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The micromechanical mechanisms that underpin tuning and dynamic range compression in the mammalian inner ear are fundamental to hearing, but poorly understood. Here, we present new, high-resolution optical measurements that directly map sound-evoked vibrations on to anatomical structures in the intact, living gerbil cochlea. The largest vibrations occur in a tightly delineated hotspot centering near the interface between the Deiters’ and outer hair cells. Hotspot vibrations are less sharply tuned, but more nonlinear, than basilar membrane vibrations, and behave non-monotonically (exhibiting hyper-compression) near their characteristic frequency. Amplitude and phase differences between hotspot and basilar membrane responses depend on both frequency and measurement angle, and indicate that hotspot vibrations involve longitudinal motion. We hypothesize that structural coupling between the Deiters’ and outer hair cells funnels sound-evoked motion into the hotspot region, under the control of the outer hair cells, to optimize cochlear tuning and compression. Locations along the cochlea are tuned to different sound frequencies, and the individual vibration components are dynamically compressed before being converted to neural activity for further auditory processing. Here, the authors use optical coherence tomography to map sound-evoked vibrations and find a “hotspot” region with larger vibrations.

Investigating social and independent behavior structure in early life is critical for understanding development and brain maturation in social mammals. However, this investigation necessitates monitoring animals over weeks to months often with subsecond time resolution creating challenges for both lab studies focused on brief observation periods and field studies in which animal tracking can be imprecise. Here we used machine vision and two-week long continuous behavior recordings of families of gerbils, a highly social rodent, in large, undisturbed home environments to quantify the behavioral development of individual pups. We discovered that individual pups exhibited complex social behaviors from the first day they left the nest including a preference for interactions with siblings over parents. Critically, independent behaviors such as foraging for food and water emerged several days later, each with a stereotyped temporal trajectory. Analysis of individual animal development confirmed the quality of our tracking methods and the stability and distinctness of each behavioral measure. Our work supports a model in which early and sustained social interactions may be supportive of solitary exploration for physiological needs. This model suggests that understanding the development of behavioral independence as well as maturation of sensory and motor systems in social rodents such as gerbils may require integration of social behavioral knowledge earlier than typically considered.

Practice sharpens our perceptual judgments, a process known as perceptual learning. Although several brain regions and neural mechanisms have been proposed to support perceptual learning, formal tests of causality are lacking. Furthermore, the temporal relationship between neural and behavioral plasticity remains uncertain. To address these issues, we recorded the activity of auditory cortical neurons as gerbils trained on a sound detection task. Training led to improvements in cortical and behavioral sensitivity that were closely matched in terms of magnitude and time course. Surprisingly, the degree of neural improvement was behaviorally gated. During task performance, cortical improvements were large and predicted behavioral outcomes. In contrast, during nontask listening sessions, cortical improvements were weak and uncorrelated with perceptual performance. Targeted reduction of auditory cortical activity during training diminished perceptual learning while leaving psychometric performance largely unaffected. Collectively, our findings suggest that training facilitates perceptual learning by strengthening both bottom-up sensory encoding and top-down modulation of auditory cortex.

Rodents' ultrasonic vocalizations (USVs) provide useful information for assessing their social behaviors. Despite previous efforts in classifying subcategories of time-frequency patterns of USV syllables to study their functional relevance, methods for detecting vocal elements from continuously recorded data have remained sub-optimal. Here, we propose a novel procedure for detecting USV segments in continuous sound data containing background noise recorded during the observation of social behavior. The proposed procedure utilizes a stable version of the sound spectrogram and additional signal processing for better separation of vocal signals by reducing the variation of the background noise. Our procedure also provides precise time tracking of spectral peaks within each syllable. We demonstrated that this procedure can be applied to a variety of USVs obtained from several rodent species. Performance tests showed this method had greater accuracy in detecting USV syllables than conventional detection methods.

The brainstem’s lateral superior olive (LSO) is thought to be crucial for localizing high-frequency sounds by coding interaural sound level differences (ILD). Its neurons weigh contralateral inhibition against ipsilateral excitation, making their firing rate a function of the azimuthal position of a sound source. Since the very first in vivo recordings, LSO principal neurons have been reported to give sustained and temporally integrating ‘chopper’ responses to sustained sounds. Neurons with transient responses were observed but largely ignored and even considered a sign of pathology. Using the Mongolian gerbil as a model system, we have obtained the first in vivo patch clamp recordings from labeled LSO neurons and find that principal LSO neurons, the most numerous projection neurons of this nucleus, only respond at sound onset and show fast membrane features suggesting an importance for timing. These results provide a new framework to interpret previously puzzling features of this circuit.

There are two main factors explaining variation among species and the evolution of characters along phylogeny: adaptive change, including phenotypic and genetic responses to selective pressures, and phylogenetic inertia, or the resemblance between species due to shared phylogenetic history. Phenotype-habitat colour match, a classic Darwinian example of the evolution of camouflage (crypsis), offers the opportunity to test the importance of historical versus ecological mechanisms in shaping phenotypes among phylogenetically closely related taxa. To assess it, we investigated fur (phenotypic data) and habitat (remote sensing data) colourations, along with phylogenetic information, in the species-rich Gerbillus genus. Overall, we found a strong phenotype-habitat match, once the phylogenetic signal is taken into account. We found that camouflage has been acquired and lost repeatedly in the course of the evolutionary history of Gerbillus . Our results suggest that fur colouration and its covariation with habitat is a relatively labile character in mammals, potentially responding quickly to selection. Relatively unconstrained and substantial genetic basis, as well as structural and functional independence from other fitness traits of mammalian colouration might be responsible for that observation.

Auditory sensory outer hair cells are thought to amplify sound-induced basilar membrane vibration through a feedback mechanism to enhance hearing sensitivity. For optimal amplification, the outer hair cell-generated force must act on the basilar membrane at an appropriate time at every cycle. However, the temporal relationship between the outer hair cell-driven reticular lamina vibration and the basilar membrane vibration remains unclear. By measuring sub-nanometer vibrations directly from outer hair cells using a custom-built heterodyne low-coherence interferometer, we demonstrate in living gerbil cochleae that the reticular lamina vibration occurs after, not before, the basilar membrane vibration. Both tone- and click-induced responses indicate that the reticular lamina and basilar membrane vibrate in opposite directions at the cochlear base and they oscillate in phase near the best-frequency location. Our results suggest that outer hair cells enhance hearing sensitivity through a global hydromechanical mechanism, rather than through a local mechanical feedback as commonly supposed. What is the quietest sound the ear can detect? All sounds begin as vibrating air molecules, which enter the ear and cause the eardrum to vibrate. We can detect vibrations that move the eardrum by a distance of less than one picometer. That’s one thousandth of a nanometer, or about 100 times smaller than a hydrogen atom. But how does the ear achieve this level of sensitivity? Vibrations of the eardrum cause three small bones within the middle ear to vibrate. The vibrations then spread to the cochlea, a fluid-filled spiral structure in the inner ear. Tiny hair cells lining the cochlea move as a result of the vibrations. There are two types of hair cells: inner and outer. Outer hair cells amplify the vibrations. It is this amplification that enables us to detect such small movements of the eardrum. Inner hair cells then convert the amplified vibrations into electrical signals, which travel via the auditory nerve to the brain. The bases of outer hair cells are connected to a structure called the basilar membrane, while their tops are anchored to a structure called the reticular lamina. It was generally assumed that outer hair cells amplify vibrations of the basilar membrane via a local positive feedback mechanism that requires the hair cells to vibrate first. But by comparing the timing of reticular lamina and basilar membrane vibrations in gerbils, He et al. show that this is not the case. Outer hair cells vibrate after the basilar membrane, not before. This indicates that outer hair cells use a mechanism other than commonly assumed local feedback to amplify sounds. The results presented by He et al. change our understanding of how the cochlea works, and may help bioengineers to design better hearing aids and cochlea implants. Millions of patients worldwide who suffer from hearing loss may ultimately stand to benefit.

In nature, animal vocalizations can provide crucial information about identity, including kinship and hierarchy. However, lab-based vocal behavior is typically studied during brief interactions between animals with no prior social relationship, and under environmental conditions with limited ethological relevance. Here, we address this gap by establishing long-term acoustic recordings from Mongolian gerbil families, a core social group that uses an array of sonic and ultrasonic vocalizations. Three separate gerbil families were transferred to an enlarged environment and continuous 20-day audio recordings were obtained. Using a variational autoencoder (VAE) to quantify 583,237 vocalizations, we show that gerbils exhibit a more elaborate vocal repertoire than has been previously reported and that vocal repertoire usage differs significantly by family. By performing gaussian mixture model clustering on the VAE latent space, we show that families preferentially use characteristic sets of vocal clusters and that these usage preferences remain stable over weeks. Furthermore, gerbils displayed family-specific transitions between vocal clusters. Since gerbils live naturally as extended families in complex underground burrows that are adjacent to other families, these results suggest the presence of a vocal dialect which could be exploited by animals to represent kinship. These findings position the Mongolian gerbil as a compelling animal model to study the neural basis of vocal communication and demonstrates the potential for using unsupervised machine learning with uninterrupted acoustic recordings to gain insights into naturalistic animal behavior. Every time you speak, the sounds coming out of your mouth may carry more meaning that you may have intended; they may reveal, for example, which country, city or even neighborhood you may be coming from. Indeed, the vocal patterns that humans use to communicate differ from one population to the next, creating an array of languages, dialects and accents. Such diversity has also been identified in various social species across the animal kingdom. Naked mole rats, for instance, which live underground in complex societies, exhibit different ‘dialects’ depending on their group of origin. Yet studying the vocal patterns of animals has remained difficult, especially for species inhabiting burrows or other environments difficult to access. Aiming to bypass these limitations, Peterson et al. adopted a ‘naturalistic’ approach that allowed them to capture the vocal calls of three families of Mongolian gerbils living undisturbed in enclosures that mimic features of their natural environment. These animals spend their lives underground in tight-knit families, with multiple groups often being in close proximity. Researchers have speculated that individuals may rely on vocal cues to identify whether they are part of the same colony, as they are often too far from each other to rely on sight or smell. Over half a million vocalizations obtained continuously through the course of 20 days were analyzed using an artificial intelligence technique known as unsupervised machine learning. The analyses helped add new types of calls to the gerbil vocal repertoire, but also highlighted its complexity. In particular, they revealed that the animals could combine individual vocal elements into complex sequences. More importantly, this approach showed that gerbil families have vocal dialects that are stable across weeks, with each group displaying a preference for certain call types (i.e. words) and certain sequential patterns (i.e. phrases). These findings demonstrate the benefits of the approach developed by Peterson et al. for the study of animal vocalizations. Going forward, they also suggest that the Mongolian gerbil could be used as an animal model to study the neural basis of vocal communication.

Individuals colonizing new areas at expanding ranges encounter numerous and unpredictable stressors. Exposure to unfamiliar environments suggests that colonists would differ in stress levels from residents living in familiar conditions. Few empirical studies tested this hypothesis and produced mixed results, and the role of stress regulation in colonization remains unclear. Studies relating stress levels to colonization mainly use a geographical analysis comparing established colonist populations with source populations. We used faecal glucocorticoid metabolites (FGMs) to assess both spatial and temporal dynamics of stress levels in an expanding population of midday gerbils ( Meriones meridianus ). We demonstrated that adult males and females had higher FGM levels in newly emerged colonies, compared with the source population, but differed in the pattern of FGM dynamics post-foundation. In males, FGM levels sharply decreased in the second year after colony establishment. In females, FGM levels did not change with time and remained high despite the decreasing environmental unpredictability, exhibiting among-individual variation. Increased stress levels of colonist males damping with time post-colonization suggest they are flexible in responding to immediate changes in environmental uncertainty. On the contrary, high and stable over generations stress levels uncoupled from the changes in the environmental uncertainty in female colonists imply that they carry a relatively constant phenotype associated with the reactive coping strategy favouring colonization. We link sex differences in consistency and plasticity in stress regulation during colonization to the sex-specific life-history strategies.

Foraging animals have several tools for managing the risk of predation, and the foraging games between them and their predators. Among these, time allocation is foremost, followed by vigilance and apprehension. Together, their use influences a forager's time allocation and giving-up density (GUD) in depletable resource patches. We examined Allenby's gerbils (Gerbilus andersoni allenbyi) exploiting seed resource patches in a large vivarium under varying moon phases in the presence of a red fox (Vulpes vulpes). We measured time allocated to foraging patches electronically and GUDs from seeds left behind in resource patches. From these, we estimated handling times, attack rates and quitting harvest rates (QHRs). Gerbils displayed greater vigilance (lower attack rates) at brighter moon phases (full < wane < wax < new). Similarly, they displayed higher GUDs at brighter moon phases (wax > full > new > wane). Finally, gerbils displayed higher QHRs at new and waxing moon phases. Differences across moon phases not only reflect changing time allocation and vigilance, but changes in the state of the foragers and their marginal value of energy. Early in the lunar cycle, gerbils rely on vigilance and sacrifice state to avoid risk; later they defend state at the cost of increased time allocation; finally their state can recover as safe opportunities expand. In the predator–prey foraging game, foxes may contribute to these patterns of behaviours by modulating their own activity in response to the opportunities presented in each moon phase.