Neural evidence for recognition of naturalistic videos in monkey hippocampus

Abstract

The role of the hippocampus in recognition memory has long been a source of debate. Tasks used to study recognition that typically require an explicit probe, where the participant must make a response to prove they remember, yield mixed results on hippocampal involvement. Here, we tasked monkeys to freely view naturalistic videos, and only tested their memory via looking times for two separate novel v. repeat video conditions on each trial. Notably, a large proportion of hippocampal neurons differentiated these videos via changes in firing rates time-locked to the duration of their presentation on screen, and not during the delay period between them as would be expected for working memory. Single neurons often contributed to both retrieval conditions, and did so across many trials with trial-unique video content, suggesting they detect familiarity. The majority of neurons contributing to the classifier showed an enhancement in firing rate on repeat compared to novel videos, a pattern which has not previously been shown in hippocampus. These results suggest the hippocampus contributes to recognition memory via familiarity during free-viewing. Significance StatementRecognition memory enables distinction of new from previously encountered stimuli. In the majority of recognition memory work, humans or animals are tasked to explicitly identify whether a stimulus is old or new. In some of these studies--but for unknown reasons not others--there is evidence of hippocampal involvement. Here, when we present trial-unique, naturalistic videos to monkeys, firing rates from many single hippocampal neurons surprisingly differentiate new from repeated videos. The ability of these hippocampal neurons to detect recently-viewed stimuli, despite the videos unfamiliar content, suggests they contribute to memory. These results are consistent with hippocampal involvement in the familiarity aspect of recognition memory during free-viewing.