Flexible use of memory by food-caching birds in a laboratory behavioral paradigm

Abstract

Memory is used by animals to influence navigational decisions, and neural activity in memory-related brain regions correlates to spatial variables. However, navigation is a rich behavior that contains a mix of memory-guided and memory-independent strategies. Disentangling the contribution of these strategies to navigation is therefore critical for understanding how memory influences behavioral output. To address this issue, we studied the natural spatial behavior of the chickadee, a food-caching bird. These birds hide food items at concealed, scattered locations and retrieve their caches later in time. We designed an apparatus that allows chickadees to cache and retrieve food while navigating in a laboratory arena. This apparatus enabled detailed, automated, and high-throughput tracking of key behavioral variables - including caches, retrievals, and investigations of cache sites. We built probabilistic models to fit these behavioral data using a combination of various mnemonic and non-mnemonic factors. We find that chickadees use some navigational strategies that are independent of cache memories, including opportunistic foraging and spatial biases. They combine these strategies with spatially precise and long-lasting memories of which sites contain caches and which sites they have previously checked and found to be empty. These memories are used in a context-dependent manner. During caching, chickadees avoid sites that already contain food. During retrieval, they are instead attracted to such occupied sites. These results show that a single memory can be used flexibly by a chickadee to achieve at least two unrelated behavioral goals. Our apparatus enables studying this flexibility in a tractable spatial paradigm.