Rapid memory stabilization by transient theta coherence in the human medial temporal lobe

Abstract

Presenting stimuli again after presentation of intervening stimuli improves their retention, an effect known as the spacing effect. However, using event-related potentials (ERPs), we had observed that immediate, in comparison to spaced, repetition of pictures induced a positive frontal potential at 200-300 ms. This potential appeared to emanate from the left medial temporal lobe (MTL), a structure critical for memory consolidation. In this study, we tested the behavioral relevance of this signal and explored functional connectivity changes during picture repetition. We obtained high-density electroencephalographic recordings from 14 healthy subjects performing a continuous recognition task where pictures were either repeated immediately or after 9 intervening items. Conventional ERP analysis replicated the positive frontal potential emanating from the left MTL at 250-350 ms in response to immediately repeated stimuli. Connectivity analysis showed that this ERP was associated with increased coherence in the MTL region-left more that right-in the theta-band (3.5-7 Hz) 200-400 ms following immediate, but not spaced, repetition. This increase was stronger in subjects who better recognized immediately repeated stimuli after 30 min. These findings indicate that transient theta-band synchronization between the MTL and the rest of the brain at 200-400 ms reflects a memory stabilizing signal. V C 2015 Wiley Periodicals, Inc.

Absence of an early hippocampal encoding signal after medial temporal lesions: No consequence for the spacing effect

“…Thus, it appears that both MTLs (and hippocampi) are necessary to produce this signal. This result is compatible with a previous study of electrical coherence: during the processing of immediately repeated stimuli, the extended MTL of both sides, rather than only the left side, displayed increased connectivity in the theta frequency band with the rest of the brain (Theze et al, 2016).…”

“…First, amnesic patients with Wernicke-Korsakoff syndrome did not produce this signal (Nahum et al, 2015). Second, electric coherence of the MTL in response to immediately repeated stimuli in this period correlated with later recognition (Theze, Guggisberg, Nahum, & Schnider, 2016); stronger coherence predicted better recognition after 30 min. These studies suggest that early, transient activation of the MTL upon repetition of information held in STM is linked to encoding of information in LTM, possibly also to the SE.…”

“…The main interest of the study was the presence or absence of the frontal potential in response to One-Back items observed in previous studies (James et al, 2009;Nahum et al, 2015;Theze et al, 2016).…”

“…In the present study we explored the involvement of the MTL in immediate stimulus repetition and its influence on the SE. A group of subjects with focal MTL lesions due to stroke made the same continuous recognition task as in the earlier studies (James et al, 2009;Nahum et al, 2011;Theze et al, 2016) containing stimuli that were repeated immediately or after presentation of nine intervening items.…”

Early signal from the hippocampus for memory encoding

“…Using a continuous recognition task, James, Morand, Bareellona‐Lehmann, Michel, and Schnider () found that immediate repetition of pictures transiently activated the MTL in this period. Subsequent studies not only confirmed the hippocampal provenance of this signal using depth electrodes (Nahum et al, ), but also indicated a memory‐protective effect (Thézé, Guggisberg, Nahum, & Schnider, ). Patients having amnesia due to Wernicke–Korsakoff disease (Nahum et al, ) or medial temporal stroke (Tautvydaitė et al, ) did not exhibit this signal.…”