DENTATE NETWORK ACTIVITY IS NECESSARY FOR SPATIAL WORKING MEMORY BY SUPPORTING CA3 SHARP-WAVE RIPPLE GENERATION AND PROSPECTIVE FIRING OF CA3 NEURONS

Complex spatial working memory (WM) tasks have been shown to require both hippocampal sharp wave ripple (SWR) activity and dentate gyrus (DG) neuronal activity. We therefore asked whether DG inputs to CA3 contribute to spatial WM by promoting SWR generation. Recordings from DG and CA3 while rats performed a dentate-dependent WM task on an 8-arm radial maze revealed that the activity of dentate neurons and the incidence rate of SWRs both increased during reward consumption. We then found reduced reward-related CA3 SWR generation without direct input from dentate granule neurons. Furthermore, CA3 cells with place fields in not-yet visited arms preferentially fired during SWRs at reward locations, and these prospective CA3 firing patterns were more pronounced for correct trials and were dentate dependent. These results indicate that coordination of CA3 neuronal activity patterns by DG is necessary for the generation of neuronal firing patterns that support goal-directed behavior and memory.