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bioRxiv2017

Imitation Predicts Social Favor in Adolescent Rhesus Macaques (Macaca mulatta)

ObjectivesImitation is a highly conserved component of animal behavior with multifaceted connections to sociality across taxa. One intriguing consequence of imitation in primates is that it promotes positive social feedback from the imitated toward the imitator. This suggests that imitation in primates may facilitate positive social interactions, but few studies have tracked imitation in socially housed primates. Here, we designed a novel ethogram to characterize imitation between conspecifics, to better understand whether imitation is associated with affiliation between primates in a semi-natural setting.\n\nMaterials and MethodsIn this study, 15 juvenile rhesus macaques (Macaca mulatta) were observed at the California National Primate Research Center. Using focal sampling, frequencies of imitative events (e.g. following, postural mimicry, etc.) by the focal were observed over a course of 12 weeks. In separate observations, focal social behavior (e.g. aggression, play, etc.) was also observed.\n\nResultsSubjects that exhibited higher degrees of imitation were not necessarily more prosocial, but, consistent with our hypothesis, they received significantly more play overtures from social partners (p<.01). In addition, imitation rates generally decrease with age.\n\nConclusionsTogether, these results suggest that imitation is associated with receiving positive social behavior in a complex, semi-natural setting in primates, and that imitation may be more common in adolescence as opposed to adulthood. These preliminary results in a small sample set represent an important step in characterizing imitation in context of social interactions during development. Tracking these behaviors over time will elucidate whether imitation is directly recruiting these positive social interactions, as has been demonstrated in captivity.

animal behavior and cognition↗

bioRxiv2017

Opponent assessment and conflict resolution through mutual motor coordination

Most animals fight by repeating complex stereotypic behaviors, yet the internal structure of these behaviors has rarely been dissected in detail. We characterized the internal structure of fighting behaviors by developing a machine learning pipeline that measures and classifies the behavior of individual unmarked animals on a sub-second timescale. This allowed us to quantify several previously hidden features of zebrafish fighting strategies. We found strong correlations between the velocity of the attacker and the defender indicating a dynamic matching of approach and avoidance efforts consistent with the cumulative assessment model of aggression. While velocity matching was ubiquitous, the spatial dynamics of attacks showed phase-specific differences. Contest phase attacks were characterized by a paradoxical side-ways attraction of the retreating animal towards the attacker suggesting that the defender combines avoidance maneuvers with display maneuvers. Post-resolution attacks lacked display-like features and the the defender was avoidance-focused. From the perspective of the winner, game theory modeling further suggested that highly energetically costly post resolution attacks occurred because the winner was trying to increase its relative dominance over the loser. Overall, the rich structure of zebrafish motor coordination during fighting indicates a greater complexity and layering of strategies than has previously been recognized.

animal behavior and cognition↗

bioRxiv2017

Characterization of a Novel Model of Overuse-Induced Calcific Achilles Tendinopathy in Mice: Contralateral Tendinopathy Following Unilateral Tenotomy

ObjectiveTo develop a simple but reproducible overuse induced animal model of Achilles tendinopathy in mice for better understanding the underlying mechanism and prevention of calcific Achilles tendinopathy.\n\nMethods80 C57/B6 mice (8-9 weeks old) were employed and randomly divided into control group and experimental group. Unilateral Achilles tenotomy was performed on the right hindlimb of experiment group. After 12 weeks, the onset of Achilles tedinopathy in the contralateral Achilles tendon was determined by radiological assessment, histological analysis, electron microscopy observation and biomechanical test.\n\nResultsThe onset of calcific Achilles tendinopathy in contralateral Achilles tendon was confirmed after 12 weeks unilateral tenotomy. The contralateral Achilles tendon of experimental group was characterized as hypercelluarity, neovascularization and fused collagen fiber disarrangement, compared to the control group. Importantly, intratendon endochondral ossification and calcaneus deformity was featured in contralateral Achilles tendon. Additionally, poor biomechanical properties in the contralateral Achilles tendon revealed the incidence of Achilles tedinopathy.\n\nConclusionWe hereby introduce a novel simple but reproducible spontaneous contralateral calcific Achilles tendinopathy model in mice, which represents the overuse conditions during the tendinopathy development in human-beings. It should be a useful tool to further study the underlying pathogenesis of calcific Achilles tendinopathy.

animal behavior and cognition↗

bioRxiv2017

Variation in context dependent foraging behavior across pollinators

Pollinator foraging behavior has direct consequences for plant reproduction and has been implicated in driving floral trait evolution. Exploring the degree to which pollinators exhibit flexibility in foraging behavior will add to a mechanistic understanding of how pollinators can impact selection on plant traits. Although plants have evolved suites of floral traits to attract pollinators, flower color is a particularly important aspect of the floral display. Some pollinators show strong innate color preference, but many pollinators display flexibility in preference due to learning associations between rewards and color, or due to variable perception of color in different environments or plant communities. This study examines the flexibility in flower color preference of two groups of native butterfly pollinators under natural field conditions. Our study reveals that pipevine swallowtails and skippers, the predominate pollinators of the two native Texas Phlox species, display distinct patterns of color preferences across different contexts. Pipevine swallowtails exhibit highly flexible color preferences and likely utilize other floral traits to make foraging decisions. In contrast, skippers have consistent color preferences and likely use flower color as a primary cue for foraging. As a result of this variation in color preference flexibility, the two pollinator groups impose concordant selection on flower color in some contexts but discordant selection in other contexts. This variability could have profound implications for how flower traits respond to pollinator-mediated selection. Our findings suggest that studying dynamics of behavior in natural field conditions is important for understanding plant-pollinator interactions.

animal behavior and cognition↗

bioRxiv2017

A Real-Time Double Error Correction Model of Associative Learning

In this paper a formal model of associative learning is presented which incorporates representational and computational mechanisms that, as a coherent corpus, empower it to make accurate predictions of a wide variety of phenomena that so far have eluded a unified account in learning theory. In particular, the Double Error Dynamic Asymptote (DDA) model introduces: 1) a fully-connected network architecture in which stimuli are represented as temporally clustered elements that associate to each other, so that elements of one cluster engender activity on other clusters, which naturally implements neutral stimuli associations and mediated learning; 2) a predictor error term within the traditional error correction rule (the double error), which reduces the rate of learning for expected predictors; 3) a revaluation associability rate that operates on the assumption that the outcome predictiveness is tracked over time so that prolonged uncertainty is learned, reducing the levels of attention to initially surprising outcomes; and critically 4) a biologically plausible variable asymptote, which encapsulates the principle of Hebbian learning, leading to stronger associations for similar levels of cluster activity. The outputs of a set of simulations of the DDA model are presented along with empirical results from the literature. Finally, the predictive scope of the model is discussed.

animal behavior and cognition↗

bioRxiv2017

Learning the structure of the world: The adaptive nature of state-space and action representations in multi-stage decision-making

State-space and action representations form the building blocks of decision-making processes in the brain; states map external cues to the current situation of the agent whereas actions provide the set of motor commands from which the agent can choose to achieve specific goals. Although these factors differ across environments, it is not currently known whether or how accurately state and action representations are acquired by the agent because previous experiments have typically provided this information a priori through instruction or pre-training. Here we show that, in the absence of such a priori knowledge, state and action representations adapt to reflect the structure of the world. We used a sequential decision-making task in rats in which they were required to pass through multiple states before reaching the goal, and for which the number of states and how they map onto external cues were not known a priori. We found that, early in training, animals selected actions as if the task was not sequential and outcomes were the immediate consequence of the most proximal action. During the course of training, however, rats recovered the true structure of the environment and made decisions based on the expanded state-space, reflecting the multiple stages of the task. We found a similar pattern with actions; early in training animals only considered the execution of single actions whereas, after training, they created useful action sequences that expanded the set of available actions. We conclude that the profile of choices shows a gradual shift from simple representations of actions and states to more complex structures compatible with the structure of the world.

animal behavior and cognition↗

bioRxiv2017

Fluid mediated self-organization of ventilation in honeybee nests

European honey bees (Apis mellifera) live in large congested nest cavities with a single opening that limits passive ventilation. These nests are actively ventilated by individual bees which fan their wings at the nest entrance when the local air temperature exceeds a threshold. Here we show that colonies with relatively large nest entrances use an emergent ventilation strategy where fanning bees self-organize to form fanning groups, separating regions of continuous inflow and outflow. The observed spatio-temporal patterns correlate the air velocity and air temperature along the entrances to the distribution of fanning bees. A mathematical model that couples these variables to known fanning behavior of individuals recapitulates their collective dynamics. Additionally, the model makes predictions about the temporal stability of the fanning group as a function of the temperature difference between the environment and the nest. Consistent with these predictions, we observe that the fanning groups drift, cling to the entrance boundaries, break-up and reform as the ambient temperature varies over a period of days. Overall, our study shows how honeybees use flow-mediated communication to self-organize into a steady-state in fluctuating environments.

animal behavior and cognition↗

bioRxiv2017

Postural sway during single-legged standing is dependent on the body position assumption strategy and supports the stability and mobility trade-off hypothesis

Studies that would address the problem of balance in the context of either the preceding or subsequent movement are scarce. We would like to propose the inverse relationship between stability and mobility as a general principle and that depending on the preceding action the postural sway characteristics in quiet standing would significantly differ. Thirteen female ballet school students were examined. Their mean age was: 15.1{+/-}0.95 years and the total of about 2500 (5th school grade) and 4200 (6th school grade) hours of dance training. The force plate was used to register ground reaction forces and moments. During the 30s trials subjects were to assume the Passe position in gait initiation (G-I) and gait termination (G-T) task condition. The following parameters were analyzed after restabilisation point estimation: the range of COP position, standard deviation of COP position, mean velocity in both planes and mean resultant velocity. The results showed significant differences between the G-I and G-T tasks in postural sway characteristics and confirmed our hypothesis. The practical implication of our study is the way of preparation to test position (PTTP) strategy might be as important as the measurement itself in the posture study protocols.

animal behavior and cognition↗

bioRxiv2017

Male parental investment reflects the level of partner contributions and brood value in tree swallows

Biparental care presents an interesting case of cooperation and conflict between unrelated individuals. Several models have been proposed to explain how parents should respond to changes in each others parental care to maximize their own fitness, predicting no change, partial compensation, or matching effort as a response. Here, we present an experiment in tree swallows (Tachycineta bicolor) in which we increased the parental care of females by presenting them, but not their mates, with additional nestling begging calls using automated playbacks. We performed this experiment in two populations differing in future breeding opportunities and thus the intensity of conflict over current parental care. We found that in response to a temporary increase in female parental effort, males in the northern population with lower sexual conflict matched the increased effort, whereas males in the southern population did not. We also found that increases in parental care during playbacks were driven by the females (i.e., females initiated the increased effort and their mates followed them) in the northern population but not the southern population. These results support the idea that with incomplete information about the brood value and need, cues or signals from the partner might become important in coordinating parental care.

animal behavior and cognition↗

bioRxiv2017

A synergistic transcriptional regulation of olfactory genes derives complex behavioral responses in the mosquito Anopheles culicifacies

Decoding the molecular basis of host seeking and blood feeding behavioral evolution/adaptation in the adult female mosquito may provide an opportunity to design new molecular strategy to disrupt human-mosquito interactions. However, despite the great progress in the field of mosquito olfaction and chemo-detection, little is known that how the sex-specific specialization of the olfactory system enables adult female mosquitoes to derive and manage complex blood feeding associated behavioral responses. A comprehensive RNAseq analysis of prior and post blood meal olfactory system of An. culicifacies mosquito revealed that a minor but unique change in the nature and regulation of key olfactory genes play a pivotal role in managing diverse behavioral responses. Age dependent transcriptional profiling demonstrated that adult female mosquitos chemosensory system gradually learned and matured to drive the host-seeking and blood feeding behavior at the age of 5-6 days. A zeitgeber time scale expression analysis of Odorant Binding Proteins (OBPs) unravels unique association with a late evening to midnight peak biting time. Blood meal-induced switching of unique sets of OBP genes and Odorant Receptors (ORs) expression coincides with the change in the innate physiological status of the mosquitoes. Blood meal follows up experiments provide enough evidence that how a synergistic and concurrent action of OBPs-ORs may drive prior and post blood meal complex behavioral events. Finally, tissue-specific gene expression analysis and molecular modelling predicted two uncharacterized novel sensory appendages proteins (SAP-1 & SAP2) unique to An. culicifacies mosquito and may play a central role in the host-seeking behavior.\n\nSignificanceEvolution and adaptation of blood feeding behavior not only favored the reproductive success of adult female mosquito but also make them an important disease vectors. Immediately after emergence, an environmental exposure may favor the broadly tuned olfactory system of mosquitoes to derive complex behavioral responses. But, how these olfactory derived genetic factors manage female specific pre and post blood meal associated complex behavioral responses are not well known. We unraveled synergistic actions of olfactory factors governs an innate to prime learning strategy to facilitate rapid blood meal acquisition and downstream behavioral activities. A species-specific transcriptional profiling and an in-silico analysis predict novel sensory appendages protein, as a unique target to design disorientation strategy against the mosquito Anopheles culicifacies.

animal behavior and cognition↗

bioRxiv2018

Information synergy: adding unambiguous quality information rescues social information use in ants

Animals have access to many alternative information sources when making decisions, such as private information (e.g. memory) and social information. Social insects make extensive use of social information. However, when intentional social information (e.g. pheromone trails in ants) conflicts with private information (e.g. route memories), insects often follow their private information. Why is this? We propose that an asymmetry in the type of information provided by these two information sources drives the neglect of social information: In ants, workers with certain information about the quality of a food source (memory) ignore valuable social information (pheromone trails) because the pheromone trails encode only a very ambiguous measure of food quality. This leads to a testable hypothesis: the addition of unambiguous quality information should rescue social information following. To test this, we trained ants to a poor quality (0.25M sucrose) food source, and then provided an alternative path along with either 1) no information, 2) a pheromone trail, 3) a 0.2l 1.5M sucrose droplet, providing unambiguous quality information, or 4) both a trail and a droplet. When either no or only one information source was provided (1-3), most ants (60-75%) continued following their own memory. However, the addition of unambiguous quality information (4) rescued trail following: when both a trail and a droplet were provided, 75% of ants followed the trail. In further experiments, we show that quality information gleaned from direct contact with fed nestmates produced similar effects. Using florescence microscopy, we demonstrate that food (and information) flows from fed workers to outgoing foragers, explaining the frequent contacts on trails. We propose that the type of information an information source can convey, and its ambiguity, is a strong driver of which source of information is attended to.

animal behavior and cognition↗

bioRxiv2017

Variational Treatment of Trial-by-Trial Drift-Diffusion Models of Behaviour

The Full Drift Diffusion Model (DDM) is challenging to fit to behavioural data. Precision of the fits are usually poor for some if not all parameters, and computationally expensive to obtain. Moreover, inference at the trial level for each and every parameters, threshold included, has so far been considered as impossible. Most approaches rely on strong assumptions about the model structure, such as selection of the parameters that are subject to trial-to-trial variability or prior distribution of these parameters, that usually lack precise mathematical or empirical justifications. The fact that, in most versions of the DDM, the sequence of participants choices are considered as independent and identically distributed (i.i.d.), has been mainly overlooked so far. Our contribution to the field is threefold: first, we introduce Variational Bayes as a method to fit the full DDM. Second, we relax the i.i.d. assumption, and propose a data-driven algorithm based on a Recurrent Auto-Encoder, that estimates the local posterior probability of the DDM parameters at each trial based on the sequence of parameters and data preceding the data. Finally, we show that inference at the trial level can be achieved efficiently for each and every parameter of the DDM, threshold included. This data-driven approach is highly generic and self-contained, in the sense that no external input (e.g. regressors or physiological measure) is necessary to fit the data. Using simulations and real-world examples, we show that this method outperforms by several order of magnitude the i.i.d.-based ones, either Markov Chain Monte Carlo or i.i.d.-VB.

animal behavior and cognition↗

bioRxiv2017

The study of animal behaviour as a physical science

Behaviour is the ultimate output of an animals nervous system and choosing the right action at the right time can be critical for survival. The study of the organisation of behaviour in its natural context, ethology, has historically been a primarily qualitative science. A quantitative theory of behaviour would advance research in neuroscience as well as ecology and evolution. However, animal posture typically has many degrees of freedom and behavioural dynamics vary on timescales ranging from milliseconds to years, presenting both technical and conceptual challenges. Here we review 1) advances in imaging and computer vision that are making it possible to capture increasingly complete records of animal motion and 2) new approaches to understanding the resulting behavioural data sets. With the right analytical approaches, these data are allowing researchers to revisit longstanding questions about the structure and organisation of animal behaviour and to put unifying principles on a quantitative footing. Contributions from both experimentalists and theorists are leading to the emergence of a physics of behaviour and the prospect of discovering laws and developing theories with broad applicability. We believe that there now exists an opportunity to develop theories of behaviour which can be tested using these data sets leading to a deeper understanding of how and why animals behave.

animal behavior and cognition↗

bioRxiv2017

Recurrent Neural Networks with Interpretable Cells Predict and Classify Worm Behaviour

An important goal in behaviour analytics is to connect disease state or genome variation with observable differences in behaviour. Despite advances in sensor technology and imaging, informative behaviour quantification remains challenging. The nematode worm C. elegans provides a unique opportunity to test analysis approaches because of its small size, compact nervous system, and the availability of large databases of videos of freely behaving animals with known genetic differences. Despite its relative simplicity, there are still no reports of generative models that can capture essential differences between even well-described mutant strains. Here we show that a multilayer recurrent neural network (RNN) can produce diverse behaviours that are difficult to distinguish from real worms behaviour and that some of the artificial neurons in the RNN are interpretable and correlate with observable features such as body curvature, speed, and reversals. Although the RNN is not trained to perform classification, we find that artificial neuron responses provide features that perform well in worm strain classification.

animal behavior and cognition↗

bioRxiv2017

Testing the parasite mass burden effect on host behaviour alteration in the Schistocephalus-stickleback system

Many parasites with complex life cycles modify their intermediate hosts behaviour, which has been proposed to increase transmission to their definitive host. This behavioural change could result from the parasite actively manipulating its host, but could also be explained by a mechanical effect, where the parasites physical presence affects host behaviour. We created an artificial internal parasite using silicone injections in the body cavity to test this mechanical effect hypothesis. We used the Schistocephalus solidus - threespine stickleback (Gasterosteus aculeatus) system, as this cestode can reach up to 92% of its fish host mass. Our results suggest that the mass burden brought by this macroparasite alone is not sufficient to cause behavioural changes in its host. Furthermore, our results show that wall-hugging (thigmotaxis), a measure of anxiety in vertebrates, is significantly reduced in Schistocephalus-infected sticklebacks, unveiling a new altered component of behaviour that may result from manipulation by this macroparasite.

animal behavior and cognition↗

bioRxiv2017

Experimental evidence that female rhesus macaques (Macaca mulatta) perceive variation in male facial masculinity

Among many primate species, face shape is sexually dimorphic, and male facial masculinity has been proposed to influence female mate choice and male-male competition by signalling competitive ability. However, whether conspecifics pay attention to facial masculinity has only been assessed in humans. In a study of free-ranging rhesus macaques, Macaca mulatta, we used a two-alternative look-time experiment to test whether females perceive male facial masculinity. We presented 107 females with pairs of images of male faces - one with a more masculine shape and one more feminine - and recorded their looking behaviour. Females looked at the masculine face longer than at the feminine face in more trials than predicted by chance. Although there was no overall difference in average look-time between masculine and feminine faces across all trials, females looked significantly longer at masculine faces in a subset of trials for which the within-pair difference in masculinity was most pronounced. Additionally, the proportion of time subjects looked toward the masculine face increased as the within-pair difference in masculinity increased. This study provides evidence that female macaques perceive variation in male facial shape, a necessary condition for intersexual selection to operate on such a trait. It also highlights the potential impact of perceptual thresholds on look-time experiments.

animal behavior and cognition↗

bioRxiv2017

Cyclic nature of the REM-like state in the cuttlefish Sepia officinalis

Sleep is a state of immobility characterized by three key criteria: an increased threshold of arousal, rapid reversal to an alert state, and evidence of homeostatic \"rebound sleep\" in which there is an increase of time spent in this quiescent state following sleep deprivation. Common European cuttlefish, Sepia officinalis, show states of quiescence during which they meet the last two of these three criteria, yet also show spontaneous bursts of arm and eye movements that accompany rapid changes in chromatophore patterns in the skin. Here we report that this rapid-eye-movement (REM)-like state is cyclic in nature. Iterations of the REM-like state last 2.42 {+/-} 0.22 min ({+/-}SE) and alternate with 34.01 {+/-} 1.49 min of the quiescent sleep-like state. These states alternate for durations lasting 176.89 {+/-} 36.71 min. We found clear evidence that this REM-like state (i) occurs in animals younger than previously reported; (ii) follows an ultradian pattern; (iii) includes intermittent dynamic chromatophore patterning, representing fragments of normal patterning seen in the waking state for a wide range of signaling and camouflage; and (iv) shows variability in the intensity of expression of these skin patterns between and within individuals. These data suggest that cephalopods, which are molluscs with an elaborate brain and complex behavior, possess a sleep-like state that resembles behaviorally the vertebrate REM sleep state, although the exact nature and mechanism of this form of sleep may differ from that of vertebrates.

animal behavior and cognition↗

bioRxiv2017

Paramecium Learning: New Insights and Modifications

Learning is a fundamental process in neural systems. However, microorganisms without a nervous system have been shown to possess learning abilities. Specifically, Paramecium caudatum has been previously reported to be able to form associations between lighting conditions and cathodal shocks in its swimming medium. We have replicated previous reports on this phenomenon and tested the predictions of a molecular pathway hypothesis on paramecium learning. Our results indicated that in contrast to the previous reports, paramecium can only associate higher light intensities with cathodal stimulation and it cannot associate lower light intensities with cathodal stimulation. These results found to be in line with the predictions of the previously proposed model for the molecular mechanisms of learning in paramecium which depends on the effects of cathodal shocks on the interplay between Cyclic adenosine monophosphate concentration and phototactic behavior of paramecium.

animal behavior and cognition↗