Bi-stability in cooperative transport by ants in the presence of obstacles.

To cooperatively carry large food items to the nest, individual ants conform their efforts and coordinate their motion. Throughout this expedition, collective motion is driven both by internal interactions between the carrying ants and a response to newly arrived informed ants that orient the cargo towards the nest. During the transport process, the carrying group must overcome obstacles that block their path to the nest. Here, we investigate the dynamics of cooperative transport, when the motion of the ants is frustrated by a linear obstacle that obstructs the motion of the cargo. The obstacle contains a narrow opening that serves as the only available passage to the nest, and through which single ants can pass but not with the cargo. We provide an analytical model for the ant-cargo system in the constrained environment that predicts a bi-stable dynamic behavior between an oscillatory mode of motion along the obstacle and a convergent mode of motion near the opening. Using both experiments and simulations, we show how for small cargo sizes, the system exhibits spontaneous transitions between these two modes of motion due to fluctuations in the applied force on the cargo. The bi-stability provides two possible problem solving strategies for overcoming the obstacle, either by attempting to pass through the opening, or take large excursions to circumvent the obstacle.

Emergent oscillations assist obstacle negotiation during ant cooperative transport.

Collective motion by animal groups is affected by internal interactions, external constraints, and the influx of information. A quantitative understanding of how these different factors give rise to different modes of collective motion is, at present, lacking. Here, we study how ants that cooperatively transport a large food item react to an obstacle blocking their path. Combining experiments with a statistical physics model of mechanically coupled active agents, we show that the constraint induces a deterministic collective oscillatory mode that facilitates obstacle circumvention. We provide direct experimental evidence, backed by theory, that this motion is an emergent group effect that does not require any behavioral changes at the individual level. We trace these relaxation oscillations to the interplay between two forces; informed ants pull the load toward the nest whereas uninformed ants contribute to the motion's persistence along the tangential direction. The model's predictions that oscillations appear above a critical system size, that the group can spontaneously transition into its ordered phase, and that the system can exhibit complete rotations are all verified experimentally. We expect that similar oscillatory modes emerge in collective motion scenarios where the structure of the environment imposes conflicts between individually held information and the group's tendency for cohesiveness.

Emergent exploration via novelty management.

When encountering novel environments, animals perform complex yet structured exploratory behaviors. Despite their typical structuring, the principles underlying exploratory patterns are still not sufficiently understood. Here we analyzed exploratory behavioral data from two modalities: whisking and locomotion in rats and mice. We found that these rodents maximized novelty signal-to-noise ratio during each exploration episode, where novelty is defined as the accumulated information gain. We further found that these rodents maximized novelty during outbound exploration, used novelty-triggered withdrawal-like retreat behavior, and explored the environment in a novelty-descending sequence. We applied a hierarchical curiosity model, which incorporates these principles, to both modalities. We show that the model captures the major components of exploratory behavior in multiple timescales: single excursions, exploratory episodes, and developmental timeline. The model predicted that novelty is managed across exploratory modalities. Using a novel experimental setup in which mice encountered a novel object for the first time in their life, we tested and validated this prediction. Further predictions, related to the development of brain circuitry, are described. This study demonstrates that rodents select exploratory actions according to a novelty management framework and suggests a plausible mechanism by which mammalian exploration primitives can be learned during development and integrated in adult exploration of complex environments.

Measuring behavior of animal models: faults and remedies.

Widely used behavioral assays need re-evaluation and validation against their intended use. We focus here on measures of chronic anxiety in mouse models and posit that widely used assays such as the open-field test are performed at the wrong time, for inadequate durations and using inappropriate mouse strains. We propose that behavioral assays be screened for usefulness on the basis of their replicability across laboratories.

Learning and control of exploration primitives.

Animals explore novel environments in a cautious manner, exhibiting alternation between curiosity-driven behavior and retreats. We present a detailed formal framework for exploration behavior, which generates behavior that maintains a constant level of novelty. Similar to other types of complex behaviors, the resulting exploratory behavior is composed of exploration motor primitives. These primitives can be learned during a developmental period, wherein the agent experiences repeated interactions with environments that share common traits, thus allowing transference of motor learning to novel environments. The emergence of exploration motor primitives is the result of reinforcement learning in which information gain serves as intrinsic reward. Furthermore, actors and critics are local and ego-centric, thus enabling transference to other environments. Novelty control, i.e. the principle which governs the maintenance of constant novelty, is implemented by a central action-selection mechanism, which switches between the emergent exploration primitives and a retreat policy, based on the currently-experienced novelty. The framework has only a few parameters, wherein time-scales, learning rates and thresholds are adaptive, and can thus be easily applied to many scenarios. We implement it by modeling the rodent's whisking system and show that it can explain characteristic observed behaviors. A detailed discussion of the framework's merits and flaws, as compared to other related models, concludes the paper.

Quantifying the buildup in extent and complexity of free exploration in mice.

To obtain a perspective on an animal's own functional world, we study its behavior in situations that allow the animal to regulate the growth rate of its behavior and provide us with the opportunity to quantify its moment-by-moment developmental dynamics. Thus, we are able to show that mouse exploratory behavior consists of sequences of repeated motion: iterative processes that increase in extent and complexity, whose presumed function is a systematic active management of input acquired during the exploration of a novel environment. We use this study to demonstrate our approach to quantifying behavior: targeting aspects of behavior that are shown to be actively managed by the animal, and using measures that are discriminative across strains and treatments and replicable across laboratories.

High mirror symmetry in mouse exploratory behavior.

The physicality of the world in which the animal acts-its anatomical structure, physiology, perception, emotional states, and cognitive capabilities-determines the boundaries of the behavioral space within which the animal can operate. Behavior, therefore, can be considered as the subspace that remains after secluding all actions that are not available to the animal due to constraints. The very signature of being a certain creature is reflected in these limitations that shape its behavior. A major goal of ethology is to expose those constraints that carve the intricate structure of animal behavior and reveal both uniqueness and commonalities between animals within and across taxa. Exploratory behavior in an empty arena seems to be stochastic; nevertheless, it does not mean that the moving animal is a random walker. In this study, we present how, by adding constraints to the animal's locomotion, one can gradually retain the 'mousiness' that characterizes the behaving mouse. We then introduce a novel phenomenon of high mirror symmetry along the locomotion of mice, which highlights another constraint that further compresses the complex nature of exploratory behavior in these animals. We link these findings to a known neural mechanism that could explain this phenomenon. Finally, we suggest our novel finding and derived methods to be used in the search for commonalities in the motion trajectories of various organisms across taxa.

Freedom of movement and the stability of its unfolding in free exploration of mice.

Exploration is a central component of human and animal behavior that has been studied in rodents for almost a century. The measures used by neuroscientists to characterize full-blown exploration are limited in exposing the dynamics of the exploratory process, leaving the morphogenesis of its structure and meaning hidden. By unfettering exploration from constraints imposed by hunger, thirst, coercion, and the confines of small cage and short session, using advanced computational tools, we reveal its meaning in the operational world of the mouse. Exploration consists of reiterated roundtrips of increasing amplitude and freedom, involving an increase in the number of independent dimensions along which the mouse moves (macro degrees of freedom). This measurable gradient can serve as a standard reference scale for the developmental dynamics of some aspects of the mouse's emotional-cognitive state and for the study of the interface between behavior and the neurophysiologic and genetic processes mediating it.

Ant collective cognition allows for efficient navigation through disordered environments.

The cognitive abilities of biological organisms only make sense in the context of their environment. Here, we study longhorn crazy ant collective navigation skills within the context of a semi-natural, randomized environment. Mapping this biological setting into the 'Ant-in-a-Labyrinth' framework which studies physical transport through disordered media allows us to formulate precise links between the statistics of environmental challenges and the ants' collective navigation abilities. We show that, in this environment, the ants use their numbers to collectively extend their sensing range. Although this extension is moderate, it nevertheless allows for extremely fast traversal times that overshadow known physical solutions to the 'Ant-in-a-Labyrinth' problem. To explain this large payoff, we use percolation theory and prove that whenever the labyrinth is solvable, a logarithmically small sensing range suffices for extreme speedup. Overall, our work demonstrates the potential advantages of group living and collective cognition in increasing a species' habitable range.

A locally-blazed ant trail achieves efficient collective navigation despite limited information.

Any organism faces sensory and cognitive limitations which may result in maladaptive decisions. Such limitations are prominent in the context of groups where the relevant information at the individual level may not coincide with collective requirements. Here, we study the navigational decisions exhibited by Paratrechina longicornis ants as they cooperatively transport a large food item. These decisions hinge on the perception of individuals which often restricts them from providing the group with reliable directional information. We find that, to achieve efficient navigation despite partial and even misleading information, these ants employ a locally-blazed trail. This trail significantly deviates from the classical notion of an ant trail: First, instead of systematically marking the full path, ants mark short segments originating at the load. Second, the carrying team constantly loses the guiding trail. We experimentally and theoretically show that the locally-blazed trail optimally and robustly exploits useful knowledge while avoiding the pitfalls of misleading information.

Ant groups optimally amplify the effect of transiently informed individuals.

To cooperatively transport a large load, it is important that carriers conform in their efforts and align their forces. A downside of behavioural conformism is that it may decrease the group's responsiveness to external information. Combining experiment and theory, we show how ants optimize collective transport. On the single-ant scale, optimization stems from decision rules that balance individuality and compliance. Macroscopically, these rules poise the system at the transition between random walk and ballistic motion where the collective response to the steering of a single informed ant is maximized. We relate this peak in response to the divergence of susceptibility at a phase transition. Our theoretical models predict that the ant-load system can be transitioned through the critical point of this mesoscopic system by varying its size; we present experiments supporting these predictions. Our findings show that efficient group-level processes can arise from transient amplification of individual-based knowledge.

Short and long term measures of anxiety exhibit opposite results.

Animal models of human diseases of the central nervous system, generalized anxiety disorder included, are essential for the study of the brain-behavior interface and obligatory for drug development; yet, these models fail to yield new insights and efficacious drugs. By increasing testing duration hundredfold and arena size tenfold, and comparing the behavior of the common animal model to that of wild mice, we raise concerns that chronic anxiety might have been measured at the wrong time, for the wrong duration, and in the wrong animal. Furthermore, the mice start the experimental session with a short period of transient adaptation to the novel environment (habituation period) and a long period reflecting the respective trait of the mice. Using common measures of anxiety reveals that mice exhibit opposite results during these periods suggesting that chronic anxiety should be measured during the post-habituation period. We recommend tools for measuring the transient period, and provide suggestions for characterizing the post habituation period.

Validation of the dimensionality emergence assay for the measurement of innate anxiety in laboratory mice.

The open field test is a common tool to measure innate anxiety in rodents. In the usual configuration of this test the animal is forced to explore the open arena and its behavior includes both anxiety and non-anxiety responses. However, the open arena is generally small and allows only limited expression of exploratory behavior. The recently developed dimensionality emergence assay in which an animal is housed in a home cage with free access to a large circular arena elicits graded exploration and promises to serve as a more ethological test of anxiety. Here we examined the predictive validity of this assay for anxiety-related measures in mice. First, we compared their behavior in the presence or absence of access to the home cage and found that mice with access to the home cage exhibited a gradual build-up in exploration of the arena while those without did not. Then we identified behavioral measures that responded to treatment with the anxiolytic drug diazepam. Diazepam altered several classical measures of innate anxiety, such as distance traveled and thigmotaxis, but also led to a dose-dependent acceleration of the build-up as reflected in a significantly reduced latency to attain several exploratory landmarks. Finally, we tested the utility of the dimensionality emergence assay in assessing alterations in innate anxiety reported in mice carrying a knockout allele for the serotonin 1A receptor (Htr1a). Our findings support the validity of the dimensionality emergence assay as a method to extract an expanded repertoire of behavioral measures for the assessment of anxiety in laboratory mice.

Ten ways to improve the quality of descriptions of whole-animal movement.

The demand for replicability of behavioral results across laboratories is viewed as a burden in behavior genetics. We demonstrate how it can become an asset offering a quantitative criterion that guides the design of better ways to describe behavior. Passing the high benchmark dictated by the replicability demand requires less stressful and less restraining experimental setups, less noisy data, individually customized cutoff points between the building blocks of movement, and less variable yet discriminative dynamic representations that would capture more faithfully the nature of the behavior, unmasking similarities and differences and revealing novel animal-centered measures. Here we review ten tools that enhance replicability without compromising discrimination. While we demonstrate the usefulness of these tools in the context of inbred mouse exploratory behavior they can readily be used in any study involving a high-resolution analysis of spatial behavior. Viewing replicability as a design concept and using the ten methodological improvements may prove useful in many fields not necessarily related to spatial behavior.