Theta and gamma oscillations predict encoding and retrieval of declarative memory

Abstract

Although studies in animals and patients have demonstrated that brain oscillations play a role in declarative memory encoding and retrieval, little has been done to investigate the temporal dynamics and sources of brain activity in healthy human subjects performing such tasks. In a magnetoencephalography study using pictorial stimuli, we have now identified oscillatory activity in the gamma (60-90 Hz) and theta (4.5-8.5 Hz) band during declarative memory operations in healthy participants. Both theta and gamma activity was stronger for the later remembered compared with the later forgotten items (the "subsequent memory effect"). In the retrieval session, theta and gamma activity was stronger for recognized items compared with correctly rejected new items (the "old/new effect"). The gamma activity was also stronger for recognized compared with forgotten old items (the "recognition effect"). The effects in the theta band were observed over right parietotemporal areas, whereas the sources of the effects in the gamma band were identified in Brodmann area 18/19. We propose that the theta activity is directly engaged in mnemonic operations. The increase in neuronal synchronization in the gamma band in occipital areas may result in a stronger drive to subsequent areas, thus facilitating both memory encoding and retrieval. Alternatively, the gamma synchronization might reflect representations being reinforced by top-down activity from higher-level memory areas. Our results provide additional insight on human declarative memory operations and oscillatory brain activity that complements previous electrophysiological and brain imaging studies.

Figure 1.

The experimental design used in the study. In the encoding session, subjects were shown photographs (e.g., S1, S2) and instructed to make a building/landscape decision by a button press. In the retrieval session, participants were shown pictures from the encoding session (e.g., S2) intermixed with the new stimuli (e.g., P1). They were instructed to respond to whether the picture had been shown in the previous session. Based on the answers, trials in the encoding session were classified as LR and LF. Trials in the retrieval session were labeled as HIT, CR, and MISS.

Figure 2.

Gamma activity during the encoding session: the subsequent memory effect. A, The grand average of the topography of gamma power for the LR and LF trials and their difference (LR − LF). Two adjacent clusters of occipital sensors showed significant increase in gamma power (*p < 0.01; ⁺p < 0.05). B, Grand-averaged time–frequency representations of power from one significant sensor showing the time course of gamma oscillations for LR, LF, and their difference. C, Grand-averaged gamma power averaged between 60 and 90 Hz for both conditions for the same sensor as in B. D, Source reconstruction of gamma activity, averaged over subjects and overlaid on the MNI standard brain. The sources for LR and LF conditions were located bilaterally in BA18/19. The difference in power (LR − LF) revealed sources in BA18/19 as well. The power of the source representations was thresholded at half-maximum.

Figure 3.

Theta activity during the encoding session: the subsequent memory effect. A, The grand average of topography of theta power for the LR and LF trials and their difference (LR − LF). The cluster of right temporal sensors that showed significantly increased power in the LR compared with the LF condition is indicated by + signs (p < 0.05). B, Grand-averaged time–frequency representations of power from a significant representative sensor showing the time course of theta oscillations during LF, LR, and their difference. C, Grand average of theta power (4.5–8.5 Hz) for both conditions for the same sensor as in B.

Figure 4.

Gamma activity during the retrieval session: the old/new effect. A, The grand average of the topography of gamma power for HIT and CR trials and their difference (HIT − CR). A cluster of occipital sensors showed significant difference in gamma power, indicated by + signs (p < 0.05). B, Grand average of time–frequency representations of power from one significant representative sensor showing the time course of gamma oscillations in two conditions and their difference. C, Grand-averaged gamma power averaged between 60 and 90 Hz for both conditions for the same sensor as in B. D, Source reconstruction of gamma activity, averaged over subjects and overlaid on the MNI standard brain. The sources for HIT and CR conditions were located bilaterally in BA18/19. The difference in power (HIT − CR) revealed sources in BA18/19 as well. The power of the source representations was thresholded at half-maximum.

Figure 5.

Theta activity during the retrieval session: the old/new effect. A, The grand average of the topography of theta power for HIT and CR trials and their difference (HIT − CR). A cluster of right occipital sensors showed significant increase in theta power, indicated by + signs (p < 0.05). B, Grand average of time–frequency representations of power from one significant representative sensor showing the time course of theta oscillations in two conditions and their difference. C, Grand average of theta power (4.5–8.5 Hz) for both conditions for the same sensor as in B.

Figure 6.

Gamma activity in the retrieval session: the recognition effect. A, The grand average of the topography of gamma power for HIT and MISS items and their difference (HIT − MISS). Two adjacent clusters of occipital sensors showed significant increase in gamma power (*p < 0.01; ⁺p < 0.05). B, Grand-averaged time–frequency representations of power from one significant sensor associated with HIT versus MISS items and the subtraction of two conditions. C, Grand-averaged gamma power averaged between 60 and 90 Hz for both conditions for the same sensor as in B. D, Source reconstruction of gamma activity, averaged over subjects and overlaid on the MNI standard brain. The sources for HIT and MISS conditions were located bilaterally in BA18/19. The difference in power (HIT − MISS) revealed sources in BA18/19 as well. The power of the source representations was thresholded at half-maximum.