Interaction of memory systems is controlled by context in both food-storing and non-storing birds

Animals and humans have multiple memory systems. While both black-capped chickadees (Poecile atricapillus) and dark-eyed juncos (Junco hyemalis) are under selective pressure to remember reliable long-term spatial locations (habit memory), chickadees must additionally quickly form and rapidly update spatial memory for unique cache sites (one-trial memory). We conducted a series of three experiments in which we assessed the degree to which habit and one-trial memory were expressed in both species as a function of training context. In Experiment 1, birds failed to demonstrate habits on probe trials after being trained in the context of a biased Match-to-Sample task in which the same high-frequency target was always correct. In Experiment 2, habit strongly controlled performance when habits were learned as Discriminations, defining a specific training context. In Experiment 3, context no longer defined when to express habits and habit and one-trial memory competed for control of behavior. Across all experiments, birds preferentially used the memory system at test that was consistent with the context in which it was acquired. Although the memory adaptations that allow chickadees to successfully recover cached food might predispose them to favor one-trial memory, we found no species differences in the weighting of habit and one-trial memory. In the experiments here, context was a powerful factor controlling the interaction of memory systems.