Sleep, plasticity and memory from molecules to whole-brain networks

Ted Abel, Robbert Havekes, Jared M Saletin, Matthew P Walker

Research output: Contribution to journalReview articleAcademicpeer-review

241 Citations (Scopus)
39 Downloads (Pure)

Abstract

Despite the ubiquity of sleep across phylogeny, its function remains elusive. In this review, we consider one compelling candidate: brain plasticity associated with memory processing. Focusing largely on hippocampus-dependent memory in rodents and humans, we describe molecular, cellular, network, whole-brain and behavioral evidence establishing a role for sleep both in preparation for initial memory encoding, and in the subsequent offline consolidation of memory. Sleep and sleep deprivation bidirectionally alter molecular signaling pathways that regulate synaptic strength and control plasticity-related gene transcription and protein translation. At the cellular level, sleep deprivation impairs cellular excitability necessary for inducing synaptic potentiation and accelerates the decay of long-lasting forms of synaptic plasticity. In contrast, rapid eye movement (REM) and non-rapid eye movement (NREM) sleep enhance previously induced synaptic potentiation, although synaptic de-potentiation during sleep has also been observed. Beyond single cell dynamics, large-scale cell ensembles express coordinated replay of prior learning-related firing patterns during subsequent NREM sleep. At the whole-brain level, somewhat analogous learning-associated hippocampal (re)activation during NREM sleep has been reported in humans. Moreover, the same cortical NREM oscillations associated with replay in rodents also promote human hippocampal memory consolidation, and this process can be manipulated using exogenous reactivation cues during sleep. Mirroring molecular findings in rodents, specific NREM sleep oscillations before encoding refresh human hippocampal learning capacity, while deprivation of sleep conversely impairs subsequent hippocampal activity and associated encoding. Together, these cross-descriptive level findings demonstrate that the unique neurobiology of sleep exerts powerful effects on molecular, cellular and network mechanisms of plasticity that govern both initial learning and subsequent long-term memory consolidation.

Original languageEnglish
Pages (from-to)R774-R788
Number of pages15
JournalCurrent Biology
Volume23
Issue number17
DOIs
Publication statusPublished - 9-Sep-2013
Externally publishedYes

Keywords

  • Animals
  • Brain
  • Humans
  • Memory
  • Neuronal Plasticity
  • Rodentia
  • Sleep
  • Sleep Deprivation
  • Sleep, REM
  • SLOW-WAVE SLEEP
  • EYE-MOVEMENT SLEEP
  • LONG-TERM POTENTIATION
  • HIPPOCAMPAL SYNAPTIC PLASTICITY
  • ASTROCYTE-DERIVED ADENOSINE
  • CEREBRAL PROTEIN-SYNTHESIS
  • REM-SLEEP
  • DECLARATIVE MEMORY
  • DEPRIVATION IMPAIRS
  • IN-VIVO

Cite this