Learning-dependent hippocampal-striatal reorganization during sequential decision-making in pigeons

Adaptive sequential decision-making requires animals to learn how actions shape future states and rewards while adjusting behavioral strategies as experience accumulates. Although the hippocampus is implicated in state-structure representation and the striatum in value learning, how learning strategies evolve from exploratory sampling to efficient exploitation and how hippocampal-striatal interactions reorganize alongside this transition remain unclear. We trained six pigeons of undetermined sex to perform a probabilistic two-step decision task while simultaneously recording behavioral choices and hippocampal-striatal local field potentials. Strategy evolution was tracked using a dynamic reinforcement-learning framework in which model-based, model-free, and weighted model-based/model-free models were fitted across sliding windows. Hippocampal-striatal functional coordination was assessed using phase-locking analysis, and directed predictive influence was quantified using kernel Granger causality. The weighted model best explained choice dynamics, indicating a shift from model-based-like control during early acquisition toward model-free-like control during later stable performance. This behavioral shift was accompanied by two complementary neural changes: hippocampal-striatal phase coordination increased across learning, whereas hippocampus-to-striatum directed predictive influence decreased and covaried positively with model-based-like strategy weight. Direction-ratio analysis showed that hippocampus-to-striatum remained the predominant direction throughout learning, indicating reduced influence rather than directional reversal. After acquisition, hippocampus-to-striatum directed influence was not uniformly reduced but remained relatively preserved during rare, low-value, unrewarded, or less expected events. Together, these findings reveal a learning-dependent reorganization of hippocampal-striatal dynamics, in which increasing functional coordination is accompanied by reduced but condition-dependent hippocampal-to-striatal influence as behavior becomes more stable and efficient.Significance Statement Adaptive learning requires coordinated changes in behavioral strategy and neural interactions as animals progress from exploration to stable performance. Here, we show that pigeons gradually shifted from flexible, model-based-like control toward more stable, model-free-like behavior during sequential learning. In parallel, hippocampal-striatal interactions underwent a complementary reorganization: phase coordination progressively increased, whereas hippocampus-to-striatum directed predictive influence decreased with declining model-based-like control. Importantly, this directed influence remained relatively preserved during rare, low-value, or unrewarded events. These findings link behavioral strategy transition to the dynamic reorganization of hippocampal-striatal interactions, revealing how neural systems may simultaneously support efficient learned behavior while retaining sensitivity to behaviorally informative events.