Neural coding of echo-envelope disparities in echolocating bats

The effective use of echolocation requires not only measuring the delay between the emitted call and returning echo to estimate the distance of an ensonified object. To locate an object in azimuth and elevation, the bat’s auditory system must analyze the returning echoes in terms of their binaural properties, i.e., the echoes’ interaural intensity and time differences (IIDs and ITDs). The effectiveness of IIDs for echolocation is undisputed, but when bats ensonify complex objects, the temporal structure of echoes may facilitate the analysis of the echo envelope in terms of envelope ITDs. Using extracellular recordings from the auditory midbrain of the bat, Phyllostomus discolor, we found a population of neurons that are sensitive to envelope ITDs of echoes of their sonar calls. Moreover, the envelope-ITD sensitivity improved with increasing temporal fluctuations in the echo envelopes, a sonar parameter related to the spatial statistics of complex natural reflectors like vegetation. The data show that in bats envelope ITDs may be used not only to locate external, prey-generated rustling sounds but also in the context of echolocation. Specifically, the temporal fluctuations in the echo envelope, which are created when the sonar emission is reflected from a complex natural target, support ITD-mediated echolocation.     

Little Brown Bats (Myotis lucifugus) Recognize Individual Identity of Conspecifics Using Sonar Calls

Bats use sonar calls to locate prey and orient in their environment but they may also be used by conspecifics to obtain information about a caller. Statistical analysis of sonar calls provides evidence that variation carries social information about a caller, including individual identity. We hypothesized that little brown bats (Myotis lucifugus) would be able to recognize individuals given the potential fitness benefits of doing so. We performed playback trials using a habituation‐discrimination design to determine whether little brown bats are able to recognize the individual identity of a caller based on variation in their sonar calls. Each subject bat was played the calls of bat A until they habituated (defined as a 50% decrease from the beginning call rate), then the calls of bat B or a new call sequence of bat A (a control, referred to as bat A’) were played. Each subject received a unique pair of playback recordings (bat A and B) from adult female bats from the same colony (but a different colony from the subject) and the order of trials was randomized. The response measures were habituation time (s) and call rate (calls/s). Within a trial, subjects habituated to calls of bat A and transferred this habituation to the bat A’ sequence. In addition, they increased their call rates when played calls of bat B. Comparing between trials, subjects increased their call rate to the calls of bat B to a greater relative extent than to the calls of bat A’. These results provide the first evidence that bats recognize individual identity of conspecifics (as opposed to discrimination of groups), which has implications for the social interactions of bats.     

Role of broadcast harmonics in echo delay perception by big brown bats

Big brown bats (Eptesicus fuscus) emit frequency-modulated (FM) echolocation sounds containing two principal down-sweeping harmonics (FM₁ ~ 55–25 kHz, FM₂ ~ 105–50 kHz). To determine whether each harmonic contributes to perception of echo delay, bats were trained to discriminate between “split-harmonic” echoes that differed in delay. The bat’s broadcasts were picked up with microphones, and FM₁ and FM₂ were separated with highpass and lowpass filters at about 55 kHz, where they overlap in frequency. Both harmonics then were delivered from loudspeakers as positive stimuli in a 2-choice delay discrimination procedure with FM₁ delayed 3.16 ms and FM₂ delayed 3.46 ms (300 μs delay split). Negative stimuli contained FM₁ and FM₂ with the same filtering but no delay separation. These were presented at different overall delays from 11 down to 3 ms to measure the bat’s delay discrimination acuity for each harmonic in the split harmonic echoes. The bats determined the delays of both FM₁ and FM₂, but performance was overlaid by a broad pedestal of poor performance that extended for 800 μs. Splitting the harmonics by 300 μs appears to defocus the bat’s representation of delay, revealing the existence of a process for recognizing the normally simultaneous occurrence of the harmonics.     

Size Constancy in Bat Biosonar? Perceptual Interaction of Object Aperture and Distance

Perception and encoding of object size is an important feature of sensory systems. In the visual system object size is encoded by the visual angle (visual aperture) on the retina, but the aperture depends on the distance of the object. As object distance is not unambiguously encoded in the visual system, higher computational mechanisms are needed. This phenomenon is termed “size constancy”. It is assumed to reflect an automatic re-scaling of visual aperture with perceived object distance. Recently, it was found that in echolocating bats, the ‘sonar aperture’, i.e., the range of angles from which sound is reflected from an object back to the bat, is unambiguously perceived and neurally encoded. Moreover, it is well known that object distance is accurately perceived and explicitly encoded in bat sonar. Here, we addressed size constancy in bat biosonar, recruiting virtual-object techniques. Bats of the species Phyllostomus discolor learned to discriminate two simple virtual objects that only differed in sonar aperture. Upon successful discrimination, test trials were randomly interspersed using virtual objects that differed in both aperture and distance. It was tested whether the bats spontaneously assigned absolute width information to these objects by combining distance and aperture. The results showed that while the isolated perceptual cues encoding object width, aperture, and distance were all perceptually well resolved by the bats, the animals did not assign absolute width information to the test objects. This lack of sonar size constancy may result from the bats relying on different modalities to extract size information at different distances. Alternatively, it is conceivable that familiarity with a behaviorally relevant, conspicuous object is required for sonar size constancy, as it has been argued for visual size constancy. Based on the current data, it appears that size constancy is not necessarily an essential feature of sonar perception in bats.     

Discrimination of insect wingbeat-frequencies by the batRhinolophus ferrumequinum

Summary Five Greater Horseshoe bats,Rhinolophus ferrumequinum, were trained in a two-alternative forced-choice procedure to discriminate between artificial echoes of insects fluttering at different wingbeat rates. The stimuli were electronically produced phantom targets simulating fluttering insects with various wingbeat frequencies (Figs. 3, 4). Difference thresholds for wingbeat rates of 50 Hz and 100 Hz were determined. For an S+ of 50 Hz the difference threshold values lay between 2.8 and 4.6 Hz for individual bats; with an S+ of 100 Hz they increased to between 9.8 and 12.0 Hz (Figs. 5, 6, Table 1).Three bats, previously trained to discriminate between a S+ of 50 Hz and a S– with a lower wingbeat rate, were tested with higher frequency stimuli. When they had to decide between their old S+ of 50 Hz and either a 60 or 70 Hz echo two bats continued to select the 50 Hz stimulus while the third bat now preferred the faster fluttering insects (Table 2).During the discrimination task the echolocation behavior of the bats was monitored. When the phantom targets were presented all bats increased their duty-cycle of sound emission from about 40% to sometimes near 70%. They did so by either emitting longer echolocation calls or by increasing the sound repetition rate (Figs. 7, 8).The results show that Greater Horseshoe bats can determine the wingbeat rate of flying insects with an accuracy between 6 and 12%. Possible cues for flutter rate determination by cf-fm bats from natural and artificial insect echoes are discussed.Abbreviations DC duty-cycle - PD pulse duration - PI pulse interval - cf constantfrequency - fm frequency modulation     

Click-based echolocation in bats: not so primitive after all

Echolocating bats of the genus Rousettus produce click sonar signals, using their tongue (lingual echolocation). These signals are often considered rudimentary and are believed to enable only crude performance. However, the main argument supporting this belief, namely the click’s reported long duration, was recently shown to be an artifact. In fact, the sonar clicks of Rousettus bats are extremely short, ~50–100 μs, similar to dolphin vocalizations. Here, we present a comparison between the sonar systems of the ‘model species’ of laryngeal echolocation, the big brown bat (Eptesicus fuscus), and that of lingual echolocation, the Egyptian fruit bat (Rousettus aegyptiacus). We show experimentally that in tasks, such as accurate landing or detection of medium-sized objects, click-based echolocation enables performance similar to laryngeal echolocators. Further, we describe a sophisticated behavioral strategy for biosonar beam steering in clicking bats. Finally, theoretical analyses of the signal design—focusing on their autocorrelations and wideband ambiguity functions—predict that in some aspects, such as target ranging and Doppler-tolerance, click-based echolocation might outperform laryngeal echolocation. Therefore, we suggest that click-based echolocation in bats should be regarded as a viable echolocation strategy, which is in fact similar to the biosonar used by most echolocating animals, including whales and dolphins.     

Modelling simultaneous echo waveform reconstruction and localization in bats

Echolocating bats perceive the world through sound signals reflecting from the objects around them. In these signals, information is contained about reflector location and reflector identity. Bats are able to extract and separate the cues for location from those that carry identification information. We propose a model based on Wiener deconvolution that also performs this separation for a virtual system mimicking the echolocation system of the lesser spearnosed bat, Phyllostomus discolor. In particular, the model simultaneously reconstructs the reflected echo signal and localizes the reflector from which the echo originates. The proposed technique is based on a model that performs a similar task based on information from the frog’s lateral line system. We show that direct application of the frog model to the bat sonar system is not feasible. However, we suggest a technique that does apply to the bat biosonar and indicate its performance in the presence of noise.     

Roost selection and roost switching of female Bechstein’s bats (<Emphasis Type="Italic">Myotis bechsteinii</Emphasis>) as a strategy of parasite avoidance

Ectoparasites of vertebrates often spend part of their life cycle in their hosts’ home. Consequently, hosts should take into account the parasite infestation of a site when selecting where to live. In a field study, we investigated whether colonial female Bechstein’s bats (Myotis bechsteinii) adapt their roosting behaviour to the life cycle of the bat fly Basilia nana in order to decrease their contact with infective stages of this parasite. B. nana imagoes live permanently on the bat’s body but deposit puparia in the bat’s roosts. The flies metamorphose independently in the roosts, but after metamorphosis emerge only in the presence of a potential host. In a field experiment, the bats preferred non-contagious to contagious day-roosts and hence were able to detect either the parasite load of roosts or some correlate with infestation, such as bat droppings. In addition, 9 years of observational data on the natural roosting behaviour of female Bechstein’s bats indicate that the bats largely avoid re-occupying roosts when highly contagious puparia are likely to be present as a result of previous occupations of the roosts by the bat colony. Our results indicate that the females adapted their roosting behaviour to the age-dependent contagiousness (emergence probability) of the puparia. However, some infested roosts were re-occupied, which we assume was because these roosts provided advantages to the bats (e.g. a beneficial microclimate) that outweighed the negative effects associated with bat fly infestation. We suggest that roost selection in Bechstein’s bats is the outcome of a trade-off between the costs of parasite infestation and beneficial roost qualities.     

Spatial unmasking in the echolocating Big Brown Bat, <Emphasis Type="Italic">Eptesicus fuscus</Emphasis>

Masking affects the ability of echolocating bats to detect a target in the presence of clutter targets. It can be reduced by spatially separating the targets. Spatial unmasking was measured in a two-alternative-forced-choice detection experiment with four Big Brown Bats detecting a wire at 1 m distance. Depth dependent spatial unmasking was investigated by the bats detecting a wire with a diameter of 1.2 mm in front of a masker with a threshold distance of 11 cm behind the wire. For angle dependent spatial unmasking the masker was turned laterally, starting from its threshold position at 11 cm. With increasing masker angles the bats could detect thinner wires with diameters decreasing from 1.2 mm (target strength −36.8 dB) at 0° to 0.2 mm (target strength −63.0 dB) at 22°. Without masker, the bats detected wire diameters of 0.16 mm (target strength −66.2 dB), reached with masker positions beyond 23° (complete masking release). Analysis of the sonar signals indicated strategies in the echolocation behavior. The bats enhanced the second harmonics of their signals. This may improve the spatial separation between wire and masker due to frequency-dependent directionality increase of sound emission and echo reception.     

Frequency tracking and Doppler shift compensation in response to an artificial CF/FM echolocation sound in the CF/FM bat,Noctilio albiventris

Summary Bats of the speciesNoctilio albiventris emit short-constant frequency/frequency modulated (short-CF/FM) pulses with a CF component frequency at about 75 kHz. Bats sitting on a stationary platform were trained to discriminate target distance by means of echolocation. Loud, free-running artificial pulses, simulating the bat's natural CF/FM echolocation sounds or with systematic modifications in the frequency of the sounds, were presented to the bats during the discrimination trials. When the CF component of the artificial CF/FM sound was between 72 and 77 kHz, the bats shifted the frequency of the CF component of their own echolocation sounds toward that of the artificial pulse, tracking the frequency of the artificial CF component.Bats flying within a large laboratory flight cage were also presented with artificial pulses. Bats in flight lower the frequency of their emitted pulses to compensate for Doppler shifts caused by their own flight speed and systematically shift the frequency of their emitted CF component so that the echo CF frequency returns close to that of the CF component of the artificial CF/FM pulse, over the frequency range where tracking occurs.Abbreviations CF constant frequency - FM frequency modulation     

Gleaning bat echolocation calls do not elicit antipredator behaviour in the Pacific field cricket, <Emphasis Type="Italic">Teleogryllus oceanicus</Emphasis> (Orthoptera: Gryllidae)

Bats that glean prey (capture them from surfaces) produce relatively inconspicuous echolocation calls compared to aerially foraging bats and could therefore be difficult predators to detect, even for insects with ultrasound sensitive ears. In the cricket Teleogryllus oceanicus, an auditory interneuron (AN2) responsive to ultrasound is known to elicit turning behaviour, but only when the cricket is in flight. Turning would not save a cricket from a gleaning bat so we tested the hypothesis that AN2 elicits more appropriate antipredator behaviours when crickets are on the ground. The echolocation calls of Nyctophilus geoffroyi, a sympatric gleaning bat, were broadcast to singing male and walking female T. oceanicus. Males did not cease singing and females did not pause walking more than usual in response to the bat calls up to intensities of 82 dB peSPL. Extracellular recordings from the cervical connective revealed that the echolocation calls elicited AN2 action potentials at high firing rates, indicating that the crickets could hear these stimuli. AN2 appears to elicit antipredator behaviour only in flight, and we discuss possible reasons for this context-dependent function.     

Active listening for spatial orientation in a complex auditory scene

To successfully negotiate a complex environment, an animal must control the timing of motor behaviors in coordination with dynamic sensory information. Here, we report on adaptive temporal control of vocal–motor behavior in an echolocating bat, Eptesicus fuscus, as it captured tethered insects close to background vegetation. Recordings of the bat's sonar vocalizations were synchronized with high-speed video images that were used to reconstruct the bat's three-dimensional flight path and the positions of target and vegetation. When the bat encountered the difficult task of taking insects as close as 10–20 cm from the vegetation, its behavior changed significantly from that under open room conditions. Its success rate decreased by about 50%, its time to initiate interception increased by a factor of ten, and its high repetition rate “terminal buzz” decreased in duration by a factor of three. Under all conditions, the bat produced prominent sonar “strobe groups,” clusters of echolocation pulses with stable intervals. In the final stages of insect capture, the bat produced strobe groups at a higher incidence when the insect was positioned near clutter. Strobe groups occurred at all phases of the wingbeat (and inferred respiration) cycle, challenging the hypothesis of strict synchronization between respiration and sound production in echolocating bats. The results of this study provide a clear demonstration of temporal vocal–motor control that directly impacts the signals used for perception.     

Olfactory discrimination of eight food flavors in the capuchin monkey (Cebus apella): Comparison between fruity and fishy odors

Operant conditioning was used to investigate how primates discriminate between odor qualities. Eight artificial food flavors, selected from either a “Fishy” or “Aroma/Fruity” category, were used. During the presence of one of the two odors S+ or S−, the monkey was reinforced by pushing a response key when S + was presented. The tufted capuchins discriminated most accurately when both odors were Aroma. Discrimination was more accurate when S+ was Fruity odor and S− was Fishy odor. When both odors were Fishy, discrimination could not be acquired in 20 sessions. All of the flavors used, except apple, were novel for the subjects, which suggests that capuchins can innately discriminate among them. The data also suggest that Aroma odors are more salient than Fishy odors. The results also suggested an innate aversion to Fishy odors.     

On-board telemetry of emitted sounds from free-flying bats: compensation for velocity and distance stabilizes echo frequency and amplitude

To understand complex sensory-motor behavior related to object perception by echolocating bats, precise measurements are needed for echoes that bats actually listen to during flight. Recordings of echolocation broadcasts were made from flying bats with a miniature light-weight microphone and radio transmitter (Telemike) set at the position of the bat's ears and carried during flights to a landing point on a wall. Telemike recordings confirm that flying horseshoe bats (Rhinolophus ferrumequinum nippon) adjust the frequency of their sonar broadcasts to compensate for echo Doppler shifts. Returning constant frequency echoes were maintained at the bat's reference frequency +/-83 Hz during flight, indicating that the bats compensated for frequency changes with an accuracy equivalent to that at rest. The flying bats simultaneously compensate for increases in echo amplitude as target range becomes shorter. Flying bats thus receive echoes with both stabilized frequencies and stabilized amplitudes. Although it is widely understood that Doppler-shift frequency compensation facilitates detection of fluttering insects, approaches to a landing do not involve fluttering objects. Combined frequency and amplitude compensation may instead be for optimization of successive frequency modulated echoes for target range estimation to control approach and landing.     

Active head rolls enhance sonar-based auditory localization performance

Animals utilize a variety of active sensing mechanisms to perceive the world around them. Echolocating bats are an excellent model for the study of active auditory localization. The big brown bat (Eptesicus fuscus), for instance, employs active head roll movements during sonar prey tracking. The function of head rolls in sound source localization is not well understood. Here, we propose an echolocation model with multi-axis head rotation to investigate the effect of active head roll movements on sound localization performance. The model autonomously learns to align the bat’s head direction towards the target. We show that a model with active head roll movements better localizes targets than a model without head rolls. Furthermore, we demonstrate that active head rolls also reduce the time required for localization in elevation. Finally, our model offers key insights to sound localization cues used by echolocating bats employing active head movements during echolocation.     

Phase sensitivity in bat sonar revisited

An echolocating bat produces echoes consisting of the convolution of echolocation call and the impulse response (IR) of the ensonified object. A crucial question in animal sonar is whether bats are able to extract this IR from the echo. The bat inner ear generates a frequency representation of call and echo and IR extraction in the frequency domain requires accurate analysis of both magnitude and phase information. Previous studies investigating the phase sensitivity of bats using a jitter paradigm reported a temporal acuity down to 10 ns, suggesting perfect sonar phase representation. In a phantom-target playback experiment, we investigate the perceptual phase sensitivity of the bat Phyllostomus discolor using a novel approach: instead of manipulating IR phase by changing IR delay (jitter paradigm), we randomized IR phase and thus lengthened the IR over time, leaving the magnitude spectrum unchanged. Our results show that phase sensitivity, as reflected in the analysis of signal duration, appears to be much lower than phase sensitivity, as reflected in the analysis of signal onset. The current data indicate that different temporal aspects of sonar processing are encoded with very different temporal resolution and thus an overall claim of “phase sensitivity” as such cannot be maintained.     

Complex echo classification by echo-locating bats: a review

Echo-locating bats constantly emit ultrasonic pulses and analyze the returning echoes to detect, localize, and classify objects in their surroundings. Echo classification is essential for bats’ everyday life; for instance, it enables bats to use acoustical landmarks for navigation and to recognize food sources from other objects. Most of the research of echo based object classification in echo-locating bats was done in the context of simple artificial objects. These objects might represent prey, flower, or fruit and are characterized by simple echoes with a single up to several reflectors. Bats, however, must also be able to use echoes that return from complex structures such as plants or other types of background. Such echoes are characterized by superpositions of many reflections that can only be described using a stochastic statistical approach. Scientists have only lately started to address the issue of complex echo classification by echo-locating bats. Some behavioral evidence showing that bats can classify complex echoes has been accumulated and several hypotheses have been suggested as to how they do so. Here, we present a first review of this data. We raise some hypotheses regarding possible interpretations of the data and point out necessary future directions that should be pursued.     

Is tissue maturation necessary for flight? Changes in body composition during postnatal development in the big brown bat

Patterns of offspring development reflect the availability of energy and nutrients, limitations on an individual’s capacity to use available resources, and tradeoffs between the use of nutrients to support current metabolic demands and tissue growth. To determine if the long period of offspring dependency in bats is associated with the need for an advanced state of tissue maturation prior to flight, we examined body composition during postnatal growth in the big brown bat, Eptesicus fuscus. Despite their large size at birth (22% of maternal mass), newborn bats are relatively immature, containing 82% body water in fat-free mass. However, the total body water content of newborn bat pups decreases to near-adult levels in advance of weaning, while concentrations of total body fat and protein exceed adult values. In contrast to many other mammals, postnatal growth of bat pups was characterized by relatively stable concentrations of calcium and phosphorus, but declining concentrations of magnesium. These levels remained stable or rebounded in late postnatal development. This casts doubt on the hypothesis that low rates of mineral transfer necessitate an extended lactation period in bats. However, our finding of near-adult body composition at weaning is consistent with the hypothesis that extended lactation in bats is necessary for the young to achieve sufficient tissue maturity to undertake the active flight necessary for independent feeding. In this respect, bats differ from most other mammals but resemble birds that must engage in active flight to achieve nutritional independence.     

Bats' avoidance of real and virtual objects: implications for the sonar coding of object size

Fast movement in complex environments requires the controlled evasion of obstacles. Sonar-based obstacle evasion involves analysing the acoustic features of object-echoes (e.g., echo amplitude) that correlate with this object's physical features (e.g., object size). Here, we investigated sonar-based obstacle evasion in bats emerging in groups from their day roost. Using video-recordings, we first show that the bats evaded a small real object (ultrasonic loudspeaker) despite the familiar flight situation. Secondly, we studied the sonar coding of object size by adding a larger virtual object. The virtual object echo was generated by real-time convolution of the bats’ calls with the acoustic impulse response of a large spherical disc and played from the loudspeaker. Contrary to the real object, the virtual object did not elicit evasive flight, despite the spectro-temporal similarity of real and virtual object echoes. Yet, their spatial echo features differ: virtual object echoes lack the spread of angles of incidence from which the echoes of large objects arrive at a bat's ears (sonar aperture). We hypothesise that this mismatch of spectro-temporal and spatial echo features caused the lack of virtual object evasion and suggest that the sonar aperture of object echoscapes contributes to the sonar coding of object size.