Hippocampus leads ventral striatum in replay of place-reward information

Carien S Lansink, Pieter M Goltstein, Jan V Lankelma, Bruce L McNaughton, Cyriel MA Pennartz
PLoS Biol. 7(8):e1000173, 2009


Associating spatial locations with rewards is fundamental to survival in natural environments and requires the integrity of the hippocampus and ventral striatum. In joint multineuron recordings from these areas, hippocampal–striatal ensembles reactivated together during sleep. This process was especially strong in pairs in which the hippocampal cell processed spatial information and ventral striatal firing correlated to reward. Replay was dominated by cell pairs in which the hippocampal “place” cell fired preferentially before the striatal reward-related neuron. Our results suggest a plausible mechanism for consolidating place-reward associations and are consistent with a central tenet of consolidation theory, showing that the hippocampus leads reactivation in a projection area.

Author Summary

Thinking back to an exciting event often includes the scene in which the event took place. Associations between specific places and emotional events are consolidated in memory, but how this is achieved is currently unknown. Two brain areas involved in learning such associations are the hippocampus and the ventral striatum, which represent spatial and emotional information, respectively. A highly valuable object in an environment will prompt humans and animals to take action, such as approaching the object. Here, we demonstrate that a combination of spatial and emotional aspects of a learning experience is replayed in the hippocampus and the ventral striatum during sleep, which is likely to contribute to the consolidation and strengthening of memory traces. This reactivation is coordinated such that the spatial information in the hippocampus is activated shortly before the emotional information in the ventral striatum. This finding is consistent with a central prediction from Memory Consolidation Theory, namely that the hippocampus initiates and orchestrates replay in connected brain areas. In addition, sleep replay occurs at a time scale about ten times faster than during the actual experience, which makes it a mechanism suitable for strengthening synaptic connections associating place with reward. Our results shed new light on the distributed way the brain processes, links, and retrieves different aspects of memories.

Filter publications by year: