Prestimulus theta activity predicts correct source memory retrieval

Abstract

Recent evidence indicates that the processing of a stimulus can be influenced by preceding patterns of brain activity. Here we examine whether prestimulus oscillatory brain activity can influence the ability to retrieve episodic memories. Neural activity in the theta-frequency band (4-8 Hz) was enhanced before presentation of test items which elicited accurate recollection of contextual details of the prior study episode ("source retrieval"), relative to trials for which item recognition was successful but source retrieval failed. Poststimulus theta activity was also related to source retrieval, and the magnitude of poststimulus theta was predicted by the magnitude of the prestimulus theta effects. The results suggest that ongoing neural processes occurring before stimulus onset might play a critical role in readying the brain for successful memory retrieval.

Fig. 1.

Schematic depiction of the memory retrieval paradigm.

Fig. 2.

Prestimulus theta is enhanced before successful episodic retrieval. (A) Bootstrap-corrected topographic significance map of prestimulus theta-band activity differences between item-correct with source-correct (item+source) and item-correct with source-incorrect (item-only) trials during the −300 to −150 ms time window. (B) (Upper) Average theta-power time course for item+source, item-only, and item-incorrect trials at left posterior temporal electrode site T7. (Lower) Item+source versus item-only difference spectrogram at electrode T7. (C) Relationship between theta differences at T7 during the prestimulus window (−300 to −150 ms) and source memory accuracy. (D) Topographic significance map of prestimulus theta-band activity differences between item+source and item-only trials during the −150 to 0 ms time window. (E) (Upper) Average theta-power time course for item+source, item-only, and item-incorrect trials at midfrontal electrode site Fz (labeled in A). (Lower) Item+source versus item-only difference spectrogram at electrode Fz. (F) Relationship between theta differences at electrode Fz during the prestimulus window (−300 to −150 ms) and source memory accuracy. Participants who showed larger prestimulus theta differences between item+source and item-only trials at site Fz also showed higher source memory accuracy.

Fig. 3.

Poststimulus parietal theta is enhanced during successful episodic retrieval. (A) Bootstrap-corrected topographic significance map of theta-band activity differences between item+source and item-only trials during the poststimulus (450–600 ms) time window. (B) (Upper) Average theta-power time course for item+source, item-only, and item-incorrect trials for left parietal electrode P7. (Lower) Item+source versus item-only difference spectrogram at electrode P7. (C) Relationship between theta differences at electrode P7 during the poststimulus window (300–450 ms) and source memory performance. Participants with larger poststimulus theta differences between item+source and item-only trials also showed higher source memory accuracy.

Fig. 4.

Frontal prestimulus theta effects are correlated with parietal poststimulus theta effects. Topographic plot of correlations between prestimulus theta effects (−300 to 0 ms) and poststimulus theta differences between electrodes during different poststimulus time windows: 0–300 ms (A), 300–600 ms (B), and 600–900 ms (C). Significant correlations between electrodes at each latency are bootstrap-corrected for multiple comparisons (detailed in SI Methods). Arrows indicate a significant correlation, and the direction of the arrow goes from pre- to poststimulus correlation: Arrow start indicates the prestimulus electrode; arrow end (i.e., arrowhead) indicates the poststimulus electrode. The color scale indicates the magnitude of the Pearson's correlation coefficient. Note the increased correlation (B) between frontal prestimulus theta differences and left parietal poststimulus theta differences during 300–600 ms poststimulus (compare with the lower portion of Fig. 3B).