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Abstract

Sleep benefits declarative memory via a process of offline reactivation that
consolidates hippocampus dependent memory traces into neocortical
networks for stable memory storage. Based on recent evidence suggesting
that awake rehearsal can also lead to rapid systems consolidation, in this
study we investigated how sleep influences the consolidation of rehearsal-
induced early neocortical memory traces. Participants encoded and
recalled object-place associations across multiple rehearsal rounds either
in the morning (wake group, n=19) or in the evening (sleep group, n=20)
and twelve hours later after a day of wakefulness or a night of sleep. During
the task, functional brain activity was measured with fMRI. In addition to a
behavioral benefit of sleep for memory retention, we observed differential
changes between the groups in functional brain activity during memory
recall across a network spanning the precuneus, thalamus and striatum
when controlling for potentially confounding effects of time spent awake.
The effect was characterized by a robust increase in activation levels from
session 1 to session 2 in the sleep group, and a transient decrease during
the first recall repetition of session 2 in the wake group. Upregulation of
activity in the thalamus and striatum was associated with behavioral
benefits. Importantly, all three regions decreased their functional
connectivity with the hippocampus more strongly across sleep. Altogether,
our data indicate that early neocortical memory traces undergo additional
sleep-dependent memory consolidation. In addition to further promoting
consolidation mechanisms within the declarative memory subsystems,
sleep seems to specifically benefit the integration of ear ly neocortical
traces across different memory systems.