Primacy of vision shapes behavioral strategies and neural substrates of spatial navigation in marmoset hippocampus

• Published in: Nature communications Vol. 15; no. 1; p. 4053
• Main Authors: Piza, Diego B., Corrigan, Benjamin W., Gulli, Roberto A., Do Carmo, Sonia, Cuello, A. Claudio, Muller, Lyle, Martinez-Trujillo, Julio
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 14-05-2024; Nature Publishing Group; Nature Portfolio
• Subjects: 59/57; 631/378/2613; 631/378/2649; 9/30; Angular velocity; Animals; Behavior, Animal - physiology; CA1 Region, Hippocampal - cytology; CA1 Region, Hippocampal - physiology; Callithrix - physiology; Daylight; Diurnal; Ecological niches; Electrophysiological recording; Exploration; Female; Head; Head movement; Head Movements - physiology; Hippocampus; Hippocampus - physiology; Humanities and Social Sciences; Interneurons; Interneurons - physiology; Locomotion; Locomotion - physiology; Male; Monkeys & apes; multidisciplinary; Navigation; Navigation behavior; Neurons; Niches; Potential oscillations; Primates; Pyramidal cells; Pyramidal Cells - physiology; Science; Science (multidisciplinary); Selectivity; Spatial Navigation - physiology; Substrates; Theta rhythms; Velocity; Velocity head; Vision; Vision, Ocular - physiology
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-48374-2

The role of the hippocampus in spatial navigation has been primarily studied in nocturnal mammals, such as rats, that lack many adaptations for daylight vision. Here we demonstrate that during 3D navigation, the common marmoset, a new world primate adapted to daylight, predominantly uses rapid head-gaze shifts for visual exploration while remaining stationary. During active locomotion marmosets stabilize the head, in contrast to rats that use low-velocity head movements to scan the environment as they locomote. Pyramidal neurons in the marmoset hippocampus CA3/CA1 regions predominantly show mixed selectivity for 3D spatial view, head direction, and place. Exclusive place selectivity is scarce. Inhibitory interneurons are predominantly mixed selective for angular head velocity and translation speed. Finally, we found theta phase resetting of local field potential oscillations triggered by head-gaze shifts. Our findings indicate that marmosets adapted to their daylight ecological niche by modifying exploration/navigation strategies and their corresponding hippocampal specializations.
How diurnal primates develop exploration-navigation strategy and how the physiology of primate hippocampus is shaped in navigation are not fully understood. Here authors show that marmosets adapted their navigation strategies to their diurnal ecological niche. Notably, marmoset hippocampal neurons are specialized for encoding combinations of view, head direction and place, and that theta oscillations are triggered by rapid head-gaze movements.