Our research in cognitive ethology is structured around two central themes:
We investigate the fundamental mechanisms underlying learning and memory formation, primarily in organisms with relatively simple nervous systems—such as the great pond snail (Lymnaea stagnalis) —while remaining open to employing other suitable model systems, and,
We examine how biotic and abiotic environmental factors influence learning and memory, mental states, and broader cognitive processes.
Outline credits: Bat – M. Ingala; Capuchin – S. Werning; Wale – C. Huh; Raven – D. Bakken and T. M. Keesey; Wildebeest, Bovid, and Oryx – J. A. Venter, H. H. T. Prins, D. A. Balfour, R. Slotow and T. M. Keesey; Gazelle – R. Groom; Sparrow – A. Butko. Link to license: https://creativecommons.org/licenses/by/3.0/
Much of our current understanding of learning and memory is rooted in associative paradigms, exemplified by Ivan Pavlov’s classic demonstrations of stimulus–cue pairing. However, learning is not limited to such simple associations. More complex processes, such as configural learning—where combinations of stimuli are encoded as unique units—remain comparatively underexplored, particularly in organisms with simple nervous systems. This form of learning enables nuanced discrimination (e.g., when neither A nor B predicts an outcome, but their combination, AB, does) and is evident in model systems like the great pond snail (Lymnaea stagnalis), which continues to offer valuable insights into the neural basis of cognition through its tractable yet surprisingly rich behavioral repertoire.
A central focus of our research is to develop a comprehensive understanding of cognition, particularly in invertebrates and organisms with distributed nervous systems, with the broader aim of uncovering general principles of cognition across the tree of life. Our work has contributed several key insights in this area, including the demonstration of higher-order learning, interactions between distinct memory systems, the influence of social environment on learning, and the physiological and molecular underpinnings of learning and memory. Selected research projects are outlined below.
We have recently proposed a model to gain insights into Trace Conditioning, which poses a fundamental challenge to the nervous system: how to associate a conditional stimulus (CS) with an unconditional stimulus (US) when they are separated by a temporal gap. This model proposes that the brain resolves this by engaging two distinct but interacting memory systems, organized along a gradient of stimulus salience. Immediately after CS presentation, a Tier 1 sensory-trace memory is formed—this is transient, stimulus-specific, and decays rapidly over seconds to minutes. On its own, this short-lived trace is often insufficient to bridge longer delays to the US.
Crucially, when the CS–US relationship is behaviorally salient, the system transitions to a Tier 2 attention-based salience memory. This second tier is more persistent, less tied to the specific sensory features of the stimulus, and can be reactivated by internal states such as motivation or arousal. The significance of this model lies in its ability to unify how temporal gaps are bridged across systems: rather than relying on a single mechanism, it highlights a dynamic shift from passive sensory persistence to active, salience-driven representation. This provides a mechanistic framework for understanding how even simple nervous systems encode temporally discontinuous events, with broader implications for conserved principles of attention, memory consolidation, and decision-making across taxa. Link to the research article.
An adult Lymnaea stagnalis.
04062022_093405.MP4A representative behavioral assay used to quantify activity (below). A mirror positioned beneath the Petri dish allows for clear visualization of the snail's ventral surface, enabling the precise recording of rasping behavior.
Configural learning (CL) is a higher-order form of associative learning in which animals integrate multiple, often conflicting, stimuli to guide behaviour. In Lymnaea stagnalis, simultaneous exposure to a food cue (carrot odour) and a predatory cue (crayfish effluent) creates a fundamental trade-off between feeding and safety. Rather than responding reflexively to either cue, snails form a combined representation of risk and suppress feeding for a limited period (∼3 hours). This transient memory reflects a dynamic decision-making process, where the animal must balance immediate energy needs against potential predation risk.
The significance of these findings lies in demonstrating that even relatively simple nervous systems can support integrative, context-dependent decision-making. Configural learning in Lymnaea provides a tractable model to study how competing environmental signals are encoded, prioritised, and translated into adaptive behavioural outcomes. By capturing the neural basis of such trade-offs, this work offers fundamental insights into how animals resolve conflict and make survival-relevant decisions—processes that are conserved across more complex systems.
Stress has a significant influence on cognitive functioning. Our work has revealed that stress is not simply “good” or “bad” for learning, but that its effects on cognition depend critically on the type of stress an organism experiences. Using a freshwater snail as a model system, we show that some stressors—such as signals of predation—can enhance learning and memory by sharpening attention, while others can impair cognitive function by overwhelming the system. This challenges the common view of stress as a single, uniform factor and instead highlights it as a complex biological signal that activates distinct pathways with very different cognitive outcomes. The findings underscore a fundamental principle: cognition is deeply intertwined with physiological state, and understanding how different stressors shape learning is essential not only for studying animal behavior in natural environments but also for gaining insights into human performance, mental health, and how we cope with an increasingly stressful world. Link to the research article.
Taste aversion learning is one of the most universal forms of associative learning across animal taxa. A single encounter with a novel food followed hours later by illness can lead to long-lasting avoidance of that taste—a phenomenon known as the Garcia effect. Humans experience this as well, where a bout of nausea can permanently alter food preferences. In L.stagnalis, we see a strikingly similar pattern: pairing a novel food stimulus (carrot slurry) with a delayed heat shock—acting as a proxy for sickness—suppresses the feeding response to that specific taste for at least 24 hours. This effect is highly selective, affecting only the paired novel stimulus, and disappears if the food is already familiar, highlighting the importance of novelty in forming this association.
At the mechanistic level, the heat shock induces upregulation of heat shock proteins HSP70 and HSP40 in the central nervous system. Blocking this upregulation abolishes the aversive memory, suggesting these proteins play a necessary role in encoding this form of associative learning. Building on this, we have extended the paradigm to identify multiple stressors capable of inducing Garcia-like learning, as well as conditions that can either suppress or enhance memory formation. Together, this work positions Lymnaea as a powerful model for understanding the conserved cellular and molecular basis of long-delay associative learning.
Why do identical experiences produce strong memories in some individuals but not others? Using Lymnaea stagnalis, this work shows that memory formation is tightly linked to stress sensitivity. Rather than having a uniform effect, stress follows a threshold-dependent relationship: moderate stress enhances learning and supports long-term memory, while too little fails to engage memory mechanisms and excessive stress suppresses them. Importantly, these thresholds vary across individuals, leading to consistent differences in learning outcomes under identical conditions.
The key significance of these findings is that they shift the focus from the stimulus to the internal state of the organism. Variability in learning is not experimental noise, but a predictable outcome of differences in stress physiology. This provides a mechanistic framework for understanding individual differences in cognition and highlights how internal state gates memory formation. More broadly, it reveals a conserved principle: the ability to learn is not fixed, but dynamically regulated by how organisms perceive and respond to stress. Link to the research article
In a recent study led by Veronica Rivi, we show that the pond snail Lymnaea stagnalis exhibits anxiety-like behavior that can be reversed by the human anti-anxiety drug Lorazepam. This provides the first evidence of pharmacologically modulated anxiety in a molluscan model, highlighting deep evolutionary conservation of emotional states and establishing a simple system to study the biology and treatment of anxiety, and possibly other mental health disorders as well.
These findings open up powerful new avenues for investigating the evolutionary origins of anxiety and emotional regulation, while establishing Lymnaea as a tractable and ethically accessible model system. Beyond fundamental insights, this work holds promise for advancing translational research aimed at improving the understanding, treatment, and management of mental health conditions. Link to the research article.
In the second theme, we investigate the how environmental factors influence learning and memory. one such factors is the external environment, where temperature, chemical effluents, and