Auditory processing of communication calls in interacting bats.

There is strong evidence that social context plays a role in the processing of acoustic signals. Yet, the circuits and mechanisms that govern this process are still not fully understood. The insectivorous big brown bat, Eptesicus fuscus, emits a wide array of communication calls, including food-claiming calls, aggressive calls, and appeasement calls. We implemented a competitive foraging task to explore the influence of behavioral context on auditory midbrain responses to conspecific social calls. We recorded neural population responses from the inferior colliculus (IC) of freely interacting bats and analyzed data with respect to social context. Analysis of our neural recordings from the IC shows stronger population responses to individual calls during social events. For the first time, neural recordings from the IC of a copulating bat were obtained. Our results indicate that social context enhances neuronal population responses to social vocalizations in the bat IC.

Superfast Lombard response in free-flying, echolocating bats.

Acoustic cues are crucial to communication, navigation, and foraging in many animals, which hence face the problem of detecting and discriminating these cues in fluctuating noise levels from natural or anthropogenic sources. Such auditory dynamics are perhaps most extreme for echolocating bats that navigate and hunt prey on the wing in darkness by listening for weak echo returns from their powerful calls in complex, self-generated umwelts.1,2 Due to high absorption of ultrasound in air and fast flight speeds, bats operate with short prey detection ranges and dynamic sensory volumes,3 leading us to hypothesize that bats employ superfast vocal-motor adjustments to rapidly changing sensory scenes. To test this hypothesis, we investigated the onset and offset times and magnitude of the Lombard response in free-flying echolocating greater mouse-eared bats exposed to onsets of intense constant or duty-cycled masking noise during a landing task. We found that the bats invoked a bandwidth-dependent Lombard response of 0.1-0.2 dB per dB increase in noise, with very short delay and relapse times of 20 ms in response to onsets and termination of duty-cycled noise. In concert with the absence call time-locking to noise-free periods, these results show that free-flying bats exhibit a superfast, but hard-wired, vocal-motor response to increased noise levels. We posit that this reflex is mediated by simple closed-loop audio-motor feedback circuits that operate independently of wingbeat and respiration cycles to allow for rapid adjustments to the highly dynamic auditory scenes encountered by these small predators.

Ventral wing hairs provide tactile feedback for aerial prey capture in the big brown bat, Eptesicus fuscus.

Bats rely on their hand-wings to execute agile flight maneuvers, to grasp objects, and cradle young. Embedded in the dorsal and ventral membranes of bat wings are microscopic hairs. Past research findings implicate dorsal wing hairs in airflow sensing for flight control, but the function of ventral wing hairs has not been previously investigated. Here, we test the hypothesis that ventral wing hairs carry mechanosensory signals for flight control, prey capture, and handling. To test this hypothesis, we used synchronized high-speed stereo video and audio recordings to quantify flight and echolocation behaviors of big brown bats (Eptesicus fuscus) engaged in an aerial insect capture task. We analyzed prey-capture strategy and performance, along with flight kinematics, before and after depilation of microscopic hairs from the bat's ventral wing and tail membranes. We found that ventral wing hair depilation significantly impaired the bat's prey-capture performance. Interestingly, ventral wing hair depilation also produced increases in the bat's flight speed, an effect previously attributed exclusively to airflow sensing along the dorsal wing surface. These findings demonstrate that microscopic hairs embedded in the ventral wing and tail membranes of insectivorous bats provide mechanosensory feedback for prey handling and flight control.

Spatially clustered neurons encode vocalization categories in the bat midbrain.

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.

Adaptive echolocation behavior of bats and toothed whales in dynamic soundscapes.

Journal of Experimental Biology has a long history of reporting research discoveries on animal echolocation, the subject of this Centenary Review. Echolocating animals emit intense sound pulses and process echoes to localize objects in dynamic soundscapes. More than 1100 species of bats and 70 species of toothed whales rely on echolocation to operate in aerial and aquatic environments, respectively. The need to mitigate acoustic clutter and ambient noise is common to both aerial and aquatic echolocating animals, resulting in convergence of many echolocation features, such as directional sound emission and hearing, and decreased pulse intervals and sound intensity during target approach. The physics of sound transmission in air and underwater constrains the production, detection and localization of sonar signals, resulting in differences in response times to initiate prey interception by aerial and aquatic echolocating animals. Anti-predator behavioral responses of prey pursued by echolocating animals affect behavioral foraging strategies in air and underwater. For example, many insect prey can detect and react to bat echolocation sounds, whereas most fish and squid are unresponsive to toothed whale signals, but can instead sense water movements generated by an approaching predator. These differences have implications for how bats and toothed whales hunt using echolocation. Here, we consider the behaviors used by echolocating mammals to (1) track and intercept moving prey equipped with predator detectors, (2) interrogate dynamic sonar scenes and (3) exploit visual and passive acoustic stimuli. Similarities and differences in animal sonar behaviors underwater and in air point to open research questions that are ripe for exploration.

Neural coding of 3D spatial location, orientation, and action selection in echolocating bats.

Echolocating bats are among the only mammals capable of powered flight, and they rely on active sensing to find food and steer around obstacles in 3D environments. These natural behaviors depend on neural circuits that support 3D auditory localization, audio-motor integration, navigation, and flight control, which are modulated by spatial attention and action selection.

Echo feedback mediates noise-induced vocal modifications in flying bats.

Diverse animal taxa are capable of rapidly modifying vocalizations to mitigate interference from environmental noise. Echolocating bats, for example, must frequently perform sonar tasks in the presence of interfering sounds. Numerous studies have documented sound production flexibility in echolocating bats; however, it remains unknown whether noise-induced vocal modifications (NIVMs) mitigate interference effects on echoes or calls. In this study, we leverage echo level compensation behavior of echolocating bats to answer this question. Using a microphone array, we recorded echolocation calls of Hipposideros pratti trained to approach and land on a perch in the laboratory under quiet and noise conditions. We found that H. pratti exhibited echo level compensation behavior during approaching flights, which depended critically on distance to the landing perch. Broadcast noise delayed and affected the rate of echo level compensation in H. pratti. Moreover, H. pratti increased vocalization amplitude, i.e., exhibited the Lombard effect, while also adjusting call duration and bandwidth with increasing noise levels. Quantitative analyses of the data show that H. pratti relies on echo feedback, not vocal feedback, to adjust signals in the presence of noise. These findings provide compelling evidence that NIVMs in echolocating animals and non-echolocating animals operate through different mechanisms.

Doppler shift compensation performance in Hipposideros pratti across experimental paradigms.

A central aim of neuroethological research is to discover the mechanisms of natural behaviors in controlled laboratory studies. This goal, however, comes with challenges, namely the selection of experimental paradigms that allow full expression of natural behaviors. Here, we explore this problem in echolocating bats that evolved Doppler shift compensation (DSC) of sonar vocalizations to yield close matching between echo frequency and hearing sensitivity. We ask if behavioral tasks influence the precision of DSC in Pratt's roundleaf bat, Hipposideros pratti, in three classic laboratory paradigms evoking audio-vocal adjustments: Stationary bats listening to echo playbacks, bats transported on a moving pendulum, and bats flying freely. We found that experimental conditions had a strong influence on the expression of the audiovocal frequency adjustments in bats. H. pratti exhibited robust DSC in both free-flying and moving-pendulum experiments but did not exhibit consistent audiovocal adjustments in echo playback experiments. H. pratti featured a maximum compensation magnitude of 87% and a compensation precision of 0.27% in the free flight experiment. Interestingly, in the moving pendulum experiment H. pratti displayed surprisingly high-precision DSC, with an 84% maximum compensation magnitude and a 0.27% compensation precision. Such DSC performance places H. pratti among the bat species exhibiting the most precise audio-vocal control of echo frequency. These data support the emerging view that Hipposiderid bats have a high-precision DSC system and highlight the importance of selecting experimental paradigms that yield the expression of robust natural behaviors.

Sensory error drives fine motor adjustment.

Fine audiovocal control is a hallmark of human speech production and depends on precisely coordinated muscle activity guided by sensory feedback. Little is known about shared audiovocal mechanisms between humans and other mammals. We hypothesized that real-time audiovocal control in bat echolocation uses the same computational principles as human speech. To test the prediction of this hypothesis, we applied state feedback control (SFC) theory to the analysis of call frequency adjustments in the echolocating bat, Hipposideros armiger. This model organism exhibits well-developed audiovocal control to sense its surroundings via echolocation. Our experimental paradigm was analogous to one implemented in human subjects. We measured the bats' vocal responses to spectrally altered echolocation calls. Individual bats exhibited highly distinct patterns of vocal compensation to these altered calls. Our findings mirror typical observations of speech control in humans listening to spectrally altered speech. Using mathematical modeling, we determined that the same computational principles of SFC apply to bat echolocation and human speech, confirming the prediction of our hypothesis.

Sound evoked fos-like immunoreactivity in the big brown bat.

Most bat species have highly developed audio-vocal systems, which allow them to adjust the features of echolocation calls that are optimized for different sonar tasks, such as detecting, localizing, discriminating and tracking targets. Furthermore, bats can also produce a wide array of social calls to communicate with conspecifics. The acoustic properties of some social calls differ only subtly from echolocation calls, yet bats have the ability to distinguish them and reliably produce appropriate behavioral responses. Little is known about the underlying neural processes that enable the correct classification of bat social communication sounds. One approach to this question is to identify the brain regions that are involved in the processing of sounds that carry behavioral relevance. Here, we present preliminary data on neuronal activation, as measured by c-fos expression, in big brown bats (Eptesicus fuscus) exposed to either social calls, echolocation calls or kept in silence. We focused our investigation on five relevant brain areas; three within the canonical auditory pathway (auditory cortex, inferior colliculus and medial geniculate body) and two that are involved in the processing of emotive stimulus content (amygdala and nucleus accumbens). In this manuscript we report c-fos staining of the areas of interest after exposure to conspecific calls. We discuss future work designed to overcome experimental limitations and explore whether c-fos staining reveals anatomical segregation of neurons activated by echolocation and social call categories.

Natural acoustic stimuli evoke selective responses in the hippocampus of passive listening bats.

A growing body of research details spatial representation in bat hippocampus, and experiments have yet to explore hippocampal neuron responses to sonar signals in animals that rely on echolocation for spatial navigation. To bridge this gap, we investigated bat hippocampal responses to natural echolocation sounds in a non-spatial context. In this experiment, we recorded from CA1 of the hippocampus of three awake bats that listened passively to single echolocation calls, call-echo pairs, or natural echolocation sequences. Our data analysis identified a subset of neurons showing response selectivity to the duration of single echolocation calls. However, the sampled population of CA1 neurons did not respond selectively to call-echo delay, a stimulus dimension posited to simulate target distance in recordings from auditory brain regions of bats. A population analysis revealed ensemble coding of call duration and sequence identity. These findings open the door to many new investigations of auditory coding in the mammalian hippocampus.

Orienting our view of the superior colliculus: specializations and general functions.

The mammalian superior colliculus (SC) and its non-mammalian homolog, the optic tectum are implicated in sensorimotor transformations. Historically, emphasis on visuomotor functions of the SC has led to a popular view that it operates as an oculomotor structure rather than a more general orienting structure. In this review, we consider comparative work on the SC/optic tectum, with a particular focus on non-visual sensing and orienting, which reveals a broader perspective on SC functions and their role in species-specific behaviors. We highlight several recent studies that consider ethological context and natural behaviors to advance knowledge of the SC as a site of multi-sensory integration and motor initiation in diverse species.

Communication with self, friends and foes in active-sensing animals.

Animals that rely on electrolocation and echolocation for navigation and prey detection benefit from sensory systems that can operate in the dark, allowing them to exploit sensory niches with few competitors. Active sensing has been characterized as a highly specialized form of communication, whereby an echolocating or electrolocating animal serves as both the sender and receiver of sensory information. This characterization inspires a framework to explore the functions of sensory channels that communicate information with the self and with others. Overlapping communication functions create challenges for signal privacy and fidelity by leaving active-sensing animals vulnerable to eavesdropping, jamming and masking. Here, we present an overview of active-sensing systems used by weakly electric fish, bats and odontocetes, and consider their susceptibility to heterospecific and conspecific jamming signals and eavesdropping. Susceptibility to interference from signals produced by both conspecifics and prey animals reduces the fidelity of electrolocation and echolocation for prey capture and foraging. Likewise, active-sensing signals may be eavesdropped, increasing the risk of alerting prey to the threat of predation or the risk of predation to the sender, or drawing competition to productive foraging sites. The evolutionary success of electrolocating and echolocating animals suggests that they effectively counter the costs of active sensing through rich and diverse adaptive behaviors that allow them to mitigate the effects of competition for signal space and the exploitation of their signals.

Deafness in an auditory specialist, the big brown bat (Eptesicus fuscus).

Bats are long-lived animals that show presumed resistance to noise-induced and age-related hearing loss, which has been attributed to their dependence on sound processing for survival. Echolocation and basic auditory functions have been studied extensively in the big brown bat (Eptesicus fuscus), an insectivorous microchiropteran species. We conducted hearing tests and analysis of cochlear sensory cells in a group of big brown bats that exhibited anomalies in behavioral sonar tracking experiments and/or lacked neural responses to acoustic stimulation in subcortical auditory nuclei. We show for the first time the presence of profound deafness and extensive cochlear damage in an echolocating bat species. Auditory brainstem responses were abnormal or absent in these bats, and histological analyses of their cochleae revealed extensive loss of hair cells, supporting cells, and spiral ganglion neurons. The underlying cause of deafness is unknown.

Effect of background clutter on neural discrimination in the bat auditory midbrain.

The discrimination of complex sounds is a fundamental function of the auditory system. This operation must be robust in the presence of noise and acoustic clutter. Echolocating bats are auditory specialists that discriminate sonar objects in acoustically complex environments. Bats produce brief signals, interrupted by periods of silence, rendering echo snapshots of sonar objects. Sonar object discrimination requires that bats process spatially and temporally overlapping echoes to make split-second decisions. The mechanisms that enable this discrimination are not well understood, particularly in complex environments. We explored the neural underpinnings of sonar object discrimination in the presence of acoustic scattering caused by physical clutter. We performed electrophysiological recordings in the inferior colliculus of awake big brown bats, to broadcasts of prerecorded echoes from physical objects. We acquired single unit responses to echoes and discovered a subpopulation of IC neurons that encode acoustic features that can be used to discriminate between sonar objects. We further investigated the effects of environmental clutter on this population's encoding of acoustic features. We discovered that the effect of background clutter on sonar object discrimination is highly variable and depends on object properties and target-clutter spatiotemporal separation. In many conditions, clutter impaired discrimination of sonar objects. However, in some instances clutter enhanced acoustic features of echo returns, enabling higher levels of discrimination. This finding suggests that environmental clutter may augment acoustic cues used for sonar target discrimination and provides further evidence in a growing body of literature that noise is not universally detrimental to sensory encoding.NEW & NOTEWORTHY Bats are powerful animal models for investigating the encoding of auditory objects under acoustically challenging conditions. Although past work has considered the effect of acoustic clutter on sonar target detection, less is known about target discrimination in clutter. Our work shows that the neural encoding of auditory objects was affected by clutter in a distance-dependent manner. These findings advance the knowledge on auditory object detection and discrimination and noise-dependent stimulus enhancement.

Mechanosensory Hairs and Hair-like Structures in the Animal Kingdom: Specializations and Shared Functions Serve to Inspire Technology Applications.

Biological mechanosensation has been a source of inspiration for advancements in artificial sensory systems. Animals rely on sensory feedback to guide and adapt their behaviors and are equipped with a wide variety of sensors that carry stimulus information from the environment. Hair and hair-like sensors have evolved to support survival behaviors in different ecological niches. Here, we review the diversity of biological hair and hair-like sensors across the animal kingdom and their roles in behaviors, such as locomotion, exploration, navigation, and feeding, which point to shared functional properties of hair and hair-like structures among invertebrates and vertebrates. By reviewing research on the role of biological hair and hair-like sensors in diverse species, we aim to highlight biological sensors that could inspire the engineering community and contribute to the advancement of mechanosensing in artificial systems, such as robotics.

Cynthia F. Moss.

Interview with Cynthia Moss, who studies echolocating bats to understand the coordination of sensory and motor activity in 3D space at Johns Hopkins University.

Inflight head stabilization associated with wingbeat cycle and sonar emissions in the lingual echolocating Egyptian fruit bat, Rousettus aegyptiacus.

Sensory processing of environmental stimuli is challenged by head movements that perturb sensorimotor coordinate frames directing behaviors. In the case of visually guided behaviors, visual gaze stabilization results from the integrated activity of the vestibuloocular reflex and motor efference copy originating within circuits driving locomotor behavior. In the present investigation, it was hypothesized that head stabilization is broadly implemented in echolocating bats during sustained flight, and is temporally associated with emitted sonar signals which would optimize acoustic gaze. Predictions from these hypotheses were evaluated by measuring head and body kinematics with motion sensors attached to the head and body of free-flying Egyptian fruit bats. These devices were integrated with ultrasonic microphones to record sonar emissions and elucidate the temporal association with periods of head stabilization. Head accelerations in the Earth-vertical axis were asymmetric with respect to wing downstroke and upstroke relative to body accelerations. This indicated that inflight head and body accelerations were uncoupled, outcomes consistent with the mechanisms that limit vertical head acceleration during wing downstroke. Furthermore, sonar emissions during stable flight occurred most often during wing downstroke and head stabilization, supporting the conclusion that head stabilization behavior optimized sonar gaze and environmental interrogation via echolocation.

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.

Autonomous Flying With Neuromorphic Sensing.

Autonomous flight for large aircraft appears to be within our reach. However, launching autonomous systems for everyday missions still requires an immense interdisciplinary research effort supported by pointed policies and funding. We believe that concerted endeavors in the fields of neuroscience, mathematics, sensor physics, robotics, and computer science are needed to address remaining crucial scientific challenges. In this paper, we argue for a bio-inspired approach to solve autonomous flying challenges, outline the frontier of sensing, data processing, and flight control within a neuromorphic paradigm, and chart directions of research needed to achieve operational capabilities comparable to those we observe in nature. One central problem of neuromorphic computing is learning. In biological systems, learning is achieved by adaptive and relativistic information acquisition characterized by near-continuous information retrieval with variable rates and sparsity. This results in both energy and computational resource savings being an inspiration for autonomous systems. We consider pertinent features of insect, bat and bird flight behavior as examples to address various vital aspects of autonomous flight. Insects exhibit sophisticated flight dynamics with comparatively reduced complexity of the brain. They represent excellent objects for the study of navigation and flight control. Bats and birds enable more complex models of attention and point to the importance of active sensing for conducting more complex missions. The implementation of neuromorphic paradigms for autonomous flight will require fundamental changes in both traditional hardware and software. We provide recommendations for sensor hardware and processing algorithm development to enable energy efficient and computationally effective flight control.