Hippocampal neural substrates of spatial navigation in marmosets freely moving in 3 dimensions
Abstract
The hippocampus is a brain structure critical for spatial navigation and memory. Its structure is relatively conserved across mammals, but species-specific ecological adaptations may have impacted the ways in which spatial information is encoded, specially in highly visual primates.
In this dissertation I investigate how the hippocampus of the common marmoset (Callithrix jacchus) encodes spatial information during natural navigation in a 3D environment. The subjects’ head position and orientation were tracked in 3D while they foraged for reward. I recorded single units and local field potentials from the CA1 and CA3 regions of the hippocampus and found that putative pyramidal cells show mixed selectivity for view, head direction and place, cells encoding place independent of view or head direction were not found. Additionally, the subjects’ location could be decoded from a population of primarily view and head direction selective cells. Putative interneurons primarily encoded angular head velocity and translation speed in a mixed selective manner. Furthermore, we show that neurons could encode directional information for angular head velocity in the azimuth (horizontal) plane, the vertical tilt (pitch) plane or both, suggesting these directional signals play a role in updating view and head direction representations in an egocentric reference frame. Some of these cells were also modulated by jumping behaviors.
Finally, we found that theta oscillations (4-10 Hz) occur in short bouts on average lasting less than 1 second and that both theta power and phase are similarly modulated during exploratory behaviors that change the gaze such as head movements, saccades and jumps. Suggesting a common underlying mechanism to synchronize network activity in preparation for multisensory inputs.
These results advance our understanding of hippocampal function in the primate brain and suggest that spatial representations in the marmoset are shaped by its reliance on dynamic visual inputs. This work contributes to broadening our knowledge on how hippocampal networks in a highly visual species integrate multimodal sensory inputs for spatial cognition.