Context Dependent Activity in Rat Hippocampus During Performance of a Three Arm Delayed Sequence Task

The observed differential patterns of activity recorded in hippocampus during the delay period of spatial memory tasks has been proposed as representing a contextual memory being maintained for task completion. However, the majority of such evidence has been acquired using simple tasks that require only memory of experience from the previous trial across a delay in order to inform the choice on the next trial. Here we designed a novel three arm delayed spatial memory task that requires maintenance of context constructed from information beyond the immediate past choice. Surprisingly, we found that activity in the hippocampus across the delay period could not explain successful task performance because there was no differentiation during delays following the same immediate spatial history. In contrast, decoding of sharp wave ripple (SWR) events consistently predicted future behavior among multiple spatiotemporally remote goals. Finally, we show SWRs displayed future trajectories that included contextually specific versions of the same spatial location, providing the first evidence for the retention of contextual information within SWR recall. All together these findings suggest that despite evidence for contextually different plans across SWR activity as well as the preservation of contextual information in SWR content, contextual coding in the hippocampus across delay periods is primarily determined by immediate past spatial context alone and shows no evidence of differentiating the more global behavioral context.