Thesis Format
Integrated Article
Degree
Doctor of Philosophy
Program
Neuroscience
Supervisor
Martinez-Trujillo, Julio C.
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.
Summary for Lay Audience
The hippocampus is a highly interconnected region of the brain that is essential to our ability to navigate and create mental maps of space. Much of what we know about how this region represents space comes from research conducted in rodents, which rely more on their sense of smell, whiskers and touch for navigation while highly visual primates, like monkeys and humans, rely more on vision. Research has shown that hippocampal neurons in the rodent fire when an animal is in a particular location (place), similar to a brain GPS. In contrast, in virtually navigating monkeys, hippocampal neurons have been shown to fire when the animal is looking at a particular location (view) or oriented in a particular head direction. However, this has not been thoroughly studied in naturalistic real world 3D navigation.
I set out to investigate this in a small new world monkey, the marmoset. I used motion capture to track how these monkeys navigate and explore a 3D maze. I found that marmosets use fast head movements to efficiently scan the visual space, often taking extended periods of visual exploration before deciding to initiate locomotion. I then recorded electrical activity from the CA1 and CA3 regions of the hippocampus to isolate neuronal firing and low frequency voltage fluctuations (local field potential). I found that neurons represented place in combination with view and head direction, and that the amount of place information could be decoded from neuronal firing of predominantly view and head direction selective cells. Suggesting a higher influence of vision to primate spatial representations. Other groups of neurons represented how fast the animals were moving (translation speed) and how fast their heads were turning (angular head velocity). Additionally, some of these neurons also responded to specific turning directions and in combination with jumping activity.
Finally, I describe rhythmic activity in the local field potential at a frequency of 4-10 cycles per second (also known as theta oscillations). These oscillations increased after the marmosets executed head movements, rapid eye movements (saccades) and jumps. Additionally, I show that the timing of the oscillations becomes re-aligned after these events, likely increasing synchronization of neuronal activity across the hippocampus, we think this is a common mechanism by which this region processes inputs related to changes in the visual scene. By investigating these different aspects of hippocampal activity, this dissertation provides a comprehensive view of how the marmoset hippocampus represents space and self-motion during naturalistic behaviour. These findings have important implications for understanding the neural mechanisms of spatial navigation in primates and highlight both similarities and differences with rodent models.
Recommended Citation
Buitrago Piza, Diego Fernando, "Hippocampal neural substrates of spatial navigation in marmosets freely moving in 3 dimensions" (2024). Electronic Thesis and Dissertation Repository. 10499.
https://ir.lib.uwo.ca/etd/10499
Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.
supplementary movie 1