Hippocampal remapping induced by new behavior is mediated by spatial context

Abstract

The hippocampus plays a central role in episodic memory and spatial navigation. Hippocampal neurons form unique representational codes in different spatial environments, which may provide a neural substrate for context that can trigger memory recall or enable performance of context-guided memory tasks. However, new learning often occurs in a familiar location, requiring that location's representation to be updated without erasing the previously existing memory representations that may be adaptive again in the future. To study how new learning affects a previously acquired spatial memory representation, we trained mice to perform two plus maze tasks across nine days in the sequence Turn Right 1 - Go East - Turn Right 2 (three days each), while we used single-photon calcium imaging to record the activity of hundreds of neurons in dorsal CA1. One cohort of mice performed the entire experiment on the same maze (One-Maze), while the second cohort performed the Go East task on a unique maze (Two-Maze). We hypothesized that CA1 representations in One-Maze mice would exhibit more change in the spatial patterns of neuronal activity on the maze from Turn Right 1 to Turn Right 2 than would be seen in Two-Maze mice. Indeed, changes in single unit activity and in the population code were larger in the One-Maze group. We further show evidence that Two-Maze mice utilize a separate neural representation for each maze environment. Finally, we found that remapping across the two Turn Right epochs did not involve an erasure of the representation for the first Turn Right experience, as many neurons in mice from both groups maintained Turn Right-associated patterns of activity even after performing the Go East rule. These results demonstrate that hippocampal activity patterns remap in response to new learning, that remapping is greater when experiences occur in the same spatial context, and that throughout remapping information from each experience is preserved.

Using multi-task experiments to test principles of hippocampal function

“…We now consider how using multi-task experiment designs can help to investigate questions of interest within and between these different theoretical frameworks. In the spatial domain, in rats, using multiple tasks in the same spatial area has been used to investigate the activity of place cells across different tasks, showing that while place cells maintain their representation across different navigation tasks (Trullier et al, 1999), changes in memory and/or attentional demands can induce remapping (Hallock & Griffin, 2013;Levy & Hasselmo, 2023;Markus et al, 1995). Similarly, by using two tasks in the same location, it has been shown that adding an associative memory task changes the representation of space in the monkey hippocampus (Gulli et al, 2020).…”

Using multi‐task experiments to test principles of hippocampal function

“…We now consider how using multi-task experiment designs can help to investigate questions of interest within and between these different theoretical frameworks. In the spatial domain, in rats, using multiple tasks in the same spatial area has been used to investigate the activity of place cells across different tasks, showing that while place cells maintain their representation across different navigation tasks (Trullier et al, 1999), changes in memory and/or attentional demands can induce remapping (Hallock & Griffin, 2013;Levy & Hasselmo, 2023;Markus et al, 1995). Similarly, by using two tasks in the same location, it has been shown that adding an associative memory task changes the representation of space in the monkey hippocampus (Gulli et al, 2020) findings in rats showed "place cells," which activate whenever the animal is in a particular location in space relative to the external environment (Moser et al, 2017;O'Keefe & Dostrovsky, 1971).…”