Theta Oscillations at Encoding Mediate the Context-Dependent Nature of Human Episodic Memory

Tobias Staudigl, Simon Hanslmayr
2013 Current Biology  
Human episodic memory is highly context dependent. Therefore, retrieval benefits when a memory is recalled in the same context compared to a different context [1, 2] . This implies that items and contexts are bound together during encoding, such that the reinstatement of the initial context at test improves retrieval. Animal studies suggest that theta oscillations and theta-to-gamma cross-frequency coupling modulate such item-context binding [3] , but direct evidence from humans is scarce. We
more » ... vestigated this issue by manipulating the overlap of contextual features between encoding and retrieval. Participants studied words superimposed on movie clips and were later tested by presenting the word with either the same or a different movie. The results show that memory performance and the oscillatory correlates of memory formation crucially depend on the overlap of the context between encoding and test. When the context matched, high theta power during encoding was related to successful recognition, whereas the opposite pattern emerged in the context-mismatch condition. In addition, cross-frequency coupling analysis revealed a contextdependent theta-to-gamma memory effect specifically in the left hippocampus. These results reveal for the first time that context-dependent episodic memory effects are mediated by theta oscillatory activity. Results To investigate context-dependent episodic memory effects, we recorded magnetoencephalography (MEG; 148 sensors) in 18 human participants during a context memory experiment ( Figure 1A ). At encoding, words were shown superimposed on movie clips. Later, in a surprise memory test, word-movie pairs were presented again together with new word-movie pairs, and participants indicated their confidence as to whether the word was old or new using a six-point scale ranging from "very sure old" to "very sure new." To this end, half of the old words were paired with the same movie as during encoding (context-match condition), whereas the other words were paired with a different, but also old, movie (context-mismatch condition; Figure 1A ). This experiment thus utilized a direct context manipulation, which goes beyond prior studies investigating context memory via subsequent memory effects based on source memory judgments (e.g., [4] ). The rationale was that any neural correlate of context-dependent memory at encoding should vary as a function of how the memory is being tested later. Movies were chosen as context manipulation because they are known to be strong contextual memory cues [5] . Memory Retrieval Is Context Dependent Overall, the participants' mean hit rate (correct responses including "very sure old," "sure old," and "probably old") was significantly higher in the context-match than in the context-mismatch condition (68.6% versus 60.5%, respectively; t 17 = 4.76; p < 0.0005, two-tailed t test; Figure 1B ). This effect was evident in 16 out of the 18 subjects, showing that movies are indeed powerful contextual cues. Mean correct rejection rate was 66.7% (mean false alarm rate 33.3%) showing that participants were well able to distinguish between old and new words. Note that the false alarm rates were the same for the match and the mismatch conditions, because all old items (match and mismatch) were shown intermixed with new items. To investigate whether the contextdependent behavioral memory effects were driven by episodic recollection or by a modulation of general memory strength, we split the data into high-confidence hits ("very sure old") and low-confidence hits ("sure old," "probably old"). A two-way repeated-measures ANOVA revealed a significant condition 3 confidence interaction (F 1,17 = 4.801; p < 0.05; Figure 1C). Post hoc t tests indicated that the difference between high-confidence hits was significant (t 17 = 3.94; p < 0.005, twotailed t test), whereas the difference between low-confidence hits (match versus mismatch) was not significant (p > 0.5, two-tailed t test). Together, these results show that the reinstatement of contextual features at test enhances memory performance [2] and suggest that this effect is driven by episodic recollection. The context-dependent memory effect was replicated in an independent data set (67% versus 63.2%; t 22 = 3.673; p < 0.005, two-tailed t test; see Figure S1B available online) using sensory modality (auditory versus visual) as context manipulation (see experiment 2 in the Supplemental Experimental Procedures for details). Theta Power Correlates of Memory Encoding Are Context Dependent To identify oscillatory correlates of context-dependent memory formation, we contrasted subsequent memory effects (SMEs), i.e., differences between hits and misses, between the match and the mismatch condition in terms of associated activity at encoding. Time-frequency clusters of interest were identified by a two-step procedure (see Supplemental Experimental Procedures for details). Power values in the lower (2-30 Hz) and higher (30-90 Hz) frequencies were admitted to a sliding window analysis. In the lower frequency range, context-dependent SMEs were selectively identified in the theta band (Figure 2A ). Only the early effect (3.5-4.5 Hz, 0.1-0.7 s; highlighted in Figure 2A ) survived a cluster-based dependent randomization procedure (p corr < 0.05) and was evident over a cluster of central, parietal, and temporal sensors. Post hoc t tests performed on this cluster of sensors revealed a positive SME in the context-match condition (hits > misses; p < 0.01) and a negative SME in the contextmismatch condition (hits < misses; p < 0.01; Figures 2B and 2C ). Additional analysis showed that this power effect
doi:10.1016/j.cub.2013.04.074 pmid:23746635 fatcat:gaa2pcppczenvdpheigtiigtnq