Learning shifts the preferred theta phase of gamma oscillations in CA1

Abstract

Hippocampal neuronal oscillations reflect different cognitive processes and can therefore be used to dissect the role of hippocampal subfields in learning and memory. In particular, it has been suggested that encoding and retrieval is associated with slow gamma (25–55 Hz) and fast gamma (60–100 Hz) oscillations, respectively, which appear in a nested manner at specific phases of the ongoing theta oscillations (4–12 Hz). However, the relationship between memory demand and the theta phase of gamma oscillations remains unclear. Here, we assessed the theta phase preference of gamma oscillations in the CA1 region, at the starting and junction zones of a T‐maze, while rats were learning an appetitive task. We found that the theta phase preference of slow gamma showed a ~180° phase shift when animals switched from novice to skilled performance during task acquisition. This phase‐shift was not present at the junction zone, where animals chose a right or left turn within the T‐maze, suggesting that a recall/decision process had already taken place at the starting zone. Our findings indicate that slow gamma oscillations support both encoding and retrieval, depending on the theta phase at which they occur. These properties are particularly evident prior to cognitive engagement in an acquired spatial task.

Frequency matters: how changes in hippocampal theta frequency can influence temporal coding, anxiety-reduction, and memory

“…However, theta-gamma relationships are likely more complex than previously thought (Lopes-dos-Santos et al, 2018), and are often characterised when tasks are well-learned. Intriguingly, Rayan et al (2022) found that the theta-phase preference of slow-gamma and mid/fast-power shifted with learning in the starting box of a spatial reference memory task. Remarkably, the theta-phase preference of slow-gamma shifted 140 • as rats progressed from "novice" to "skilled" learners in a spatial reference memory task.…”

Phase-precession-like Effects in the Anterior Insula Cortex during Reward Expectancy

“…Phases of low-frequency oscillations, corresponding to the peak high-frequency activities, represent distinct neural signatures implicated in a range of cognitive tasks 24,25 . For example, gamma activities coupled to the peak of theta oscillations contribute to memory encoding, while those coupled to the trough of theta oscillations participate in memory retrieval [26][27][28] . When encoding sequential events, the neural pattern underlying each event is associated with different phases of low-frequency oscillations in the frontal and temporal lobes 17,20,[29][30][31][32][33][34] .…”

Electrophysiological Mechanisms in the Anterior Insula Cortex during Reward Expectancy

“…Phases of low-frequency oscillations, corresponding to the peak of high-frequency activities, represent distinct neural signatures implicated in a range of cognitive tasks (Bush & Burgess, 2020; Lopour et al, 2013). For example, gamma activities coupled to the peak of theta oscillations contribute to memory encoding, while those coupled to the trough of theta oscillations participate in memory retrieval (Kragel et al, 2020; Lopes-Dos-Santos et al, 2018; Rayan et al, 2022). When encoding sequential events, the neural pattern underlying each event is associated with different phases of low-frequency oscillations in the frontal and temporal lobes (Axmacher et al, 2010; Bahramisharif et al, 2018; Heusser et al, 2016; Lisman, 2005; Reddy et al, 2021; Siegel et al, 2009; Watrous et al, 2015; Yang et al, 2021).…”