Modulation of lateral septal and dorsomedial striatal neurons by hippocampal sharp-wave ripples, theta rhythm, and running speed

Single units were recorded in hippocampus, lateral septum (LS), and dorsomedial striatum (DMS) while freely behaving rats (n = 3) ran trials in a T-maze task and rested in a holding bucket between trials. In LS, 28% (64/226) of recorded neurons were excited and 14% (31/226) were inhibited during sharp wave ripples (SWRs). LS neurons that were excited during SWRs fired preferentially on the downslope of hippocampal theta rhythm and had firing rates that were positively correlated with running speed; LS neurons that were inhibited during SWRs fired preferentially on the upslope of hippocampal theta rhythm and had firing rates that were negatively correlated with running speed. In DMS, only 3.3% (12/366) of recorded neurons were excited and 5.7% (21/366) were inhibited during SWRs. As in LS, DMS neurons that were excited by SWRs tended to have firing rates that were positively modulated by running speed, whereas DMS neurons that were inhibited by SWRs tended to have firing rates that were negatively modulated by running speed. But in contrast with LS, these two DMS subpopulations did not clearly segregate their spikes to different phases of the theta cycle. Based on these results and a review of prior findings, we discuss how concurrent activation of spatial trajectories in hippocampus and motor representations in LS and DMS may contribute to neural computations that support reinforcement learning and value-based decision making.