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.

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.

What do mammals have to say about the neurobiology of acoustic communication?

Auditory communication is crucial across taxa, including humans, because it enables individuals to convey information about threats, food sources, mating opportunities, and other social cues necessary for survival. Comparative approaches to auditory communication will help bridge gaps across taxa and facilitate our understanding of the neural mechanisms underlying this complex task. In this work, we briefly review the field of auditory communication processing and the classical champion animal, the songbird. In addition, we discuss other mammalian species that are advancing the field. In particular, we emphasize mice and bats, highlighting the characteristics that may inform how we think about communication processing.

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.

Bats: Vision or echolocation, why not both?

Echolocation allows bats to navigate in complete darkness. Yet, some bats also have keen eyesight. A new study shows that bats integrate these sensory modalities, even when light abundance would make it possible for them to rely solely on vision.

Spatial attention in natural tasks [version 1; peer review: 2 approved with reservations].

Little is known about fine scale neural dynamics that accompany rapid shifts in spatial attention in freely behaving animals, primarily because reliable indicators of attention are lacking in standard model organisms engaged in natural tasks. The echolocating bat can serve to bridge this gap, as it exhibits robust dynamic behavioral indicators of overt spatial attention as it explores its environment. In particular, the bat actively shifts the aim of its sonar beam to inspect objects in different directions, akin to eye movements and foveation in humans and other visually dominant animals. Further, the bat adjusts the temporal features of sonar calls to attend to objects at different distances, yielding a metric of acoustic gaze along the range axis. Thus, an echolocating bat's call features not only convey the information it uses to probe its surroundings, but also provide fine scale metrics of auditory spatial attention in 3D natural tasks. These explicit metrics of overt spatial attention can be leveraged to uncover general principles of neural coding in the mammalian brain.

Social Communication in Big Brown Bats.

Bats are social mammals that display a wide array of social communication calls. Among them, it is common for most bats species to emit distress, agonistic, appeasement and infant isolation calls. Big brown bats (Eptesicus fuscus) are no different: They are gregarious animals living in colonies that can comprise hundreds of individuals. These bats live in North America and, typically found roosting in man-made structures like barns and attics, are considered common. They are insectivorous laryngeal echolocators, and while their calls and associated brain mechanisms in echolocation are well-documented, much less is known about their neural systems for analyzing social vocalizations. In this work we review what we know about the social lives of big brown bats and propose how to consolidate the nomenclature used to describe their social vocalizations. Furthermore, we discuss the next steps in the characterization of the social structure of this species and how these studies will advance both research in neuroethology and ecology of big brown bats.

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.

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.

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.

Natural Statistics as Inference Principles of Auditory Tuning in Biological and Artificial Midbrain Networks.

Bats provide a powerful mammalian model to explore the neural representation of complex sounds, as they rely on hearing to survive in their environment. The inferior colliculus (IC) is a central hub of the auditory system that receives converging projections from the ascending pathway and descending inputs from auditory cortex. In this work, we build an artificial neural network to replicate auditory characteristics in IC neurons of the big brown bat. We first test the hypothesis that spectro-temporal tuning of IC neurons is optimized to represent the natural statistics of conspecific vocalizations. We estimate spectro-temporal receptive fields (STRFs) of IC neurons and compare tuning characteristics to statistics of bat calls. The results indicate that the FM tuning of IC neurons is matched with the statistics. Then, we investigate this hypothesis on the network optimized to represent natural sound statistics and to compare its output with biological responses. We also estimate biomimetic STRFs from the artificial network and correlate their characteristics to those of biological neurons. Tuning properties of both biological and artificial neurons reveal strong agreement along both spectral and temporal dimensions, and suggest the presence of nonlinearity, sparsity, and complexity constraints that underlie the neural representation in the auditory midbrain. Additionally, the artificial neurons replicate IC neural activities in discrimination of social calls, and provide simulated results for a noise robust discrimination. In this way, the biomimetic network allows us to infer the neural mechanisms by which the bat's IC processes natural sounds used to construct the auditory scene.

Bat target tracking strategies for prey interception.

Insectivorous bats capture their prey in flight with impressive success. They rely on the echoes of their own ultrasonic vocalization that yield acoustic snapshots, which enable target tracking on a rapid time scale. This task requires the use of intermittent information to navigate a dynamically changing environment. Bats may solve this challenging task by building internal models that estimate target velocity to anticipate the future location of a prey item. This has been recently tested empirically in perched bats tracking a target moving across their acoustic field. In this report, we build on past work to propose a new model that describes bat flight trajectories employing predictive strategies. Furthermore, we compare this model with a previous model of bat target interception that has also been employed by some visually guided animals: parallel navigation. Abbreviations: HTTP, Hybrid Target Trajectory Prediction; CATD, Constant Absolute Target Direction; CB, Constant Bearing; PN, Parallel Navigation.

Echolocating bats accumulate information from acoustic snapshots to predict auditory object motion.

Unlike other predators that use vision as their primary sensory system, bats compute the three-dimensional (3D) position of flying insects from discrete echo snapshots, which raises questions about the strategies they employ to track and intercept erratically moving prey from interrupted sensory information. Here, we devised an ethologically inspired behavioral paradigm to directly test the hypothesis that echolocating bats build internal prediction models from dynamic acoustic stimuli to anticipate the future location of moving auditory targets. We quantified the direction of the bat's head/sonar beam aim and echolocation call rate as it tracked a target that moved across its sonar field and applied mathematical models to differentiate between nonpredictive and predictive tracking behaviors. We discovered that big brown bats accumulate information across echo sequences to anticipate an auditory target's future position. Further, when a moving target is hidden from view by an occluder during a portion of its trajectory, the bat continues to track its position using an internal model of the target's motion path. Our findings also reveal that the bat increases sonar call rate when its prediction of target trajectory is violated by a sudden change in target velocity. This shows that the bat rapidly adapts its sonar behavior to update internal models of auditory target trajectories, which would enable tracking of evasive prey. Collectively, these results demonstrate that the echolocating big brown bat integrates acoustic snapshots over time to build prediction models of a moving auditory target's trajectory and enable prey capture under conditions of uncertainty.

Adaptive Echolocation and Flight Behaviors in Bats Can Inspire Technology Innovations for Sonar Tracking and Interception.

Target tracking and interception in a dynamic world proves to be a fundamental challenge faced by both animals and artificial systems. To track moving objects under natural conditions, agents must employ strategies to mitigate interference and conditions of uncertainty. Animal studies of prey tracking and capture reveal biological solutions, which can inspire new technologies, particularly for operations in complex and noisy environments. By reviewing research on target tracking and interception by echolocating bats, we aim to highlight biological solutions that could inform new approaches to artificial sonar tracking and navigation systems. Most bat species use wideband echolocation signals to navigate dense forests and hunt for evasive insects in the dark. Importantly, bats exhibit rapid adaptations in flight trajectory, sonar beam aim, and echolocation signal design, which appear to be key to the success of these animals in a variety of tasks. The rich suite of adaptive behaviors of echolocating bats could be leveraged in new sonar tracking technologies by implementing dynamic sensorimotor feedback control of wideband sonar signal design, head, and ear movements.

Neural Response Selectivity to Natural Sounds in the Bat Midbrain.

Little is known about the neural mechanisms that mediate differential action-selection responses to communication and echolocation calls in bats. For example, in the big brown bat, frequency modulated (FM) food-claiming communication calls closely resemble FM echolocation calls, which guide social and orienting behaviors, respectively. Using advanced signal processing methods, we identified fine differences in temporal structure of these natural sounds that appear key to auditory discrimination and behavioral decisions. We recorded extracellular potentials from single neurons in the midbrain inferior colliculus (IC) of passively listening animals, and compared responses to playbacks of acoustic signals used by bats for social communication and echolocation. We combined information obtained from spike number and spike triggered averages (STA) to reveal a robust classification of neuron selectivity for communication or echolocation calls. These data highlight the importance of temporal acoustic structure for differentiating echolocation and food-claiming social calls and point to general mechanisms of natural sound processing across species.

Auditory communication processing in bats: What we know and where to go.

Bats are the second largest mammalian order, with over 1,300 species. These animals show diverse behaviors, diets, and habitats. Most bats produce ultrasonic vocalizations and perceive their environment by processing information carried by returning echoes of their calls. Echolocation is achieved through a sophisticated audio-vocal system that allows bats to emit and detect frequencies that can range from ten to hundreds of kilohertz. In addition, most bat species are gregarious, and produce social communication calls that vary in complexity, form, and function across species. In this article, we (a) highlight the value of bats as model species for research on social communication, (b) review behavioral and neurophysiological studies of bat acoustic communication signal production and processing, and (c) discuss important directions for future research in this field. We propose that comparative studies of bat acoustic communication can provide new insights into sound processing and vocal learning across the animal kingdom. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Requirement of NF-kappa B Activation in Different Mice Brain Areas during Long-Term Memory Consolidation in Two Contextual One-Trial Tasks with Opposing Valences.

NF-kappa B is a transcription factor whose activation has been shown to be necessary for long-term memory consolidation in several species. NF-kappa B is activated and translocates to the nucleus of cells in a specific temporal window during consolidation. Our work focuses on a one trial learning tasks associated to the inhibitory avoidance (IA) setting. Mice were trained either receiving or not a footshock when entering a dark compartment (aversive vs. appetitive learning). Regardless of training condition (appetitive or aversive), latencies to step-through during testing were significantly different to those measured during training. Additionally, these testing latencies were also different from those of a control group that only received a shock unrelated to context. Moreover, nuclear NF-kappa B DNA-binding activity was augmented in the aversive and the appetitive tasks when compared with control and naïve animals. NF-kappa B inhibition by Sulfasalazine injected either in the Hippocampus, Amygdala or Nucleus accumbens immediately after training was able to impair retention in both training versions. Our results suggest that NF-kappa B is a critical molecular step, in different brain areas on memory consolidation. This was the case for both the IA task and also the modified version of the same task where the footshock was omitted during training. This work aims to further investigate how appetitive and aversive memories are consolidated.

Surface expression of NMDA receptor changes during memory consolidation in the crab Neohelice granulata.

The aim of the present study was to analyze the surface expression of the NMDA-like receptors during the consolidation of contextual learning in the crab Neohelice granulata Memory storage is based on alterations in the strength of synaptic connections between neurons. The glutamatergic synapses undergo various forms of N-methyl-D aspartate receptor (NMDAR)-dependent changes in strength, a process that affects the abundance of other receptors at the synapse and underlies some forms of learning and memory. Here we propose a direct regulation of the NMDAR. Changes in NMDAR's functionality might be induced by the modification of the subunit's expression or cellular trafficking. This trafficking does not only include NMDAR's movement between synaptic and extra-synaptic localizations but also the cycling between intracellular compartments and the plasma membrane, a process called surface expression. Consolidation of contextual learning affects the surface expression of the receptor without affecting its general expression. The surface expression of the GluN1 subunit of the NMDAR is down-regulated immediately after training, up-regulated 3 h after training and returns to naïve and control levels 24 h after training. The changes in NMDAR surface expression observed in the central brain are not seen in the thoracic ganglion. A similar increment in surface expression of GluN1 in the central brain is observed 3 h after administration of the competitive GABAA receptor antagonist, bicuculline. These consolidation changes are part of a plasticity event that first, during the down-regulation, stabilizes the trace and later, at 3-h post-training, changes the threshold for synapse activation.