Awake hippocampal replay is not required for short-term memory

Abstract

Short-term memory (STM) on a time scale of seconds to minutes is required to successfully perform day-to-day tasks, for example when engaging in a meaningful conversation. Previous studies in both rodents and primates have correlated hippocampal cellular activity and behavioural expression of STM. This research has led to models describing the putative neural mechanism in the hippocampus that mediate STM. In these models, a key role has been given to hippocampal replay - reactivation of neurons representing a trajectory through space- but definitive causal evidence that can challenge or confirm the model is missing. In this study, we aimed to address the uncertainty around the role of awake replay in STM by collecting direct causal evidence from behaving rats. Signatures of replay events were detected in the hippocampus and disrupted using electrical stimulation of the ventral hippocampal commissure in rats that were trained on three different spatial memory tasks in a multi-arm radial maze. All tasks required memory of the recent past, but varied in the time scale over which information needed to be retained: (1) a multiple trial match-to sample task, (2) a single trial non-match to sample task and (3) a spatial sequence memory paradigm. Rats readily learned the task rules, but disruption of awake replay did not affect task performance or other behavioral measures in any of the task. Altogether, our results show for the first time with definitive causal evidence that awake replay is not required for STM of events or of their temporal order.