CF-FM Bats Research Articles

Neural responses of the auditory midbrain to naturalistic echolocation sequences in Hipposideros armiger

The functional properties of the auditory midbrain, inferior colliculus (IC), plays a critical role in James Simmons’s SCAT model of target ranging by echolocation. This SCAT model is based solely on the big brown bat producing frequency-modulated (FM) sonar calls. By contrast, there has been very limited knowledge on how the auditory midbrain may encode target ranging information in bats that produce constant-frequency (CF) sonar calls. Here, we conducted single-unit recordings from the auditory midbrain of passively listening Hipposideros armiger using naturalistic echolocation sequences. We created echolocation sequences from recordings taken from individual bats swung on a moving pendulum that evokes Doppler shift compensation (DSC) of their sonar vocalizations. Our preliminary data revealed a population of IC neurons selectively responded to DSC information in the sequences. To our surprise, we did not find neurons that encode echo delays. Considering published data on FM bats, these results suggest that the functional role of auditory midbrain for echolocation may be distinct between FM bats and CF-FM bats.

Theoretical investigation of active listening behavior based on the echolocation of CF-FM bats.

Bats perceive the three-dimensional environment by emitting ultrasound pulses from their nose or mouth and receiving echoes through both ears. To determine the position of a target object, it is necessary to know the distance and direction of the target. Certain bat species that use a combined signal of long constant frequency and short frequency modulated ultrasounds synchronize their pinnae movement with pulse emission, and this behavior has been regarded as helpful for localizing the elevation angle of a reflective sound source. However, the significance of bats' ear motions remains unclear. In this study, we construct a model of an active listening system including the motion of the ears, and conduct mathematical investigations to clarify the importance of ear motion in direction detection of the reflective sound source. In the simulations, direction detection under rigid ear movements with interaural level differences was mathematically investigated by assuming that bats accomplish direction detection using the amplitude modulation in the echoes caused by ear movements. In particular, the ear motion conditions required for direction detection are theoretically investigated through exhaustive simulations of the pseudo-motion of the ears, rather than simulations of the actual ear motions of bats. The theory suggests that only certain ear motions, namely three-axis rotation, allow for accurate and robust direction detection. Our theoretical analysis also strongly supports the behavior whereby bats move their pinnae in the antiphase mode. In addition, we suggest that simple shaped hearing directionality and well-selected uncomplicated ear motions are sufficient to achieve precise and robust direction detection. Our findings and mathematical approach have the potential to be used in the design of active sensing systems in various engineering fields.

Biomimetic sonar and the problem of finding deterministic targets in foliage

The ability of (bio)sonars to find targets-of-interest is often hampered by a cluttered environment. For example, naval sonars encounter difficulties finding mines partially or fully buried within sand. Such situations pose target identification challenges are much harder than target detection and resolution problems. There are many bat species which navigate and hunt in dense vegetation and thus must be able to identify targets-of-interest within clutter. Evolutionary adaptation of the bat biosonar system is likely to have resulted in the “discovery” of features that support making distinctions between clutter and echoes of interest. The most well-established case is given by cf-fm bats that use Doppler shifts caused by the wingbeat of a flying insect prey to identify the prey in foliage. Other bat species have been shown to use a passive sonar approach that is based on unique prey-generated acoustic signals. Some of the most interesting cases can be found in bat species that are successful in finding preys that apparently does not emit any distinguishing sounds themselves and would hence limit the bats to an active-sonar approach. Such bat species could provide model species for new ways in which the target-identification problem in clutter can be solved with active sonar.

Obstacle avoidance navigation by echolocating bat: Compared relationships between acoustic guidance and flight control in unfamiliar space and familiar space

Echolocating bats can fly without colliding with obstacles by synchronizing acoustic guidance and flight control. To research how bats adapt echolocation as they became familiar with the spaces, we made CF-FM bats (Japanese horseshoe bat) exhibit S-sharp flight repeatedly in a chamber arranged acoustically transparent chains. We found (1) flight path was changed continuously to reduce its curvature as the bats repeated the flights, resulting that the maximum flight speed increased from 2.7 to 3.0 m/s in the 1st trial to 3.2 to 3.8 m/s in the 12th (last) trial for all three bats, (2) pulse emission was reduced by 45% (66/148 pulses) from the first to the last trial, (3) they shifted the pulse direction dynamically relative to their flight direction in the 1st flight whereas the pulse direction was shifted smoothly, the bats emitted more intense pulses toward the intended flight direction as they became familiar with the space. When acrylic boards were arranged, the bats could not pass through the obstacle course until they learned the space. These suggest echolocation is changed between unfamiliar and familiar space flight and the bats adapt their echolocation to feedforward-dominant control for perceiving more at distance for path planning when they have a spatial map.

Significance of terminal frequency in FM sweeps for bat echolocation

For echolocation of CF-FM bats, the CF component is expected to detect wing-beat of flying insects. However, it also plays an important role to serve as a stable signal carrier from a distant target. Then, once the carrier frequency is removed, echo signal can be easily detected. For this purpose, Doppler-shift compensation and echo amplitude compensation must be conducted to stabilize the signal carrier. What about the FM bats? FM bats also appear to utilize a relatively long pseudo-CF component to detect wing-beats of flying insects. They might also utilize pseudo-CF component for an echo signal carrier. However, Doppler-shift compensation in FM bats has not been reported. In the inferior colliculus, majority of neurons are tuned to the pseudo-CF frequency, 20 kHz for Eptesicus fuscus while 40 kHz for Pipistrellus abramus, which are corresponding to the terminal frequencies of downward FM sweep. Overrepresentation of a particular frequency may enhance frequency discrimination, detection of insect wing-beat. Therefore, we may expect majority of cochlear nerve fibers are also tuned to the pseudo-CF frequency. However, overrepresentation of hair cells for a particular frequency does not appear to be shown. [Research supported by MEXT, Japan and Shandong University, China.]

Strategies for an echolocating FM bat, Pipistrellus abramus, to listen to weak echoes

In Japanese house bat, Pipistrellus abramus, a typical FM-bat, neurophysiological investigation in the inferior colliculus showed that about half of neurons was tuned to the terminal frequency of the downward FM seep or pseudo-CF frequency for searching insects, which was around 40 kHz. Their audiograms determined by the auditory brainstem response (ABR) and the compound action potentials (CAP) of the cochlear nerve also show the lowest threshold or maximum amplitude to be found at around 40 kHz. However, we could not find a sharp notch in their audiogram around 40 kHz, which we have usually found in CF-FM bats at round their reference CF frequency. We examined the peripheral system of Japanese house bat how they extract signals of a flying insect. A particular attention was paid on their terminal frequency of FM sweep or pseudo-CF frequency. [Research supported by MEXT of Japan.]

How flying CF-FM echolocating bats adapt to acoustically jammed environments: Quantitative evaluation

Echolocating bats face the acoustical interferences from sounds of other conspecifics; they can fly without colliding each other and avoid surrounding obstacles. The purpose of this study was to reveal how CF-FM bats extract their own echoes in acoustically jammed environments. The Japanese horseshoe bats (Rhinolophus ferrumequinum nippon) were flown with conspecifics in the flight chamber. As the number of flying bats increased from one to seven, the duration of constant frequency (CF) components decreased, whereas the terminal frequency modulated (TFM) components were extended in both time and frequency ranges. In order to quantitatively evaluate behavioral responses under jamming conditions, a flying bat was exposed by artificially synthesized CF-FM pulses. As a result, the bats also changed the CF and TFM components as observed in the group flight experiment. This shows that the bats modify the characteristics of pulses to adapt to acoustical jamming and not to adapt to spatial jamming owing to other flying bats. These results suggest that TFM component was more important than CF component in extracting their own echoes during flight in acoustically jammed conditions. We will examine echolocation behavior when we manipulate CF components in context of jamming avoidance during Doppler-shift compensation.

The cochlear size of bats and rodents derived from MRI images and histology.

From the evolutionary perspective, the ear of each animal species is built for effective processing of the biologically relevant signals used for communication and acoustically guided orientation. Because the sound pulses used by echolocating bats for orientation and rodents for communication are quite different, the basic design of the mammalian auditory system commonly shared by echolocating bats must be specialized in some manner to effectively process their species-specific sounds. The present study examines the difference in the cochlea of these animal species using MRI images and histological techniques. We report here that, although all these animal species share a similar cochlear structure, they vary in their cochlear size and turns. Bats using constant frequency-frequency-modulated pulses (CF-FM bats) and frequency-modulated pulses (FM bats) for echolocation have a larger cochlear size and more cochlear turns than rodents (mice and rats). However, CF-FM bats have the largest cochlear size and most cochlear turns. This difference in cochlear size and turns of these animal species is discussed in relation to their biologically relevant sounds and acoustic behavior.

Investigation of acoustic gaze strategy by Pipistrellus abramus and Rhinolophus ferrumequinum Nippon during obstacle avoidance flight

We investigated the acoustic gaze (angle between pulse and flight directions) and the beam width of echolocation pulses emitted by bats during obstacle avoidance flight in a chamber (7×3×2 m). Echolocation pulses were recorded by a telemetry microphone mounted on the bat’s back and a horizontal 20-ch microphone array set up in the chamber. Flight path measurements were conducted using two high-speed video cameras. While the bat showed a circular flight avoiding the surrounding walls, the acoustic gaze showed significant linear correlation to the angular velocity of the flight. This means that the bat adjusted the pulse direction to precede its own flight direction. The correlation coefficient increased with complexity of obstacle conditions. We compared changes in acoustic gaze between FM bats (mean beam width: ±50°) and CF-FM bats (mean beam width: ±22°). We found that FM bats smoothly shifted the acoustic gaze within 10° during the flight whereas the CF-FM bats frequently shifted the acoustic gaze within 25°. These results indicate that the shifting acoustic gaze by CF-FM bats compensates their own narrow beam width. Both bat species may keep approximately ±50° of their echolocation sights in order to sense the space for moving forward safely.

Adaptive beam-width control of echolocation sounds by CF–FM bats,Rhinolophus ferrumequinum nippon, during prey-capture flight

The echolocation sounds of Japanese CF-FM bats (Rhinolophus ferrumequinum nippon) were measured while the bats pursued a moth (Goniocraspidum pryeri) in a flight chamber. Using a 31-channel microphone array system, we investigated how CF-FM bats adjust pulse direction and beam width according to prey position. During the search and approach phases, the horizontal and vertical beam widths were ±22±5 and ±13±5 deg, respectively. When bats entered the terminal phase approximately 1 m from a moth, distinctive evasive flight by G. pryeri was sometimes observed. Simultaneously, the bats broadened the beam widths of some emissions in both the horizontal (44% of emitted echolocation pulses) and vertical planes (71%). The expanded beam widths were ±36±7 deg (horizontal) and ±30±9 deg (vertical). When moths began evasive flight, the tracking accuracy decreased compared with that during the approach phase. However, in 97% of emissions during the terminal phase, the beam width was wider than the misalignment (the angular difference between the pulse and target directions). These findings indicate that bats actively adjust their beam width to retain the moving target within a spatial echolocation window during the final capture stages.

Convergence of reference frequencies by multiple CF–FM bats (Rhinolophus ferrumequinum nippon) during paired flights evaluated with onboard microphones

The constant frequency component of the second harmonic (CF(2)) of echolocation sounds in Rhinolophus ferrumequinum nippon were measured using onboard telemetry microphones while the bats exhibited Doppler-shift compensation during flights with conspecifics. (1) The CF(2) frequency of pulses emitted by individual bats at rest (F (rest)) showed a long-term gradual decline by 0.22 kHz on average over a period of 3 months. The mean neighboring F (rest) (interindividual differences in F (rest) between neighboring bats when the bats were arranged in ascending order according to F (rest)) ranged from 0.08 to 0.11 kHz among 18 bats in a laboratory colony. (2) The standard deviation of observed echo CF(2) (reference frequency) for bats during paired flights ranged from 50 to 90 Hz, which was not significantly different from that during single flights. This finding suggests that during paired flights, bats exhibit Doppler-shift compensation with the same accuracy as when they fly alone. (3) In 60% (n = 29) of the cases, the difference in the reference frequency between two bats during paired flights significantly decreased compared to when the bats flew alone. However, only 15% of the cases (n = 7) showed a significant increase during paired flights. The difference in frequency between two bats did not increase even when the reference frequencies of the individuals were not statistically different during single flights.

Findings on bat sonar through Telemike system

In order to understand how bats conduct echolocation recording what they listen to is essential. Then, we developed an onboard wireless telemetry microphone system (Telemike) for flying bats in our flight chamber. We also developed a sensitive microphone array system for field recordings and for the flight chamber. Some data through microphone array with Telemike will also be introduced. Both CF-FM (Hipposideros turpis, Hipposideros terasensis and Rhinolophus ferrumequinum nippon) and FM bats (Pipistrellus abramus, Miniopterus fuliginosus, and Eptesicus fuscus) were used in the flight chamber experiments, while only FM bats (Pipistrellus abramus and Eptesicus fuscus) were used for the field experiments. In the flight chamber experiment, through Telemike Doppler-shift compensation was confirmed from flying CF-FM bats. Echo amplitude compensation was found in both FM and CF-FM bats. The bats can fly without any collision against walls or their conspecifics in a narrow space. Telemike has recorded overlapped echoes originated from adjacent bats. How they extract weak echo signals in the situation where own echoes are masked by echoes of other bats may be revealed by Telemike experiments. Further, how bats get information from extremely weak echoes coming from a flying small insect will also be clarified in our experiments with Telemike. [Research supported by ONR grant]

Beam-width control of echolocation pulses in Japanese CF-FM bats (Rhinolophus ferrumequinum nippon) during aerial prey hunting.

Beam-width control of echolocation pulses in Japanese CF-FM bats (Rhinolophus ferrumequinum nippon) during aerial prey hunting.

Doppler-shift compensation in the Taiwanese leaf-nosed bat (Hipposideros terasensis) recorded with a telemetry microphone system during flight

Biosonar behavior was examined in Taiwanese leaf-nosed bats (Hipposideros terasensis; CF-FM bats) during flight. Echolocation sounds were recorded using a telemetry microphone mounted on the bat's head. Flight speed and three-dimensional trajectory of the bat were reconstructed from images taken with a dual high-speed video camera system. Bats were observed to change the intensity and emission rate of pulses depending on the distance from the landing site. Frequencies of the dominant second harmonic constant frequency component (CF2) of calls estimated from the bats' flight speed agreed strongly with observed values. Taiwanese leaf-nosed bats changed CF2 frequencies depending on flight speed, which caused the CF2 frequencies of the Doppler-shifted echoes to remain constant. Pulse frequencies were also estimated using echoes returning directly ahead of the bat and from its sides for two different flight conditions: landing and U-turn. Bats in flight may periodically alter their attended angles from the front to the side when emitting echolocation pulses.

Measurement of biosonar signals of echolocating bat during flight by a telemetry system

A telemetry microphone system (Telemike) has been developed, which can be mounted on the bat’s head, to measure acoustic characteristics of emitted pulses and returning echoes. The system allows us to monitor what the bat listens to during its flight. A high-speed video camera system has been also adopted together with the Telemike to trace positions in space of the flying bat for analyzing temporal pulse emission patterns. With those devices, how the CF-FM bats execute parallel time-sharing real-time processing during their flight can be investigated. Doppler-shift compensation, echo amplitude compensation and processing for multiple target detections were observed. Some of the evidence found by the Telemike will be introduced and discussed. [Work partly supported by the Innovative Cluster Creation Project promoted by MEXT and by a grant to RCAST at Doshisha University from MEXT.]

Narrowband target tracking using a biomimetic sonarhead

This work presents a target tracking method that exploits both the physics of narrowband echolocation and appropriate movements of the sensor, taking inspiration from narrowband (CF-FM) bats. The platform used in this work is RoBat, a biomimetic sonarhead mounted on a mobile platform. Two different techniques are integrated in the tracker. First, Barshan’s and Kuc’s method for estimating target range and azimuth angle is adapted to the geometry of the sonarhead. Next, Walker’s arc scanning hypothesis for target elevation estimation in CF-FM bats is implemented, applying curve fitting for an accurate estimation of the peak-delay. The integration of both techniques in a preliminary 3D tracking system is performed applying both methods independently.

The use of Doppler in Sonar-based mobile robot navigation: inspirations from biology

So-called CF–FM bats are highly mobile creatures who emit long calls in which much of the energy is concentrated in a single frequency. These bats face sensor interpretation problems very similar to those of mobile robots provided with ultrasonic sensors, while navigating in cluttered environments. This paper presents biologically-inspired engineering on the use of narrowband Sonar in mobile robotics. It replicates, using robotics as a modelling medium, methods CF–FM bats use to exploit Doppler-shifts––a rich source of information not used by commercial robotic ultrasonic range sensors––in different tasks. The experimental platform for the work is RoBat, a 6 DOF biomimetic sonarhead mounted on a commercial 3 DOF mobile platform. The platform is provided with signal processing capabilities inspired by the bat's auditory system. The CF–FM bat modifies––increasing or decreasing––the carrier frequency of its own calls, compensating the Doppler-shift produced when the bat, the reflector or both are moving. This echolocating behaviour, called Doppler-shift compensation, is successfully implemented in RoBat. Inspired by this behaviour, a convoy navigation controller following a set of simple Doppler-dependent rules is successfully devised. The performance of the controller is satisfactory despite low Doppler-shift resolution caused by the lower velocity of the robot when compared to real bats. Finally, Müller's hypothesis on the use of acoustic flow by CF–FM bats for obstacle avoidance is also implemented in RoBat, resulting in a crude estimation of the target's passing distance at small bearing angles, which improves as the angle increases, nevertheless sufficing for avoiding the two reflectors of the experiment.

Estimating Doppler Shift Using Bat-Inspired Cochlear Filter Bank Models: A Comparison of Methods for Echoes from Single and Multiple Reflectors

This work presents biologically inspired engineering on the use of narrowband sonar in mobile robotics. It replicates, using robotics as a modeling medium, elements of how CF-FM bats process the constant frequency part of their emitted call for estimating Doppler shift in the echoes. The experimental platform for the work is RoBat, a 6-DOF biomimetic sonar head mounted on a 3-DOF mobile platform. Two models of the signal processing performed by the bat's cochlea were implemented, based on sets of bandpass filters followed by full-wave rectification and lowpass filtering. One filter bank uses Butterworth filters whose center frequencies vary linearly across the set. The alternative filter bank uses gammatone filters, with center frequencies varying nonlinearly across the set. Two methods of estimating Doppler shift from the return echoes after cochlear signal processing were implemented. The first was a simple energy-weighted average of filter center frequencies. The second was a novel neural-network-based technique. Each method was tested with each of the cochlear models and evaluated in the context of several dynamic tasks in which RoBat was moved at different velocities toward stationary echo sources such as walls and posts. Overall, the performance of the linear filter bank was more consistent than the gammatone. The same applies to the artificial neural network, with consistently better noise performance than the weighted average. The effect of multiple reflectors contained in a single echo was also analyzed in terms of error in Doppler-shift estimation assuming a single wider reflector.

Animal Sonar: Processes and Performance

<i>Animal Sonar: Processes and Performance</i>

Discrimination of insect wingbeat-frequencies by the batRhinolophus ferrumequinum

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.