A map of visual space in the primate entorhinal cortex

Abstract

Examination of spatial representations in the entorhinal cortex of monkeys performing a visual memory task reveals individual neurons that emit action potentials when the monkey fixates multiple discrete locations in the visual field, and suggests that entorhinal cortex neurons encode space during visual exploration, even without locomotion. Grid cells — neurons located in the entorhinal cortex that exhibit place-modulated activity — provide the brain with the spatial information and spatial memory needed during navigation. The cells have been extensively studied in rodents, but there have been no single-unit analyses of grid cells in primates. Here, Elizabeth Buffalo and colleagues record entorhinal cortex neural activity in monkeys performing a visual memory task involving images on a computer monitor. The resulting data directly demonstrate the existence of grid cells in primates, and show that these cells are active during visuospatial exploration, even when the animal is not moving and is simply searching with its eyes. Place-modulated activity among neurons in the hippocampal formation presents a means to organize contextual information in the service of memory formation and recall1,2. One particular spatial representation, that of grid cells, has been observed in the entorhinal cortex (EC) of rats and bats3,4,5, but has yet to be described in single units in primates. Here we examined spatial representations in the EC of head-fixed monkeys performing a free-viewing visual memory task6,7. Individual neurons were identified in the primate EC that emitted action potentials when the monkey fixated multiple discrete locations in the visual field in each of many sequentially presented complex images. These firing fields possessed spatial periodicity similar to a triangular tiling with a corresponding well-defined hexagonal structure in the spatial autocorrelation. Further, these neurons showed theta-band oscillatory activity and changing spatial scale as a function of distance from the rhinal sulcus, which is consistent with previous findings in rodents4,8,9,10. These spatial representations may provide a framework to anchor the encoding of stimulus content in a complex visual scene. Together, our results provide a direct demonstration of grid cells in the primate and suggest that EC neurons encode space during visual exploration, even without locomotion.