Learning New Vocabulary Implicitly During Sleep Transfers With Cross-Modal Generalization Into Wakefulness.

Matthieu Koroma,Maxime Elbaz,Sid Kouider,Damien Léger

doi:10.3389/fnins.2022.801666

Abstract

New information can be learned during sleep but the extent to which we can access this knowledge after awakening is far less understood. Using a novel Associative Transfer Learning paradigm, we show that, after hearing unknown Japanese words with sounds referring to their meaning during sleep, participants could identify the images depicting the meaning of newly acquired Japanese words after awakening (N = 22). Moreover, we demonstrate that this cross-modal generalization is implicit, meaning that participants remain unaware of this knowledge. Using electroencephalography, we further show that frontal slow-wave responses to auditory stimuli during sleep predicted memory performance after awakening. This neural signature of memory formation gradually emerged over the course of the sleep phase, highlighting the dynamics of associative learning during sleep. This study provides novel evidence that the formation of new associative memories can be traced back to the dynamics of slow-wave responses to stimuli during sleep and that their implicit transfer into wakefulness can be generalized across sensory modalities.

Highlights

It is well established that memories acquired during the day can be consolidated during sleep (Walker et al, 2003; Rasch and Born, 2013)
This effect came from a higher memory performance for words from the non-Rapid Eye Movement (NREM) list compared to words that were not presented during sleep, i.e., the control list
Memory was above chance level for words from the NREM list [59%, CI = (52, 66)], Cohen’s d = 0.58, twotailed Student’s t-test against chance level [50%, t(21) = 2.7, p = 0.013, corrected for false discovery rate (Benjamini and Yekutieli, 2001; Figure 2A)]

Summary

Introduction

It is well established that memories acquired during the day can be consolidated during sleep (Walker et al, 2003; Rasch and Born, 2013). Whether new information can be acquired during sleep has, given rise to controversial or inconsistent results until recently [e.g., Bruce et al, 1970; see Peigneux et al (2001) for a review]. A series of convergent findings have demonstrated that learning during sleep is a reality, its extent and flexibility remain to be clarified [Arzi et al, 2012; see Puchkova (2020) for a review]. Evidence of learning during sleep was initially limited to fairly simple mechanisms such as sensory conditioning (Arzi et al, 2012, 2014) and perceptual encoding (Ruch et al, 2014; Andrillon and Kouider, 2016; Andrillon et al, 2017). Recent results reveal that verbal associations can be acquired during sleep, demonstrating that the learning abilities of the sleeping brain can extend to higher levels of representations (Züst et al, 2019).

Methods

Results

Conclusion