Sharp-Wave Ripples in Primates Are Enhanced near Remembered Visual Objects

The hippocampus plays an important role in memory for events that are distinct in space and time. One of the strongest, most synchronous neural signals produced by the hippocampus is the sharp-wave ripple (SWR), observed in a variety of mammalian species during offline behaviors, such as slow-wave sleep [1-3] and quiescent waking and pauses in exploration [4-8], leading to long-standing and widespread theories of its contribution to plasticity and memory during these inactive or immobile states [9-14]. Indeed, during sleep and waking inactivity, hippocampal SWRs in rodents appear to support spatial long-term and working memory [4, 15-23], but so far, they have not been linked to memory in primates. More recently, SWRs have been observed during active, visual scene exploration in macaques [24], opening up the possibility that these active-state ripples in the primate hippocampus are linked to memory for objects embedded in scenes. By measuring hippocampal SWRs in macaques during search for scene-contextualized objects, we found that SWR rate increased with repeated presentations. Furthermore, gaze during SWRs was more likely to be near the target object on repeated than on novel presentations, even after accounting for overall differences in gaze location with scene repetition. This proximity bias with repetition occurred near the time of target object detection for remembered targets. The increase in ripple likelihood near remembered visual objects suggests a link between ripples and memory in primates; specifically, SWRs may reflect part of a mechanism supporting the guidance of search based on past experience.