New learning during sleep

Ruch, Simon; Züst, Marc; Wiest, Roland; Henke, Katharina (28 June 2019). New learning during sleep (Unpublished). In: Annual Meeting Swiss Society for Sleep Research, Sleep Medicine and Chronobiology (SSSSC) 2019. Université de Fribourg, Fribourg, Switzerland. 27.06.-28.06.2019.

Background:
Can humans learn new information while asleep? Sleep lacks the consciousness and the neurochemical milieu (e.g. high acetylcholine) thought to be critical for learning. Furthermore, sleep’s contribution to memory consolidation and synaptic renormalization might conflict with de novo learning. Learning while asleep thus appears to be impossible. Yet, growing evidence suggests that the sleeping brain is able to process and store simple information such as single sounds and words or novel associations between tones and odours. To study more complex forms of learning, we tested whether humans can form novel verbal associations during slow-wave sleep. We hypothesized that learning during sleep would depend on the presence of peaks of slow-waves during word presentation because peaks define brief, wake-like periods of enhanced neural excitability during sleep.

Methods:
We played pairs of foreign-sounding pseudowords and randomly selected German translation words (e.g. “tofer = Haus”, or “aryl = Schlüssel”) to 41 German speaking participants who were in slow-wave sleep during an afternoon nap. After the nap, we administered an implicit memory test in which participants had to guess whether the foreign-sounding words designated a small or large object. Successful learning during sleep should yield above chance guessing accuracy with respect to the sleep-played translation word (i.e. “tofer” should be said to represent a “large”, “aryl” a “small” object).

Results:
Participants’ performance in the implicit memory test exceeded chance level, which is evidence of successful learning during sleep. Analyses of slow-wave activity during word presentation suggested that learning during sleep was bound to slow-wave peaks: implicit memory performance was best when presentation of the second word of a pair (e.g., ‘‘Haus’’ of ‘‘tofer = Haus’’) coincided with an ongoing peak during sleep. fMRI recorded in a subset of participants at test suggested that implicit retrieval of sleep-formed memories activated hippocampus.

Conclusions:
We conclude that humans unconsciously formed new verbal associations during sleep and that learning was mediated by the neural activity and excitability provided by slow-wave peaks. Despite sleep’s role in memory consolidation and synaptic renormalization, the sleeping brain thus retains its learning ability even for complex forms of learning such as the acquisition of hippocampus-dependent verbal relational memories.

Acknowledgements:
The findings presented in this talk have been published in the Journal Current Biology: Züst, M. A., Ruch, S., Wiest, R., & Henke, K. (2019). Implicit Vocabulary Learning during Sleep Is Bound to Slow-Wave Peaks. Current Biology, 29(4), 541–553. https://doi.org/10.1016/j.cub.2018.12.038

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