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 across contexts.
Figure 1: Graphical summary of cognitive abilities in the wild. Reproduced from Szabo et al. (2022) under the CC BY 4.0 license. © 2022 The Author(s). Published by Elsevier Ltd.
Szabo, B., Valencia-Aguilar, A., Damas-Moreira, I., & Ringler, E. (2022). Wild cognition – linking form and function of cognitive abilities within a natural context. Current Opinion in Behavioral Sciences, 45, 101115. https://doi.org/10.1016/j.cobeha.2022.101115
Much of our current understanding of learning and memory is rooted in simple associative paradigms, exemplified by Ivan Pavlov’s classical conditioning through stimulus–cue pairing. However, real-world cognition extends far beyond simple associations. Animals must often interpret combinations of signals, resolve conflicts, and make decisions under uncertainty—processes captured by more complex forms of learning such as configural learning, where combinations of stimuli are encoded as unique units rather than the sum of their individual parts. Despite their importance, these higher-order processes remain comparatively underexplored, particularly in organisms with simple nervous systems. Yet, as work in model systems like the great pond snail Lymnaea stagnalis reveals, even relatively simple brains can support surprisingly rich and flexible behaviours, offering a powerful window into the fundamental principles of cognition.
At the heart of our research is a unifying goal: to understand how learning, memory, decision-making, and internal states such as stress interact to shape behaviour across the tree of life. Focusing on invertebrates and organisms with simple nervous systems, we aim to uncover general, evolutionarily conserved rules of cognition. Our work shows that cognition is not a single process but an emergent property of interacting systems—where memory is shaped by time, decisions arise from competing information, and learning is dynamically modulated by physiological state. In pursuing this, we have uncovered key insights into higher-order learning, interactions between distinct memory systems, the influence of social and environmental context, and the physiological and molecular underpinnings of learning and memory. Together, this research programme positions simple systems as powerful models for addressing some of the most fundamental questions in neuroscience, with implications that extend from basic biology to human cognition and mental health.
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.
Building on this idea that memory is not static but shaped by context, our work next asks how organisms deal with multiple, competing pieces of information at once.
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 behavior. In Lymnaea stagnalis, simultaneous exposure to a food (carrot which they find delicious) and a predatory cue (chemical/tactile cues of crayfish predators) 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. This Intermediate-term 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 most living systems.
But real-world decisions are rarely made in a vacuum—they are shaped by stress, a powerful internal state that can alter how information is processed.
Stress has a significant influence on cognitive function. 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 or more than one stressor at a time, 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.
This interplay between timing, context, and stress becomes especially striking in forms of learning where cause and effect are separated by long delays.
Importantly, not all individuals respond to these experiences in the same way—leading us to explore why learning differs from one individual to another.
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.
Finally, these insights naturally extend into a broader and deeply relevant question: can simple systems help us understand mental wellbeing itself?
In a recent study led by Veronica Rivi, we show that the pond snail Lymnaea stagnalis exhibits anxiety-like behaviour that can be reversed by the human anti-anxiety drug Alprazolam. 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 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.
Together, this research program reveals a unifying theme: learning, memory, decision-making, and even emotional states are not isolated processes—they are deeply interconnected and continuously shaped by time, context, and stress. By uncovering these principles in a simple organism, we move closer to understanding the fundamental rules that govern cognition across all life, including humans.
In the second theme, we investigate how environmental factors - biotic and abiotic influence learning and memory. In particular, we are interested in understanding the effect of temperature, diet, chemical pollutants, and pharmacological byproducts on behavior, molecular physiology and cognition. This will enable Lymnaea and its related taxa to serve as models to understand the effects of a changing climate on aquatic invertebrates, establish links between cognition and diet, understand and mitigate pollutants, and develop novel drugs and treatments.
Our studies on the pond snail Lymnaea stagnalis show that organisms respond very differently to temperature extremes: cold exposure pushes them into an energy-saving, survival mode, while heat triggers stronger changes in brain activity, including learning to avoid harmful conditions. This distinction is important in the context of climate change, which is increasing not just average temperatures but also extreme and unpredictable heat events. The findings suggest that heat stress may have deeper impacts on animal behavior and cognition, potentially altering feeding, affecting memory processes, and survival, while cold stress may limit growth and reproduction through energy conservation. Overall, the study highlights that the ability of species to cope with climate change depends on complex biological responses, and that rising temperatures could fundamentally reshape how organisms behave and interact within ecosystems.
Building on the previous findings, this study shows that not all stressors affect animals in the same way at a deeper biological level. In pond snails (Lymnaea stagnalis), different types of stress—such as heat, lack of food, predator presence, or infection—change the activity of a key brain system called the endocannabinoid system, which helps regulate stress, energy use, immunity, and even mental states. In simple terms, the snail’s brain “tunes” itself differently depending on the kind of stress it experiences. This complements the earlier study by showing how these stress-specific behavioral changes (like learning under heat stress) are controlled at a molecular level. Together, the studies reveal that environmental stress—especially rising temperatures linked to climate change—not only changes behaviour but also rewires fundamental brain pathways that control survival. This is significant because climate change exposes organisms to multiple, overlapping stressors, meaning their ability to cope will depend on these complex internal systems, ultimately shaping which species can adapt and which may decline.
Our studies show that exposure to commonly used agricultural insecticides can disrupt basic life functions in pond snails (Lymnaea stagnalis). Acute exposure of snails to these chemicals led to changes in standard homeostatic behaviours like feeding and shell regeneration, and their ability to learn and remember was impaired. In simple terms, chemicals meant to protect crops can unintentionally “confuse” the brains and bodies of non-target organisms living in nearby water bodies. This is significant because insecticide use often goes hand-in-hand with broader agrochemical overuse (including fertilizers), which washes into ponds, lakes, and rivers through runoff. Together, these pollutants degrade freshwater ecosystems, affecting not just snails but entire food webs. The study highlights that excessive and unregulated chemical use in agriculture can have hidden but serious consequences on animal behaviour and ecosystem health, ultimately threatening biodiversity and the stability of environments that many species—including humans—depend on.