Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations

Abstract

Learning is assumed to induce specific changes in neuronal activity during sleep that serve the consolidation of newly acquired memories. To specify such changes, we measured electroencephalographic (EEG) coherence during performance on a declarative learning task (word pair associations) and subsequent sleep. Compared with a nonlearning control condition, learning performance was accompanied with a strong increase in coherence in several EEG frequency bands. During subsequent non-rapid eye movement sleep, coherence only marginally increased in a global analysis of EEG recordings. However, a striking and robust increase in learning-dependent coherence was found when analyses were performed time-locked to the occurrence of slow oscillations (<1 Hz). Specifically, the surface-positive half-waves of the slow oscillation resulting from widespread cortical depolarization were associated with distinctly enhanced coherence after learning in the slow-oscillatory, delta, slow-spindle, and gamma bands. The findings identify the depolarizing phase of the slow oscillations in humans as a time period particularly relevant for a reprocessing of memories in sleep.

Fig. 2.

Coherence analysis time-locked to slow oscillation. (A) Traces exemplifying extraction of slow oscillation (middle trace) and spindle activity (bottom trace) from sleep EEG (upper trace) in a single subject. Shaded area, the depolarizing positive-going phase of the slow oscillation; black bar, the preceding –1- to 0-sec interval used in some analyses as reference. (B) Coherence maps for slow oscillatory (Left), delta (Center), lower spindle (Right Lower), and gamma (Right Lower) bands during the positive-going phase of slow oscillation (time-locked to the negative peak of slow oscillation and adjusted to the preceding 1-sec interval). Maps indicate results for the entire subject sample (n = 13). Significant coherence differences (P < 0.05) were marked with solid lines for higher coherence during the learning condition and dashed lines for higher coherence during the nonlearning condition. In addition, electrode sites are indicated at which power on the learning condition was significantly (P < 0.05) higher (•) or lower (which never happened) in comparison with the nonlearning condition. Bar diagrams indicate total number of greater coherences in the learning (hatched bars) and nonlearning (white bars) condition. ***, P < 0.001; *, P < 0.05.

Fig. 1.

Coherence maps during task performance before sleep in the classical EEG bands (Upper) and during stage 2 sleep and SWS, respectively, in the slow-oscillation and gamma bands, which were the only bands revealing significant coherence maps in the global analysis of sleep recordings (Lower). Maps indicate results for the entire subject sample (n = 13). Coherences were calculated for 276 pairs of electrode sites (○). Significant coherence differences (P < 0.05) were marked with solid lines for higher coherence during the learning condition and dashed lines for higher coherence during the nonlearning condition. Total numbers of electrode pairs with significant coherence differences between learning (L) and nonlearning (NL) and results of the χ² tests are indicated below each map. A map was marked NS (not significant) if the χ² tests failed to indicate significance. In addition, electrode sites are indicated at which power in the learning condition was significantly (P < 0.05) higher (•) or lower (inserted second circle) in comparison with the nonlearning condition.