Subicular Plateaus Signal Reward Locations during Goal-Directed Behavior

Abstract

The hippocampus is essential for spatial learning, yet how its principal output structure, the subiculum, encodes behaviorally relevant information during navigation remains poorly understood. Because subicular neurons exhibit prominent burst firing, elucidating how this bursting is generated during behavior is critical. Using in vivo whole-cell recordings from dorsal subiculum neurons in head-fixed mice performing a goal-directed navigation task, we show that many bursts correspond to plateau events consisting of a series of action potentials riding on a large ([~]20-30 mV) sustained subthreshold depolarization. Subicular plateaus were synaptic in origin and required NMDA receptor activation. Organizing plateaus by the membrane potential preceding their onset revealed distinct behavioral associations. Plateaus initiated from relatively hyperpolarized membrane potentials preferentially clustered near reward locations, whereas plateaus initiated from more depolarized membrane potentials were more spatially distributed and showed weaker reward specificity. Reward-related clustering required a fixed, learned reward location and dynamically rearranged during learning of a new reward location. Together, our findings identify subicular plateaus as a prominent cellular substrate of hippocampal bursting output and demonstrate that intracellular membrane potential state organizes the behavioral associations of subicular plateaus during goal-directed learning.