The Hippocampus in Pigeons Contributes to the Model-Based Valuation and the Relationship between Temporal Context States

Abstract

Model-based decision-making guides organism behavior by the representation of the relationships between different states. Previous studies have shown that the mammalian hippocampus (Hp) plays a key role in learning the structure of relationships among experiences. However, the hippocampal neural mechanisms of birds for model-based learning have rarely been reported. Here, we trained six pigeons to perform a two-step task and explore whether their Hp contributes to model-based learning. Behavioral performance and hippocampal multi-channel local field potentials (LFPs) were recorded during the task. We estimated the subjective values using a reinforcement learning model dynamically fitted to the pigeon’s choice of behavior. The results show that the model-based learner can capture the behavioral choices of pigeons well throughout the learning process. Neural analysis indicated that high-frequency (12–100 Hz) power in Hp represented the temporal context states. Moreover, dynamic correlation and decoding results provided further support for the high-frequency dependence of model-based valuations. In addition, we observed a significant increase in hippocampal neural similarity at the low-frequency band (1–12 Hz) for common temporal context states after learning. Overall, our findings suggest that pigeons use model-based inferences to learn multi-step tasks, and multiple LFP frequency bands collaboratively contribute to model-based learning. Specifically, the high-frequency (12–100 Hz) oscillations represent model-based valuations, while the low-frequency (1–12 Hz) neural similarity is influenced by the relationship between temporal context states. These results contribute to our understanding of the neural mechanisms underlying model-based learning and broaden the scope of hippocampal contributions to avian behavior.