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We introduce two EEG techniques, one based on conventional monopolar electrodes and one based on a novel tripolar electrode, to record for the first time auditory brainstem responses (ABRs) from the scalp of unanesthetized, unrestrained big brown bats. Stimuli were frequency-modulated (FM) sweeps varying in sweep direction, sweep duration, and harmonic structure. As expected from previous invasive ABR recordings, upward-sweeping FM signals evoked larger amplitude responses (peak-to-trough amplitude in the latency range of 3-5 ms post-stimulus onset) than downward-sweeping FM signals. Scalp-recorded responses displayed amplitudelatency trading effects as expected from invasive recordings. These two findings validate the reliability of our noninvasive recording techniques. The feasibility of recording noninvasively in unanesthetized, unrestrained bats will energize future research uncovering electrophysological signatures of perceptual and cognitive processing of biosonar signals in these animals, and allows for better comparison with ABR data from echolocating cetaceans, where invasive experiments are heavily restricted. Because experiments can be repeated in the same animal over time without confounds of stress or anesthesia, our technique requires fewer captures of wild bats, thus helping to preserve natural populations and addressing the goal of reducing animal numbers used for research purposes.

Big brown bats emit wideband frequency modulated (FM) ultrasonic pulses for echolocation. They perceive target range from echo delay and target size from echo amplitude. Their sounds contain two prominent down-sweeping harmonic sweeps (FM1, ∼55-22 kHz; FM2, ∼100-55 kHz), which are affected differently by propagation out to the target and back to the bat. FM2 is attenuated more than FM1 during propagation. Bats anchor target ranging asymmetrically on the low frequencies in FM1, while FM2 only contributes if FM1 is present as well. These experiments tested whether the bat’s ability to discriminate target size from the amplitude of echoes is affected by selectively attenuating upper or lower frequencies. Bats were trained to perform an echo amplitude discrimination task with virtual echo targets 83 cm away. While echo delay was held constant and echo amplitude was varied to estimate threshold, either lower FM1 frequencies or higher FM2 frequencies were attenuated. The results parallel effects seen in echo delay experiments; bats’ performance was significantly poorer when the lower frequencies in echoes were attenuated, compared to higher frequencies. The bat’s ability to distinguish between virtual targets at the same simulated range from echoes arriving at the same delay indicates a high level of focused attention for perceptual isolation of one and suppression of the other.

Understanding the relationships between biosonar and flight in bats requires synchronized recordings of the echo inputs and the flight kinematics of the animals. Here, integrated arrays of 50 high-speed camera and 32 ultrasonic microphones have been set up to collect the data that is necessary for achieving this goal. The arrays are set up to record bats as they fly through an an obstacle course inside a cylindrical tunnel. Due to the complexity of the received signals in these scenarios, we have been developing custom strategies that rely on a combination of compressed sensing and deep learning to reconstruct the acoustic field inside the tunnel from the microphone-array measurements. By using a combination of the high-speed video and acoustic data, it can be attempted to determine the bat's location in the array from the image data and then reconstruct the properties of the sound fields that were emitted and received at this position using the acoustic array data. The goal of this research is to eventually determine the dynamic characteristics of the bat's biosonar emissions such as beampatterns and potentially time-variant characteristics as well as the biosonar inputs that the bats rely on for controlling their flight behaviors.

Studying model organisms in their natural environments is essential for advancing bioinspired science and technology. Echolocating bats can be models to inspire new technology for sonar sensing, mobility with flapping flight as well as the integration of these two capabilities. Bat species belonging to genera such as Rhinolophus and Hipposideros stand out for their ability to navigate and hunt prey in dense vegetation. To further the study of echolocation and flight strategies in these genera, field-based research methods have been used to observe, record, and capture bats in Brunei Darussalam. This work was conducted at Andulau Forest Reserve on the border of Belait and Tutong Districts, various other field sites in Tutong District, as well as at Mata Mata in Brunei-Muara District from June 2022 through August 2022. Harp traps were primarily used to capture bats, a less invasive capture technique compared to other types of netting and thought to be more effective against the sophisticated echolocation capabilities of these bats. Acoustic recordings were collected at trap sites and upon processing. These recordings can be utilized to advance passive acoustic monitoring and to improve software that can distinguish species based on sonar characteristics which can also support general biodiversity monitoring.

Many bat species rely on biosonar as their primary source of sensory information about their environments. Species that are able to navigate amid dense vegetation use this biosonar information to guide highly dexterous flight maneuvers. Understanding the connection between biosonar inputs and flight outputs poses a challenge, because the flight apparatus of bats has the most degrees of freedom of any flight system—whether natural or man-made. At the same time, the biosonar inputs consist of just two one-dimensional acoustic time signals (i.e., echoes received at the two ears). Due to the complexity and large variability in the echoes and the flight maneuvers of bats, understanding the input-output relationships requires the ability to collect large amounts of quantitative data on the acoustics and the flight kinematics. In addition, comparing different bat species could offer a window into the principles behind the evolutionary co-adaptation of biosonar and flight. To accomplish this, a cylindrical flight tunnel that integrates synchronized arrays of 50 high-speed video cameras and 32 ultrasonic microphones has been set up on the island of Borneo. This instrument is complemented by a set of custom deep-learning techniques that can handle the large amounts of data that are being produced.

To investigate the active sensing strategies used by echolocating bats of the genera Rhinolophus and Hipposideros, we have constructed a 9-meter long flight tunnel, which incorporates an array of 32 ultrasonic microphones distributed throughout the tunnel. Rhinolophus and Hipposideros are of special interest because of their highly flexible biosonar system; these bats emit pulses from their nasal cavities, using complex noseleaf structures to quickly and precisely alter the beam-form and direction of emissions. Additionally, each species utilizes a unique combination of constant-frequency (CF) and frequency-modulated (FM) ultrasonic signals with varying durations, repetition rates, and frequencies. We plan to trap several species of wild Bornean bats of these genera and fly individual bats through the tunnel; a time-of-arrival algorithm will be used to localize the position of each bat at the time of each biosonar pulse emission, and an amplitude-comparison method to measure the horizontal and vertical direction of each emission from the bat’s noseleaf. We will also incorporate relatively simple foliage obstacles into the tunnel; this will create complex acoustic clutter and allow us to determine how bats of different species adjust their biosonar sampling strategies in order to navigate around novel obstacles in a cluttered environment.

Summary We challenged four big brown bats to maneuver through abrupt turns in narrow corridors surrounded by dense acoustic clutter. We quantified bats' performance, sonar beam focus, and sensory acquisition rate. Performance was excellent in straight corridors, with sonar beam aim deviating less than 5° from the corridor midline. Bats anticipated an upcoming abrupt turn to the right or left by slowing flight speed and shifting beam aim to “look” proactively into one side of the corridor to identify the new flightpath. All bats mastered the right turn, but two bats consistently failed the left turn. Bats increased their sensory acquisition rate when confronting abrupt turns in both successful and failed flights. Limitations on biosonar performance reflected failures to switch beam aim and to modify a learned spatial map, rather than failures to update acquisition rate., Graphical abstract, Highlights • Echolocating bats use sonar to identify flightpaths through dense, cluttered scenes • Bats learn new flightpaths by switching beam aim before encountering obstacles • Bats see their environment in depth, Biological Sciences; Zoology; Animals; Ethology