Interactions between hippocampus and visceral organs in sleep and wakefulness

Abstract

Exteroception is attenuated during sleep, while interoceptive signals may remain active. If so, they can trigger responses in their target areas, including the hippocampus, which is known to receive information from the internal organs and is susceptible to oversynchronization while triggered. 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 in 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 where gastrointestinal motility is more active, 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 StatementWhat 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, in some cases, this association increases in SWS for respiratory and periodic duodenal activities. Our data revealed specificity of hippocampal neurons to both type of visceral activity and state of vigilance, suggesting that hippocampal network is shaped by visceral activity in a state-dependent manner. Our results highlight the factors underlying the comorbidities of epilepsy with gastrointestinal, cardiac or respiratory disorders.