How coupled slow oscillations, spindles and ripples coordinate neuronal processing and communication during human sleep

Using direct recordings from human MTL neurons during sleep, Staresina et al. reveal that neuronal firing and communication-thought to underlie synaptic plasticity and learning-are controlled by coupled slow oscillations, spindles and ripples. Learning and plasticity rely on fine-tuned regulation of neuronal circuits during offline periods. An unresolved puzzle is how the sleeping brain, in the absence of external stimulation or conscious effort, coordinates neuronal firing rates (FRs) and communication within and across circuits to support synaptic and systems consolidation. Using intracranial electroencephalography combined with multiunit activity recordings from the human hippocampus and surrounding medial temporal lobe (MTL) areas, we show that, governed by slow oscillation (SO) up-states, sleep spindles set a timeframe for ripples to occur. This sequential coupling leads to a stepwise increase in (1) neuronal FRs, (2) short-latency cross-correlations among local neuronal assemblies and (3) cross-regional MTL interactions. Triggered by SOs and spindles, ripples thus establish optimal conditions for spike-timing-dependent plasticity and systems consolidation. These results unveil how the sequential coupling of specific sleep rhythms orchestrates neuronal processing and communication during human sleep.

Automated summary

Using direct recordings from human MTL neurons during sleep, the study reveals that neuronal firing and communication are controlled by coupled slow oscillations, spindles, and ripples. These dynamics establish optimal conditions for synaptic plasticity and systems consolidation during sleep. The results shed light on how specific sleep rhythms orchestrate neuronal processing and communication in the sleeping brain.