Clarice A Diebold, Jennifer Lawlor, Kathryne Allen, Grace Capshaw, Megan G Humphrey, Diego Cintron-De Leon, Kishore V Kuchibhotla, Cynthia F Moss

Current Biology, 34(23), 5507-5517

Echolocating bats rely on rapid processing of auditory information to guide moment-to-moment decisions related to echolocation call design and flight path selection. The fidelity of sonar echoes, however, can be disrupted in natural settings due to occlusions, noise, and conspecific jamming signals. Behavioral sensorimotor adaptation to external blocks of relevant cues has been studied extensively, but little is known about adaptations that mitigate internal sensory flow interruption. How do bats modify their sensory-guided behaviors in natural tasks when central auditory processing is interrupted? Here, we induced internal sensory interruptions by reversibly inactivating excitatory neurons in the inferior colliculus (IC) using ligand-activated inhibitory designer receptors exclusively activated by designer drugs (DREADDs). Bats were trained to navigate through one of three open windows in a curtain to obtain a food reward, while their echolocation and flight behaviors were quantified with synchronized ultrasound microphone and stereo video recordings. Under control conditions, bats reliably steered through the open window, only occasionally contacting the curtain edge. Suppressing IC excitatory activity elevated hearing thresholds, disrupted overall performance in the task, increased the frequency of curtain contact, and led to striking compensatory sensorimotor adjustments. DREADDs-treated bats modified flight trajectories to maximize returning echo information and adjusted sonar call design to boost detection of obstacles. Sensorimotor adaptations appeared immediately and did not change over successive trials, suggesting that these behavioral adaptations are mediated through existing neural circuitry. Our findings highlight the remarkable rapid adaptive strategies bats employ to compensate for internal sensory interruptions to effectively navigate their environments.

Grace Capshaw, Clarice A Diebold, Danielle M Adams, Jack Rayner, Gerald S Wilkinson, Cynthia F Moss, Amanda M Lauer

Proceedings B 291 (2034), 20241560

Hearing mediates many behaviors critical for survival in echolocating bats, including foraging and navigation. Most mammals are susceptible to progressive age-related hearing loss; however, the evolution of biosonar, which requires the ability to hear low-intensity echoes from outgoing sonar signals, may have selected against the development of hearing deficits in echolocating bats. Although many echolocating bats exhibit exceptional longevity and rely on acoustic behaviors for survival to old age, relatively little is known about the aging bat auditory system. In this study, we used DNA methylation to estimate the ages of wild-caught big brown bats ( Eptesicus fuscus ) and measured hearing sensitivity in young and aging bats using auditory brainstem responses (ABRs) and distortion product otoacoustic emissions (DPOAEs). We found no evidence for hearing deficits in aging bats, demonstrated by comparable thresholds and similar ABR wave and DPOAE amplitudes across age groups. We additionally found no significant histological evidence for cochlear aging, with similar hair cell counts, afferent, and efferent innervation patterns in young and aging bats. Here we demonstrate that big brown bats show minimal evidence for age-related loss of peripheral hearing sensitivity and therefore represent informative models for investigating mechanisms that may preserve hearing function over a long lifetime.

J Lawlor, MJ Wohlgemuth, CF Moss, KV Kuchibhotla

bioRxiv

Rapid categorization of vocalizations enables adaptive behavior across species. While categorical perception is thought to arise in the neocortex, humans and other animals could benefit from functional organization of ethologically-relevant sounds at earlier stages in the auditory hierarchy. Here, we developed two-photon calcium imaging in the awake echolocating bat (Eptesicus fuscus) to study encoding of sound meaning in the Inferior Colliculus, which is as few as two synapses from the inner ear. Echolocating bats produce and interpret frequency sweep-based vocalizations for social communication and navigation. Auditory playback experiments demonstrated that individual neurons responded selectively to social or navigation calls, enabling robust population-level decoding across categories. Strikingly, category-selective neurons formed spatial clusters, independent of tonotopy within the IC. These findings support a revised view of categorical processing in which specified channels for ethologically-relevant sounds are spatially segregated early in the auditory hierarchy, enabling rapid subcortical organization of call meaning.

NB Kothari, M Wohlgemuth, CF Moss

The Journal of the Acoustical Society of America 142

Our natural world is three-dimensional. A fundamental requirement of spatial orientating behaviors in the natural environment is the representation of 3D sensory space. Despite the importance of 3D sensory coding of a natural scene to guide movement, most neurophysiological investigations of this problem have been limited to studies of restrained subjects, tested with 2D, artificial stimuli. Here we show for the first time that auditory neurons in the midbrain superior colliculus of the free-flying echolocating bat encode 3D egocentric sensory space, and that sonar-guided inspection of objects in the environment sharpens spatial tuning of single neurons. Combining wireless multichannel neural recordings from free-flying bats, synchronized with video and audio data, and an echo model that computes the flying animal’s instantaneous, stimulus space, we demonstrate 3D echo-evoked receptive fields of single auditory midbrain neurons in animals orienting in a complex environment. We discovered that the bat’s active sonar inspection of objects dramatically tightens range tuning of single neurons and shifts peak activity to represent closer distances. Our research demonstrates dynamic 3D space coding in a freely moving mammal engaged in a real-world navigation task.

N Ulanovsky, CF Moss

Nature neuroscience 10 (2)

The hippocampus is crucial for episodic and spatial memory. In freely moving rodents, hippocampal pyramidal neurons show spatially selective firing when the animal passes through a neuron's 'place-field', and theta-band oscillation is continuously present during locomotion. Here we report the first hippocampal recordings from echolocating bats, mammals phylogenetically distant from rodents, which showed place cells very similar to those of rodents. High-frequency 'ripple' oscillations were also rodent-like. Theta oscillation, however, differed from rodents in two important ways: (i) theta occurred when bats explored the environment without locomoting, using distal sensing through echolocation, and (ii) theta was not continuous, but occurred in short intermittent bouts. The intermittence of theta suggests that models of hippocampal function that rely on continuous theta may not apply to bats. Our data support the hypothesis that theta oscillation in the mammalian hippocampus is involved in sequence learning and hence, theta power should increase with sensory-input rate—which explains why theta power correlates with running speed in rodents and with echolocation call rate in bats.

Y Yovel, B Falk, CF Moss, N Ulanovsky

Science 327 (5966)

Is centering a stimulus in the field of view an optimal strategy to localize and track it? We demonstrated, through experimental and computational studies, that the answer is no. We trained echolocating Egyptian fruit bats to localize a target in complete darkness, and we measured the directional aim of their sonar clicks. The bats did not center the sonar beam on the target, but instead pointed it off axis, accurately directing the maximum slope (“edge”) of the beam onto the target. Information-theoretic calculations showed that using the maximum slope is optimal for localizing the target, at the cost of detection. We propose that the tradeoff between detection (optimized at stimulus peak) and localization (optimized at maximum slope) is fundamental to spatial localization and tracking accomplished through hearing, olfaction, and vision.

Susanne Sterbing-D'Angelo, Mohit Chadha, Chen Chiu, Ben Falk, Wei Xian, Janna Barcelo, John M Zook, Cynthia F Moss

Proceedings of the National Academy of Sciences

Bats are the only mammals capable of powered flight, and they perform impressive aerial maneuvers like tight turns, hovering, and perching upside down. The bat wing contains five digits, and its specialized membrane is covered with stiff, microscopically small, domed hairs. We provide here unique empirical evidence that the tactile receptors associated with these hairs are involved in sensorimotor flight control by providing aerodynamic feedback. We found that neurons in bat primary somatosensory cortex respond with directional sensitivity to stimulation of the wing hairs with low-speed airflow. Wing hairs mostly preferred reversed airflow, which occurs under flight conditions when the airflow separates and vortices form. This finding suggests that the hairs act as an array of sensors to monitor flight speed and/or airflow conditions that indicate stall. Depilation of different functional regions of the bats’ wing membrane altered the flight behavior in obstacle avoidance tasks by reducing aerial maneuverability, as indicated by decreased turning angles and increased flight speed.

Jinhong Luo, Cynthia F Moss

Proceedings of the National Academy of Sciences

Many species of bat emit acoustic signals and use information carried by echoes reflecting from nearby objects to navigate and forage. It is widely documented that echolocating bats adjust the features of sonar calls in response to echo feedback; however, it remains unknown whether audiovocal feedback contributes to sonar call design. Audiovocal feedback refers to the monitoring of one’s own vocalizations during call production and has been intensively studied in nonecholocating animals. Audiovocal feedback not only is a necessary component of vocal learning but also guides the control of the spectro-temporal structure of vocalizations. Here, we show that audiovocal feedback is directly involved in the echolocating bat’s control of sonar call features. As big brown bats tracked targets from a stationary position, we played acoustic jamming signals, simulating calls of another bat, timed to selectively perturb audiovocal feedback or echo feedback. We found that the bats exhibited the largest call-frequency adjustments when the jamming signals occurred during vocal production. By contrast, bats did not show sonar call-frequency adjustments when the jamming signals coincided with the arrival of target echoes. Furthermore, bats rapidly adapted sonar call design in the first vocalization following the jamming signal, revealing a response latency in the range of 66 to 94 ms. Thus, bats, like songbirds and humans, rely on audiovocal feedback to structure sonar signal design.