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Authors & Affiliations
Juan F. Ramirez-Villegas, Damaris K. Rangel-Guerrero, Peter Baracskay, Jozsef Csicsvari
Abstract
Current theories establish that memories are transiently stored in the hippocampus and transferred to the neocortex for long-term storage during sleep. These processes involve brain-wide plastic changes, heralded by macroscopic brain activities that occur upon changes in the neuromodulatory activity of the brainstem. The brainstem prompts periods of both enduring and transient changes of neuronal excitability that modify the activity of other sub-structures in a precise manner. Thus, brainstem activity may play a critical role in memory formation. However, the specific neural mechanisms that allow brainstem nuclei to participate in this process remain poorly understood. Here, six wild-type Long Evans rats were chronically implanted with recording micro-drives incorporating recording electrodes concurrently targeting the hippocampus, the lateral geniculate nucleus (dLG), and the parabrachial nucleus (PBn). Animals were recorded during the acquisition of a spatial memory task and subsequent sleep. We show that global changes in neuronal activity were accompanied by the occurrence of concurrent high-synchrony neural events in the PBn-dLG electrical activity. These episodes displayed electrical characteristics consistent with pontogeniculooccipital (PGO) waves. The brainstem transiently modulates hippocampal high-synchrony events through PGO waves, coupling with hippocampal sharp wave-ripples and REM-associated phasic theta waves. Crucially, spatial learning resulted in an increase in the coupling between PGO waves and hippocampal events, where the features of post-sleep PGO waves correlated with memory performance. The results of this investigation indicate that the putative control of hippocampal ensembles by PGO waves may correspond to windows for promoting plasticity during sleep, leading to memory consolidation and synaptic homeostasis.