Incidental Encoding and Retrieval of Episodic-Like Memory in Rats: A Novel Behavioral Task

There is a pressing need for an ecologically relevant behavioral task that would enable the study of elementary aspects of episodic memory. In everyday life, episodic memories are acquired incidentally in a single-encounter fashion and are composed of sub-events separated by time gaps. We designed a behavioral task called One-Trial Trace Escape Reaction (OTTER), in which rats incidentally associated two temporally discontinuous stimuli. In OTTER, rats associate a neutral acoustic cue (conditioned stimulus, CS) with an aversive stimulus (unconditioned stimulus, US) which occurs two seconds later: we call this sequence CS-2s-US. In the first few sessions, rats are habituated to two similar environmental contexts (A and B); each context consists of interconnected dark and light sub-areas. Next, in the pairing session, rats experience CS-2s-US in the dark sub-area of one of the environmental contexts (either A or B). The US is terminated immediately after a rat escapes into the light sub-area. During the recall session 24 hours later, rats are presented with only the CS in the alternate environmental context (B or A) and their behavioral response is observed. Our results show that 50% of handled rats and 14% of non-handled rats responded to the CS by escaping to the light sub-area although they experienced only a single CS-2s-US pairing. The capacity to acquire a CS-2s-US association in a single CS-2s-US pairing indicates that rodents are able to form incidental temporal associations. The OTTER behavioral task offers a flexible high throughput tool to study memories acquired incidentally after a single experience.