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 later-recalled 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.

Fig. 1.

Partial least squares analysis of theta amplitudes. The bottom plot in A shows the relative contribution of each frequency (between 3 Hz and 8 Hz) to the topographic maps shown at the top, indicating peak differences around 7 Hz. Blue regions in the maps denote higher theta amplitudes for later-recalled than later-forgotten words; red regions denote the converse. Maps display bootstrap ratios (BR) of the sensor saliences to their standard errors (analogous to z scores). One short, 7-Hz wavelet was used for B. The real parts of the wavelets used are shown at the top.

Fig. 2.

Time course of theta amplitude responses. (A) Later-recalled words (solid lines) are associated with stronger prestimulus increases in theta amplitude than are later-forgotten words (dashed lines) at left anterior temporal sensors (Upper Left) and stronger poststimulus decreases in theta amplitude at right posterior occipitotemporal sensors (Upper Right). Amplitude is given in femtotesla (fT). Gray bars indicate significant differences at P < 0.05. (Lower) Graphs show the corresponding t values as a function of time, with the dotted lines indicating the significance threshold (df = 23, P < 0.05). (B) Effects of level of processing (deep vs. shallow) at study. The prestimulus increase and poststimulus decrease in theta amplitude for later-recalled words are independent of level of processing. Error bars denote SEM.

Fig. 3.

Recall rates across participants (y axis) as a function of LOP (black vs. gray) and theta amplitude (x axis; ranks 1 to 5).

Fig. 4.

Current density reconstructions of prestimulus theta amplitudes. Later-recalled words (Left) are associated with a stronger theta current source than are later-forgotten words (Right) in the medial temporal lobe. Upper shows the right hemisphere is in the foreground, with the brain tilted to expose the ventromedial surface of the left temporal lobe. Lower shows the reverse.