UCSF

The brain’s ability to associate experiences with subsequent rewards is fundamental to learning and memory and critical for animal survival. The neural substrates of this process are only partially understood, but are thought to rely on interactions between the hippocampus and nucleus accumbens (NAc). In particular, hippocampal input to the NAc is thought to be crucial for learning and remembering links between spatial information and reward. Hippocampal projections to the NAc arise from both the ventral hippocampus (vH) and the dorsal hippocampus (dH), and studies using optogenetic interventions have demonstrated that either vH or dH input to the NAc can support behaviors dependent on spatial-reward associations. It remains unclear, however, whether dH, vH, or both coordinate memory processing of spatial-reward information in the hippocampal-NAc circuit under normal conditions. Moreover, as dH and vH are thought to encode different aspects of an experience, whether the hippocampus can compartmentalize different types of information to circuits in the NAc is unknown. Times of memory reactivation within and outside the hippocampus are marked by hippocampal sharp-wave ripples (SWRs), discrete events which facilitate investigation of inter-regional information processing. It is unknown whether dH and vH SWRs act in concert or separately to engage NAc neuronal networks, and whether either dH or vH SWRs are preferentially linked to spatial-reward representations. To address these questions, we performed simultaneous extracellular recordings using multi-tetrode arrays in the dH, vH, and NAc of rats learning and performing an appetitive spatial task and during sleep. We report that dH and vH SWRs occur asynchronously, and that individual NAc neurons activated during SWRs from one subdivision of the hippocampus are typically suppressed or unmodulated during SWRs from the other. Furthermore, NAc neurons activated during dH versus vH SWRs show markedly different task-related firing patterns, with NAc representations related to space and reward selectively activated during dH SWRs and not vH SWRs. Our findings reveal that dorsal and ventral hippocampal interactions with the NAc are temporally and anatomically separable at times of memory processing. This work suggests that the dH-NAc and vH-NAc networks provide distinct information channels, with the dH-NAc channel dedicated to linking spatial paths with reward and reward-seeking actions. More broadly, these circuit dynamics could provide a potential neural substrate for the brain’s ability to compartmentalize aspects of experience in memory.