How honey bees make fast and accurate decisions.

Honey bee ecology demands they make both rapid and accurate assessments of which flowers are most likely to offer them nectar or pollen. To understand the mechanisms of honey bee decision-making, we examined their speed and accuracy of both flower acceptance and rejection decisions. We used a controlled flight arena that varied both the likelihood of a stimulus offering reward and punishment and the quality of evidence for stimuli. We found that the sophistication of honey bee decision-making rivalled that reported for primates. Their decisions were sensitive to both the quality and reliability of evidence. Acceptance responses had higher accuracy than rejection responses and were more sensitive to changes in available evidence and reward likelihood. Fast acceptances were more likely to be correct than slower acceptances; a phenomenon also seen in primates and indicative that the evidence threshold for a decision changes dynamically with sampling time. To investigate the minimally sufficient circuitry required for these decision-making capacities, we developed a novel model of decision-making. Our model can be mapped to known pathways in the insect brain and is neurobiologically plausible. Our model proposes a system for robust autonomous decision-making with potential application in robotics.

In the natural world, decision-making processes are often intricate and challenging. Animals frequently encounter situations where they have limited information on which to rely to guide them, yet even simple choices can have far-reaching impact on survival. Each time a bee sets out to collect nectar, for example, it must use tiny variations in colour or odour to decide which flower it should land on and explore. Each 'mistake' is costly, wasting energy and exposing the insect to potential dangers. To learn how to refine their choices through trial-and-error, bees only have at their disposal a brain the size of a sesame seed, which contains fewer than a million neurons. And yet, they excel at this task, being both quick and accurate. The underlying mechanisms which drive these remarkable decision-making capabilities remain unclear. In response, MaBouDi et al. aimed to explore which strategies honeybees adopt to forage so effectively, and the neural systems that may underlie them. To do so, they released the insects in a 'field' containing artificial flowers in five different colours. The bees were trained to link each colour with a certain likelihood of receiving either a sugary liquid (reward) or bitter quinine (punishment); they were then tested on this knowledge. Next, MaBouDi et al. recorded how the bees would navigate a 'reduced evidence' test, where the colour of the flowers were ambiguous and consisted in various blends of the originally rewarded or punished colours; and a 'reduced reward likelihood' test, where the sweet recompense was offered less often than before. Response times and accuracy rates revealed a complex pattern of decision-making processes. How quickly the insects made a choice, and the types of mistakes they made (such as deciding to explore a non-rewarded flower, or to ignore a rewarded one) were dependent on both the quality of the evidence and the certainty of the reward. Such sophistication and subtlety in decision-making is comparable to that of primates. Next, MaBouDi et al. developed a computational model which could faithfully replicate the pattern of decisions exhibited by the bees, while also being plausible biologically. This approach offered insights into how a small brain could execute such complex choices 'on the fly', and the type of neural circuits that would be required. Going forward, this knowledge could be harnessed to design more efficient decision-making algorithms for artificial systems, and in particular for autonomous robotics.

Asynchrony rescues statistically optimal group decisions from information cascades through emergent leaders.

It is usually assumed that information cascades are most likely to occur when an early but incorrect opinion spreads through the group. Here, we analyse models of confidence-sharing in groups and reveal the opposite result: simple but plausible models of naive-Bayesian decision-making exhibit information cascades when group decisions are synchronous; however, when group decisions are asynchronous, the early decisions reached by Bayesian decision-makers tend to be correct and dominate the group consensus dynamics. Thus early decisions actually rescue the group from making errors, rather than contribute to it. We explore the likely realism of our assumed decision-making rule with reference to the evolution of mechanisms for aggregating social information, and known psychological and neuroscientific mechanisms.

Magnitude-sensitive reaction times reveal non-linear time costs in multi-alternative decision-making.

Optimality analysis of value-based decisions in binary and multi-alternative choice settings predicts that reaction times should be sensitive only to differences in stimulus magnitudes, but not to overall absolute stimulus magnitude. Yet experimental work in the binary case has shown magnitude sensitive reaction times, and theory shows that this can be explained by switching from linear to multiplicative time costs, but also by nonlinear subjective utility. Thus disentangling explanations for observed magnitude sensitive reaction times is difficult. Here for the first time we extend the theoretical analysis of geometric time-discounting to ternary choices, and present novel experimental evidence for magnitude-sensitivity in such decisions, in both humans and slime moulds. We consider the optimal policies for all possible combinations of linear and geometric time costs, and linear and nonlinear utility; interestingly, geometric discounting emerges as the predominant explanation for magnitude sensitivity.

Negative feedback may suppress variation to improve collective foraging performance.

Social insect colonies use negative as well as positive feedback signals to regulate foraging behaviour. In ants and bees individual foragers have been observed to use negative pheromones or mechano-auditory signals to indicate that forage sources are not ideal, for example being unrewarded, crowded, or dangerous. Here we propose an additional function for negative feedback signals during foraging, variance reduction. We show that while on average populations will converge to desired distributions over forage patches both with and without negative feedback signals, in small populations negative feedback reduces variation around the target distribution compared to the use of positive feedback alone. Our results are independent of the nature of the target distribution, providing it can be achieved by foragers collecting only local information. Since robustness is a key aim for biological systems, and deviation from target foraging distributions may be costly, we argue that this could be a further important and hitherto overlooked reason that negative feedback signals are used by foraging social insects.

Magnitude-sensitivity: rethinking decision-making.

Magnitude-sensitivity refers to the result that performance in decision-making, across domains and organisms, is affected by the total value of the possible alternatives. This simple result offers a window into fundamental issues in decision-making and has led to a reconsideration of ecological decision-making, prominent computational models of decision-making, and optimal decision-making. Moreover, magnitude-sensitivity has inspired the design of new robotic systems that exploit natural solutions and apply optimal decision-making policies. In this article, we review the key theoretical and empirical results about magnitude-sensitivity and highlight the importance that this phenomenon has for the understanding of decision-making. Furthermore, we discuss open questions and ideas for future research.

Approximations of algorithmic and structural complexity validate cognitive-behavioral experimental results.

Being able to objectively characterize the intrinsic complexity of behavioral patterns resulting from human or animal decisions is fundamental for deconvolving cognition and designing autonomous artificial intelligence systems. Yet complexity is difficult in practice, particularly when strings are short. By numerically approximating algorithmic (Kolmogorov) complexity (K), we establish an objective tool to characterize behavioral complexity. Next, we approximate structural (Bennett's Logical Depth) complexity (LD) to assess the amount of computation required for generating a behavioral string. We apply our toolbox to three landmark studies of animal behavior of increasing sophistication and degree of environmental influence, including studies of foraging communication by ants, flight patterns of fruit flies, and tactical deception and competition (e.g., predator-prey) strategies. We find that ants harness the environmental condition in their internal decision process, modulating their behavioral complexity accordingly. Our analysis of flight (fruit flies) invalidated the common hypothesis that animals navigating in an environment devoid of stimuli adopt a random strategy. Fruit flies exposed to a featureless environment deviated the most from Levy flight, suggesting an algorithmic bias in their attempt to devise a useful (navigation) strategy. Similarly, a logical depth analysis of rats revealed that the structural complexity of the rat always ends up matching the structural complexity of the competitor, with the rats' behavior simulating algorithmic randomness. Finally, we discuss how experiments on how humans perceive randomness suggest the existence of an algorithmic bias in our reasoning and decision processes, in line with our analysis of the animal experiments. This contrasts with the view of the mind as performing faulty computations when presented with randomized items. In summary, our formal toolbox objectively characterizes external constraints on putative models of the "internal" decision process in humans and animals.

Memory and communication efficient algorithm for decentralized counting of nodes in networks.

Node counting on a graph is subject to some fundamental theoretical limitations, yet a solution to such problems is necessary in many applications of graph theory to real-world systems, such as collective robotics and distributed sensor networks. Thus several stochastic and naïve deterministic algorithms for distributed graph size estimation or calculation have been provided. Here we present a deterministic and distributed algorithm that allows every node of a connected graph to determine the graph size in finite time, if an upper bound on the graph size is provided. The algorithm consists in the iterative aggregation of information in local hubs which then broadcast it throughout the whole graph. The proposed node-counting algorithm is on average more efficient in terms of node memory and communication cost than its previous deterministic counterpart for node counting, and appears comparable or more efficient in terms of average-case time complexity. As well as node counting, the algorithm is more broadly applicable to problems such as summation over graphs, quorum sensing, and spontaneous hierarchy creation.

Better tired than lost: Turtle ant trail networks favor coherence over short edges.

Creating a routing backbone is a fundamental problem in both biology and engineering. The routing backbone of the trail networks of arboreal turtle ants (Cephalotes goniodontus) connects many nests and food sources using trail pheromone deposited by ants as they walk. Unlike species that forage on the ground, the trail networks of arboreal ants are constrained by the vegetation. We examined what objectives the trail networks meet by comparing the observed ant trail networks with networks of random, hypothetical trail networks in the same surrounding vegetation and with trails optimized for four objectives: minimizing path length, minimizing average edge length, minimizing number of nodes, and minimizing opportunities to get lost. The ants' trails minimized path length by minimizing the number of nodes traversed rather than choosing short edges. In addition, the ants' trails reduced the opportunity for ants to get lost at each node, favoring nodes with 3D configurations most likely to be reinforced by pheromone. Thus, rather than finding the shortest edges, turtle ant trail networks take advantage of natural variation in the environment to favor coherence, keeping the ants together on the trails.

When less is more: Robot swarms adapt better to changes with constrained communication.

To effectively perform collective monitoring of dynamic environments, a robot swarm needs to adapt to changes by processing the latest information and discarding outdated beliefs. We show that in a swarm composed of robots relying on local sensing, adaptation is better achieved if the robots have a shorter rather than longer communication range. This result is in contrast with the widespread belief that more communication links always improve the information exchange on a network. We tasked robots with reaching agreement on the best option currently available in their operating environment. We propose a variety of behaviors composed of reactive rules to process environmental and social information. Our study focuses on simple behaviors based on the voter model-a well-known minimal protocol to regulate social interactions-that can be implemented in minimalistic machines. Although different from each other, all behaviors confirm the general result: The ability of the swarm to adapt improves when robots have fewer communication links. The average number of links per robot reduces when the individual communication range or the robot density decreases. The analysis of the swarm dynamics via mean-field models suggests that our results generalize to other systems based on the voter model. Model predictions are confirmed by results of multiagent simulations and experiments with 50 Kilobot robots. Limiting the communication to a local neighborhood is a cheap decentralized solution to allow robot swarms to adapt to previously unknown information that is locally observed by a minority of the robots.

Non-numerical strategies used by bees to solve numerical cognition tasks.

We examined how bees solve a visual discrimination task with stimuli commonly used in numerical cognition studies. Bees performed well on the task, but additional tests showed that they had learned continuous (non-numerical) cues. A network model using biologically plausible visual feature filtering and a simple associative rule was capable of learning the task using only continuous cues inherent in the training stimuli, with no numerical processing. This model was also able to reproduce behaviours that have been considered in other studies indicative of numerical cognition. Our results support the idea that a sense of magnitude may be more primitive and basic than a sense of number. Our findings highlight how problematic inadvertent continuous cues can be for studies of numerical cognition. This remains a deep issue within the field that requires increased vigilance and cleverness from the experimenter. We suggest ways of better assessing numerical cognition in non-speaking animals, including assessing the use of all alternative cues in one test, using cross-modal cues, analysing behavioural responses to detect underlying strategies, and finding the neural substrate.

Honeybees solve a multi-comparison ranking task by probability matching.

Honeybees forage on diverse flowers which vary in the amount and type of rewards they offer, and bees are challenged with maximizing the resources they gather for their colony. That bees are effective foragers is clear, but how bees solve this type of complex multi-choice task is unknown. Here, we set bees a five-comparison choice task in which five colours differed in their probability of offering reward and punishment. The colours were ranked such that high ranked colours were more likely to offer reward, and the ranking was unambiguous. Bees' choices in unrewarded tests matched their individual experiences of reward and punishment of each colour, indicating bees solved this test not by comparing or ranking colours but by basing their colour choices on their history of reinforcement for each colour. Computational modelling suggests a structure like the honeybee mushroom body with reinforcement-related plasticity at both input and output can be sufficient for this cognitive strategy. We discuss how probability matching enables effective choices to be made without a need to compare any stimuli directly, and the use and limitations of this simple cognitive strategy for foraging animals.

Multiscale Modelling Tool: Mathematical modelling of collective behaviour without the maths.

Collective behaviour is of fundamental importance in the life sciences, where it appears at levels of biological complexity from single cells to superorganisms, in demography and the social sciences, where it describes the behaviour of populations, and in the physical and engineering sciences, where it describes physical phenomena and can be used to design distributed systems. Reasoning about collective behaviour is inherently difficult, as the non-linear interactions between individuals give rise to complex emergent dynamics. Mathematical techniques have been developed to analyse systematically collective behaviour in such systems, yet these frequently require extensive formal training and technical ability to apply. Even for those with the requisite training and ability, analysis using these techniques can be laborious, time-consuming and error-prone. Together these difficulties raise a barrier-to-entry for practitioners wishing to analyse models of collective behaviour. However, rigorous modelling of collective behaviour is required to make progress in understanding and applying it. Here we present an accessible tool which aims to automate the process of modelling and analysing collective behaviour, as far as possible. We focus our attention on the general class of systems described by reaction kinetics, involving interactions between components that change state as a result, as these are easily understood and extracted from data by natural, physical and social scientists, and correspond to algorithms for component-level controllers in engineering applications. By providing simple automated access to advanced mathematical techniques from statistical physics, nonlinear dynamical systems analysis, and computational simulation, we hope to advance standards in modelling collective behaviour. At the same time, by providing expert users with access to the results of automated analyses, sophisticated investigations that could take significant effort are substantially facilitated. Our tool can be accessed online without installing software, uses a simple programmatic interface, and provides interactive graphical plots for users to develop understanding of their models.

Inhibition and Excitation Shape Activity Selection: Effect of Oscillations in a Decision-Making Circuit.

Decision making is a complex task, and its underlying mechanisms that regulate behavior, such as the implementation of the coupling between physiological states and neural networks, are hard to decipher. To gain more insight into neural computations underlying ongoing binary decision-making tasks, we consider a neural circuit that guides the feeding behavior of a hypothetical animal making dietary choices. We adopt an inhibition motif from neural network theory and propose a dynamical system characterized by nonlinear feedback, which links mechanism (the implementation of the neural circuit and its coupling to the animal's nutritional state) and function (improving behavioral performance). A central inhibitory unit influences evidence-integrating excitatory units, which in our terms correspond to motivations competing for selection. We determine the parameter regime where the animal exhibits improved decision-making behavior and explain different behavioral outcomes by making the link between accessible states of the nonlinear neural circuit model and decision-making performance. We find that for given deficits in nutritional items, the variation of inhibition strength and ratio of excitation and inhibition strengths in the decision circuit allows the animal to enter an oscillatory phase that describes its internal motivational state. Our findings indicate that this oscillatory phase may improve the overall performance of the animal in an ongoing foraging task and underpin the importance of an integrated functional and mechanistic study of animal activity selection.

Abstract concept learning in a simple neural network inspired by the insect brain.

The capacity to learn abstract concepts such as 'sameness' and 'difference' is considered a higher-order cognitive function, typically thought to be dependent on top-down neocortical processing. It is therefore surprising that honey bees apparantly have this capacity. Here we report a model of the structures of the honey bee brain that can learn sameness and difference, as well as a range of complex and simple associative learning tasks. Our model is constrained by the known connections and properties of the mushroom body, including the protocerebral tract, and provides a good fit to the learning rates and performances of real bees in all tasks, including learning sameness and difference. The model proposes a novel mechanism for learning the abstract concepts of 'sameness' and 'difference' that is compatible with the insect brain, and is not dependent on top-down or executive control processing.

Evidence for the speed-value trade-off: human and monkey decision making is magnitude sensitive.

Complex natural systems from brains to bee swarms have evolved to make adaptive multifactorial decisions. Recent theoretical and empirical work suggests that many evolved systems may take advantage of common motifs across multiple domains. We are particularly interested in value sensitivity (i.e., sensitivity to the magnitude or intensity of the stimuli or reward under consideration) as a mechanism to resolve deadlocks adaptively. This mechanism favours long-term reward maximization over accuracy in a simple manner, because it avoids costly delays associated with ambivalence between similar options; speed-value trade-offs have been proposed to be evolutionarily advantageous for many kinds of decision. A key prediction of the value-sensitivity hypothesis is that choices between equally-valued options will proceed faster when the options have a high value than when they have a low value. However, value-sensitivity is not part of idealised choice models such as diffusion to bound. Here we examine two different choice behaviours in two different species, perceptual decisions in humans and economic choices in rhesus monkeys, to test this hypothesis. We observe the same value sensitivity in both human perceptual decisions and monkey value-based decisions. These results endorse the idea that neural decision systems make use of the same basic principle of value-sensitivity in order to resolve costly deadlocks and thus improve long-term reward intake.

Psychophysical Laws and the Superorganism.

Through theoretical analysis, we show how a superorganism may react to stimulus variations according to psychophysical laws observed in humans and other animals. We investigate an empirically-motivated honeybee house-hunting model, which describes a value-sensitive decision process over potential nest-sites, at the level of the colony. In this study, we show how colony decision time increases with the number of available nests, in agreement with the Hick-Hyman law of psychophysics, and decreases with mean nest quality, in agreement with Piéron's law. We also show that colony error rate depends on mean nest quality, and difference in quality, in agreement with Weber's law. Psychophysical laws, particularly Weber's law, have been found in diverse species, including unicellular organisms. Our theoretical results predict that superorganisms may also exhibit such behaviour, suggesting that these laws arise from fundamental mechanisms of information processing and decision-making. Finally, we propose a combined psychophysical law which unifies Hick-Hyman's law and Piéron's law, traditionally studied independently; this unified law makes predictions that can be empirically tested.

Interactions between immunotoxicants and parasite stress: Implications for host health.

Many organisms face a wide variety of biotic and abiotic stressors which reduce individual survival, interacting to further reduce fitness. Here we studied the effects of two such interacting stressors: immunotoxicant exposure and parasite infection. We model the dynamics of a within-host infection and the associated immune response of an individual. We consider both the indirect sub-lethal effects on immunosuppression and the direct effects on health and mortality of individuals exposed to toxicants. We demonstrate that sub-lethal exposure to toxicants can promote infection through the suppression of the immune system. This happens through the depletion of the immune response which causes rapid proliferation in parasite load. We predict that the within-host parasite density is maximised by an intermediate toxicant exposure, rather than continuing to increase with toxicant exposure. In addition, high toxicant exposure can alter cellular regulation and cause the breakdown of normal healthy tissue, from which we infer higher mortality risk of the host. We classify this breakdown into three phases of increasing toxicant stress, and demonstrate the range of conditions under which toxicant exposure causes failure at the within-host level. These phases are determined by the relationship between the immunity status, overall cellular health and the level of toxicant exposure. We discuss the implications of our model in the context of individual bee health. Our model provides an assessment of how pesticide stress and infection interact to cause the breakdown of the within-host dynamics of individual bees.

The influence of the few: a stable 'oligarchy' controls information flow in house-hunting ants.

Animals that live together in groups often face difficult choices, such as which food resource to exploit, or which direction to flee in response to a predator. When there are costs associated with deadlock or group fragmentation, it is essential that the group achieves a consensus decision. Here, we study consensus formation in emigrating ant colonies faced with a binary choice between two identical nest-sites. By individually tagging each ant with a unique radio-frequency identification microchip, and then recording all ant-to-ant 'tandem runs'-stereotyped physical interactions that communicate information about potential nest-sites-we assembled the networks that trace the spread of consensus throughout the colony. Through repeated emigrations, we show that both the order in which these networks are assembled and the position of each individual within them are consistent from emigration to emigration. We demonstrate that the formation of the consensus is delegated to an influential but exclusive minority of highly active individuals-an 'oligarchy'-which is further divided into two subgroups, each specialized upon a different tandem running role. Finally, we show that communication primarily occurs between subgroups not within them, and further, that such between-group communication is more efficient than within-group communication.

The evolution of mutualism with modifiers.

Mutualisms are widespread, yet their evolution has received less theoretical attention than within-species social behaviors. Here, we extend previous models of unconditional pairwise interspecies social behavior, to consider selection for donation but also for donation-suppressing modifiers. We present conditions under which modifiers that suppress costly donation receive either positive or negative selection; assortment only at the donation locus always leads to selection for donation suppression, as in within-species greenbeard traits. However, genomewide assortment with modifier loci can lead to intermediate levels of donation, and these can differ in the two species even when payoffs from donation are additive and symmetric. When costly donation between species can evolve without being suppressed, we argue that it is most appropriately explained by indirect fitness benefits within the donating species, using partner species as vectors for altruism. Our work has implications for identifying both the stability and the ultimate beneficiaries of social behavior between species.

Individual Confidence-Weighting and Group Decision-Making.

Group-living species frequently pool individual information so as to reach consensus decisions such as when and where to move, or whether a predator is present. Such opinion-pooling has been demonstrated empirically, and theoretical models have been proposed to explain why group decisions are more reliable than individual decisions. Behavioural ecology theory frequently assumes that all individuals have equal decision-making abilities, but decision theory relaxes this assumption and has been tested in human groups. We summarise relevant theory and argue for its applicability to collective animal decisions. We consider selective pressure on confidence-weighting in groups of related and unrelated individuals. We also consider which species and behaviours may provide evidence of confidence-weighting, paying particular attention to the sophisticated vocal communication of cooperative breeders.