Functional role of gamma and theta oscillations in episodic memory

Abstract

The primary aim of this review is to examine evidence for a functional role of gamma and theta oscillations in human episodic memory. It is proposed here that gamma and theta oscillations allow for the transient interaction between cortical structures and the hippocampus for the encoding and retrieval of episodic memories as described by the hippocampal memory indexing theory (Teyler and DiScenna, 1986). Gamma rhythms can act in the cortex to bind perceptual features and in the hippocampus to bind the rich perceptual and contextual information from diverse brain regions into episodic representations. Theta oscillations act to temporally order these individual episodic memory representations. Through feedback projections from the hippocampus to the cortex these gamma and theta patterns could cause the reinstatement of the entire episodic memory representation in the cortex. In addition, theta oscillations could allow for top-down control from the frontal cortex to the hippocampus modulating the encoding and retrieval of episodic memories.

Figure 1

Gamma and theta power during encoding. (A) Grand average of the topography of gamma power for later remembered (LR) and later forgotten (LF) and their difference (LR-LF). Plus signs represent right temporal sensors that showed a significant power increase for LR compared to LF. (B) Grand average time-frequency plots of power from one significant right temporal sensor showing the time course of gamma oscillations for LR, LF, and their difference. (C) Grand average gamma power averaged between 60 and 90 Hz for LR and LF for the same sensor as B. (D) Grand average of the topography of theta power for later remembered (LR) and later forgotten (LF) and their difference (LR-LF). (E) Grand average time-frequency plots of power from one significant sensor showing the time course of theta oscillations for LR, LF, and their difference. (F) Grand average theta power averaged between 4.5 and 8.5 Hz for LR and LF for the same sensor as E (reprinted with permission from Osipova et al., 2006).

Figure 2

Gamma phase synchronization for encoding. Difference of phase synchronization between rhinal cortex and hippocampus (%) relative to prestimulus baseline for subsequently recalled minus not recalled words. Blue indicates more phase desynchronization, red indicates more phase synchronization, ranging from −30% to +30% change from prestimulus baseline. Phase synchronization differences for successfully recalled versus not recalled were greatest for 36–40Hz from 100–300 ms and 500–600 ms (reprinted with permission from Fell et al., 2001).

Figure 3

Phase precession. When the animal enters a place field, the theta rhythm resets so that the cells firing to the place field will be activated at the peak of the theta cycle. Inputs arriving at the peak of the theta rhythm induce LTP. The activated place cells are then strengthened by LTP so that the same environmental cues will evoke firing at earlier phases of the theta rhythm on subsequent cycles (reprinted with permission from Axmacher, Mormann, Fernández, Elger, & Fell, 2006).

Figure 4

Gamma and theta power during retrieval. (A) Grand average of the topography of gamma power for hits (HIT) and correct rejections (CR) and their difference (HIT-CR). P lus signs represent right occipital sensors that showed a significant power increase for HIT compared to CR. (B) Grand average time-frequency plots of power from one significant right occipital sensor showing the time course of gamma oscillations for HIT and CR and their difference. (C) Grand average gamma power averaged between 60 and 90 Hz for HIT and CR for the same sensor as B. (D) Grand average of the topography of theta power for hits (HIT) and correct rejections (CR) and their difference (HIT-CR). (E) Grand average time-frequency plots of power from one significant sensor showing the time course of theta oscillations for HIT and CR and their difference. (F) Grand average theta power averaged between 60 and 90 Hz for HIT and CR for the same sensor as E (reprinted with permission from Osipova et al., 2006).