Spatial exploration and navigation in the primate hippocampus

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Project Summary. Human and nonhuman primates are highly visual animals that are predominantly active during the daylight hours. Yet our understanding of the neural mechanisms supporting spatial navigation is largely based on studies of nocturnal, burrowing rodents with poor vision. Indeed, studies of human and nonhuman primates have already demonstrated that spatial positions can be encoded in the hippocampus exclusively by visual inspection of a scene (i.e. spatial-view cells). At the same time, primate hippocampus also comprises populations of neurons that encode self-position in a scene during locomotion (i.e. place cells). Ultimately, primate representations of space must integrate these parallel threads of spatial information, but precisely how this occurs within the primate hippocampus is entirely unknown. Here we propose to address this fundamental question by leveraging several conceptual, technical and computational innovations to examine the neural basis of spatial representations in the hippocampus of marmoset monkeys. Aim 1 complements our previous work demonstrating canonical place cells in marmoset hippocampus during free-navigation to characterize whether neurons in this neural structure can also encode space through visual exploration of a scene. Aim 2 seeks to systematically characterize behavioral strategies in marmosets when searching for food in naturalistic 3-dimensional `forest' environments. Specifically, we will test how visual exploration and physical navigation of the landscape complement each other in marmoset spatial behavior. Experiments in Aim 3 build on these results to record the activity of hippocampal neurons of freely-moving marmosets in the same 3D naturalistic environments. By integrating head-mounted, wireless eye-tracking technology and video tracking of the animals position in space, we will explicate the role of different primate hippocampal subfields for exploration and navigation.