Stimulation augments spike sequence replay and memory consolidation during slow-wave sleep

Abstract

Newly acquired memory traces are spontaneously reactivated during slow-wave sleep (SWS), leading to the consolidation of recent memories. Empirical studies found that sensory stimulation during SWS selectively enhances memory consolidation and the effect depends on the phase of stimulation. In this new study, we aimed to understand the mechanisms behind the role of sensory stimulation on memory consolidation using computational models implementing effects of neuromodulators to simulate transitions between awake and SWS sleep, and synaptic plasticity to allow the change of synaptic connections due to the training in awake or replay during sleep. We found that when closed-loop stimulation was applied during the Down states (900-2700) of sleep slow oscillation, particularly right before transition from Down to Up state, it significantly affected the spatio-temporal pattern of the slow-waves and maximized memory replay. In contrast, when the stimulation was presented during the Up states (2700-3600 and 00-900), it did not have a significant impact on the slow-waves or memory performance after sleep. For multiple memories trained in awake, presenting stimulation cues associated with specific memory trace could selectively augment replay and enhance consolidation of that memory and interfere with consolidation of the others (particularly weak) memories. Our study proposes a synaptic level mechanism of how memory consolidation is affected by sensory stimulation during sleep.Significance statementStimulation, such as training-associated cues or auditory stimulation, during sleep can augment consolidation of the newly encoded memories. In this study, we used a computational model of the thalamocortical system to describe the mechanisms behind the role of stimulation in memory consolidation during slow-wave sleep. Our study suggested that stimulation preferentially strengthens the memory traces when delivered at specific phase of slow oscillations just before Down to Up state transition when it makes the largest impact on the spatio-temporal pattern of sleep slow waves. In the presence of multiple memories, presenting sensory cues during sleep could selectively strengthen selected memories. Our study proposes a synaptic level mechanism of how memory consolidation is affected by sensory stimulation during sleep.

Response of sleep slow oscillations to acoustic stimulation is evidenced by distinctive synchronization processes

“…This hypothesis further suggests the existence of some nonexplicit cortical conditions that determine cortical sensitivity to the stimulation (i.e., whether the stimulation would boost SOs dynamics, whether it would be completely ineffective, or even induce awakenings). In line with this hypothesis, recent analyses suggest that the amplitude of SO peaks may facilitate global synchronization of post-neuronal down-states, thereby enhancing the amplitudes of the resulting slow wave troughs (Navarrete et al, 2022;Torres et al, 2021;Wei et al, 2020). Congruently, we found that large and synchronous C1 and C3 events were increased by stimuli during large peaks of the SOs (with average amplitudes larger than +40 μV across all EEG channels, Figures 2e & 2f).…”

Thalamo-cortical spiking model of incremental learning combining perception, context and NREM-sleep

“…Another major aspect of our work is the effect of sleep on the network and on the memories stored in it. The role played by sleep in memory consolidation has been widely studied from an experimental point of view [46,47], but only recently it has become the object of theoretical and computational modelizations [27,[48][49][50]. In our work, we investigated computationally the effect of slow oscillations on the structure and the performances of the network when the STDP plasticity is turned on.…”

Selection of stimulus parameters for enhancing slow wave sleep events with a Neural-field theory thalamocortical computational model

“…Wei et al [21,42,43] tested several ways of closed-loop stimulation, including the protocol of Ngo et al [3], in a cellular level model. Their results showed that the correct spatio-temporal localization of stimuli could facilitate the replay of a cortical sequence associated with the stimulation site, pointing to the need for peaks nesting for strengthening the neural connections.…”

“…An alternative approach to improving the stimulation paradigm that attempts to increase SP and SO events during SWS is the use of mathematical models of brain activity [20,21]. In this way, mechanistic insights about the generation of SP and SO activity can guide the search for a better stimulation that maximizes its efficacy.…”