Motivational states activate distinct hippocampal representations to guide goal-directed behaviors

Adaptive behaviors are guided by motivation and memory. Motivational states specify goals, and memory can inform motivated behavior by providing detailed records of past experiences when goals were obtained. These 2 fundamental processes interact to guide animals to biologically relevant targets, but the neuronal mechanisms that integrate them remain unknown. To investigate these mechanisms, we recorded unit activity from the same population of hippocampal neurons as rats performed identical tasks while either food or water deprived. We compared the influence of motivational state (hunger and thirst), memory demand, and spatial behavior in 2 tasks: hippocampus-dependent contextual memory retrieval and hippocampus-independent random foraging. We found that: (i) hippocampal coding was most strongly influenced by motivational state during contextual memory retrieval, when motivational cues were required to select among remembered, goal-directed actions in the same places; (ii) the same neuronal populations were relatively unaffected by motivational state during random foraging, when hunger and thirst were incidental to behavior, and signals derived from deprivation states thus informed, but did not determine, hippocampal coding; and (iii) prospective coding in the contextual retrieval task was not influenced by allocentric spatial trajectory, but rather by the animal's deprivation state and the associated, non-spatial target, suggesting that hippocampal coding includes a wide range of predictive associations. The results show that beyond coding spatiotemporal context, hippocampal representations encode the relationships between internal states, the external environment, and action to provide a mechanism by which motivation and memory are coordinated to guide behavior.