Theta and gamma oscillations during encoding predict subsequent recall

Abstract

Electrophysiological and hemodynamic measures of human brain activity have been shown to distinguish between episodes of encoding items that are later recalled versus those that are not recalled (Paller and Wagner, 2002). Using intracranial recordings from 793 widespread cortical and subcortical sites in 10 epileptic patients undergoing invasive monitoring, we compared oscillatory power at frequencies ranging from 2 to 64 Hz as participants studied lists of common nouns. Significant increases in oscillatory power during encoding predicted subsequent recall, with this effect predominantly in the 4-8 Hz (theta) and 28-64 Hz (gamma) frequency bands. Sites exhibiting increased theta activity during successful encoding were clustered in right temporal and frontal cortex, whereas those exhibiting increased gamma activity appeared bilaterally at widespread cortical locations. These findings implicate theta and gamma oscillatory activity, across a widespread network of cortical regions, in the formation of new episodic memories.

Figure 1.

Increased oscillatory power during encoding predicts subsequent recall. a plots the Wilcoxon rank sum statistic (W_s) for the difference in power between recalled and not recalled words across frequencies from 2 to 64 Hz for recordings taken from an electrode in the inferior-temporal region of subject 3 [Talairach coordinates (left-right, anterior-posterior, inferior-superior) = (-7.1, 8.3, -18.3)]. At this site, power in the 4-8 Hz theta band was higher during the encoding of subsequently recalled words. (The filled gray region represents the 95% confidence interval.) b shows data taken from an electrode in the left temporal-occipital region of subject 4 [Talairach coordinates (left-right, anterior-posterior, inferior-superior) = (-58.3, -57.9, -3.5)]. At this site, power in the 28-64 Hz gamma band was higher during the encoding of subsequently recalled words. c shows the number of electrodes exhibiting significantly greater oscillatory power during successful encoding across frequencies from 2 to 64 Hz. The dashed black line indicates the type I error rate for this analysis (see Materials and Methods). d illustrates the locations of electrodes exhibiting significant power increases in the 4-8 Hz theta band during successful encoding (black symbols; each symbol represents electrodes from a single subject) and those that did not (gray circles). Electrode locations are illustrated on five views of a standard brain. Top left, Right lateral view. Top right, Left lateral view. Center, Inferior view. Bottom left, Left sagittal interhemispheric view. Bottom right, Right sagittal interhemispheric view. e shows the analogous effect for the 28-64 Hz gamma band.

Figure 2.

Decreased oscillatory power during encoding predicts subsequent recall. a plots the Wilcoxon rank sum statistic (W_s) for the difference in power between recalled and not recalled words across frequencies from 2 to 64 Hz for recordings taken from an electrode in the left inferior-temporal region of subject 8 [Talairach coordinates (left-right, anterior-posterior, inferior-superior) = (-30.0, -17.0, -36.3)]. At this site, power in the 9-28 Hz alpha/beta band was lower during the encoding of subsequently recalled words. (The filled gray region represents the 95% confidence interval.) b shows the number of electrodes exhibiting significantly lower oscillatory power during successful encoding across frequencies from 2 to 64 Hz. The dashed black line indicates the type I error rate for this analysis (see Materials and Methods). c illustrates the locations of electrodes exhibiting significant power decreases in the 9-28 Hz alpha/beta band during successful encoding (black symbols; each symbol represents electrodes from a single subject) and those that did not (gray circles). The topographical maps follow the same format seen in Figure 1.

Figure 3.

Time courses of oscillatory SMEs. Averaged across electrodes that exhibited a significant positive SME in the 4-8 Hz theta frequency band (see Materials and Methods), the shaded blue region in a illustrates times (0-2 sec) and frequencies (2-64 Hz) when power was significantly greater during the encoding of subsequently recalled words. b illustrates the average time course for electrodes exhibiting a significant positive oscillatory SME in the 28-64 Hz gamma frequency band. c plots the average time course for electrodes exhibiting a significant negative oscillatory SME in the alpha and beta bands. The color bar to the right of each panel plots the p values for the difference between recalled and not recalled power (blue shades indicate significant increases in oscillations predicting recall, and red shades indicate significant decreases).