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

Diego B Piza; Benjamin W Corrigan; Roberto A Gulli; Sonia Do Carmo; A Claudio Cuello; Lyle Muller; Julio Martinez-Trujillo

doi:10.1038/s41467-024-48374-2

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

Nat Commun. 2024 May 14;15(1):4053. doi: 10.1038/s41467-024-48374-2.

Authors

Diego B Piza^{1

2}, Benjamin W Corrigan^{1

2

3}, Roberto A Gulli⁴, Sonia Do Carmo⁵, A Claudio Cuello⁵, Lyle Muller^{2

6}, Julio Martinez-Trujillo^{7

8

9

10

11}

Affiliations

¹ Schulich School of Medicine and Dentistry, Western University, London, ON, Canada.
² Robarts Research Institute, Western University, London, ON, Canada.
³ Department of Biology, Faculty of Science, York University, Toronto, ON, Canada.
⁴ Zuckerman Institute, Columbia University, New York, NY, USA.
⁵ Department of Pharmacology and Therapeutics, McGill University, Montreal, QC, Canada.
⁶ Department of Applied Mathematics, Western University, London, ON, Canada.
⁷ Schulich School of Medicine and Dentistry, Western University, London, ON, Canada. julio.martinez@robarts.ca.
⁸ Robarts Research Institute, Western University, London, ON, Canada. julio.martinez@robarts.ca.
⁹ Department of Physiology and Pharmacology, Western University, London, ON, Canada. julio.martinez@robarts.ca.
¹⁰ Department of Psychiatry, Western University, London, ON, Canada. julio.martinez@robarts.ca.
¹¹ Department of Clinical Neurological Sciences, Western University, London, ON, Canada. julio.martinez@robarts.ca.

Abstract

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.

MeSH terms

Animals
Behavior, Animal / physiology
CA1 Region, Hippocampal / cytology
CA1 Region, Hippocampal / physiology
Callithrix* / physiology
Female
Head Movements / physiology
Hippocampus* / physiology
Interneurons / physiology
Locomotion / physiology
Male
Pyramidal Cells / physiology
Spatial Navigation* / physiology
Vision, Ocular / physiology