Biology subjects

Marshall, J. A. R.

Publications and source records attributed to Marshall, J. A. R..

12 recordsLinked to original sources

bioRxiv2023

A neuromorphic model of active vision shows spatio-temporal encoding in lobula neurons can aid pattern recognition in bees

Bees' remarkable visual learning abilities make them ideal for studying active information acquisition and representation. Here, we develop a biologically inspired model to examine how flight behaviours during visual scanning shape neural representation in the insect brain, exploring the interplay between scanning behaviour, neural connectivity, and visual encoding efficiency. Incorporating non-associative learning, adaptive changes without reinforcement, and exposing the model to sequential natural images during scanning, we obtain results that closely match neurobiological observations. Active scanning and non-associative learning dynamically shape neural activity, optimising information flow and representation. Lobula neurons, crucial for visual integration, self-organise into orientation-selective cells with sparse, decorrelated responses to orthogonal bar movements. They encode a range of orientations, biased by input speed and contrast, suggesting co-evolution with scanning behaviour to enhance visual representation and support efficient coding. To assess the significance of this spatiotemporal coding, we extend the model with circuitry analogous to the mushroom body, a region linked to associative learning. The model demonstrates robust performance in pattern recognition, implying a similar encoding mechanism in insects. Integrating behavioural, neurobiological, and computational insights, this study highlights how spatiotemporal coding in the lobula efficiently compresses visual features, offering broader insights into active vision strategies and bio-inspired automation.

neuroscience↗

bioRxiv2023

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.

neuroscience↗

bioRxiv2022

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.

animal behavior and cognition↗

bioRxiv2021

Automated video tracking and flight analysis show how bumblebees solve a pattern discrimination task using active vision

Active vision, the ability of the visual system to actively sample and select relevant information out of a visual scene through eye and head movements, has been explored in a variety of animal species. Small-brained animals such as insects might rely even more on sequential acquisition of pattern features since there might be less parallel processing capacity in their brains than in vertebrates. To investigate how active vision strategies enable bees to solve visual tasks, here, we employed a simple visual discrimination task in which individual bees were presented with a multiplication symbol and a 45{degrees} rotated version of the same pattern ("plus sign"). High-speed videography of unrewarded tests and analysis of the bees flight paths shows that only a small region of the pattern is inspected before successfully accepting a target or rejecting a distractor. The bees scanning behaviour of the stimuli differed for plus signs and multiplication signs, but for each of these, the flight behaviour was consistent irrespective of whether the pattern was rewarding or unrewarding. Bees typically oriented themselves at ~{+/-}30{degrees} to the patterns such that only one eye had an unobscured view of stimuli. There was a significant preference for initially scanning the left side of the stimuli. Our results suggest that the bees movement may be an integral part of a strategy to efficiently analyse and encode their environment. Summary statementAutomated video tracking and flight analysis is proposed as the next milestone in understanding mechanisms underpinning active vision and cognitive visual abilities of bees.

animal behavior and cognition↗

bioRxiv2020

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.

ecology↗

bioRxiv2020

Honey bees solve a multi-comparison ranking task by probability matching

Honey bees forage on a range of flowers, all of which can vary unpredictably in the amount and type of rewards they offer. In this environment bees are challenged with maximising 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 challenged bees with 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 matching their preferences to their history of reinforcement for each colour. We used a computational model to explore the feasibility of this probability matching strategy for the honey bee brain. The model suggested a structure like the honey bee mushroom body with reinforcement-related plasticity at both input and output was 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 utility and limitations of this simple cognitive strategy for foraging animals.

animal behavior and cognition↗

bioRxiv2019

Comment on 'Optimal Policy for Multi-Alternative Decisions'

AO_SCPLOWBSTRACTC_SCPLOWOptimality analysis has recently been proposed for value-based decision-making, in which decision agents are rewarded by the value of the selected option. This contrasts with psychophysics where decision agents are typically rewarded only if they choose the correct or best option. The analysis of optimal policies for value-based decisions raises interesting and surprising parallels with decision rules proposed for accuracy-based decisions in binary and multi-alternative cases, and explains experimentally-observed deviations from rationality. However, the analysis assumes that decision agents should treat time as a linear cost, and thus optimise their Bayes Risk from decisions. A more naturalistic assumption is that future rewards are geometrically discounted, since they are less likely to be realised in an uncertain world. Changing the way in which time is costed leads to substantive changes in the resulting optimal policies, explains empirical data that previously could not be explained, and makes falsifiable predictions for future experiments.

animal behavior and cognition↗

bioRxiv2019

Better tired than lost: turtle ant trail networks favor coherence over shortest paths

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. Author SummaryWe investigated the trail networks of arboreal turtle ants in the canopy of the tropical forest, to ask what characterizes the colonys choice of foraging paths within the vegetation. We monitored day to day changes in the junctions and edges of trail networks of colonies in the dry forest of western Mexico. We compared the paths used by the ants to simulated random paths in the surrounding vegetation. We found that the paths of turtle ants prioritize coherence, keeping ants together on the trail, over minimizing the average edge length. The choice of paths reduces the number of junctions in the trail where ants could get lost, and favors junctions with a physical configuration that makes it likely that successive ants will reinforce the same path. Our work suggests that design principles that emphasize keeping information flow constrained to streamlined, coherent trails may be useful in human-designed distributed routing and transport networks or robot swarms.

ecology↗

bioRxiv2018

Quorums enable optimal pooling of independent judgements

Majority-voting and the Condorcet Jury Theorem pervade thinking about collective decision-making. Thus, it is typically assumed that majority-voting is the best possible decision mechanism, and that scenarios exist where individually-weak decision-makers should not pool information. Condorcet and its applications implicitly assume that only one kind of error can be made, yet signal detection theory shows two kinds of errors exist, false positives and false negatives. We apply signal detection theory to collective decision-making to show that majority voting is frequently sub-optimal, and can be optimally replaced by quorum decision-making. While quorums have been proposed to resolve within-group conflicts, or manage speed-accuracy trade-offs, our analysis applies to groups with aligned interests undertaking single-shot decisions. Our results help explain the ubiquity of quorum decision-making in nature, relate the use of sub- and super-majority quorums to decision ecology, and may inform the design of artificial decision-making systems.\n\nImpact StatementTheory typically assumes that majority voting is optimal; this is incorrect - majority voting is typically sub-optimal, and should be replaced by sub-majority or super-majority quorum voting. This helps explain the prevalence of quorum-sensing in even the simplest collective systems, such as bacterial communities.

ecology↗

bioRxiv2018

Inhibition and excitation shape activity selection: effect of oscillations in a decision-making circuit

Decision-making is a complex task and requires adaptive mechanisms that facilitate efficient behaviour. Here, we consider a neural circuit that guides the behaviour of an animal in ongoing binary choice tasks. 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 function (increasing reproductive value). 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 behaviour, and explain different behavioural outcomes by making the link between bifurcation analysis of the nonlinear neural circuit model and decision-making performance. We find that the animal performs best if it tunes internal parameters of the neural circuit in accordance with the underlying bifurcation structure. In particular, variation of inhibition strength and excitation-over-inhibition ratio have a crucial effect on the decision outcome, by allowing the animal to break decision deadlock and 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. Our results underpin the importance of an integrated functional and mechanistic study of animal activity selection.\n\nAuthor summaryOrganisms frequently select activities, which relate to economic, social and perceptual decision-making problems. The choices made may have substantial impact on their lives. In foraging decisions, for example, animals aim at reaching a target intake of nutrients; it is generally believed that a balanced diet improves reproductive success, yet little is known about the underlying mechanisms that integrate nutritional needs within the brain. In our study, we address this coupling between physiological states and a decision-making circuit in the context of foraging decisions. We consider a model animal that has the drive to eat or drink. The motivation to select and perform one of these activities (i.e. eating or drinking), is processed in artificial neuronal units that have access to information on how hungry and thirsty the animal is at the point it makes the decision. We show that inhibitory and excitatory mechanisms in the neural circuit shape ongoing binary decisions, and we reveal under which conditions oscillating motivations may improve the overall performance of the animal. Our results indicate that inefficient or pathological decision-making may originate from suboptimal modulation of excitation and inhibition in the neurobiological network.

neuroscience↗

bioRxiv2018

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 same-ness 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.

neuroscience↗

bioRxiv2017

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 synergistically to further reduce fitness. Here we studied the effects of two such synergistically 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. 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 honey bee health. Our model provides an assessment of how pesticide stress and infection interact to cause the synergistic breakdown of the within-host dynamics of individual honey bees.

epidemiology↗