The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats

The mechanisms underlying off‐line consolidation of memory during sleep are elusive. Learning of hippocampus‐dependent tasks increases neocortical slow oscillation synchrony, and thalamocortical spindle and hippocampal ripple activity during subsequent non‐rapid eye movement sleep. Slow oscillations representing an oscillation between global neocortical states of increased (up‐state) and decreased (down‐state) neuronal firing temporally group thalamic spindle and hippocampal ripple activity, which both occur preferentially during slow oscillation up‐states. Here we examined whether slow oscillations also group learning‐induced increases in spindle and ripple activity, thereby providing time‐frames of facilitated hippocampus‐to‐neocortical information transfer underlying the conversion of temporary into long‐term memories. Learning (word‐pairs in humans, odor–reward associations in rats) increased slow oscillation up‐states and, in humans, shaped the timing of down‐states. Slow oscillations grouped spindle and rat ripple activity into up‐states under basal conditions. Prior learning produced in humans an increase in spindle activity focused on slow oscillation up‐states. In rats, learning induced a distinct increase in spindle and ripple activity that was not synchronized to up‐states. Event‐correlation histograms indicated an increase in spindle activity with the occurrence of ripples. This increase was prolonged after learning, suggesting a direct temporal tuning between ripples and spindles. The lack of a grouping effect of slow oscillations on learning‐induced spindles and ripples in rats, together with the less pronounced effects of learning on slow oscillations, presumably reflects a weaker dependence of odor learning on thalamo‐neocortical circuitry. Slow oscillations might provide an effective temporal frame for hippocampus‐to‐neocortical information transfer only when thalamo‐neocortical systems are already critically involved during learning