Dorsal and ventral hippocampus engage opposing networks in the nucleus accumbens

Abstract

2Memories of positive experiences require the brain to link places, events, and reward outcomes. 3Neural processing underlying the association of spatial experiences with reward is thought to 4 depend on interactions between the hippocampus and the nucleus accumbens (NAc) 1-9 . 5Hippocampal projections to the NAc arise from both the ventral hippocampus (vH) and the 6 dorsal hippocampus (dH) 6-12 , and studies using optogenetic interventions have demonstrated that 7 either vH 5,6 or dH 7 input to the NAc can support behaviors dependent on spatial-reward 8 associations. It remains unclear, however, whether dH, vH, or both coordinate memory 9processing of spatial-reward information in the hippocampal-NAc circuit under normal 10 conditions. Times of memory reactivation within and outside the hippocampus are marked by 11 hippocampal sharp-wave ripples (SWRs) [13][14][15][16][17][18][19] , discrete events which facilitate investigation of 12 inter-regional information processing. It is unknown whether dH and vH SWRs act in concert or 13 separately to engage NAc neuronal networks, and whether either dH or vH SWRs are 14 preferentially linked to spatial-reward representations. Here we show that dH and vH SWRs 15 occur asynchronously in the awake state and that NAc spatial-reward representations are 16 selectively activated during dH SWRs. We performed simultaneous extracellular recordings in 17 the dH, vH, and NAc of rats learning and performing an appetitive spatial task and during 18 sleep. We found that individual NAc neurons activated during SWRs from one subdivision of 19 the hippocampus were typically suppressed or unmodulated during SWRs from the other. NAc 20 neurons activated during dH versus vH SWRs showed markedly different task-related firing 21 patterns. Only dH SWR-activated neurons were tuned to similarities across spatial paths and past 22 reward, indicating a specialization for the dH-NAc, but not vH-NAc, network in linking reward 23 to discrete spatial paths. These temporally and anatomically separable hippocampal-NAc 24 interactions suggest that dH and vH coordinate opposing channels of mnemonic processing in 25 the NAc. 26