Mizumori, S. J. Y. | bioRxiv Science

bioRxiv2025

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

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.

neuroscience↗

bioRxiv2023

Flexible decision-making is related to strategy learning, vicarious trial and error, and medial prefrontal rhythms during spatial set-shifting

A hallmark of behavioral flexibility is the ability to update behavior in response to changes in context. Most studies tend to rely on error counting around reward contingency or rule switches to measure flexibility, but these measures are difficult to adapt in a way that allows shorter timescale flexibility estimates. Further, choice accuracy does not account for other markers of flexibility, such as the hesitations and decision reversals humans and other animals often exhibit as decisions unfold, a behavior often called vicarious trial and error (VTE). To relate observable information about decision-making to latent aspects like learning and behavioral flexibility, we quantified changes in decision-making strategy using a previously developed, recency-weighted Bayesian inference algorithm. By comparing models of strategy use with decision history to generate strategy likelihood estimates on a trial-by-trial basis, the algorithm enabled us to identify learning points, and served as the basis for the development of a behavioral flexibility score. Aligning flexibility scores to learning points showed that flexibility peaked around estimated learning points and near peaks in VTE rate. However, we occasionally observed VTE during periods of low flexibility, where it often led to incorrect choices, suggesting the likely existence of multiple VTE-types. Additionally, we built on the decades of research suggesting a prominent role for the medial prefrontal cortex in enabling behavioral flexibility by recording field potentials from the medial prefrontal cortex during task performance. We observed changes in different field potential frequency bands that varied with respect to the different behavioral measures we used to characterize learning and decision-making. Overall, we demonstrate the use of multiple measures that jointly assess relationships between learning, behavioral flexibility, and decision-making behaviors. Further, we used these complementary measures to demonstrate that a particular decision-making behavior, VTE, was likely to be a marker of deliberation at some times, and uncertainty at others. Finally, we validate these measures by showing that theta, beta, and gamma rhythms in the medial prefrontal cortex vary with respect to both observable and latent aspects of behavior.

neuroscience↗