Excitatory and inhibitory modulation of septal and striatal neurons during hippocampal sharp-wave ripple events

Single-units were recorded in hippocampus, septum, and striatum while freely behaving rats (n=3) ran trials in a T-maze task, and rested in a holding bucket between trials. During periods of motor inactivity, SWRs triggered excitatory responses from 28% (64/226) and inhibitory responses from 14% (31/226) of septal neurons. By contrast, only 4% (14/378) of striatal neurons were excited and 6% (24/378) were inhibited during SWRs. In both structures, SWR-responsive neurons exhibited greater spike coherence with hippocampal theta rhythm than neurons that did not respond to SWRs. In septum, neurons that were excited by SWRs fired at late phases of the theta cycle, whereas neurons that were inhibited by SWRs fired at early phases of the theta cycle. By contrast, SWR-responsive striatal neurons did not show consistent phase preferences during the theta cycle. A subset of SWR-responsive neurons in septum (55/95) and striatum (26/38) behaved as speed cells, with firing rates that were positively or negatively modulated by the rats running speed. In both structures, firing rates of most SWR-excited speed cells were positively modulated by running speed, whereas firing rates of most SWR-inhibited speed cells were negatively modulated by running speed. These findings are consistent with a growing body of evidence that SWRs can activate subcortical representations of motor actions in conjunction with hippocampal representations of places and states, which may be important for storing and retrieving values of state-action pairs during reinforcement learning and memory consolidation.