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Pitch discrimination performance of ferrets and humans on a go/no-go task.

Animal models are widely used to examine the neurophysiological basis of human pitch perception, and it is therefore important to understand the similarities and differences in pitch processing across species. Pitch discrimination performance is usually measured using two-alternative forced choice (2AFC) procedures in humans and go/no-go tasks in animals, potentially confounding human-to-animal comparisons. We have previously shown that pitch discrimination thresholds of ferrets on a 2AFC task are markedly poorer than those reported for go/no-go tasks in other non-human species (Walker et al., 2009). To better compare the pitch discrimination performance of ferret with other species, here we measure pitch change detection thresholds of ferrets and humans on a common, appetitive go/no-go task design. We found that ferrets pitch thresholds were ~10 times larger than that of humans on the go/no-go task, and were within the range of thresholds reported in other non-human species. Interestingly, ferrets thresholds were 100 times larger than human thresholds on a 2AFC pitch discrimination task using the same stimuli. These results emphasize that sensory discrimination thresholds can differ across tasks, particularly for non-human animals. Performance on our go/no-go task is likely to reflect different neurobiological processes than that on our 2AFC task, as the former required the subjects only to detect a pitch change while the latter required them to label the direction of the pitch change.\n\nABBREVIATIONS\n\nHIGHLIGHTSO_LIPitch discrimination thresholds of ferrets were 10 times larger than those of humans on a go/no-go task\nC_LIO_LIFerrets pitch thresholds are similar to those reported for a range of other mammals\nC_LIO_LIPitch thresholds of ferrets, but not humans, were drastically better on the go/no-go task than a 2AFC task using the same stimuli\nC_LI

animal behavior and cognition

An Automated Approach to the Quantitation of Vocalizations and Vocal Learning in the Songbird

Studies of learning mechanisms critically depend on the ability to accurately assess learning outcomes. This assessment can be impeded by the often complex, multidimensional nature of behavior. We present a novel, automated approach to evaluating imitative learning that is founded in information theory. Conceptually, our approach estimates the amount of information present in a reference behavior that is absent from the learned behavior. We validate our approach through examination of songbird vocalizations, complex learned behaviors the study of which has provided many insights into sensory-motor learning in general and vocal learning in particular. Historically, learning has been holistically assessed by human inspection or through comparison of specific song features selected by experimenters (e.g. fundamental frequency, spectral entropy). In contrast, our approach relies on statistical models that broadly capture the structure of each song, and then uses these models to estimate the amount of information in the reference song but absent from the learned song. We show that our information theoretic measure of song learning (contrast entropy) is well correlated with human evaluation of song learning. We then expand the analysis beyond song learning and show that contrast entropy also detects the typical song deterioration that occurs following deafening. More broadly, this approach potentially provides a framework for assessing learning across a broad range of similarly structured behaviors.\n\nAuthor SummaryMeasuring learning outcomes is a critical objective of research into the neural, molecular, and behavioral mechanisms that support learning. Demonstration that a given manipulation results in better or worse learning outcomes requires an accurate and consistent measurement of learning quality. However, many behaviors (e.g. speech, walking, and reading) are complex and multidimensional, confounding the assessment of learning. One behavior subject to such confounds, vocal learning in Estrildid finches, has emerged as a vital model for sensory motor learning broadly and human speech learning in particular. Here, we demonstrate a new approach, founded in information theory, to the assessment of learning for complex high dimensional behaviors. Conceptually, we determine the amount of information (across many dimensions) present in a reference behavior and then assess how much of that information is present in the resultant learned behavior. We show that this measure provides an accurate, holistic, and automated assessment of vocal learning in Estrildid finches. Potentially, this same approach could be deployed to assess shared content in any multidimensional data, behavioral or otherwise.

animal behavior and cognition

Chance, long tails, and inference: a non-Gaussian, Bayesian theory of vocal learning in songbirds

Traditional theories of sensorimotor learning posit that animals use sensory error signals to find the optimal motor command in the face of Gaussian sensory and motor noise. However, most such theories cannot explain common behavioral observations, for example that smaller sensory errors are more readily corrected than larger errors and that large abrupt (but not gradually introduced) errors lead to weak learning. Here we propose a new theory of sensorimotor learning that explains these observations. The theory posits that the animal learns an entire probability distribution of motor commands rather than trying to arrive at a single optimal command, and that learning arises via Bayesian inference when new sensory information becomes available. We test this theory using data from a songbird, the Bengalese finch, that is adapting the pitch (fundamental frequency) of its song following perturbations of auditory feedback using miniature headphones. We observe the distribution of the sung pitches to have long, non-Gaussian tails, which, within our theory, explains the observed dynamics of learning. Further, the theory makes surprising predictions about the dynamics of the shape of the pitch distribution, which we confirm experimentally.

animal behavior and cognition

Impaired social contacts with familiar anesthetized conspecific in CA3-restricted BDNF knockout mice

Familiarity is the vital characteristic conveyed by social cues to determine behaviors towards conspecific. Here we characterize social contacts to familiar vs unfamiliar male conspecific, anesthetized to eliminate inter-male aggression. During initial 10 min (phase-1), subjects contacted demonstrators vigorously regardless of familiarity. During subsequent 80 min (phase-2), however, they contacted more with familiar than unfamiliar conspecifics. Then, this test was applied on highly aggressive mice with hippocampal CA3-restricted BDNF knockout (KO), in which aggression may mask other behaviors. KO showed less preference to contacting familiar conspecific than wild type (WT) during phase-2 but no differences during phase-1. Among non-social behaviors, eating duration was shorter in the presence of familiar than unfamiliar conspecific in WT, but same in KO. Additionally, KO exhibited reduced pain sensitization. Altogether, these findings suggest that KO has deficits in circuits that process social cues from familiar conspecifics and pain and, possibly, underlie empathy-like behaviors.

animal behavior and cognition

Double-digest RAD sequencing outperforms microsatellite loci at assigning paternity and estimating relatedness: a proof of concept in a highly promiscuous bird

Information on genetic relationships among individuals is essential to many studies of the behavior and ecology of wild organisms. Parentage and relatedness assays based on large numbers of SNP loci hold substantial advantages over the microsatellite markers traditionally used for these purposes. We present a double-digest restriction site-associated DNA sequencing (ddRAD-seq) analysis pipeline that, as such, simultaneously achieves the SNP discovery and genotyping steps and which is optimized to return a statistically powerful set of SNP markers (typically 150-600 after stringent filtering) from large numbers of individuals (up to 240 per run). We explore the tradeoffs inherent in this approach through a set of experiments in a species with a complex social system, the variegated fairy-wren (Malurus lamberti), and further validate it in a phylogenetically broad set of other bird species. Through direct comparisons with a parallel dataset from a robust panel of highly variable microsatellite markers, we show that this ddRAD-seq approach results in substantially improved power to discriminate among potential relatives and considerably more precise estimates of relatedness coefficients. The pipeline is designed to be universally applicable to all bird species (and with minor modifications to many other taxa), to be cost- and time-efficient, and to be replicable across independent runs such that genotype data from different study periods can be combined and analyzed as field samples are accumulated.

animal behavior and cognition

Insects and incest: field evidence for dangerous liaisons in a parasitoid wasp

O_LISib mating avoidance is a pervasive behaviour, which likely evolves in species that sare subject to inbreeding depression. Laboratory studies have provided elegant demonstrations, but small-scale bioassays often minimize the costs associated with mate finding and mate-choice and may for this reason produce spurious findings.\nC_LIO_LIWe inferred the mating behaviour of the parasitoid wasp Venturia canescens from the genetic analyses of natural populations. We used V. canescens as a model organism because in this species, laboratory experiments have shown that sib mating yields a 25% decrease in fertile offspring, and congruently, sib mating is partially avoided.\nC_LIO_LIOur study consisted in genotyping 86 wild-caught males, 155 wild-caught-females and their 226 daughters at eighteen microsatellite loci. With these data, we were able to reconstruct the genotype of females mate and estimate the relatedness of each mating pairs.\nC_LIO_LIWe found that the effective rate of sib mating does not differ from the probability that sibs encounter one another at random, which suggest a sib mating tolerance in this species. However, complementary lab experiments confirmed that kin discrimination exist in this species, with related pairs having a lower mating latency.\nC_LIO_LIThese results suggest that V. canescens tolerate sib mating in the field despite kin discrimination, and therefore call into question the common beliefs on inbreeding depression in species with single-locus complementary sex determination. This inbreeding tolerance also opens up the question of the maintenance of the kin discrimination in this species.\nC_LI

animal behavior and cognition

Social learning strategies for matters of taste

Most choices people make are about \"matters of taste\" on which there is no universal, objective truth. Nevertheless, people can learn from the experiences of individuals with similar tastes who have already evaluated the available options--a potential harnessed by recommender systems. We mapped recommender system algorithms to models of human judgment and decision making about \"matters of fact\" and recast the latter as social learning strategies for \"matters of taste.\" Using computer simulations on a large-scale, empirical dataset, we studied how people could leverage the experiences of others to make better decisions. Our simulation showed that experienced individuals can benefit from relying mostly on the opinions of seemingly similar people; inexperienced individuals, in contrast, cannot reliably estimate similarity and are better off picking the mainstream option despite differences in taste. Crucially, the level of experience beyond which people should switch to similarity-heavy strategies varies substantially across individuals and depends on (i) how mainstream (or alternative) an individuals tastes are and (ii) the level of dispersion in taste similarity with the other people in the group.

animal behavior and cognition

Refresh my memory: Episodic memory reinstatements intrude on working memory maintenance

A fundamental question in memory research is how different forms of memory interact. Previous research has shown that people rely on working memory (WM) in short-term recognition tasks; a common view is that episodic memory (EM) only influences performance on these tasks when WM maintenance is disrupted. However, retrieval of memories from EM has been widely observed during brief periods of quiescence, raising the possibility that EM retrievals during maintenance-critically, before a response can be prepared-might affect short-term recognition memory performance even in the absence of distraction. We hypothesized that this influence would be mediated by the lingering presence of reactivated EM content in WM. We obtained support for this hypothesis in three experiments, showing that delay-period EM reactivation introduces incidentally-associated information (context) into WM, and that these retrieved associations negatively impact subsequent recognition, leading to substitution errors (Experiment 1) and slowing of accurate responses (Experiment 2). fMRI pattern analysis showed that slowing is mediated by the content of EM reinstatement (Experiment 3). These results expose a previously hidden influence of EM on WM, raising new questions about the adaptive nature of their interaction.

animal behavior and cognition

Navigating infection risk during oviposition and larval foraging in a holometabolous insect

Deciding where to eat and raise offspring carries important fitness consequences for all animals, especially if foraging, feeding and reproduction increase the risk of exposure to pathogens. In insects with complete metamorphosis, foraging occurs mainly during the larval stage, while oviposition decisions are taken by adult-stage females. Selection for infection avoidance behaviours may therefore be developmentally uncoupled. Using a combination of experimental infections and behavioural choice assays, here we tested if Drosophila melanogaster fruit flies avoid potentially infectious environments at distinct developmental stages. When given conspecific fly carcasses as a food source, larval-stage flies did not discriminate between carcasses that were clean or infected with the pathogenic Drosophila C Virus (DCV), even though scavenging was a viable route of DCV transmission. Adult females however, discriminated between different oviposition sites, laying more eggs near a clean rather than an infectious carcass if they were healthy; DCV-infected females did not discriminate between the two environments. While potentially risky, laying eggs near potentially infectious carcasses was always preferred to sites containing only fly medium. Our findings suggest that infection avoidance can play an important role in how mothers provision their offspring, and underline the need to consider infection avoidance behaviours at multiple life-stages.

animal behavior and cognition

Sugar intake elicits a small-scale search behavior in flies and honey bees that involves capabilities found in large-scale navigation

Social insects, particularly bees and ants, show exceptional large-scale navigational skills to find and carry back food to their nests. Honey bees further evolved a symbolic communication to direct nest mates to attractive food sources. Till now it is unclear how these capabilities evolved. Sixty years ago, Vincent Dethier demonstrated that a small-scale sugar-elicited search behavior identified in flies shows remarkable similarities with honey bee dance behavior. Those findings suggested that both behaviors are based on common mechanisms and are likely evolutionary related. We now present for the first time a detailed comparison of the sugar-elicited search behavior in Drosophila melanogaster and Apis mellifera. In both species, intake of sugar elicits a complex of searching responses. The most obvious response was an increase in turning frequency, but more importantly we found that flies and honey bees returned to the location of the sugar drop. They even returned to the food location when we prevented them from using visual and chemosensory cues indicating that this small scale local search involves path integration mechanisms. Finally, we show that visual landmarks presented in the vicinity of the sugar drop affected the search trajectory and in honey bees the sugar intake induced learning of landmarks. Together, our experiments indicate that the sugar-elicited local search exhibits two major behavioral capabilities of large-scale navigation, path integration and landmark orientation.\n\nSignificance StatementTo search for food social insects evolved sophisticated strategies of spatial orientation and large-scale navigation. We now show that even a small-scale local search behavior in solitary flies and social honey bees involves path integration and landmark learning two major mechanisms of large-scale navigation. We propose that in the future sugar-elicited local search can be used to identify neural circuits involved in navigation, path integration, and landmark learning.

animal behavior and cognition

Exploration and generalization in vast spaces

From foraging for food to learning complex games, many aspects of human behaviour can be framed as a search problem with a vast space of possible actions. Under finite search horizons, optimal solutions are generally unobtainable. Yet how do humans navigate vast problem spaces, which require intelligent exploration of unobserved actions? Using a variety of bandit tasks with up to 121 arms, we study how humans search for rewards under limited search horizons, where the spatial correlation of rewards (in both generated and natural environments) provides traction for generalization. Across a variety of diifferent probabilistic and heuristic models, we find evidence that Gaussian Process function learning--combined with an optimistic Upper Confidence Bound sampling strategy--provides a robust account of how people use generalization to guide search. Our modelling results and parameter estimates are recoverable, and can be used to simulate human-like performance, providing insights about human behaviour in complex environments.

animal behavior and cognition

Regressions Fit for Purpose: Models of Locust Phase State Must Not Conflate Morphology With Behaviour

Locusts are defined by their capacity to transform between two very distinct integrated phenotypes or phases in response to changes in population density: a solitarious phase, which occurs when densities are low, and a gregarious phase, which arises as a consequence of crowding and can form very large and economically damaging swarms. The two phases differ fundamentally in their behaviour, physiology and morphology. A large body of work on the mechanistic basis of behavioural phase transitions has relied on multivariate logistic regression (LR) models to estimate the probability of behavioural gregariousness from multiple behavioural variables. Martin-Blazquez and Bakkali (2017, Entomologia Experimentalis et Applicata 163, 9-25) have recently proposed standardised LR models for estimating an overall gregariousness level from a combination of behavioural and, unusually, morphometric variables. Here I develop a detailed argument to demonstrate that the premise of such an overall gregariousness level is fundamentally flawed. Since locust phase transformations intrinsically entail a decoupling of behaviour and morphology, phase state cannot meaningfully be conflated onto a single axis. LR models that do so are therefore of very limited value for any analysis of phase transitions. I furthermore show why behavioural predictor variables should not be adjusted by measures of body size that themselves differ between phases. I discuss the models fitted by Martin-Blazquez and Bakkali (2017) to highlight potential pitfalls in statistical methodology that must be avoided when applying LR to the analysis of behavioural phase state. Finally, I reject the idea that standardised models provide a valid shortcut to estimating phase state across different developmental stages, strains or species. The points addressed here are pertinent to any research on transitions between complex phenotypes and behavioural syndromes.

animal behavior and cognition

DEET as a feeding deterrent

The insect repellent N,N-diethyl-3-methylbenzamide (DEET), is a multimodal compound that acts as a spatial repellent as well as an irritant (contact repellent), thus being perceived by the insects olfactory and gustatory systems as an odorant and a tastant, respectively. Soon after DEET was developed, almost 6 decades ago, it was reported that it reduced mosquito feeding on blood mixed with this repellent. It is now known that the mosquito proboscis senses contact repellents with the tips (labella) of the labium, which remain in direct contact with the outer layers of the skin, while the stylets, including the feeding deterrent sensor (labrum), penetrate the skin. We designed a behavioral assay that allowed us to tease apart contact repellency from feeding deterrence. First, we demonstrate here that when DEET was mixed with blood and covered by Parafilm(R) layers, it did not leak to the outer surface. In our assays, the mean number of landings and duration of contacts with surfaces covering blood mixed with DEET or blood plus solvent (dimethyl sulfoxide) did not differ significantly. The feeding times, however, were significantly different. When blood was mixed either with 0.1 or 1% DEET, female southern house mosquitoes spent significantly less time feeding than the time spent feeding on blood mixed only with the solvent. By contrast, there were no significant differences in the mean times of feeding on blood containing 1% picaridin and blood plus solvent. Like DEET, the contact repellent and insecticide, permethrin, caused a significant reduction in feeding time. We, therefore, concluded, that in this context, DEET and permethrin act as feeding deterrents.

animal behavior and cognition

Forecasting crowd dynamics through coarse-grained data analysis

Understanding and predicting the collective behaviour of crowds is essential to improve the efficiency of pedestrian flows in urban areas and minimize the risks of accidents at mass events. We advocate for the development of a & \"crowd forecasting system\"whereby real-time observations of crowds are coupled to fast and reliable models to produce rapid predictions of the crowd movement and eventually help crowd managers choose between tailored optimization strategies. Here, we propose a Bi-directional Macroscopic (BM) model as the core of such a system. Its key input is the fundamental diagram for bi-directional flows, i.e. the relation between the pedestrian fluxes and densities. We design and run a laboratory experiments involving a total of 119 participants walking in opposite directions in a circular corridor and show that the model is able to accurately capture the experimental data in a typical crowd forecasting situation. Finally, we propose a simple segregation strategy for enhancing the traffic efficiency, and use the BM model to determine the conditions under which this strategy would be beneficial. The BM model, therefore, could serve as a building block to develop on the fly prediction of crowd movements and help deploying real-time crowd optimization strategies.

animal behavior and cognition

Comparing colours using visual models

Lay SummaryAn outstanding challenge for the study of colour traits is how best to use \"colour spaces\" to represent their visual perception, particularly when asking questions of colour-difference (e.g. the (dis)similarity of males and females, mimics and models, or sister species, to a given viewer). We use simulations to show that existing methods fail to statistically and biologically estimate the separation of groups in colour space, and we suggest a flexible, robust, alternative that avoids those pitfalls.\n\nAbstractColour in nature presents a striking dimension of variation, though understanding its function and evolution largely depends on our ability to capture the perspective of relevant viewers. This goal has been radically advanced by the development and widespread adoption of colour spaces, which allow for the viewer-subjective estimation of colour appearance. Most studies of colour in camouflage, aposematism, sexual selection, and other signalling contexts draw on these models, with the shared analytical objective of estimating how similar (or dissimilar) colour samples are to a given viewer. We summarise popular approaches for estimating the separation of samples in colour space, and use a simulation-based approach to test their efficacy with common data structures. We show that these methods largely fail to estimate the separation of colour samples by neglecting (i) the statistical distribution and within-group variation of the data, and/or (ii) the discriminability of groups relative to the observers visual capabilities. Instead, we formalize the two questions that must be answered to establish both the statistical presence and theoretical magnitude of colour differences, and propose a two-step, permutation-based approach that achieves this goal. Unlike previous methods, our suggested approach accounts for the multidimensional nature of visual model data, and is robust against common colour-data features such as heterogeneity and outliers. We demonstrate the pitfalls of current methods and the flexibility of our suggested framework using an example from the literature, with recommendations for future inquiry.

animal behavior and cognition

The evolution of thermoregulatory nesting behaviour in Peromyscus mice

Structures built by animals, such as nests, often can be considered extended phenotypes that facilitate the study of animal behaviour. For rodents, nest building is both an important form of behavioural thermoregulation and a critical component of parental care. Changes in nest structure or the prioritization of nesting behaviour are therefore likely to have consequences for survival and reproduction, and both biotic and abiotic environmental factors are likely to influence the adaptive value of such differences. Here we first develop a novel assay to investigate interspecific variation in the nesting behaviour of deer mice (genus Peromyscus). Using this assay, we find that, while there is some variation in the complexity of the nests built by Peromyscus mice, differences in the latency to begin nest construction are more striking. Four of the seven taxa examined here build nests within an hour of being given nesting material, but this latency to nest is not related to ultimate differences in nest structure, suggesting that the ability to nest is relatively conserved within the genus, but species differ in their prioritization of nesting behaviour. We also find that latency to nest is not correlated with body size, climate, or the construction of burrows that create microclimates. However, the four taxa with short nesting latencies all have monogamous mating systems, suggesting that differences in nesting latency may be related to social environment. This detailed characterization of nesting behaviour within the genus provides an important foundation for future studies of the genetic and neurobiological mechanisms that contribute to the evolution of behaviour.

animal behavior and cognition

Widespread utilization of passive energy recapture in swimming medusae

Recently, it has been shown that some medusae are capable of swimming very efficiently, i.e.; with a low cost of transport, and that this is in part due to passive energy recapture (PER) which occurs during bell relaxation. We compared the swimming kinematics among a diverse array of medusae, varying in taxonomy, morphology and propulsive and foraging modes, in order to evaluate the prevalence of PER in medusae. We found that while PER is commonly observed among taxa, the magnitude of the contribution to overall swimming varied greatly. The ability of medusae to utilize PER was not related to morphology and swimming performance but was controlled by their swimming kinematics. Utilizing PER required the medusae to pause after bell expansion and individuals could modulate their PER by changing their pause duration. Passive energy recapture can greatly enhance swimming efficiency but there appear to be trade-offs associated with utilizing PER.

animal behavior and cognition

The role of stimulus similarity on the summation effect in human causal learning

Several contemporary models of associative learning anticipate that the higher responding to a compound of two cues separately trained with a common outcome than to each of the cues alone -a summation effect-is modulated by the similarity between the cues forming the compound. Here, we explored this hypothesis in a series of causal learning experiments with humans. Participants were presented with two visual cues that separately predicted a common outcome and later asked for the outcome predicted by the compound of the two cues. Importantly, the cues similarity was varied between groups through changes in shape, spatial position, color, configuration and rotation. In variance with the predictions of these models, we observed similar and strong levels of summation in both groups across all manipulations of similarity (Experiments 1-5). The summation effect was significantly reduced by manipulations intended to impact assumptions about the causal independence of the cues forming the compound, but this reduction was independent of stimulus similarity (Experiment 6). These results are problematic for similarity-based models and can be more readily explained by rational approaches to causal learning.

animal behavior and cognition