Probing the nature of episodic memory in rodents

Episodic memory (EM) specifies the experience of retrieving information of an event at the place and time of occurrence. Whether non-human animals are capable of EM remains debated, whereas evidence suggests that they have a memory system akin to EM. We here trace the development of various behavioral paradigms designed to study EM in non-human animals, in particular the rat. We provide an in-depth description of the available behavioral tests which combine three spontaneous object exploration paradigms, namely novel object preference (for measuring memory for "what"), novel location preference (for measuring memory for "where") and temporal order memory (memory for "when"), into a single trial to gauge a memory akin to EM. Most important, we describe a variation of such a test in which each memory component interacts with the others, demonstrating an integration of diverse mnemonic information. We discuss why a behavioral model of EM must be able to assess the ability to integrate "what", "where" and "when" information into a single experience. We attempt an interpretation of the various tests and review the studies that have applied them in areas such as pharmacology, neuroanatomy, circuit analysis, and sleep. Finally, we anticipate future directions in the search for neural mechanisms of EM in the rat and outline model experiments and methodologies in this pursuit.