Rhythmic modulation of dorsal hippocampus across distinct behavioral timescales during spatial set-shifting

Abstract

Previous work has shown frequency-specific modulation of dorsal hippocampus (dHPC) neural activity during simple behavioral tasks, suggesting shifts in neural population activity throughout different task phases and animal behaviors. Relatively little is known about task-relevant orchestrated shifts in theta, beta, and gamma rhythms across multiple behavioral timescales during a complex task that requires repeated adaptation of behavioral strategies based on changing reward contingencies. To address this gap in knowledge, we used a spatial set-shifting task to determine whether dHPC plays a specific role in strategy switching. The task requires rats to use two spatial strategies on an elevated plus maze: 1) alternating between East and West reward locations or 2) always going to the same reward location (e.g., only East or only West). Across specific timescales (session-based alignments, comparisons of trial types, within trial epochs), dHPC associated differentially with all three temporal categories. Across a session, we observed a decrease in theta and beta power before, and an increase in theta power after, the target strategy changed. Beta power was increased around the point at which rats learn the current rule. Comparing trial types, on trials before a rat learned the correct strategy, beta power increased. Within a single trial, after an incorrect (but not correct) choice, beta and gamma power increased while the rat returned to start a new trial. If gamma (but not beta) power was high during this return, the rat was more likely to make a correct choice on the next trial. On the other hand, low gamma power during the return was associated with incorrect trials. Rhythmic activity in dHPC, therefore, appears to track task demands, with the strength of each rhythmic frequency differentially associating with specific behaviors across three distinct timescales.