There is compelling evidence that sleep contributes to the long-term consolidation of new memories1. This function of sleep has been linked to slow (<1 Hz) potential oscillations, which predominantly arise from the prefrontal neocortex and characterize slow wave sleep2,3,4. 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 time5. 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 interest6,7,8. 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.
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We thank H. Koller for help in designing the stimulation apparatus, H. Schuster, H. Siebner, B. Rasch and U. Wagner for discussions of our results, and A. Otterbein, S. Uyanik, P. Paul, R. Krebs and M. Rohwer for technical assistance. This work is supported by the Deutsche Forschungsgemeinschaft.
Author Contributions L.M. and H.H. conducted the experiments. L.M., M.M. and J.B. analysed the data and wrote the paper.
This file contains Supplementary Methods and Results, describing the methods in detail and corresponding supplementary results (including analyses of spindle counts and controls of unspecific cognitive and hormonal effects); Supplementary Figure 1 and Legend, Supplementary Table 1: Sleep during the nights of Stimulation and Sham stimulation and Supplementary references.
This file contains the lists in English and German used in the word-paired associate learning task.