Hiroshi Riquimaroux

Echo-intensity compensation in echolocating bats (Pipistrellus abramus) during flight measured by a telemetry microphone

An onboard microphone (Telemike) was developed to examine changes in the basic characteristics of echolocation sounds of small frequency-modulated echolocating bats, Pipistrellus abramus. Using a dual high-speed video camera system, spatiotemporal observations of echolocation characteristics were conducted on bats during a landing flight task in the laboratory. The Telemike allowed us to observe emitted pulses and returning echoes to which the flying bats listened during flight, and the acoustic parameters could be precisely measured without traditional problems such as the directional properties of the recording microphone and the emitted pulse, or traveling loss of the sound in the air. Pulse intensity in bats intending to land exhibited a marked decrease by 30 dB within 2 m of the target wall, and the reduction rate was approximately 6.5 dB per halving of distance. The intensity of echoes returning from the target wall indicated a nearly constant intensity (-42.6 +/- 5.5 dB weaker than the pulse emitted in search phase) within a target distance of 2 m. These findings provide direct evidence that bats adjust pulse intensity to compensate for changes in echo intensity to maintain a constant intensity of the echo returned from the approaching target at an optimal range.

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.

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

SUMMARY 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.

Adaptive echolocation sounds of insectivorous bats, Pipistrellus abramus, during foraging flights in the field

Echolocation pulses emitted by wild Pipistrellus abramus were investigated while foraging for insects in the field. Similar to other European pipistrelles, the frequency structure during foraging varied. During the search phase, the bats emitted long shallow frequency-modulated pulses 9-11 ms in duration, whereas the maximum pulse duration of the bats approaching a large target wall in the laboratory was 3 ms. No significant difference was observed between decreases in the interpulse interval during these two approach flights. It is concluded that the bats use a long quasi-constant frequency pulse to find a weak echo from a small prey target.

Echolocation and flight strategy of Japanese house bats during natural foraging, revealed by a microphone array system.

Using only a microphone array system, echolocation pulses and three-dimensional flight paths in the frequency-modulated bat, Pipistrellus abramus, during natural foraging, were simultaneously examined. During the search phase, the inter-pulse interval, pulse duration, and moving distance of the bat between successive emissions were relatively constant at around 89.5 ± 18.7 ms, 6.90 ± 1.31 ms, and 0.50 ± 0.20 m, respectively. The bats started to decrease these acoustical parameters within 2-3 m of the prey capture point. For every emission along a flight path, the distance between a bat and its prey capture point was calculated as both direct distance to capture (DDC), which corresponded to the target distance, and flight distance to capture (FDC) along the flight path. The DDC matched the FDC after the start of the approach phase, indicating that foraging bats followed a straight-ahead path to the target. In addition, the duration of the quasi-constant frequency component of emitted pulses was slightly extended just before the convergence of the DDC with the FDC. These findings suggest that the bats confirm the presence of target prey by extending the duration of the pulse and then select a straight-ahead approach by forecasting the movement of the prey.

Classification of vocalizations in the Mongolian gerbil, Meriones unguiculatus

The Mongolian gerbil (Meriones unguiculatus) has been an important model system in auditory physiology, but its natural sounds are not well known. Vocalizations produced by colonies of adult gerbils were recorded during various social interactions in a standard laboratory animal-rearing facility. Sound recordings were made continuously for 24 h. This species exhibited a rich repertoire of vocalizations that varied in spectrotemporal structure. Calls were classified into 13 distinct syllable types. These syllables were further categorized into eight simple syllables and five composite syllables, which could be described by combinations of two to three simple syllables. The durations of individual syllables ranged from 30 to 330 ms with fundamental frequencies of 5 to 50 kHz. Those with lower fundamental frequencies typically contained more harmonic components (up to nine). Analysis of syllable sequences indicated that syllables may be combined into three types of simple phrases. These results provide a basis for future studies not only of the behavioral significance of vocalization, but also of the neural basis of vocal communication in the Mongolian gerbil.

Behavioral evidence for auditory induction in a species of rodent: Mongolian gerbil (Meriones unguiculatus)

When a segment of sound of interest is interrupted by a loud extraneous noise, humans perceive that the missing sound continues during the intrusive noise. This restoration of auditory information occurs in perceptions of both speech and non-speech sounds (e.g., tone bursts), a phenomenon referred to as auditory induction. In this study, Mongolian gerbils were trained with standard Go/No-Go operant conditioning to discriminate continuous tone bursts (the Go stimulus) from tone bursts with a silent gap in the middle (the No-Go stimulus). Noise was added to Go and No-Go stimuli to determine the condition under which induction would occur. The Mongolian gerbils engaged in Go responses to No-Go stimuli only when the noise spectrally surrounding the tone was of the same duration as the silent portion of the No-Go stimulus; these results match those previously reported in primates (humans and macaque monkeys). The result presents not only the evidence of the auditory induction in a rodent species but also suggests that similar mechanisms for restoring missing sounds are shared among mammals. Additionally, our findings demonstrated that the rodent can serve as a valuable animal model for future studies of perceptual restoration.

Vocalization control in Mongolian gerbils (Meriones unguiculatus) during locomotion behavior

The vocalization behavior of Mongolian gerbils, a model animal of auditory physiology, was examined. A pair of gerbils was placed in a chamber, and their species-specific vocalizations and locomotive behaviors were recorded and analyzed. Two types of calls were predominantly produced: high-frequency upward frequency-modulated (HU-FM) calls and low-frequency multi-harmonic frequency-modulated (LM-FM) calls. Emission rates of HU-FM calls significantly decreased as the distance between the two gerbils increased, and playback of simulated HU-FM calls increased the emission rates. Acoustic analysis of HU-FM calls showed that the calls exhibited a stereotypic spectro-temporal structure including a fixed inter-onset interval (100-175 ms) and that individual differences in the frequency could convey the body size of the callers. The timing of HU-FM calls was highly synchronized with jump movements when an animal vocalized while jumping, suggesting the existence of tight locomotor-vocal coupling. Conversely, LM-FM calls were observed only when the gerbils tactilely contacted with each other while fighting over a food. These results suggest that Mongolian gerbils change the rates of call emissions and call types (e.g., LM-FM or HU-FM calls) in response to changes in visual and possibly tactile and auditory information. The functions of both calls are discussed in terms of their acoustic structures.

Adaptive SONAR sounds by echolocating bats

Like dolphins, bats are known to possess highly developed SONAR systems in air. Echolocating bats can be divided into two groups: the CF-FM and FM bats depending on frequency structure of their pulses. In this study, we used one of Japanese FM bat species, Pipistrellus abramus. The echolocation behavior was examined for two different flight tasks: (a) field recording while capturing insects in the open area, and (b) recording for a landing approach to a target wall in the laboratory. We acoustically compared these two echolocations by the bats while approaching a target. In the field and laboratory, repetition rates of pulse emission in the search phase were constant at approximately 10 pulses/s. When approach phase was started, the bats increased the repetition rate of the pulse emission to 140-190 pulses/s. We found that the pulse duration was dynamically decreased from 10 to 0.5 ms during prey capturing in the field, whereas it ranged from 0.5 to 3-4 ms in the laboratory. A CF-like portion (a narrow slope portion at the end of pulse) was observed to follow the initial FM sweep beyond approximately 2 m of the target distance in the laboratory. Interestingly, the CF-like portion was found to be extended by the bats in the field and such long pulse duration was never seen in the laboratory. This suggests that FM bats use not only broadband signals, but also narrowband signals for echolocation in the far target range as CF-FM bat species. Biosonar animals might have been supposed to adapt their echolocation to underlying physical law in nature or their environment through their evolutionary history. These comparative studies between the field and laboratory recordings are expected to help our understanding of bats biosonar system, and various echolocation strategies employed by the bats will contribute to develop artificial SONAR system or new echo-sensing devices in the future.

Audiovisual integration in the primary auditory cortex of an awake rodent.

Much is known about the behavioral and physiological aspects of multimodal integration in primates, whereas less is known about the extent of audiovisual integration in other species. This study investigated the temporal integration of audiovisual stimuli in the primary auditory cortex (A1) of a standard animal model of auditory physiology: the Mongolian gerbil (Meriones unguiculatus). We recorded single unit responses to auditory and visual stimuli in the A1 of awake gerbils. A tone burst (auditory stimulus) paired with a flashing light (visual stimulus) at differing lag times (from 0 to ±160ms) was presented contralateral to the recording site. As a result, the auditory response was altered significantly by the visual stimulus in more than 25% of the A1 units. The effect of the visual stimulus on the auditory response decreased as the time lag between the two modalities increased. The influence of the visual stimulus remained relatively greater when it preceded rather than followed the auditory stimulus. These results suggest that the A1 and earlier (subcortical) auditory structures of the rodent are capable of temporally integrating information from auditory and visual modalities.