Two star mazes, but a single representation of space in the monkey hippocampus
Résumé
How does the brain code similarities between different experiences while also discriminating their specificity? Studies of spatial memory have provided ample evidence that different episodes are coded by distinct patterns of cell activity. In the rodent foraging for food, hippocampal cells signal the animal's location through a place field. These place fields change when elements of the environment are altered, and a global remapping occurs when the animal is placed in different enclosures. Here we asked how hippocampal cells in the monkey code two virtual reality environments bearing a similarity of structure but different visual landmarks. We previously showed that the primate hippocampus codes space during wayfinding in more complex ways than simple place-coding, and includes task-related information, among which the progression towards the goal (Wirth et al., 2017, PLoS Biol 15(2): e2001045). We now compare the activity maps obtained when the animal searches for a hidden reward in a familiar, well-known star maze vs. a novel maze of same shape, but differing in the visible landmarks. We showed that while 35% coded only one environment, 29% of cells coded both environments. In 71% of the latter cells, activity maps showed a higher cross-correlation than expected by chance between the familiar and the novel maze. Thus, while physical landmarks changed, these cells maintained a goal-centered and task-related representation of space. This abstract representation progressively formed as a function of learning, as the cross-correlation steadily increased across learning epochs. Crucially, this progression was apparent when decoding cell activity in task-related state space or goal-centered physical space, but not as a function of either view direction or point of gaze. To summarize, some cells abstracted from the physical details of the maps and only coded high-level, goal-and task-related information in schema-like representation; the other maze-selective cells could concurrently represent the uniqueness of the perceptual and/or episodic experience.