Gaze-informed, task-situated representation of space in primate hippocampus during virtual navigation
Résumé
To elucidate how gaze informs the construction of mental space during wayfinding in visual species like primates, we jointly examined navigation behavior, visual exploration, and hip-pocampal activity as macaque monkeys searched a virtual reality maze for a reward. Cells sensitive to place also responded to one or more variables like head direction, point of gaze, or task context. Many cells fired at the sight (and in anticipation) of a single landmark in a viewpoint-or task-dependent manner, simultaneously encoding the animal's logical situation within a set of actions leading to the goal. Overall, hippocampal activity was best fit by a fine-grained state space comprising current position, view, and action contexts. Our findings indicate that counterparts of rodent place cells in primates embody multidimensional, task-situated knowledge pertaining to the target of gaze, therein supporting self-awareness in the construction of space. Author summary In the brain of mammalian species, the hippocampus is a key structure for episodic and spatial memory and is home to neurons coding a selective location in space (" place cells "). These neurons have been mostly investigated in the rat. However, species such as rodents and primates have access to different olfactory and visual information, and it is still unclear how their hippocampal cells compare. By analyzing hippocampal activity of non-human primates (rhesus macaques) while they searched a virtual environment for a reward, we show that space coding is more complex than a mere position or orientation selectivity. Rather, space is represented as a combination of visually derived information and task-related knowledge. Here, we uncover how this multidimensional representation emerges from gazing at the environment at key moments of the animal's exploration of space. We show that neurons are active for precise positions and actions related to the landmarks gazed at by the animals. Neurons were even found to anticipate the appearance of landmarks, sometimes responding to a landmark that was not yet visible. Overall, the place fields of primate hippocampal neurons appear as the projection of a multidimen-sional memory onto physical space.
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