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

Abstract

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.

Hippocampal gamma‐band Synchrony and pupillary responses index memory during visual search

“…We did not explicitly evaluate object‐in‐scene memory per se in this study, thus the enhanced gamma synchrony early after scene onset may be considered a more general scene familiarity effect. Of note, higher‐frequency sharp wave ripples in these same brain regions are suppressed at the time of scene onset, and recover only later on, in association with remembered targets (Leonard and Hoffman, ). Taken together, this may suggest different modes of operation in the primate hippocampus as contextual cues emerge and recollection unfolds.…”

Spatial representations in the primate hippocampus, and their functions in memory and navigation

“…Two additional phenomena relevant to anticipatory effects have been reported previously. First, it was observed that sharp wave ripples were enhanced near remembered visual objects (Leonard and Hoffman, 2017). Second, oscillatory activity was found to synchronize with visual exploration, through a theta phase reset at saccades (Hoffman et al, 2013;Jutras et al, 2013).…”

A Closer Look at the Hippocampus and Memory

“…Critically, the reliability of theta phase-reset by visual fixations correlated with successful memory formation [31]. Furthermore, other neural signals of memory processing by hippocampus include sharp-wave ripples [33], which have been observed during visual exploration in the nonhuman primate [34], particularly for fixations in close proximity to target stimuli in a memory task [35]. In studies with rodents, memory is usually expressed via exploration, making it difficult to determine the extent to which hippocampal activity in these studies reflects memory processing versus exploration, including sensory sampling and exploration-related aspects of spatial navigation [36].…”