An evolutionary conserved division-of-labor between hippocampal and neocortical sharp-wave ripples organizes information transfer during sleep

Abstract The hippocampal sharp-wave ripple (SW-R) is the key substrate of the hippocampal-neocortical dialogue underlying memory formation. Recently, it became evident that SW-R are not unique to archicortex, but constitute a wide-spread neocortical phenomenon. To date, little is known about morphological and functional similarities between archi- and neocortical SW-R. Leveraging intracranial recordings from the human hippocampus and prefrontal cortex during sleep, our results reveal region-specific functional specializations, albeit a near-uniform morphology. While hippocampal SW-R trigger directional hippocampal-to-neocortical information flow, neocortical SW-R reduce information flow to minimize interference. At the population level, hippocampal SW-R confined population dynamics to a low-dimensional subspace, while neocortical SW-R diversified the population response; functionally uncoupling the hippocampal-neocortical network. Critically, our replication in rodents demonstrated the same division-of-labor between archi-and neocortical SW-R. These results uncover an evolutionary preserved mechanism where coordinated interplay between hippocampal and neocortical SW-R temporally segregates hippocampal information transfer from neocortical processing.