Evidence for Human Fronto-Central Gamma Activity during Long-Term Memory Encoding of Word Sequences

Although human gamma activity (30–80 Hz) associated with visual processing is often reported, it is not clear to what extend gamma activity can be reliably detected non-invasively from frontal areas during complex cognitive tasks such as long term memory (LTM) formation. We conducted a memory experiment composed of 35 blocks each having three parts: LTM encoding, working memory (WM) maintenance and LTM retrieval. In the LTM encoding and WM maintenance parts, participants had to respectively encode or maintain the order of three sequentially presented words. During LTM retrieval subjects had to reproduce these sequences. Using magnetoencephalography (MEG) we identified significant differences in the gamma and beta activity. Robust gamma activity (55–65 Hz) in left BA6 (supplementary motor area (SMA)/pre-SMA) was stronger during LTM rehearsal than during WM maintenance. The gamma activity was sustained throughout the 3.4 s rehearsal period during which a fixation cross was presented. Importantly, the difference in gamma band activity correlated with memory performance over subjects. Further we observed a weak gamma power difference in left BA6 during the first half of the LTM rehearsal interval larger for successfully than unsuccessfully reproduced word triplets. In the beta band, we found a power decrease in left anterior regions during LTM rehearsal compared to WM maintenance. Also this suppression of beta power correlated with memory performance over subjects. Our findings show that an extended network of brain areas, characterized by oscillatory activity in different frequency bands, supports the encoding of word sequences in LTM. Gamma band activity in BA6 possibly reflects memory processes associated with language and timing, and suppression of beta activity at left frontal sensors is likely to reflect the release of inhibition directly associated with the engagement of language functions

The paradigm.

<p>A) The task was composed of 35 blocks with each three parts: LTM encoding/rehearsal (9 or 11 trials), WM maintenance (6 or 7 trials) and LTM retrieval. B) In the LTM and WM trials, three words were presented sequentially (0.6 s/word) followed by a rehearsal interval of 3.4 s. C) In retrieval trials, participants reconstructed the word sequences learned during LTM encoding. Three words were shown and each represented by a button. Participants were asked to reproduce the initial order of the words by pressing the buttons in the correct order.</p

Correlation between gamma and beta power.

<p>Correlation between modulations of gamma and beta power at the sensors where the significant effects were found, over subjects (N = 23). A negative correlation was found between gamma and beta power modulations (r = −0.48, p = 0.022).</p

Subsequent memory effect in the gamma band.

<p>A subsequent memory effect was observed in the gamma band (55–65 Hz over left central sensors) when comparing later remembered to later forgotten LTM trials. The effect was significant when considering the first half of the retention interval and including only left fronto-central sensors. The right panel shows the difference in gamma activity when normalized with the variance (z-values) and confirms that the dominant effect is indeed at left central sensors.</p

LTM−WM: effects in the beta band.

<p>A) Time-frequency representation of the sensors in the significant cluster and topographical representations of beta band activity when comparing the rehearsal interval of LTM encoding and WM maintenance trials. A decrease in beta power (15–27 Hz) is shown at sensors marked in the topographical plot. The topography of the z-values is shown in the most right panel. B,C) The sources of the decrease of beta power when comparing LTM encoding to WM maintenance. The sources of this effect are widespread but include LIFG and left insula. Z-values of the statistical comparison (B) and power values between half of the maximum to the maximum value are shown (C). D) The average beta power from sensors in the significant cluster shows the time-course of the effect for all conditions separately during word presentation and rehearsal. E) There was a negative correlation between beta power (LTM−WM/LTM+WM) and performance for each subject on the LTM retrieval test (r = −0.52, p = 0.011, N = 23).</p