Linking place and view: Organizing space through saccades and fixations between primate posterior parietal cortex and hippocampus

Abstract

Humans primarily rely on vision to explore and guide actions in spatial environments. The parietal cortex is thought to withhold a unified representation of the visual space allowing to direct saccades to salient cues, while the hippocampus provides a memory-based cognitive place map of the environment. Understanding how these two representations interact during navigation is a key question. To probe the link between view and place, we compared neural activity in the posterior parietal cortex and hippocampus of macaques navigating in a virtual maze. When analyzed as a function of the animals position in the virtual environment, more neurons in the parietal cortex displayed spatial selectivity compared to the hippocampus. We hypothesized that such modulation by self-position in the parietal cortex might stem from processing visual cues of the environment through exploratory saccades and fixations. However, we established that position-selectivity was not solely correlated with simple oculomotor dynamics. Rather, spatial selectivities in the PPC and the HPC originated from cells driven by direct fixations of maze paths or landmarks. However, while a substantial proportion of PPC and HPC cells displayed selectivity towards landmarks features, such as their side of appearance or their identity, we also revealed different task-related maze segmentation between regions. Indeed, when animal gazed at paths, activity in parietal cortex revealed anticipation of reward while that of the hippocampus suggested reward outcome processing. On the other hand, when animals gazed at a landmark already present in the field of view, parietal activity tended to occur close to intersections, while that of hippocampus was more spatially distributed. Finally, at the population level, neurons in both regions anticipated landmarks before they appeared in the field of view, suggesting a shared knowledge of the spatial layout and a collective active role in memory-guided visual exploration across regions. Taken together, these findings shed light on the neural processes that link place and view, through action- and memory-driven exploration of objects in space.