Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Memory Consolidation Potentiated by Slow Oscillations During Sleep


Nature 444, 610-613 (30 November 2006)

Boosting slow oscillations during sleep potentiates memory

Lisa Marshall, Halla Helgadóttir, Matthias Mölle and Jan Born

University of Lübeck, Department of Neuroendocrinology, Haus 23a, Ratzeburger Allee 160, 23538 Lübeck, Germany


There is compelling evidence that sleep contributes to the long-term consolidation of new memories. This function of sleep has been linked to slow (<1 Hz) potential oscillations, which predominantly arise from the prefrontal neocortex and characterize slow wave sleep. However, oscillations in brain potentials are commonly considered to be mere epiphenomena that reflect synchronized activity arising from neuronal networks, which links the membrane and synaptic processes of these neurons in time. Whether brain potentials and their extracellular equivalent have any physiological meaning per se is unclear, but can easily be investigated by inducing the extracellular oscillating potential fields of interest. Here we show that inducing slow oscillation-like potential fields by transcranial application of oscillating potentials (0.75 Hz) during early nocturnal non-rapid-eye-movement sleep, that is, a period of emerging slow wave sleep, enhances the retention of hippocampus-dependent declarative memories in healthy humans. The slowly oscillating potential stimulation induced an immediate increase in slow wave sleep, endogenous cortical slow oscillations and slow spindle activity in the frontal cortex. Brain stimulation with oscillations at 5 Hz—another frequency band that normally predominates during rapid-eye-movement sleep—decreased slow oscillations and left declarative memory unchanged. Our findings indicate that endogenous slow potential oscillations have a causal role in the sleep-associated consolidation of memory, and that this role is enhanced by field effects in cortical extracellular space.

Slow oscillations reflect widespread 'up' and 'down' states of network activity. These oscillations are generated within the neocortex and are most prominent during slow wave sleep (SWS); the up and down states reflect, respectively, global neuronal depolarization with excitation, and neuronal hyperpolarization with neuronal silence. Essentially owing to its synchronizing influence on neuronal activity within the neocortex and in dialogue with thalamic and hippocampal circuitry, the slow oscillation has been suspected to underlie the consolidation of memory during sleep. The slow oscillation signal peaks at 0.7–0.8 Hz, although spectral components can extend into the slow delta band (1–4 Hz). We have examined the role of slow oscillations in memory consolidation by inducing them through transcranial application of oscillating potentials during early nocturnal non-rapid-eye-movement (non-REM) sleep after a learning period.

Hippocampus-dependent declarative memory was assessed by a paired-associate learning task, with memory retention measured by the difference in the number of words recalled when tested after sleep and the number recalled at learning before sleep. As expected from previous studies using the same procedure, retrieval testing after sleep showed an increase in performance, compared to learning before sleep, in both the slow oscillation stimulation and the sham stimulation conditions.

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