Novel insights into the role of eye movements during REM sleep in memory consolidation.

Abstract

A large and consistent literature converges in pointing out how hippocampus-dependent memories benefit from slow wave activity during non-rapid eye movement sleep (NREM). The declarative memory traces are repeatedly reactivated during slow-wave sleep (SWS), promoting long-term storage at the cortical level [1, 2]. Sleep also supports the consolidation of procedural memory underlying problem-solving and the acquisition of new rules or cognitive strategies [3–5], but in this context, the specific role of SWS is more controversial. While some studies support the possible involvement of SWS [6, 7], others propose rapid eye movement (REM) sleep as the main responsible for the sleep-dependent integration of information supporting creative problem solving [8]. Meanwhile, the iterative and synergic interleaving of REM and NREM stage characteristics has been recently conceptualized to explain the sleep effect on creative problem-solving skills [3]. However, evidence of specific cortical processes representing the actual reactivation of this kind of memories during paradoxical sleep is still scarce. Another gap in the literature addressing the relationship between REM sleep and memory function is represented by the common practice of considering paradoxical sleep as a homogeneous state, especially in human studies [9]. However, from decades, two neurophysiologically distinct REM substates have been identified [9, 10], namely the tonic and phasic REM sleep, and the available literature suggested a functional heterogeneity of these two substates in memory consolidation [11–13]. In the August issue of SLEEP, van den Berg and collaborators [14] addressed some of these open and scarcely explored questions, providing novel insight into the role of the electroencephalographic (EEG) activity during human tonic and phasic REM sleep in the consolidation of novel problem-solving skills. Two different groups of healthy young participants (n = 20 per group) performed the Tower of Hanoi task before and after (1) an undisturbed 8-hour period of sleep, or (2) a same-length wake period. Each group also took part in another similar condition (in counterbalanced order) in which a non-learning control task was performed. The study [14] adopted a quite novel approach to address the involvement of REM sleep in memory consolidation, evaluating the event-related spectral perturbations (ERSP) time-locked to the eye movement (EM) peaks. This analysis allowed the authors to estimate specific oscillatory EEG components surrounding EMs during REM sleep, unraveling stable cortical patterns associated with EMs in the post-learning night compared with the control (non-learning) condition. Furthermore, the authors [14] classified the EMs during REM sleep into “bursts,” defining phasic REM state, and “isolated” EMs, proposed as a proxy of tonic REM state. This categorization led to evaluating the differential contribution of phasic and tonic REM sleep to the consolidation of problem-solving skills. Besides confirming the beneficial effect of sleep on problem-solving performance [3, 4], the study highlighted an intriguing relationship between sleep-dependent behavioral improvement and the EEG correlates of EMs that characterize post-learning REM sleep. In detail, the patterns accompanying EMs during post-learning phasic REM sleep, as compared to a control night, included increased oscillations in the 2–16 Hz range following the EMs peak, which differed as a function of scalp location and frequency (prefrontal ~2 Hz, central ~7 Hz, occipital ~8 Hz, and ~16 Hz). During post-learning tonic REM sleep, EMs were preceded by increased activity in the 9–14 Hz range in central (~9 Hz, ~14 Hz), parietal (~13 Hz), and occipital areas (~4Hz, ~6 Hz, and ~12 Hz), and followed by increases at ~3 and ~6 Hz in prefrontal and occipital regions, respectively. Interestingly, the changes in the oscillatory activities of phasic REM sleep were correlated with the overnight changes in behavioral performance (speed/accuracy), while no significant association has been found for tonic REM sleep. Overall, the presence of post-learning variations in the EEG activity time-locked to EMs during REM sleep indicates an engagement of the cortical processes that occur during EMs in the procedural memory consolidation. This evidence involves both phasic and tonic REM periods, albeit only those changes that occurred during phasic REM periods were predictive of the improvement in cognitive performance, suggesting a different functional role of the two substates in the sleep-dependent consolidation processes. In discussing the results, the authors [14] interpreted the cortical activity in the ~8–16 Hz range as sensorimotor rhythms (SMR), although others have defined the same activity as Mu [15]. Moreover, all the activity in the ~2–8 Hz range has been defined