Brain-wide modulation of temporal and rate codes during hippocampal sharp wave ripples

Sharp wave ripples are brief, highly synchronous bursts of activity in the local field potential and population activity of the hippocampus. They occur predominantly during periods of inactivity and are crucial for the transfer of short-term memories in the hippocampus to long-term memories in the cortex. How this process exactly takes place at the neuronal level, however, is still largely unknown. To answer this question, we leveraged a large publicly available dataset of simultaneous Neuropixels recordings across the brain from the International Brain Laboratory collaboration. We analyzed 74 sessions in which at least one probe was inserted in the dorsal hippocampus (10,577 detected ripples, 7951 neurons in 15 brain regions). We found that ripples significantly modulated spiking rates of 20-60% of neurons in all recorded brain regions. It is thought that the underlying principle of memory consolidation during ripples is the replay of specific patterns of spiking activity. To investigate this, we used SpikeShip, a method to extract temporal patterns from population spiking. We found that, during ripples, the hippocampus and the entorhinal cortex showed highly consistent spike patterns while no consistent patterns were observed in downstream target regions, like the dorsal cortex. In these areas, however, assemblies of neurons did become active during and shortly after ripples. This suggests that, during memory consolidation, information is first conveyed from the hippocampus to the entorhinal cortex in a temporal code after which it is converted to a rate code by neuronal assemblies in the dorsal cortex and other target regions.