isolation calls. Auditory and masked thresholds were higher at sound frequencies used for group-specific foraging calls and echolocation calls. Isolation calls meet the requirements of individual signatures and facilitate parent-offspring recognition. Many bat species produce isolation calls with peak energy between 10 and 25 kHz, which corresponds with the frequency region of highest sensitivity in those species for which audiogram data are available. These findings suggest that selection for accurate offspring recognition exerts a strong influence on the sensory system of P. hastatus and likely on other species of group-living bats.

Acoustic Stimulation↗
PubMed2006

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↗
PubMed2000

Consequences of outer hair cell damage for otoacoustic emissions and audio-vocal feedback in the mustached bat.

The cochlea of the mustached bat is adapted to process ultrasonic echolocation signals. To assess the involvement of active sound amplification by outer hair cells in high-frequency hearing and in audio-vocal interaction, selective hair cell damage was induced by the antibiotic Amikacin. Amikacin preferentially damaged the first row of outer hair cells in the basal cochlear turn. The cochlear regions coding for the second-harmonic constant-frequency component of the echolocation call (CF2) at 61 kHz and for frequencies between 75 and 100 kHz were the most affected. This was reflected in an increase of mechanical thresholds obtained by measuring distortion-product otoacoustic emissions. During initial periods of minor hair cell damage, when thresholds had deteriorated by less than 40 dB, a sharp, mechanical, cochlear resonance that is responsible for enhanced tuning to 61 kHz was still measurable as a stimulus-frequency otoacoustic emission and its frequency decreased by 350 Hz. The persistence of the resonance suggests that passive structures like the tectorial or basilar membrane are important for generation of the resonance. Behaviorally, the bats reacted to the change in cochlear micromechanics with a decrease of their CF2 frequency by 360 Hz. After larger hair cell damage, when the cochlear resonance had disappeared, the bats vocalized only sparsely and the CF2 frequency increased by up to 2 kHz, which may correspond to a state without audiovocal feedback. This indicates that audio-vocal feedback in the nondamaged animal works to lower the call frequency.

Animals↗
PubMed1985

Evoked acoustic emissions and cochlear microphonics in the mustache bat, Pteronotus parnellii.

In the echolocating bat, Pteronotus parnellii, otoacoustic responses at a frequency of 62 kHz are measurable in the external ear canal during continuous and after transient acoustic stimulation. These responses are interpreted to represent emissions from the cochlea. They can reach an amplitude as large as 70 dB SPL and occur in the frequency range most important for echolocation, namely on the average about 700 Hz above the constant frequency component of the orientation calls. A sharp maximum of the amplitude of cochlear microphonic potentials at about 62 kHz could be correlated with the emission frequency. In one bat an evoked otoacoustic response changed to a spontaneous otoacoustic emission. The frequency and amplitude of the evoked otoacoustic responses reversibly decreased after exposure for 1 min to continuous sounds of more than 85 dB SPL with frequencies of about 2.5-7.5 kHz above the emission frequency. Similar effects occurred during anaesthesia or cooling. A possible relation between the existence of otoacoustic emissions and morphological specializations of the cochlea is discussed.

Acoustic Impedance Tests↗
PubMed1988

Time is traded for intensity in the bat's auditory system.

Disparities in time and intensity are the two chief cues animals use for localizing a sound source in space. Echolocating bats belonging to the family Molossidae emit brief, ultrasonic signals for orientation that sweep downward about an octave over the duration of the pulse. Due to acoustic shadowing and the directional properties of the ears, pronounced interaural intensity disparities are created that vary as a function of azimuth. However, due to the small headwidth of these animals, azimuthal changes create small interaural time disparities that are at most 30 microseconds. The experiments in this report are concerned with the binaural processing of time and intensity disparities using brief FM signals that simulate the animal's natural echolocation calls. Binaural neurons receiving excitation from one ear and inhibition from the other (E-I neurons) were recorded from the inferior colliculus of Mexican free-tailed bats. The majority of units sampled were highly sensitive for temporal disparities of 100-300 microseconds, and a few had significant changes in discharge probability when interaural time was changed by 10-20 microseconds. However, all E-I neurons were also sensitive to intensity disparities. With only one exception, all E-I neurons traded time for intensity. On the average, each decibel difference in intensity could be compensated for by advancing or delaying the inhibitory sound by 47 microseconds. The main conclusion is that the auditory system processes interaural disparities by transforming level differences at the two ears into latency differences. Thus the discharge probability of each binaural neuron is determined largely by the arrival times of the discharges from the excitatory and inhibitory ears. In view of the substantial time-intensity trading ratios, the small interaural time disparities produced by azimuthal locations off the midline play no role in shaping the response properties of these neurons. Specific examples of how time-intensity trades can translate into a high spatial selectivity are presented.

Animals↗
PubMed2006

Directional hearing in a silicon cricket.

Phonotaxis is the ability to orient towards or away from sound sources. Crickets can locate conspecifics by phonotaxis to the calling (mating) song they produce, and can evade bats by negative phonotaxis from echolocation calls. The behaviour and underlying physiology have been studied in some depth, and the auditory system solves this complex problem in a unique manner. Experiments conducted on a simulation model of the system indicated that the mechanism output a directional signal to sounds ahead at calling song frequency and to sounds behind at echolocation frequencies. We suggest that this combination of responses helps simplify later processing in the cricket. To further explore this result, an analogue, very large scale integrated (aVLSI) circuit model of the mechanism was designed and built; results from testing this agreed with the simulation. The aVLSI circuit was used to test a further hypothesis about the potential advantages of the positioning of the acoustic inputs for sound localisation during walking. There was no clear advantage to the directionality of the system in their location. The aVLSI circuitry is now being extended to use on a robot along with previously modelled neural circuitry to better understand the complete sensorimotor pathway.

Animals↗
PubMed2002

The effect of sound duration on rate-amplitude functions of inferior collicular neurons in the big brown bat, Eptesicus fuscus.

During echolocation, the amplitude and duration of echo pulses of the big brown bat, Eptesicus fuscus, covary throughout the entire course of hunting. The purpose of this study was to examine if variation in sound duration might affect the amplitude selectivity of inferior collicular (IC) neurons of this bat species under free-field stimulation conditions. A family of rate-amplitude functions of each IC neuron was obtained with different sound durations. The effect of sound duration on the neuron's amplitude selectivity was then studied by examining the type, best amplitude, dynamic range and slope of each rate-amplitude function. The rate-amplitude functions of 83 IC neurons determined with different sound durations were either monotonic, saturated or non-monotonic. Neurons with monotonic rate-amplitude functions had the highest best amplitude, largest dynamic range but smallest slope. Neurons with non-monotonic rate-amplitude functions had the lowest best amplitude, smallest dynamic range but largest slope. The best amplitude, dynamic range and slope of neurons with saturated rate-amplitude functions were intermediate between these two types. Rate-amplitude functions of one group (47, 57%) of IC neurons changed from one type to another with sound duration and one-third of these neurons were tuned to sound duration. As a result, the best amplitude, dynamic range, and slope also varied with sound duration. However, rate-amplitude functions of the other group (36, 43%) of IC neurons were hardly affected by sound duration and two-thirds of these neurons were tuned to sound duration. Biological relevance of these findings in relation to bat echolocation is discussed.

Acoustic Stimulation↗