A Conserved Mammalian Hippocampal Navigation Motif Reconfigured for Primate Vision

Spatial navigation requires the brain to continuously sample the external world while evaluating internal representations of space. In rodents, this process unfolds through alternating periods of locomotion and pauses. During pauses, hippocampal sharp-wave ripples (SWRs) rates increase, likely reflecting the broadcast of spatial memories that guide navigation. Whether similar dynamics govern navigation in primates remains unknown. Here, we recorded hippocampal activity in freely moving marmosets navigating a 3D maze. Like rodents, marmosets alternated between locomotion and pauses. However, pauses were long and showed an increase in SWR rates relative to locomotion. SWRs were most prominent when animals maintained stable head orientations toward rewarded locations and were reduced during rapid exploratory head movements. SWR rates further increased when spatial memories were used to guide navigation. Our findings reveal a phylogenetically conserved motif linking behavioral states during spatial navigation to hippocampal SWR dynamics across mammals and show how primate visual specializations have adapted this motif to support vision-guided navigation. Significance StatementOur results reveal a phylogenetically conserved hippocampal navigation motif that has persisted despite major evolutionary changes in mammalian sensory ecology. Across species, navigation alternates between external exploration and internal evaluation, with SWRs marking periods of memory-guided computation. However, primate evolution reshaped the behavioral expression of this motif by coupling it to active visual sampling, gaze control, and foveal inspection of landmarks. Thus, evolution appears to have preserved a core hippocampal algorithm for navigation while adapting its sensory inputs and behavioral context to the demands of diurnal, vision-guided life.