Between-subject prediction reveals a shared representational geometry in the rodent hippocampus

• Published in: Current biology Vol. 31; no. 19; pp. 4293 - 4304.e5
• Main Authors: Chen, Hung-Tu, Manning, Jeremy R., van der Meer, Matthijs A.A.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 11.10.2021
• Subjects: Animals; generalization; Hippocampus - physiology; hyperalignment; Memory, Episodic; Neurons - physiology; pattern completion; pattern separation; place cells; Rats; remapping; Rodentia; hyperalignment; pattern separation; pattern completion; generalization; place cells; remapping
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2021.07.061

The rodent hippocampus constructs statistically independent representations across environments (“global remapping”) and assigns individual neuron firing fields to locations within an environment in an apparently random fashion, processes thought to contribute to the role of the hippocampus in episodic memory. This random mapping implies that it should be challenging to predict hippocampal encoding of a given experience in one subject based on the encoding of that same experience in another subject. Contrary to this prediction, we find that by constructing a common representational space across rats in which neural activity is aligned using geometric operations (rotation, reflection, and translation; “hyperalignment”), we can predict data of “right” trials (R) on a T-maze in a target rat based on (1) the “left” trials (L) of the target rat and (2) the relationship between L and R trials from a different source rat. These cross-subject predictions relied on ensemble activity patterns, including both firing rate and field location, and outperformed a number of control mappings, such as those based on permuted data that broke the relationship between L and R activity for individual neurons and those based solely on within-subject prediction. This work constitutes proof of principle for successful cross-subject prediction of ensemble activity patterns in the hippocampus and provides new insights in understanding how different experiences are structured, enabling further work identifying what aspects of experience encoding are shared versus unique to an individual. •Place-cell activity was geometrically aligned across multiple subjects•Activity from one subject can be used to predict withheld data in another subject•Both overall firing rate relationships and specific firing locations contribute•Simulations verify that cross-subject prediction is impossible in aligned random data How the rodent hippocampus encodes a given experience in the coordinated activity of “place cells” is idiosyncratic for individual subjects, but Chen et al. demonstrate a relationship between the encoding of distinct but related experiences (left and right trials on a T-maze) that is preserved across subjects.