Oscillatory Reinstatement Enhances Declarative Memory

Abstract

Declarative memory recall is thought to involve the reinstatement of neural activity patterns that occurred previously during encoding. Consistent with this view, greater similarity between patterns of activity recorded during encoding and retrieval has been found to predict better memory performance in a number of studies. Recent models have argued that neural oscillations may be crucial to reinstatement for successful memory retrieval. However, to date, no causal evidence has been provided to support this theory, nor has the impact of oscillatory electrical brain stimulation during encoding and retrieval been assessed. To explore this we used transcranial alternating current stimulation over the left dorsolateral prefrontal cortex of human participants [n = 70, 45 females; age mean (SD) = 22.12 (2.16)] during a declarative memory task. Participants received either the same frequency during encoding and retrieval (60–60 or 90–90 Hz) or different frequencies (60–90 or 90–60 Hz). When frequencies matched there was a significant memory improvement (at both 60 and 90 Hz) relative to sham stimulation. No improvement occurred when frequencies mismatched. Our results provide support for the role of oscillatory reinstatement in memory retrieval.SIGNIFICANCE STATEMENT Recent neurobiological models of memory have argued that large-scale neural oscillations are reinstated to support successful memory retrieval. Here we used transcranial alternating current stimulation (tACS) to test these models. tACS has recently been shown to induce neural oscillations at the frequency stimulated. We stimulated over the left dorsolateral prefrontal cortex during a declarative memory task involving learning a set of words. We found that tACS applied at the same frequency during encoding and retrieval enhances memory. We also find no difference between the two applied frequencies. Thus our results are consistent with the proposal that reinstatement of neural oscillations during retrieval supports successful memory retrieval.

A review of neurobiological factors underlying the selective enhancement of memory at encoding, consolidation, and retrieval

“…Hence, SCERT assumes that selective memory enhancement is not elicited by the occurrence of specific oscillatory activity per se, but rather selective memory enhancement is elicited when the frequency of oscillatory activity during retrieval is congruent with that which occurred during encoding. This is known as the oscillatory reinstatement hypothesis (Javadi et al, 2017).…”

“…In attempt to provide the first causal evidence for the oscillatory reinstatement hypothesis, Javadi et al (2017) used transcranial alternating current stimulation (tACS) to experimentally induce implicit neural contexts during encoding and retrieval. Notably, tACS is a non-invasive electrical brain stimulation technique which has the capacity for neuronal entrainment whereby neural oscillations synchronise to the specific frequency of stimulation (Antal & Paulus, 2013;Helfrich et al, 2014).…”

“…The American psychologist, William James, acknowledged this discrepancy over 100 years ago with his question noted above. Since then, researchers have attempted to identify which factors determine whether a memory will be selectively enhanced in comparison to other memories (Buchanan & Adolphs, 2002;Javadi, Glen, Halkiopoulos, Schulz, & Spiers, 2017;LaBar & Cabeza, 2006;LeBlanc, McConnell, & Monteiro, 2015;McGaugh, 2018;Oudiette & Paller, 2013;Rasch & Born, 2013;Watrous & Ekstrom, 2014). This review will discuss how factors contribute to selective memory enhancement during each stage of processing: encoding, consolidation, and retrieval.…”

Theta Phase-dependent Modulation of Perception by Concurrent Transcranial Alternating Current Stimulation and Periodic Visual Stimulation

“…In the present study, we used concurrent tACS applied over the early visual cortex (V1) or dorsolateral prefrontal cortex (DLPFC) and visual stimulation in the theta (4.1 Hz) range to investigate if varying phase synchrony between them can affect perceptual performance in a visual matching task. We included DLPFC as a control location as it is associated with higher level cognitive processes such as short and long-term memory (e.g., Crowley, Bendor, & Javadi, 2019;Curtis & D'Esposito, 2003;Javadi, Glen, Halkiopoulos, Schulz, & Spiers, 2017;Javadi & Walsh, 2012) Therefore, it would not be likely to affect lower level perceptual performance. We also investigated if alpha stimulation (10 Hz) would affect task performance as this is another frequency range that has been repeatedly linked to visual perception (e.g., Babiloni, Vecchio, Bultrini, Luca Romani, & Rossini, 2005;Busch et al, 2009;Chai et al, 2018;Kanai et al, 2008;Mathewson et al, 2009;Spaak et al, 2014).…”

The modulatory effect of oscillatory reinstatement during slow-wave sleep on declarative memory consolidation

“…The first causal evidence in support of SCERT's assumption that memory recall is facilitated by the reinstatement of neural oscillations was demonstrated using transcranial alternating current stimulation (tACS) to experimentally induce implicit neural contexts during encoding and retrieval (Javadi et al, 2017). Notably, tACS is a non-invasive electrical brain stimulation technique which has the capacity for neuronal entrainment whereby neural MODULATION OF DECLARATIVE MEMORY CONSOLIDATION 5 oscillations synchronise to the frequency of stimulation (Antal & Paulus, 2013;Helfrich et al, 2014;Strüber, Rach, Trautmann-Lengsfeld, Engel, & Hermann, 2014).…”