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Complementary contributions of non-REM and REM sleep to visual learning.

ABSTRACT: Sleep is beneficial for learning. However, it remains unclear whether learning is facilitated by non-rapid eye movement (NREM) sleep or by REM sleep, whether it results from plasticity increases or stabilization, and whether facilitation results from learning-specific processing. Here, we trained volunteers on a visual task and measured the excitatory and inhibitory (E/I) balance in early visual areas during subsequent sleep as an index of plasticity. The E/I balance increased during NREM sleep irrespective of whether pre-sleep learning occurred, but it was associated with post-sleep performance gains relative to pre-sleep performance. In contrast, the E/I balance decreased during REM sleep but only after pre-sleep training, and the decrease was associated with stabilization of pre-sleep learning. These findings indicate that NREM sleep promotes plasticity, leading to performance gains independent of learning, while REM sleep decreases plasticity to stabilize learning in a learning-specific manner.

SUBMITTER: Tamaki M

PROVIDER: S-EPMC7483793 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Complementary contributions of non-REM and REM sleep to visual learning.

Tamaki Masako M Wang Zhiyan Z Barnes-Diana Tyler T Guo DeeAnn D Berard Aaron V AV Walsh Edward E Watanabe Takeo T Sasaki Yuka Y

Nature neuroscience 20200720 9

Sleep is beneficial for learning. However, it remains unclear whether learning is facilitated by non-rapid eye movement (NREM) sleep or by REM sleep, whether it results from plasticity increases or stabilization, and whether facilitation results from learning-specific processing. Here, we trained volunteers on a visual task and measured the excitatory and inhibitory (E/I) balance in early visual areas during subsequent sleep as an index of plasticity. The E/I balance increased during NREM sleep ...[more]

PMID: 32690968

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Project description:Highlights • Exploratory study: no systematically altered sleep macrostructure in MDD patients.• Non-REM fast sleep spindle amplitudes higher in unmedicated patients.• Antidepressants altered slow-wave activity and coupling to fast sleep spindles.• Long-term, not short-term medication linked to lower spindle density in patients.• Medicated patients had impaired procedural memory consolidation. Disturbed sleep is a key symptom in major depressive disorder (MDD). REM sleep alterations are well described in the current literature, but little is known about non-REM sleep alterations. Additionally, sleep disturbances relate to a variety of cognitive symptoms in MDD, but which features of non-REM sleep EEG contribute to this, remains unknown. We comprehensively analyzed non-REM sleep EEG features in two central channels in three independently collected datasets (N = 284 recordings of 216 participants). This exploratory and descriptive study included MDD patients with a broad age range, varying duration and severity of depression, unmedicated or medicated, age- and gender-matched to healthy controls. We explored changes in sleep architecture including sleep stages and cycles, spectral power, sleep spindles, slow waves (SW), and SW-spindle coupling. Next, we analyzed the association of these sleep features with acute measures of depression severity and overnight consolidation of procedural memory. Overall, no major systematic alterations in non-REM sleep architecture were found in patients compared to controls. For the microstructure of non-REM sleep, we observed a higher spindle amplitude in unmedicated patients compared to controls, and after the start of antidepressant medication longer SWs with lower amplitude and a more dispersed SW-spindle coupling. In addition, long-term, but not short-term medication seemed to lower spindle density. Overnight procedural memory consolidation was impaired in medicated patients and associated with lower sleep spindle density. Our results suggest that alterations of non-REM sleep EEG in MDD might be more subtle than previously reported. We discuss these findings in the context of antidepressant medication intake and age.

Dataset Information

Complementary contributions of non-REM and REM sleep to visual learning.

Publications

Complementary contributions of non-REM and REM sleep to visual learning.

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