Portet, C.; Thellier, F.; Aguilera, M.; Blondel, T.; Herbeaux, K.; Mursch, C.; Jackson, J.; Battaglia, D. A.; Sych, Y.; Goutagny, R.

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.