Slow-γ Rhythms Coordinate Cingulate Cortical Responses to Hippocampal Sharp-Wave Ripples during Wakefulness

Behavioral changes in response to reward require monitoring past behavior relative to present outcomes. This is thought to involve a fine coordination between the hippocampus (HIPP), which stores and replays memories of past events, and cortical regions such as cingulate cortex, responsible for behavioral planning. Sharp-wave ripple (SWR)-mediated memory replay in the HIPP of awake rodents contributes to learning, but cortical responses to hippocampal SWR during wakefulness are not known. We now show that in rats, during quiet-wakefulness, cingulate neurons exhibit significant responses to SWR, as well as increased modulation by the accompanying hippocampal local field potential slow-γ oscillation, a rhythm associated with intra-hippocampal information processing. The magnitude of cingulate neurons' responses to SWR is significantly correlated with the degree of their modulation by HIPP slow-γ. We hypothesize that during pauses cingulate neurons transiently access episodic information concerning previous choices, replayed by HIPP SWR, to evaluate past trajectories in light of their outcome.