Natural switches in behaviour rapidly modulate hippocampal coding.

Throughout their daily lives, animals and humans often switch between different behaviours. However, neuroscience research typically studies the brain while the animal is performing one behavioural task at a time, and little is known about how brain circuits represent switches between different behaviours. Here we tested this question using an ethological setting: two bats flew together in a long 135 m tunnel, and switched between navigation when flying alone (solo) and collision avoidance as they flew past each other (cross-over). Bats increased their echolocation click rate before each cross-over, indicating attention to the other bat1-9. Hippocampal CA1 neurons represented the bat's own position when flying alone (place coding10-14). Notably, during cross-overs, neurons switched rapidly to jointly represent the interbat distance by self-position. This neuronal switch was very fast-as fast as 100 ms-which could be revealed owing to the very rapid natural behavioural switch. The neuronal switch correlated with the attention signal, as indexed by echolocation. Interestingly, the different place fields of the same neuron often exhibited very different tuning to interbat distance, creating a complex non-separable coding of position by distance. Theoretical analysis showed that this complex representation yields more efficient coding. Overall, our results suggest that during dynamic natural behaviour, hippocampal neurons can rapidly switch their core computation to represent the relevant behavioural variables, supporting behavioural flexibility.

Evolution of inner ear neuroanatomy of bats and implications for echolocation.

Phylogenomics of bats suggests that their echolocation either evolved separately in the bat suborders Yinpterochiroptera and Yangochiroptera, or had a single origin in bat ancestors and was later lost in some yinpterochiropterans1-6. Hearing for echolocation behaviour depends on the inner ear, of which the spiral ganglion is an essential structure. Here we report the observation of highly derived structures of the spiral ganglion in yangochiropteran bats: a trans-otic ganglion with a wall-less Rosenthal's canal. This neuroanatomical arrangement permits a larger ganglion with more neurons, higher innervation density of neurons and denser clustering of cochlear nerve fascicles7-13. This differs from the plesiomorphic neuroanatomy of Yinpterochiroptera and non-chiropteran mammals. The osteological correlates of these derived ganglion features can now be traced into bat phylogeny, providing direct evidence of how Yangochiroptera differentiated from Yinpterochiroptera in spiral ganglion neuroanatomy. These features are highly variable across major clades and between species of Yangochiroptera, and in morphospace, exhibit much greater disparity in Yangochiroptera than Yinpterochiroptera. These highly variable ganglion features may be a neuroanatomical evolutionary driver for their diverse echolocating strategies4,14-17 and are associated with the explosive diversification of yangochiropterans, which include most bat families, genera and species.

A social foraging trade-off in echolocating bats reveals that they benefit from some conspecifics but are impaired when many are around.

Social foraging is very common in the animal kingdom. Numerous studies have documented collective foraging in various species and many reported the attraction of various species to foraging conspecifics. It is nonetheless difficult to quantify the benefits and costs of collective foraging, especially in the wild. We examined the benefits and costs of social foraging using on-board microphones mounted on freely foraging Molossus nigricans bats. This allowed us to quantify the bats' attacks on prey and to assess their success as a function of conspecific density. We found that the bats spent most of their time foraging at low conspecific densities, during which their attacks were most successful in terms of prey items captured per time unit. Notably, their capture rate dropped when conspecific density became either too high or too low. Our findings thus demonstrate a clear social foraging trade-off in which the presence of a few conspecifics probably improves foraging success, whereas the presence of too many impairs it.

Auditory cortical regions show resting-state functional connectivity with the default mode-like network in echolocating bats.

Echolocating bats are among the most social and vocal of all mammals. These animals are ideal subjects for functional MRI (fMRI) studies of auditory social communication given their relatively hypertrophic limbic and auditory neural structures and their reduced ability to hear MRI gradient noise. Yet, no resting-state networks relevant to social cognition (e.g., default mode-like networks or DMLNs) have been identified in bats since there are few, if any, fMRI studies in the chiropteran order. Here, we acquired fMRI data at 7 Tesla from nine lightly anesthetized pale spear-nosed bats (Phyllostomus discolor). We applied independent components analysis (ICA) to reveal resting-state networks and measured neural activity elicited by noise ripples (on: 10 ms; off: 10 ms) that span this species' ultrasonic hearing range (20 to 130 kHz). Resting-state networks pervaded auditory, parietal, and occipital cortices, along with the hippocampus, cerebellum, basal ganglia, and auditory brainstem. Two midline networks formed an apparent DMLN. Additionally, we found four predominantly auditory/parietal cortical networks, of which two were left-lateralized and two right-lateralized. Regions within four auditory/parietal cortical networks are known to respond to social calls. Along with the auditory brainstem, regions within these four cortical networks responded to ultrasonic noise ripples. Iterative analyses revealed consistent, significant functional connectivity between the left, but not right, auditory/parietal cortical networks and DMLN nodes, especially the anterior-most cingulate cortex. Thus, a resting-state network implicated in social cognition displays more distributed functional connectivity across left, relative to right, hemispheric cortical substrates of audition and communication in this highly social and vocal species.

Convergence in hearing-related genes between echolocating birds and mammals.

Echolocation, the detection of objects by means of sound waves, has evolved independently in diverse animals. Echolocators include not only mammals such as toothed whales and yangochiropteran and rhinolophoid bats but also Rousettus fruit bats, as well as two bird lineages, oilbirds and swiftlets. In whales and yangochiropteran and rhinolophoid bats, positive selection and molecular convergence has been documented in key hearing-related genes, such as prestin (SLC26A5), but few studies have examined these loci in other echolocators. Here, we examine patterns of selection and convergence in echolocation-related genes in echolocating birds and Rousettus bats. Fewer of these loci were under selection in Rousettus or birds compared with classically recognized echolocators, and elevated convergence (compared to outgroups) was not evident across this gene set. In certain genes, however, we detected convergent substitutions with potential functional relevance, including convergence between Rousettus and classic echolocators in prestin at a site known to affect hair cell electromotility. We also detected convergence between Yangochiroptera, Rhinolophidea, and oilbirds in TMC1, an important mechanosensory transduction channel in vertebrate hair cells, and observed an amino acid change at the same site within the pore domain. Our results suggest that although most proteins implicated in echolocation in specialized mammals may not have been recruited in birds or Rousettus fruit bats, certain hearing-related loci may have undergone convergent functional changes. Investigating adaptations in diverse echolocators will deepen our understanding of this unusual sensory modality.

Bats expand their vocal range by recruiting different laryngeal structures for echolocation and social communication.

Echolocating bats produce very diverse vocal signals for echolocation and social communication that span an impressive frequency range of 1 to 120 kHz or 7 octaves. This tremendous vocal range is unparalleled in mammalian sound production and thought to be produced by specialized laryngeal vocal membranes on top of vocal folds. However, their function in vocal production remains untested. By filming vocal membranes in excised bat larynges (Myotis daubentonii) in vitro with ultra-high-speed video (up to 250,000 fps) and using deep learning networks to extract their motion, we provide the first direct observations that vocal membranes exhibit flow-induced self-sustained vibrations to produce 10 to 95 kHz echolocation and social communication calls in bats. The vocal membranes achieve the highest fundamental frequencies (fo's) of any mammal, but their vocal range is with 3 to 4 octaves comparable to most mammals. We evaluate the currently outstanding hypotheses for vocal membrane function and propose that most laryngeal adaptations in echolocating bats result from selection for producing high-frequency, rapid echolocation calls to catch fast-moving prey. Furthermore, we show that bats extend their lower vocal range by recruiting their ventricular folds-as in death metal growls-that vibrate at distinctly lower frequencies of 1 to 5 kHz for producing agonistic social calls. The different selection pressures for echolocation and social communication facilitated the evolution of separate laryngeal structures that together vastly expanded the vocal range in bats.

Changes in primary visual and auditory cortex of blind and sighted adults following 10 weeks of click-based echolocation training.

Recent work suggests that the adult human brain is very adaptable when it comes to sensory processing. In this context, it has also been suggested that structural "blueprints" may fundamentally constrain neuroplastic change, e.g. in response to sensory deprivation. Here, we trained 12 blind participants and 14 sighted participants in echolocation over a 10-week period, and used MRI in a pre-post design to measure functional and structural brain changes. We found that blind participants and sighted participants together showed a training-induced increase in activation in left and right V1 in response to echoes, a finding difficult to reconcile with the view that sensory cortex is strictly organized by modality. Further, blind participants and sighted participants showed a training induced increase in activation in right A1 in response to sounds per se (i.e. not echo-specific), and this was accompanied by an increase in gray matter density in right A1 in blind participants and in adjacent acoustic areas in sighted participants. The similarity in functional results between sighted participants and blind participants is consistent with the idea that reorganization may be governed by similar principles in the two groups, yet our structural analyses also showed differences between the groups suggesting that a more nuanced view may be required.

Sustainable pest control inspired by prey-predator ultrasound interactions.

Nocturnal moths evolved ultrasound-triggered escape maneuvers for avoiding predatory bats emitting ultrasonic echolocation calls. Using ultrasound for pest control is not a novel concept, but the technique has not been systemized because of the moths' habituation to sounds and the narrow directionality of conventional ultrasound speakers. Here, we report the use of pulsed ultrasonic white noise, which contributes to achieving ecologically concordant plant protection. An ultrasonic pulse, which is temporal mimicry of the search-phase pulse in the echolocation calls of a sympatric bat, was identified using neuroethological screening of eared moth-repelling ultrasounds; these pulses elicit flight-stopping reactions in moths but have no or little auditory adaptation. Such repellent ultrasounds broadcast from the cylindrical omni-azimuth ultrasound emitters suppressed the intrusion of gravid females of pest moths into cultivation fields. Thus, egg numbers and plant damage by hatched larvae were drastically reduced, enabling farmers to substantially skip applications of chemical insecticides for controlling moth pests.

Insectivorous bats form mobile sensory networks to optimize prey localization: The case of the common noctule bat.

Animals that depend on ephemeral, patchily distributed prey often use public information to locate resource patches. The use of public information can lead to the aggregation of foragers at prey patches, a mechanism known as local enhancement. However, when ephemeral resources are distributed over large areas, foragers may also need to increase search efficiency, and thus apply social strategies when sampling the landscape. While sensory networks of visually oriented animals have already been confirmed, we lack an understanding of how acoustic eavesdropping adds to the formation of sensory networks. Here we radio-tracked a total of 81 aerial-hawking bats at very high spatiotemporal resolution during five sessions over 3 y, recording up to 19 individuals simultaneously. Analyses of interactive flight behavior provide conclusive evidence that bats form temporary mobile sensory networks by adjusting their movements to neighboring conspecifics while probing the airspace for prey. Complementary agent-based simulations confirmed that the observed movement patterns can lead to the formation of mobile sensory networks, and that bats located prey faster when networking than when relying only on local enhancement or searching solitarily. However, the benefit of networking diminished with decreasing group size. The combination of empirical analyses and simulations elucidates how animal groups use acoustic information to efficiently locate unpredictable and ephemeral food patches. Our results highlight that declining local populations of social foragers may thus suffer from Allee effects that increase the risk of collapses under global change scenarios, like insect decline and habitat degradation.

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.

Anti-bat ultrasound production in moths is globally and phylogenetically widespread.

Warning signals are well known in the visual system, but rare in other modalities. Some moths produce ultrasonic sounds to warn bats of noxious taste or to mimic unpalatable models. Here, we report results from a long-term study across the globe, assaying moth response to playback of bat echolocation. We tested 252 genera, spanning most families of large-bodied moths, and document anti-bat ultrasound production in 52 genera, with eight subfamily origins described. Based on acoustic analysis of ultrasonic emissions and palatability experiments with bats, it seems that acoustic warning and mimicry are the raison d'être for sound production in most moths. However, some moths use high-duty-cycle ultrasound capable of jamming bat sonar. In fact, we find preliminary evidence of independent origins of sonar jamming in at least six subfamilies. Palatability data indicate that jamming and warning are not mutually exclusive strategies. To explore the possible organization of anti-bat warning sounds into acoustic mimicry rings, we intensively studied a community of moths in Ecuador and, using machine-learning approaches, found five distinct acoustic clusters. While these data represent an early understanding of acoustic aposematism and mimicry across this megadiverse insect order, it is likely that ultrasonically signaling moths comprise one of the largest mimicry complexes on earth.

The Occipital Place Area Is Recruited for Echo-Acoustically Guided Navigation in Blind Human Echolocators.

In the investigation of the brain areas involved in human spatial navigation, the traditional focus has been on visually guided navigation in sighted people. Consequently, it is unclear whether the involved areas also support navigational abilities in other modalities. We explored this possibility by testing whether the occipital place area (OPA), a region associated with visual boundary-based navigation in sighted people, has a similar role in echo-acoustically guided navigation in blind human echolocators. We used fMRI to measure brain activity in 6 blind echolocation experts (EEs; five males, one female), 12 blind controls (BCs; six males, six females), and 14 sighted controls (SCs; eight males, six females) as they listened to prerecorded echolocation sounds that conveyed either a route taken through one of three maze environments, a scrambled (i.e., spatiotemporally incoherent) control sound, or a no-echo control sound. We found significantly greater activity in the OPA of EEs, but not the control groups, when they listened to the coherent route sounds relative to the scrambled sounds. This provides evidence that the OPA of the human navigation brain network is not strictly tied to the visual modality but can be recruited for nonvisual navigation. We also found that EEs, but not BCs or SCs, recruited early visual cortex for processing of echo acoustic information. This is consistent with the recent notion that the human brain is organized flexibly by task rather than by specific modalities.SIGNIFICANCE STATEMENT There has been much research on the brain areas involved in visually guided navigation, but we do not know whether the same or different brain regions are involved when blind people use a sense other than vision to navigate. In this study, we show that one part of the brain (occipital place area) known to play a specific role in visually guided navigation is also active in blind human echolocators when they use reflected sound to navigate their environment. This finding opens up new ways of understanding how people navigate, and informs our ability to provide rehabilitative support to people with vision loss.

Molecular adaptations underlying high-frequency hearing in the brain of CF bats species.

BACKGROUND: The majority of bat species have developed remarkable echolocation ability, especially for the laryngeally echolocating bats along with high-frequency hearing. Adaptive evolution has been widely detected for the cochleae in the laryngeally echolocating bats, however, limited understanding for the brain which is the central to echolocation signal processing in the auditory perception system, the laryngeally echolocating bats brain may also undergo adaptive changes. RESULT: In order to uncover the molecular adaptations related with high-frequency hearing in the brain of laryngeally echolocating bats, the genes expressed in the brain of Rhinolophus ferrumequinum (CF bat) and Myotis pilosus (FM bat) were both detected and also compared. A total of 346,891 genes were detected and the signal transduction mechanisms were annotated by the most abundant genes, followed by the transcription. In hence, there were 3,088 DEGs were found between the two bat brains, with 1,426 highly expressed in the brain of R. ferrumequinum, which were significantly enriched in the neuron and neurodevelopmental processes. Moreover, we found a key candidate hearing gene, ADCY1, playing an important role in the R. ferrumequinum brain and undergoing adaptive evolution in CF bats. CONCLUSIONS: Our study provides a new insight to the molecular bases of high-frequency hearing in two laryngeally echolocating bats brain and revealed different nervous system activities during auditory perception in the brain of CF bats.

Musculoskeletal morphogenesis supports the convergent evolution of bat laryngeal echolocation.

The order Chiroptera (bats) is the second largest group of mammals. One of the essential adaptations that have allowed bats to dominate the night skies is laryngeal echolocation, where bats emit ultrasonic pulses and listen to the returned echo to produce high-resolution 'images' of their surroundings. There are two possible scenarios for the evolutionary origin of laryngeal echolocation in bats: (1) a single origin in a common ancestor followed by the secondary loss in Pteropodidae, or (2) two convergent origins in Rhinolophoidea and Yangochiroptera. Although data from palaeontological, anatomical, developmental and genomic studies of auditory apparatuses exist, they remain inconclusive concerning the evolutionary origin of bat laryngeal echolocation. Here we compared musculoskeletal morphogenesis of the larynx in several chiropteran lineages and found distinct laryngeal modifications in two echolocating lineages, rhinolophoids and yangochiropterans. Our findings support the second scenario that rhinolophoids and yangochiropterans convergently evolved advanced laryngeal echolocation through anatomical modifications of the larynx for ultrasonic sound generation and refinement of the auditory apparatuses for more detailed sound perception.

Effects of insect pursuit on the Doppler shift compensation in a hipposiderid bat.

Doppler shift compensation (DSC) is a unique feature observed in certain species of echolocating bats and is hypothesized to be an adaptation to detecting fluttering insects. However, current research on DSC has primarily focused on bats that are not engaged in foraging activities. In this study, we investigated the DSC performance of Pratt's roundleaf bat, Hipposideros pratti, which was trained to pursue insects in various motion states within a laboratory setting. Our study yielded three main results. First, H. pratti demonstrated highly precise DSC during insect pursuit, aligning with previous findings of other flutter-detecting foragers during orientation or landing tasks. Second, we found that the motion state of the insect prey had little effect on the DSC performance of H. pratti. Third, we observed variations in the DSC performance of H. pratti throughout the course of insect pursuit. The bats exhibited the highest DSC performance during the phase of maximum flight speed but decreased performance during the phase of insect capture. These findings of high precision overall and the time-dependent performance of DSC during insect pursuit support the hypothesis that DSC is an adaptation to detecting fluttering insects.

Clutter resilience via auditory stream segregation in echolocating greater mouse-eared bats.

Bats use echolocation to navigate and hunt in darkness, and must in that process segregate target echoes from unwanted clutter echoes. Bats may do this by approaching a target at steep angles relative to the plane of the background, utilizing their directional transmission and receiving systems to minimize clutter from background objects, but it remains unknown how bats negotiate clutter that cannot be spatially avoided. Here, we tested the hypothesis that when movement no longer offers spatial release, echolocating bats mitigate clutter by calling at lower source levels and longer call intervals to ease auditory streaming. We trained five greater mouse-eared bats (Myotis myotis) to land on a spherical loudspeaker with two microphones attached. We used a phantom-echo setup, where the loudspeaker/target transmitted phantom clutter echoes by playing back the bats' own calls at time delays of 1, 3 and 5 ms with a virtual target strength 7 dB higher than the physical target. We show that the bats successfully landed on the target, irrespective of the clutter echo delays. Rather than decreasing their source levels, the bats used similar source level distributions in clutter and control trials. Similarly, the bats did not increase their call intervals, but instead used the same distribution of call intervals across control and clutter trials. These observations reject our hypothesis, leading us to conclude that bats display great resilience to clutter via short auditory integration times and acute auditory stream segregation rather than via biosonar adjustments.

Tiger beetles produce anti-bat ultrasound and are probable Batesian moth mimics.

Echolocating bats and their eared insect prey are in an acoustic evolutionary war. Moths produce anti-bat sounds that startle bat predators, signal noxiousness, mimic unpalatable models and jam bat sonar. Tiger beetles (Cicindelidae) also purportedly produce ultrasound in response to bat attacks. Here we tested 19 tiger beetle species from seven genera and showed that they produce anti-bat signals to playback of authentic bat echolocation. The dominant frequency of beetle sounds substantially overlaps the sonar calls of sympatric bats. As tiger beetles are known to produce defensive chemicals such as benzaldehyde and hydrogen cyanide, we hypothesized that tiger beetle sounds are acoustically advertising their unpalatability. We presented captive big brown bats (Eptesicus fuscus) with seven different tiger beetle species and found that 90 out of 94 beetles were completely consumed, indicating that these tiger beetle species are not aposematically signalling. Instead, we show that the primary temporal and spectral characteristics of beetle warning sounds overlap with sympatric unpalatable tiger moth (Arctinae) sounds and that tiger beetles are probably Batesian mimics of noxious moth models. We predict that many insect taxa produce anti-bat sounds and that the acoustic mimicry rings of the night sky are hyperdiverse.

Echolocating bats rely on an innate speed-of-sound reference.

Animals must encode fundamental physical relationships in their brains. A heron plunging its head underwater to skewer a fish must correct for light refraction, an archerfish shooting down an insect must "consider" gravity, and an echolocating bat that is attacking prey must account for the speed of sound in order to assess its distance. Do animals learn these relations or are they encoded innately and can they adjust them as adults are all open questions. We addressed this question by shifting the speed of sound and assessing the sensory behavior of a bat species that naturally experiences different speeds of sound. We found that both newborn pups and adults are unable to adjust to this shift, suggesting that the speed of sound is innately encoded in the bat brain. Moreover, our results suggest that bats encode the world in terms of time and do not translate time into distance. Our results shed light on the evolution of innate and flexible sensory perception.

Hearing sensitivity: An underlying mechanism for niche differentiation in gleaning bats.

Tropical ecosystems are known for high species diversity. Adaptations permitting niche differentiation enable species to coexist. Historically, research focused primarily on morphological and behavioral adaptations for foraging, roosting, and other basic ecological factors. Another important factor, however, is differences in sensory capabilities. So far, studies mainly have focused on the output of behavioral strategies of predators and their prey preference. Understanding the coexistence of different foraging strategies, however, requires understanding underlying cognitive and neural mechanisms. In this study, we investigate hearing in bats and how it shapes bat species coexistence. We present the hearing thresholds and echolocation calls of 12 different gleaning bats from the ecologically diverse Phyllostomid family. We measured their auditory brainstem responses to assess their hearing sensitivity. The audiograms of these species had similar overall shapes but differed substantially for frequencies below 9 kHz and in the frequency range of their echolocation calls. Our results suggest that differences among bats in hearing abilities contribute to the diversity in foraging strategies of gleaning bats. We argue that differences in auditory sensitivity could be important mechanisms shaping diversity in sensory niches and coexistence of species.