Interactions between hippocampus and visceral organs in sleep and wakefulness

Exteroception is attenuated during sleep, while interoceptive signals may remain active. If so, they can potentially trigger responses in their target areas, including the hippocampus, which is known to receive information from the internal organs. We investigated whether the hippocampus is synchronized to various visceral events in sleep and wakefulness. Activity of hippocampal neurons and local field potentials (LFPs) was co-registered with respiration, heart rate and myoelectric signals of the stomach and duodenum in two adult female cats over multiple sleep-wake cycles. Visceral event-triggered and neuronal spike-triggered (bootstrapping-based) analyses were performed on data obtained during wakefulness and SWS. Synchronization between visceral and hippocampal activities occurred in both wakefulness and SWS. However, hippocampal cells and LFPs showed preferences for one state only. Consistent with prior studies, we found the strongest link between high-amplitude respiratory events and hippocampal activity, with significantly higher occurrence during SWS. Both stomach and duodenal signals were also represented in hippocampal activity. Motility-associated duodenal myoelectric signals correlated with hippocampal activity more during wakefulness, while synchronization between regular duodenal waves and the hippocampus was more frequent during SWS. We conclude that the interoceptive signals reach the hippocampus in both sleep and wakefulness and suggest that they have the potential to oversynchronize any ongoing synchronized slow-wave activities in the hippocampal network during slow wave sleep (SWS).Significance Statement What types of sensory input shapes hippocampal activity and regulates its rhythmical structure is important for understanding both normal and paroxysmal hippocampal dynamics. We find that synchronization between interoceptive signals and hippocampal neural activity exists during wakefulness and is preserved during SWS. Moreover, this association increases in SWS for respiratory and periodic duodenal activities. Our data revealed different hippocampal neurons being related to different types of visceral activity and different states of vigilance. Our results also highlight the potential link between epilepsy and signals from cardiac, respiratory and gastrointestinal systems.