Author ORCID Identifier

https://orcid.org/0000-0001-6143-3633

Date of Award

Fall 9-30-2024

Document Type

Thesis (Ph.D.)

Department or Program

Psychological & Brain Sciences

First Advisor

Matthijs van der Meer

Abstract

An intelligent system must balance generalizing across similar experiences with maintaining the distinctiveness of each experience. This thesis explores how the hippocampus manages this balance through its neural representations to support adaptive behavior. In Chapter 1, I provide an overview of key hippocampal phenomena that contribute to this process, including remapping, splitter signal, and replay. In Chapter 2, I challenge the concept of random remapping by showing that it is possible to predict, better than chance, how a given experience will be encoded in the hippocampus across different subjects. This suggests that encoding of related experiences, which was previously thought to be random, actually follows a structured and generalizable pattern shared across individuals. In Chapter 3, I investigate how the hippocampus updates its activity patterns to generalize behaviors learned in one experience to another. Specifically, when a new aversive memory becomes linked to a previously neutral one, I show that the representation of the neutral context changes to become more similar to that of the aversive context. Importantly, this shift is modulated by the animal's behavioral state. In Chapter 4, I present a normative explanation for "paradoxical replay," a phenomenon where rats replay less-experienced trajectories during tasks with unbalanced experience. I demonstrate that paradoxical replay serves an adaptive function, protecting certain task representations under these conditions. Additionally, I show a striking correlation between greater splitter strength and a larger bias toward paradoxical replay, highlighting a novel interaction between the nature of task representations and the function role of replay. Lastly, in Chapter 5, I discuss open questions and propose future research directions to further investigate how the hippocampus supports the balance between generalization and differentiation through its neural representations.

Original Citation

Hung-Tu Chen, Jeremy R. Manning, Matthijs A.A. van der Meer, Between-subject prediction reveals a shared representational geometry in the rodent hippocampus, Current Biology, Volume 31, Issue 19, 2021, Pages 4293-4304.e5, ISSN 0960-9822, https://doi.org/10.1016/j.cub.2021.07.061. (https://www.sciencedirect.com/science/article/pii/S0960982221010514) Abstract: Summary 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. Keywords: place cells; remapping; generalization; pattern completion; pattern separation; hyperalignment

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