Claustral pathway coordinates distributed cortical dynamics with hippocampal output during sleep to promote memory consolidation

Abstract

The claustrum is a broadly connected subcortical structure proposed to coordinate distributed cortical activity. Claustral neurons are recruited during synchronized brain states and contribute to sleep-dependent memory consolidation, primarily through effects on cortical dynamics. Yet the claustrum also innervates the subicular complex, a major hippocampal output node, raising the possibility that it may regulate both cortical state and hippocampo-cortical dialogue during sleep. Here, we identify a projection-defined population of claustral neurons targeting the subicular complex, CLAsc, that is preferentially recruited during slow-wave sleep and tracks cortical and subicular sleep dynamics. Optogenetic activation of CLAsc neurons during post-learning sleep enhanced spatial memory consolidation without detectable changes in ripple occurrence or slow-oscillation-spindle coupling. Instead, CLAsc activation imposed a stereotyped cortical-subicular motif: a brief gamma-rich Up state followed by a coordinated Down state across prefrontal, retrosplenial and subicular regions. Within this gamma-rich Up state, interareal coherence increased, gamma bursts became synchronized, and lagged directed interactions were transiently reorganized, including an enhanced prefrontal-to-subicular component. Together, these findings identify the claustrum as a state-dependent coordinator that transforms ongoing cortical and hippocampal-output activity into coordinated network transitions during sleep, providing a circuit mechanism through which distributed brain states may support memory consolidation.