Temporal associations between sleep slow oscillations, spindles and ripples

Abstract

The systems consolidation of memory during slow-wave sleep (SWS) is thought to rely on a dialogue between hippocampus and neocortex that is regulated by an interaction between neocortical slow oscillations (SOs), thalamic spindles and hippocampal ripples. Here, we examined the occurrence rates of and the temporal relationships between these oscillatory events in rats, to identify the possible direction of interaction between these events under natural conditions. To facilitate comparisons with findings in humans, we combined frontal and parietal surface EEG with local field potential (LFP) recordings in medial prefrontal cortex (mPFC) and dorsal hippocampus (dHC). Consistent with a top-down driving influence, EEG SO upstates were associated with an increase in spindles and hippocampal ripples. This increase was missing in SO upstates identified in mPFC recordings. Ripples in dHC recordings always followed the onset of spindles consistent with spindles timing ripple occurrence. Comparing ripple activity during co-occurring SO-spindle events with that during isolated SOs or spindles, suggested that ripple dynamics during SO-spindle events are mainly determined by the spindle, with only the SO downstate providing a global inhibitory signal to both thalamus and hippocampus. As to bottom-up influences, we found an increase in hippocampal ripples ~200 ms before the SO downstate, but no similar increase of spindles preceding SO downstates. Overall, the temporal pattern is consistent with a loop-like scenario where, top-down, SOs can trigger thalamic spindles which, in turn, regulate the occurrence of hippocampal ripples. Ripples, bottom-up, and independent from thalamic spindles, can contribute to the emergence of neocortical SOs.

Keywords: hippocampus; medial prefrontal cortex; rat; slow-wave sleep.