Goal-directed spatial learning is crucial for the survival of animals, in which the formation of the route from the current location to the goal is one of the central problems. A distributed brain network comprising the hippocampus and prefrontal cortex has been shown to support such capacity, yet it is not fully understood how the most similar brain regions in birds, the hippocampus (Hp) and nidopallium caudolaterale (NCL), cooperate during route formation in goal-directed spatial learning. Hence, we examined neural activity in the Hp-NCL network of pigeons and explored the connectivity dynamics during route formation in a goal-directed spatial task. We found that behavioral changes in spatial learning during route formation are accompanied by modifications in neural patterns in the Hp-NCL network. Specifically, as pigeons learned to solve the task, the spectral power in both regions gradually decreased. Meanwhile, elevated hippocampal theta (5 to 12 Hz) connectivity and depressed connectivity in NCL were also observed. Lastly, the interregional functional connectivity was found to increase with learning, specifically in the theta frequency band during route formation. These results provide insight into the dynamics of the Hp-NCL network during spatial learning, serving to reveal the potential mechanism of avian spatial navigation.

Research in reinforcement learning indicates that animals respond differently to positive and negative reward prediction errors, which can be calculated by assuming learning rate bias. Many studies have shown that humans and other animals have learning rate bias during learning, but it is unclear whether and how the bias changes throughout the entire learning process. Here, we recorded the behavior data and the local field potentials (LFPs) in the striatum of five pigeons performing a probabilistic learning task. Reinforcement learning models with and without learning rate biases were used to dynamically fit the pigeons’ choice behavior and estimate the option values. Furthemore, the correlation between the striatal LFPs power and the model-estimated option values was explored. We found that the pigeons’ learning rate bias shifted from negative to positive during the learning process, and the striatal Gamma (31 to 80 Hz) power correlated with the option values modulated by dynamic learning rate bias. In conclusion, our results support the hypothesis that pigeons employ a dynamic learning strategy in the learning process from both behavioral and neural aspects, providing valuable insights into reinforcement learning mechanisms of non-human animals.

Navigation is a complex task in which the hippocampus (Hp), which plays an important role, may be involved in interactions between different frequency bands. However, little is known whether this cross-frequency interaction exists in the Hp of birds during navigation. Therefore, we examined the electrophysiological characteristics of hippocampal cross-frequency interactions of domestic pigeons (Columba livia domestica) during navigation. Two goal-directed navigation tasks with different locomotor modes were designed, and the local field potentials (LFPs) were recorded for analysis. We found that the amplitudes of high-frequency oscillations in Hp were dynamically modulated by the phase of co-occurring theta-band oscillations both during ground-based maze and outdoor flight navigation. The high-frequency amplitude sub-frequency bands modulated by the hippocampal theta phase were different at different tasks, and this process was independent of the navigation path and goal. These results suggest that phase–amplitude coupling (PAC) in the avian Hp may be more associated with the ongoing cognitive demands of navigational processes. Our findings contribute to the understanding of potential mechanisms of hippocampal PAC on multi-frequency informational interactions in avian navigation and provide valuable insights into cross-species evolution.

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.

Understanding value learning in animals is a key focus in cognitive neuroscience. Current models used in research are often simple, and while more complex models have been proposed, it remains unclear which assumptions align with actual value-learning strategies of animals. This study investigated the computational mechanisms behind value learning in pigeons using a free-choice task. Three models were constructed based on different assumptions about the role of the basal ganglia's dual pathways and synaptic plasticity in value computation, followed by model comparison and neural correlation analysis. Among the three models tested, the dual-pathway reinforcement learning model with Hebbian rules most closely matched the pigeons' behavior. Furthermore, the striatal gamma band connectivity showed the highest correlation with the values estimated by this model. Additionally, enhanced beta band connectivity in the nidopallium caudolaterale supported value learning. This study provides valuable insights into reinforcement learning mechanisms in non-human animals.

Animals making decisions under uncertainty must use learned value estimates to distinguish advantageous from disadvantageous options. In mammals, the striatum is a key substrate for value-related processing, but whether analogous network-level dynamics are present in birds remains unclear. Here, we recorded 16-channel local field potentials (LFPs) from the striatum of six pigeons performing a probabilistic two-choice task and combined these recordings with computational modeling of behavior. Across training, pigeons increasingly favored the advantageous option. Dynamic model comparison further showed that choice strategy changed across learning, from an early reliance on immediate feedback to a later pattern better captured by Rescorla–Wagner reinforcement-learning (RW-RL) value updating. Using trial-by-trial phase-locking values (PLVs) to construct weighted striatal functional networks, we found that PLV-based network coordination increased with learning and was selectively associated with the RW-RL-estimated value of the higher-payoff option, with the strongest effects in the gamma band (30–80 Hz). Within trials, network coordination evolved from the pre-choice period to the outcome period and was differentially modulated by both choice (S+ versus S−) and reward feedback. Together, these findings suggest that avian striatal LFP network dynamics are linked to learned option value and value-guided choice, and provide comparative evidence that the avian striatum may exhibit network-level dynamics that are functionally analogous, but not necessarily identical, to aspects of mammalian striatal processing.