Medial temporal theta state before an event predicts episodic encoding success in humans

Abstract

We report a human electrophysiological brain state that predicts successful memory for events before they occur. Using magnetoencephalographic recordings of brain activity during episodic memory encoding, we show that amplitudes of theta oscillations shortly preceding the onsets of words were higher for laterrecalled than for later-forgotten words. Furthermore, single-trial analyses revealed that recall rate in all 24 participants tested increased as a function of increasing prestimulus theta amplitude. This positive correlation was independent of whether participants were preparing for semantic or phonemic stimulus processing, thus likely signifying a memory-related theta state rather than a preparatory task set. Source analysis located this theta state to the medial temporal lobe, a region known to be critical for encoding and recall. These findings provide insight into state-related aspects of memory formation in humans, and open a perspective for improving memory through theta-related brain states.hippocampus ͉ magnetoencephalography ͉ memory ͉ oscillations ͉ prestimulus T he neurocognitive processing that is instantiated by an event determines the longevity and quality of memory for that event. Studies using electrophysiological (1-3) and hemodynamic (4-9) techniques have shown that episodic memory-the ability to recollect an event and its spatiotemporal context-is associated with specific patterns of brain activity during the time the event is originally experienced. Recent observations that perception of a stimulus can be influenced by prestimulus brain activity (10, 11) raise the additional possibility that the brain state immediately preceding an event could predict later episodic memory. This possibility is supported by findings in rodents that the amplitude of hippocampal theta (3-8 Hz) oscillations, which are held to be important modulators of the induction of synaptic plasticity (12)(13)(14), is associated with enhanced learning in classical conditioning even before stimulus onset (15)(16)(17). Because the medial temporal lobe (MTL) and, in particular, the hippocampus are also critical for episodic memory encoding in humans (18)(19)(20), prestimulus mediotemporal theta states might be linked to effective episodic memory encoding.For prestimulus brain activity to qualify as a general encodingrelated state, it should be associated with encoding success independent of preparatory factors related to the cognitive control of particular task demands. A recent event-related potential (ERP) study of episodic memory showed that prestimulus, frontal-negative slow shifts predicted successful encoding of words 250 ms before the onset of word presentation (21). Critically, this prestimulus effect was observed only if the prestimulus task cue required a semantic judgment on the word and not when the task cue required an orthographic judgment (21). Therefore, this prestimulus ERP difference depended on a specific task set and is unlikely to reflect a general encodingrelated state.To examine whether prestimulus the...

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

“…This result is consistent with studies in human patients with epilepsy showing positive correlations between prestimulus theta in the MTL and memory (40)(41)(42), and it suggests that theta oscillations are involved in "preparatory" mechanisms that bring the hippocampus into an "online" state (5). Because the monkeys in the current study were not explicitly trained to form a memory of the stimuli, it is unlikely that this preparatory state reflects an overt intention, or motivation, to remember the stimulus.…”

“…We next considered whether there was any relationship between modulations in theta-band power and recognition memory performance on the VPLT. In view of previous studies showing positive correlations between prestimulus theta in the human MTL and memory (40)(41)(42), we examined the possibility that the strength of theta-band activity during the baseline period leading up to stimulus onset might predict the strength of memory encoding. We calculated the power in the 3-to 20-Hz range for each LFP during the 800 ms before novel presentations of the 30 stimuli for which the monkey showed the best subsequent recognition memory (high recognition) and before novel presentations of the 30 stimuli for which the monkey showed the worst subsequent recognition memory (low recognition).…”

Slow-theta power decreases during item-place encoding predict spatial accuracy of subsequent context recall

“…In fact, as we confirmed with post hoc analyses, we did not find positive prestimulus SMEs in hippocampal sources. Although other studies ana lyzing the encoding of words have found positive SMEs in prestimulus theta of MTL regions, including hippocampus (Fell et al, 2011;Guderian et al, 2009), it was recently demonstrated that increased prestimulus hippocampal theta activity only predicts subsequent item recognition (Merkow et al, 2014). However, free recall, which depends more on associative encoding as our task, shows a negative SME in post stimulus hippocampal slow theta.…”

“…However, other studies have reported negative SMEs in the broad theta band (Burke et al, 2013;Guderian et al, 2009;Long et al, 2014;Sederberg et al, 2007). These theta power decreases are seen during the successful encoding of single items and inter item associations (Greenberg et al, 2015) and are widely detected with surface sensors or iEEG contacts targeting medial temporal lobe (MTL) and fronto temporal structures (Greenberg et al, 2015;Long et al, 2014).…”

Differences in EEG power in young and mature healthy adults during an incidental/spatial learning task are related to age and execution efficiency

“…It has been proposed that several aspects of theta activity are involved in the sustained attention to and maintenance of information in working memory (increasing power with increasing memory load) as well as in episodic encoding and retrieval (transient increase of theta power as a consequence of event-related synchronization, mainly in parietal sites) (Klimesch 1999;Klimesch et al 2010). Additionally, an increase in the theta oscillations in temporal regions preceding the presentation of a stimulus predicts its successful encoding (Guderian et al 2009). Therefore, induced responses in both the EEG theta and gamma bands show higher activity when previously observed items are correctly recognized compared with the induced responses when novel items are correctly rejected (old/new effect) during information retrieval periods (Osipova et al 2006).…”