Contributions of hippocampus and striatum to memory-guided behavior depend on past experience

Abstract

The hippocampal and striatal memory systems operate independently and in parallel in supporting spatial and response learning, respectively, when animals are explicitly trained in one task. Here, we investigated whether this principle continues to hold when animals are concurrently trained in two types of tasks. Rats were trained on a plus maze in either a spatial navigation or a cue response task (individual training), while a third set of rats acquired both (concurrent training). Subsequently, the rats underwent either sham surgery or neurotoxic lesions of the hippocampus (HPC), medial dorsal striatum (DSM) or lateral dorsal striatum (DSL), followed by retention testing. Finally, rats in the individual training condition also acquired the novel other task. When rats learned one task, HPC and DSL selectively supported spatial navigation cue response, respectively. However, when rats learned both tasks, HPC and DSL additionally supported the behavior incongruent with the processing style of the corresponding memory system. DSM significantly contributed to performance regardless of task or training procedure. Experience with the cue response task facilitated subsequent spatial learning, while experience with spatial navigation delayed both simultaneous and subsequent response learning. These findings suggest that multiple principles govern the interactions among memory systems.\n\nSignificance StatementCurrently, we distinguish among several types of memories, each supported by a distinct neural circuit. The memory systems are thought to operate independently and in parallel. Here, we demonstrate that the hippocampus and the dorsal striatum memory systems indeed operate independently and in parallel when rats learn one type of task at a time, but interact co-operatively and in synergism when rats concurrently learn two types of tasks. Furthermore, new learning is modulated by past experiences. These results can be explained by a model in which independent and parallel information processing that occurs in the separate memory-related neural circuits is supplemented by information transfer between the memory systems at the level of the cortex.